Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Diet of Worms† Emended: An Update of
Polychaete Feeding Guilds
Appendix A
Family-by-Family Updates
Peter A. Jumars1, 3, Kelly M. Dorgan*, 2 & Sara M. Lindsay3
Ira C. Darling Marine Center, University of Maine, 193 Clark’s Cove Road, Walpole, Maine
04573; e-mail: [email protected]
1
Dauphin Island Sea Lab, 101 Bienville Boulevard, Dauphin Island, Alabama 36528; e-mail:
[email protected]
2
School of Marine Sciences, University of Maine, Orono, Maine 04469; e-mail: slindsay@maine.
edu
3
*Corresponding author
Acknowledgments
This appendix was improved by corrections and additions from J Bailey-Brock, JA Blake,
K Fauchald, MC Gambi, R Goto, PA Hutchings, G Kobayashi, LA Levin, WF Magalhães, A
Martínez Garcia, ME Rice, SA Rice, & MM Summers. PA Jumars was supported by NSF grants
OCE-0851172 and OCE-1260232. SM Lindsay was supported by NSF grant OCE-0851172.
NSF grant OCE-1029160 supported KM Dorgan.
†
The late Ralph A. Lewin suggested the title used by Fauchald & Jumars (1979). Those coauthors, having been
raised Lutheran, eagerly adopted his suggestion. They were surprised when some of the devout took offense,
perhaps not realizing that the 1979 “Diet” was less threatening than the 1521 Imperial Diet of Worms. J. Malcolm
Shick sedulously pointed out that our 1979 use was not as original as we had thought, quoting William SavilleKent (1893, p. 331), who considered Palolo worms (Eunicidae), “...well worthy of further investigation from both a
scientific and a gastronomic view. Presuming a happy combination of the two, we may look forward to a nineteenth
or twentieth century revival of the [Polynesian] ‘Diet of Worms’ ... with all the decorum of a Greenwich whitebait
dinner.”
Fauchald K, Jumars PA. 1979. The diet of worms: a study of polychaete feeding guilds. Oceanogr. Mar. Biol. Ann.
Rev. 17: 193-284.
Saville-Kent W. 1893. The Great Barrier Reef of Australia: Its Products and Potentialities. London: WH Allen & Co
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A1
Table of Contents (click to reach page)
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Table of Contents
Family name Starting page
Family template explained A5
AberrantidaeA7
AcoetidaeA8
AcrocirridaeA10
AeolosomatidaeA13
AlciopidaeA15
AlvinellidaeA17
AmpharetidaeA20
Ammocharidae See Oweniidae
AmphinomidaeA27
Antillesomatidae (sipunculan) A32
AntonbruunidaeA33
AphroditidaeA34
ApistobranchidaeA39
Arabellidae See Oenonidae
ArenicolidaeA40
Aspidosiphonidae (sipunculans) A48
Asteriomyzostomatidae (myzostomes) A51
Asteromyzostomatidae (myzostomes) A52
Bogueidae See Maldandidae
Bonelliidae (echiurans) A53
Calamyzidae See Chrysopetalidae
Caobangiidae See Sabellidae
CapitellidaeA58
ChaetopteridaeA63
ChrysopetalidaeA69
CirratulidaeA72
CossuridaeA80
CtenodrilidaeA83
DinophilidaeA86
DiurodrilidaeA87
DorvilleidaeA88
Echiuridae (echiurans) A95
Eenymeenymyzostomatidae (myzostomes) A98
Endomyzostomatidae (myzostomes) A100
EulepethidaeA101
EunicidaeA102
EuphrosinidaeA108
FabriciidaeA110
FauveliopsidaeA114
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A2
Table of Contents (click to reach page)
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07 November 2014
Family name Starting page
Flabelligeridae A116
GlyceridaeA119
Golfingiidae (sipunculans) A125
GoniadidaeA131
HartmaniellidaeA133
HesionidaeA135
Heterospionidae See Longosomatidae
HistriobdellidaeA139
IchthyotomidaeA141
Ikedidae (echiurans) A142
IospilidaeA144
IphionidaeA145
Iphitimidae See Dorvilleidae
Lacydoniidae A147
LaetmonectidaeA148
LongosomatidaeA148
LopadorrhynchidaeA150
LumbrineridaeA152
Lysaretidae See Lumbrineridae & Oenonidae
MagelonidaeA156
MaldanidaeA161
Mycomyzostoma calcidicola (myzostome)A168
Myzostomatidae (myzostomes) A169
Nautiliniellidae See Chrisopetalidae
NephtyidaeA171
NereididaeA178
NerillidaeA187
OenonidaeA190
OnuphidaeA192
OpheliidaeA196
OrbiniidaeA201
OweniidaeA207
Palmyridae See Aphroditidae
ParalacydoniidaeA211
ParaonidaeA212
ParergodrilidaeA216
PectinariidaeA217
Phascolosomatidae (sipunculans) A221
PholoidaeA225
Pholoididae See Sigalionidae
PhyllodocidaeA228
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Family name Starting page
PilargidaeA232
Pisionidae See Sigalionidae
PoecilochaetidaeA234
PoeobidaeA236
PolygordiidaeA238
PolynoidaeA240
Polyodontidae See Acoetidae
PontodoridaeA246
ProtodrilidaeA247
Protodriloididae A250
Protomyzostomatidae (myzostomes) A251
Psammodrilidae A252
Pseudocirratulidae A253
Pulvinomyzostomatidae (myzostomes) A254
Questidae See Orbiniidae
SabellariidaeA255
Sabellongidae See Sabellidae
SabellidaeA259
SaccocirridaeA265
ScalibregmatidaeA268
SerpulidaeA274
SiboglinidaeA280
SigalionidaeA284
Siphonosomatidae (sipunculans) A287
Sipunculidae (sipunculans) A289
SphaerodoridaeA294
SpintheridaeA297
SpionidaeA298
Stelechopodidae (myzostomes) A312
SternaspidaeA313
SyllidaeA316
TerebellidaeA325
Thalassematidae (echiurans) A333
TomopteridaeA338
TrichobranchidaeA340
TrochochaetidaeA344
TyphloscolecidaeA345
UncispionidaeA347
Urechidae (echiurans) A348
YndolaciidaeA350
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A4
Family Template
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Jumars, Dorgan & Lindsay
07 November 2014
Family, formal or informal higher taxon, if stable
Classifications, especially above the family level, are in flux. Although molecular data indicate
that many higher taxonomic groups are in need of revision, we include more traditionally defined
families where we anticipate that they are more familiar to users or more useful in describing
morphotypes that correspond with feeding guilds. Clitellids, sipunculans, and echiurans fall in
molecular genetic analysis as clades within polychaetes (Struck et al. 2007, Zrzavý et al. 2009).
Questions remain about whether myzostomes are basal protostomes outside or within Phylum
Annelida or instead platyzoan relatives (Zrzavý et al. 2009). We include them but exclude
clitellids for lack of our familiarity with oligochaetes and leeches.
Diversity and systematics
We give a very conservative estimate of numbers of species (excluding subspecies) and genera
based, unless otherwise noted, on living species fully accepted by the World Register of Marine
Species <http://www.marinespecies.org/> accessed during the period from 1 September 2013
to 7 October 2014. Hereafter we refer to this authority as WoRMS. By the time you read
this sentence there may well be more species in the taxon. We exclude from our counts taxa
known only from the fossil record. We provide one or more references to systematic position
of the family, focusing on recent and pending changes. Where possible we distinguish adult
morphotypes within the family and provide an estimate or range of body sizes.
Habitat
We provide a low-resolution summary of known habitats occupied by the family. Benthic
species can be epifaunal or infaunal. They can occupy soft sediments or hard substrata, the latter
by attachment, boring, or nestling in crevices. For benthos we indicate rough depth intervals as
shelf, bathyal, abyssal and (or) hadal ranges. For pelagic taxa, we indicate whether the taxon is
limited to the upper mixed layer, occupies mid waters or inhabits the bottom boundary layer.
In our usage, ventral and dorsal for any anatomical features are determined by position
with respect to the nerve chord, i.e., in the reference frame of the body with the nerve chord
running ventrally. Departure of the in situ feeding posture from a ventral-side-down anatomical
orientation can be important in feeding mechanics, so we indicate feeding postures as well when
they differ from anatomically ventral-side down. Burrow or tube morphologies and orientations
are also relevant in this regard.
Sensory and feeding structures
We include details of nuchal organs, antennae, tentacles, palps, and eyes, which are used for
chemosensing, mechanosensing, light detection and in a few cases image formation, as sensory
capabilities that are potentially important in feeding. Again with respect to morphology, ventral
refers to position relative to the ventral nerve chord. Feeding and digestive structures include
external morphology and internal anatomy, including pharyngeal structure, with the caveat that
internal morphology is rarely reported in polychaetes. We rely largely on Beesley et al. (2000)
and Rouse & Pleijel (2001) for our family summaries, updated as necessary. Authorship in these
compendia varies by family and so is given separately for each family where used. Complete
publisher information is given, however, only under the references for this template (p. A7).
Motility
We retain Fauchald & Jumars’ (1979, hereafter “F&J”) ordinal scheme of motile, discretely
motile or sessile again focused on feeding biology. A motile species moves to eat, whereas a
discretely motile species may stay in place indefinitely and can feed without moving (often with
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A5
Family Template
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
the help of extensible tentacles or palps and ambient sediment transport) but remains capable of
moving. A sessile species, if displaced from its surroundings, is unable to resume function.
Illustrations
We list a small number of illustrations relevant to the feeding structures and habits of members of
the family. To avoid repetition for nearly every family, we underrepresent informative and artful
photographs collected in plates within Beesley et al. (2000) and Rouse & Pleijel (2001).
Feeding
The bulk of our effort falls under this subheading. We provide summaries of research results
published since F&J up to 7 November 2014. We cite publications prior to F&J in this appendix
only if they were omitted by F&J, have been challenged subsequently or are acutely relevant
to interpretations being made. We therefore strongly caution that an appreciation for the
weight of evidence underlying current understanding by family requires a reading of both F&J
and the current appendix entry. Our bibliography for the intervening decades is large but not
exhaustive; where possible it relies on recent and comprehensive papers to summarize changes in
understanding since 1979. We also expressly exclude references that simply used F&J to classify
trophic positions of species without testing those classifications.
Information under this subheading focuses especially on direct observations of feeding, gut
contents, and results of feeding experiments, including in particular selection experiments with
alternative foods and (in the case of deposit and suspension feeders) multiple particle types. We
summarize information gleaned from lipid analyses in identifying prey-predator relationships.
We assess stable isotope results, mainly from δ13C and δ15N analyses, using 13C results
primarily to distinguish alternative food sources at the base of the trophic pyramid and 15N results
primarily to estimate trophic levels. We restrict 15N data largely to ordinal comparisons of δ15N
within a site and within Polychaeta. One phenomenon that becomes apparent from this process
is that subsurface deposit feeders often—but neither always nor everywhere—have δ15N values
above the value expected of an animal that feeds on sediments. Some of this effect is clearly due
to feeding on refractory buried material enriched in 15N compared with fresh phytodetritus, but—
whatever the causes—this inconsistent enrichment complicates interpretation of trophic levels
from δ15N. Our listings of published stable isotope results are not exhaustive. Multiple detrital
sources sometimes result in relatively small dynamic ranges in δ15N among polychaete taxa (e.g.,
Mittermayr et al. 2014) that in other places segregate worms much more clearly into trophic
levels. In general we avoid data sets with small dynamic ranges or few polychaete species.
Recent findings raise additional doubts about the strength of inference from lipid profiles and
stable isotopic enrichments. Thurber (2014) in feeding experiments with diverse eukaryotic and
prokaryotic foods found Ophryotrocha labronica (Dorvilleidae) to generally be more depleted
in 15N than their foods and to change very little in lipid profiles. The profiles they maintained
resembled those of animals inferred to ingest phytoplankton, a food that was not used in these
growth experiments.
Guild membership
We summarize feeding strata, strata in which worms reside, structures used in food encounter,
feeding methods, motilities and diets.
Research questions and opportunities
• We highlight knowledge gaps.
• We suggest research questions to which the family is particularly well suited.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A6
Family Template
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
References
Beesley PL, Ross GJ, Glasby CJ, eds. 2000. Fauna of Australia, Vol. 4A, Polychaetes and Allies:
The Southern Synthesis. Canberra: CSIRO Publishing
Fauchald K, Jumars PA. 1979. The diet of worms: A study of polychaete feeding guilds.
Oceanogr. Mar. Biol. Ann. Rev. 17:193-284
Mittermayr A, Fox SE, Sommer U. 2014. Temporal variation in stable isotope composition (δ13C,
δ15N and δ34S) of a temperate Zostera marina food web. Mar. Ecol. Prog. Ser. 505:95–105
Rouse GW, Pleijel, F. 2001. Polychaetes. Oxford: Oxford University Press
Struck TH, Schult N, Kusen T, Hickman E, Bleidorn C, et al. 2007. Annelid phylogeny and the
status of Sipuncula and Echiura. BMC Evol. Biol. 7:57, 11 pp.
Thurber AR. 2014. Diet-dependent incorporation of biomarkers: implications for foodweb studies using stable isotope and fatty acid analyses with special application to
chemosynthetic environments. Mar. Ecol. doi:10.1111/maec.12192
Zrzavý J, Říha1 P, Piálek L, Janouškovec J. Phylogeny of Annelida (Lophotrochozoa): totalevidence analysis of morphology and six genes. BMC Evol. Biol. 9:189, 14 pp.
Aberrantidae
Diversity and systematics
This small family of small worms is a good place to start because it quickly lays to rest any
notion that relations between external and internal morphology and food-web function in
polychaetes are well understood. Aberrantidae are represented by a single genus, Aberranta,
whose 4 known members are < 7 mm long. Recent molecular genetic analyses place them near
Nerillidae and Amphinomidae and suggest some affiliation with Eunicida (Worsae et al. 2005,
Zrzavý et al. 2009). Aberrantids may well be jawless, pedomorphic relatives of Dorvilleidae
(Worsae et al. 2005).
Habitat
Aberrantids occur in muds and sands under 4 - 300 m of water (Martínez & Adarraga 2011).
Sensory and feeding structures
Individuals carry a pair of ciliated, ventrally inserted palps and a medial antenna. Prostomial
eyes may be present laterally. Nuchal organs are inconspicuous, ciliated patches located laterally
in the groove between the prostomium and the first annulus. Ciliated tracts on the palps lead
through the mouth into the ventral, muscular pharynx. The mouth bears a U-shaped lower lip.
Motility
A midventral ciliated band (Worsae et al. 2005) is used in ciliary gliding (Mackie et al. 2005), a
motility mode common to many meiofaunal polychaete species (Struck 2006).
Illustrations
Mackie et al. (2005) present line drawings of all four known species. Scanning electron
micrographs in Rouse (2001, Fig. 44.1) of an undescribed Aberranta sp. show extensive
ciliary fields, including the convergence of the two ciliated palp grooves on the mouth and the
midventral ciliary band.
Feeding
There is virtually no diet information (Mackie et al. 2005). Small body sizes suggest that
aberrantids are specialists on finding and selecting high-quality foods for ingestion, i.e., bacterial
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A7
Aberrantidae
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Jumars, Dorgan & Lindsay
07 November 2014
films, diatoms, or other protists, but this suggestion needs verification for specific foods. They
appear to be too small to profit from bulk deposit feeding.
Guild membership
We conjecture that Aberranta spp. are motile epibenthic and interstitial feeders using ciliated,
grooved palps, the lower lip and the eversible pharynx to encounter and feed selectively on
microbial films, microphytobenthos and rich organic detritus. They likely feed on smaller items
and films microphagously but on larger items (e.g., diatoms) macrophagously.
Research questions and opportunities
• Any feeding information will be the first.
• How capable are the palps, lower lip and eversible pharynx in freeing microbial films and
detrital particles from various substrata?
References
Mackie ASY, Pleijel F, Rouse GW. 2005. Revision of Aberranta Hartman, 1965 (Aberrantidae:
Annelida), with descriptions of new species from the Mediterranean and Hong Kong. Mar.
Ecol. 26:197–208
Pleijel F. 2001. Aberrantidae Wolf, 1987. See Rouse & Pleijel 2001, pp. 175–6
Struck TH. 2006. Progenetic species in polychaetes (Annelida) and problems assessing their
phylogenetic affiliation. Integr. Comp. Biol. 46:558–68
Worsaae K, Nygren A, Rouse GW, Giribet G, Persson J, et al. 2005. Phylogenetic position
of Nerillidae and Aberranta (Polychaeta, Annelida), analysed by direct optimization of
combined molecular and morphological data. Zool. Scr. 34:313–28
Zrzavý J, Říha P, Piálek L, Janouškovec J. 2009. Phylogeny of Annelida (Lophotrochozoa): totalevidence analysis of morphology and six genes. BMC Evol. Biol. 9:189 doi:10.1186/14712148-9-189. 14 pp.
Acoetidae, Aphroditiformia
Diversity and systematics
Acoetidae comprise about 60 species in 10 genera, 4 of them monotypic. In molecular genetic
distance, acoetids fall nearer to Polynoidae than do the other 5 families of scaleworms (Norlinder
et al. 2012). Prior to Pettibone’s (1989) revision, the family was known as Polyodontidae.
Acoetids are typically robust, dorsoventrally compressed worms up to 4 cm wide and 2 m long.
Habitat
Acoetids occupy diverse bottom types from low intertidal to about 1500 m water depths
(Pettibone 1989).
Sensory and feeding structures
Acoetids are extensively equipped with sensory appendages. The prostomium and first
(tentacular) segment appear fused and carry eyes, long palps, antennae, and tentacular cirri. In
some species the eyes are very large and stalked (termed ommatophores). Pettibone (1989)
identified four groups based on prostomial characteristics. Acoetids lack a distinct peristomium.
As do other scaleworms, they have a pair (upper and lower) of jaws with two large teeth on
each, and typically some smaller ones located lateral to the large ones. The jaws are attached to
a muscular, eversible pharynx that bears a circlet of distal sensory papillae when everted. They
bear putative venom glands that Wolf (1986) described as appearing smaller and less developed
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A8
Acoetidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
than those of other scaleworms (likely associated with their scavenging habits).
Motility
Acoetids share notopodial spinning glands with Aphroditidae. Whereas in aphroditids the glands
produce the dorsal “felt,” in Acoetids they secrete material of similar appearance that is used to
cement local mud or sand and debris into a thick, strong, fibrous tube, often with a substantial
collar around its upper rim. The tube opening may either be flush with the sediment-water
interface or protrude above it, or the tube may be attached to hard substrata (Stimpson 1856,
Watson 1895, Barnich & Steene 2003). The tube is not much longer than the worm. Its tube
is not as thoroughly described, but Sthenelanella among the more closely related sigalionids
(cf. Norlinder et al. 2012) also has notopodial spinning glands (Pettibone 1989) and spins a
fibrous tube incorporating ambient sediments (Day 1967). Acoetids show reluctance to leave
the tube entirely (Acoetes lupina, Stimpson 1856; Panthalis oerstedi, Watson 1895; Polyodontes
vanderloosi, Barnich & Steene 2003) but P. oerstedi was noted to move occasionally (Watson
1895), and P. vanderloosi took up residence as fairly large individuals where they apparently had
not been previously (Barnich & Steene 2003). Reluctance to leave the tube and the seemingly
large investment in tube construction give the impression that individuals are sessile, but in situ
data on tube-leaving frequencies are lacking. Acoetids clearly can make new tubes (Watson
1895) and so fit our criteria for discrete motility.
Illustrations
Watson (1865) presents line drawings of the external anatomy and also of the tube of Panthalis
oerstedi. In her revision, Pettibone (1989) displays the diversity of anterior appendages.
Palmero et al.’s (2008) stippled line drawings are also informative regarding anterior anatomy.
Fig. 3 in Barnich & Steene (2003) is a spectacular color photograph of Polyodontes vanderloosi
in situ. An intimidating look into the ommatophores of Eupolyodontes cf. batabanoensis is
provided at <http://doris.ffessm.fr>.
Feeding
Both aquarium (Stimpson 1856, Watson 1895) and field (Barnich & Steene 2003) observations
indicate that worms feed without entirely leaving their tubes. Ben-Eliahu & Fiege (1994)
reported a pandalid decapod taken from the gut of a Sicilian specimen of Euarche tubifex.
Acoetids can be caught on baited fish hooks (Eisig 1887, Parenzan 1980). Fished specimens
usually lack the majority of their posterior segments, but it is not known in most cases whether
the missing segments remained in the tube or were lost during retrieval. For the largest reported
specimen caught by fishing (2 m long, 2 cm diam.), however, all 2 m came to the surface in a
water depth of 50 m before the rear 170 cm detached (Saint-Loup 1889).
Stable isotopic data from a single individual confirm a high trophic level. Polyodontes
maxillosus from the Bay of Banyuls-sur-Mer displayed levels of 15N enrichment similar to those
of lumbrinerids, glycerids and an oenonid from the same site (Carlier et al. 2007).
Guild membership
Acoetids are discretely motile, tube-building, sit-and-wait scavengers and carnivores utilizing a
pair of jaws for epibenthic food capture and mastication. Their foraging range appears limited to
less than a body length from the tube opening. They are usually infaunal in sands and muds but
may alternatively attach the tube to hard substrata.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A9
Acoetidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Research questions and opportunities
• Frequencies of tube leaving and their causes in nature remain to be identified. They may be
low enough to make acoetids effectively sessile. It would be interesting to obtain estimates
of the energy required to construct a new tube.
• Dietary breadth is unexplored. No lipid analyses are available to constrain the realized diet.
• Identity, toxicity, and other functions of the putative venom remain to be established.
References
Barnich R, Steene R. 2003. Description of a new species of Polyodontes Renieri in Blainville,
1828 (Polychaeta: Acoetidae) from Papua New Guinea. The Beagle: Records of the Museums
and Art Galleries of the Northern Territory 19:91-96
Ben-Eliahu N, Fiege D. 1994. Polychaetes of the family Acoetidae (= Polyodontidae) from the
Levant and the Central Mediterranean with a description of a new species of Eupanthalis,
Mémoir. Mus. Natl. Hist. Sér. A, Zool. 162:145-161
Carlier A, Riera P, Amouroux J-M, Bodiou J-Y, Grémare A. 2007. Benthic trophic network in the
Bay of Banyuls-sur-Mer (northwest Mediterranean, France): An assessment based on stable
carbon and nitrogen isotopes analysis. Estuar. Coast. Shelf Sci. 72:1-15
Day JH. 1967. A Monograph on the Polychaeta of South Africa. Part 1. Errantia. London:
British Museum of Natural History
Eisig H. 1887. Monographie der Capitelliden des Golfes von Neapol und der Angrezenden
Meeres-Abschnitte nebst Untersuchungen zur Vergleichenden Anatomie und Physiologie.
Fauna und Flora des Golfes von Neapal, Monograpie 16:1–906.
Norlinder E, Nygren A, Wiklund H, Pleijel F. 2012. Phylogeny of scale-worms (Aphroditiformia,
Annelida), assessed from 18SrRNA, 28SrRNA, 16SrRNA, mitochondrial cytochrome c
oxidase subunit I (COI), and morphology. Mol. Phylogen. Evol. 65:490–500
Palmero AM, Martínez A, Brito MDC, Núñez J. 2008. Acoetidae (Annelida, Polychaeta) from
the Iberian Peninsula, Madeira and Canary islands, with description of a new species.
Arquipélago. Life Mar. Sci. 25:49-62
Parenzan P. 1980. Un reperto interessante nel mare di Porto Cesareo. Thalassia Salentina
10:135-137.
Pettibone M.H., 1989a. Revision of the aphroditoid polychaetes of the family Acoetidae Kinberg
(= Polydontidae Augener) and reestablishment of Acoetes Audouin and Milne-Edwards,
1832, and Euarche Ehlers, 1887. Smithson. Contrib. Zool. 464:1–138
Saint-Loup R. 1889. Sur le Polyodontes maxillosus. C. R. Acad. Sci. 109:412–14
Stimpson W. 1856. On some remarkable marine invertebrata inhabiting the shores of South
Carolina. Proc. Boston Soc. Nat. Hist. 6:307–9
Watson AT. 1895. Observations on the tube-forming habits of Panthalis oerstedi. Proc. Liverpool
Biol. Soc. 9:169–88
Wolf PS. 1986. A new genus and species of interstitial Sigalionidae and a report on the presence
of venom glands in some scale-worm families (Annelida: polychaeta). Proc. Biol. Soc. Wash.
99:79-83
Acrocirridae, Cirratuliformia
Diversity and systematics
Acrocirridae comprise about 50 species distributed among 10 genera, three of them monotypic.
Molecular genetic analyses have revealed distinct benthic and pelagic clades and have confirmed
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
affinity of acrocirrids with flabelligerids and cirratulids (Osborn & Rouse 2010).
Benthic species have weakly developed parapodia with sparse chaetae and comprise two
morphotypes, one grub-like and the other elongate. The former typically are covered with
papillae and often adherent sediments or foraminiferan tests (e.g., Flabellichaeta incrusta in
Salazar-Vallejo et al. 2007). The largest benthic acrocirrids are members of Acrocirrus that can
reach 7 cm in length (Hutchings 2000). Tubes have not been noted.
Four genera, Chauvinelia, Helmetophorus, Swima, and Teuthidodrilus, bear abundant
swimming chaetae and are observed or presumed to be pelagic. The abundant, closely spaced
chaetae, typically longer than the body width, resemble and function as paddles on the ends
of noto- and neuropodia that are much better developed than those of benthic forms. Well
preserved specimens carry a gelatinous sheath and can also reach lengths of about 7 cm (Osborn
et al. 2011a, b). Two additional body plans have been reported among pelagic species but have
yet to be formally described (Osborn et al. 2011a).
Habitat
Shallow-water representatives (mostly Acrocirrus and Macrochaeta) are often found in small,
sediment-filled crevices in heterogenous environments, but some species may be small enough
to be interstitial (e.g., Núñez et al. 1997). Flabelligena, Flabelligella, and Flabellichaeta are
predominantly bathyal and abyssal. Acrocirrids are widely distributed but rarely dominant in
deep-sea sediments, but in the Angola Basin at depths of 5000 - 5500 m Flabelligella spp. can
constitute > 5% of benthic polychaete individuals (Fiege et al. 2010). Pelagic forms inhabit
bottom boundary layers of the deep ocean, and may also be present in particle-rich mid waters
(Salazar-Vallejo et al. 2007; Osborn et al. 2009, 2011a, b).
Sensory and feeding structures
Benthic acrocirrids are similar in general appearance to some flabelligerids but lack an anterior
chaetal cage. The peristomium projects forward, displacing the prostomium dorsally. The
head is retractable in Chauvinelia and Flabelligella (Rouse 2001). Shallow-water species may
bear up to three pairs of prostomial ocelli. Most benthic genera (Acrocirrus, Macrochaeta,
Flabelligena, and Flabellichaeta) and all pelagic forms carry a pair of forward-projected, ciliated
palps inserted on the peristomium above the mouth (Rouse 2001). Flabelligella has been
described to lack palps, but Rouse (2001) warned that palps are fragile and may have been lost
from specimens of this genus. The ventral buccal organ is unarmed and presumably eversible.
Benthic and pelagic forms typically have 1 - 4—but as many as 8—pairs, of anterior branchiae
on their first few segments. The palp and branchial array in planktonic forms has apparent
mechanoreceptive ability (Osborn et al. 2011a).
Nuchal organs are unusually diverse among acrocirrids. In Acrocirrus, they can be a pair
of transverse, grooved, ciliated, crescentic elevations just below the palp insertions (Okuda
1934). In Macrochaeta, they can be a pair of shallow, ciliated grooves at the posterior margin
of the prostomium (Banse 1969). In pelagic forms they are located between the palps and first
branchiae and take a wide range of shapes, from simple, straight to arcuate ridges in Swima spp.
(Osborn et al. 2011a) to elaborate, projecting branching structures in Teuthidodrilus (Osborn et
al. 2011b).
Motility
The presence of papillae with adherent sediments or foraminiferans in many benthic species
(e.g., Salazar-Vallejo et al. 2007) does not appear compatible with rapid burrowing. Tentacles
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Jumars, Dorgan & Lindsay
07 November 2014
in general among benthic species are a means to feed from a substantial area without frequent
movement to a new location. Video observations suggest that pelagic forms of Swima and
Teuthidodrilus are neutrally buoyant, not requiring thrust or lift to stay suspended, but swim
anatomically backward (which is also downward in their normal orientation) when mechanically
disturbed; some taxa can release autotomized branchiae that bioluminesce, presumably aiding
their escape from predators (Osborn et al. 2011a, b).
Illustrations
Photographs and drawings of pelagic forms in Osborn et al. (2009; 2011a, b) are remarkable.
Rouse (2001) provides informative photographs of Acrocirrus and drawings of Macrochaeta.
Feeding
Benthic species are assumed to use their palps to deposit feed (Pettibone 1982), but no direct
observations appear to have been published. Surface deposit feeding in Macrochaeta is
supported by the observation that an undescribed species of this genus was discovered by a diver
because it left distinctive tracks on the sediment surface in a Mexican anchialine cave (Gonzalez
et al. 2012). Flabelligena, Flabelligella, and Flabellichaeta are predominantly bathyal and
abyssal and may also deposit feed, though their generally small sizes (< 1 cm long) and the
small sizes of many Macrochaeta spp. suggest specialization on organic-rich items for ingestion.
Osborn et al. (2011b) suggested based on video observations that Teuthidodrilus samae feeds on
large particle aggregates in deep-sea bottom boundary layers. Likely encounter mechanisms are
gravitational deposition and turbulent shear.
Guild membership
We tentatively assign the larger benthic acrocirrids (≥ 1 cm long) to be tentaculate, discretely
motile, surface deposit feeders, but members of the smaller species and life stages may be
specialists on labile foods that remain to be identified, possibly including foraminiferans as well
as fresh phytodetritus. We cannot yet rule out the possibility of subsurface deposit feeding in
larger forms. Acrocirrids can be interstitial or epifaunal in and on coarse sediments; the extent to
which they are infaunal in finer sands and muds is unknown. We tentatively assign pelagic forms
to be passive suspension feeders using mechanosensing and chemosensing and thus likely to
detect larger aggregates more efficiently.
Research questions and opportunities
• Direct observations of feeding in any benthic species would be the first.
• Stable isotopic analyses and lipid profiles of pelagic and smaller benthic species could be
informative, although small body size in the latter makes such studies challenging.
• Data on motility of benthic species are lacking.
• Comparison of pharyngeal structure with related cirratulids could provide insight into
potential differences or similarities in feeding behaviors.
References
Banse K. 1969. Acrocirridae n. fam. (Polychaeta Sedentaria). J. Fish. Board Can. 26:2595–620
Fiege D, Ramey PA, Ebbe B. 2010. Diversity and distributional patterns of Polychaeta in the
deep South Atlantic. Deep-Sea Res. Pt. I 57:1329–44
Gonzalez BC, Borda E, Carvalho R, Schulze A. 2012. Polychaetes from the Mayan underworld:
phylogeny, evolution, and cryptic diversity. Natura Croatica 21:51–3
Hutchings. 2000. Family Acrocirridae. See Beesley et al. 2000, pp. 202-3
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Acrocirridae
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Núñez J, Ocana O, Brito MDC. 1997. Two new species (Polychaeta: Fauveliopsidae and
Nerillidae) and other polychaetes from the marine lagoon cave of Jameos del Agua,
Lanzarote (Canary Islands). Bull. Mar. Sci. 60:252–60
Okuda S. 1934. The polychaete genus Acrocirrus, from Japanese waters (with nine text-figures).
J. Fac. Sci. Hokkaido Imperial Univ. Series ⅤⅠ. Zoology. 2:197–209
Osborn KJ, Haddock SHD, Pleijel F, Madin LP, Rouse GW. 2009. Deep-sea, swimming worms
with luminescent “bombs.” Science 325:964
Osborn KJ, Haddock SHD, Rouse GW. 2011a. Swima (Annelida, Acrocirridae), holopelagic
worms from the deep Pacific. Zool. J. Linn. Soc. 163:663–78
Osborn KJ, Madin LP, Rouse GW. 2011b. The remarkable squidworm is an example of
discoveries that await in deep-pelagic habitats. Biol. Lett. 7:449–53
Osborn KJ, Rouse GW. 2010. Phylogenetics of Acrocirridae and Flabelligeridae (Cirratuliformia,
Annelida). Zool. Scr. 40: 204–19
Pettibone MH. 1982. Annelida. In Synopsis and Classification of Living Organisms, ed. SP
Parker, 2:1–47
Rouse GW. 2001. Acrocirridae Banse, 1969. See Pleijel & Rouse 2001, pp. 209–11
Salazar-Vallejo SI, Gillet P, Carrera-Parra LF. 2007. Revision of Chauvinelia, redescriptions of
Flabellichaeta incrusta, and Helmetophorus rankini, and their recognition as acrocirrids
(Polychaeta: Acrocirridae). J. Mar. Biol. Ass. U. K. 87:465–77
Aeolosomatidae
Diversity and systematics
Aeolosomatidae are meiofaunal in size and are known from (cf. Rouse 2001): several species
in the genus Aeolosoma; a single species in Rheomorpha that lacks chaetae; Nectohelmins
dasysoma, only partially described in a short meeting abstract (Kincaid & Ruffolo 1988) and
also lacking chaetae; and, Hystricosoma chappuisi, known only from the external surfaces of
European crayfish. N. dasysoma probably will be renamed when it is more fully described,
and H. chappuisi has been considered to belong more properly in Aeolosoma (Pop 1975,
Rouse 2001). Historically considered to fall within Clitellata, molecular genetic studies place
aelosomatids outside, but possibly as a sister group (Struck & Purschke 2005).
Habitat
Aeolosoma spp., with the exception of A. maritimum, are found mostly in fresh and estuarine
rather than marine waters. All the other genera are limited to fresh waters. Aeolosoma spp.
can occur in eutrophic microenvironments (Singer 1978, Falconi et al. 2007), but they are not
characteristic of the most eutrophic fresh waters (Sãrkà 1994). R. neiswestnovae was first
discovered living interstitially (Ruttner-Kolisko 1955) and is much more characteristic of
oligotrophic, undisturbed conditions (Sãrkà 1994).
Sensory and feeding structures
Aeolosomatids lack anterior appendages and ocelli. They have heavily ciliated, rounded
prostomia whose ciliary fields funnel ventrally toward a U-shaped, muscular lower lip on the
peristomium. They bear a muscular, ventral, non-eversible pharynx. In A. hemprichi and all
other Aeolosomatidae nuchal organs are present as ciliated pits near the rear of the prostomium
in the lateral fringes of the prostomial ciliary field; they are most ventral in A. viride (Hessling &
Purschke 2000).
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Motility
Singer (1978) described cultured A. hemprichi as swimming over the substrate using ventral
cilia or pushing through soft material in an earthworm-like fashion while using long chaetae to
anchor. Ruttner-Kolisko (1955) described an additional inchworming form of locomotion in R.
neiswestnovae. N. dasysoma is ciliated over its entire body surface, giving it a distinctive (but
otherwise undescribed) swimming behavior cf. Kincaid & Ruffolo (1988).
Illustrations
Ruttner-Kolisko (1955, Fig. 1-3) provides line drawings of external morphology of Rheomorpha
neiswestnovae and illustrates inchworming motion by adhesion to a rigid surface (her Fig. 4-5)
that it uses in addition to ciliary gliding with its extensive prostomial ciliary fields. Singer (1978,
Fig. 5) details, in a stippled line drawing, the anterior ventral structure of Aeolosoma hemprichi.
Feeding
Singer (1978) described A. hemprichi as using ventral cilia to “constantly push debris toward the
mouth” while moving through soft material. He described an alternative suction-feeding mode
on fouling films of harder substrata as beginning by a sealing off of the sphincter between the
pharynx and esophagus. The worm then lifted the anterior body above the substratum and drove
it downward and forward before flattening its anterior through simultaneous contraction of the
dorsoventral prostomial muscle fibers, then raising the central portion and creating low pressure
that Singer (1978) suggested would lift particles off the substrate. Kincaid & Ruffolo (1988)
indicated that N. dasysoma created low pressure by rapid dilation of the pharynx. This suction
in both species likely “vacuums” up particles freed by abrasion of the prostomium (especially
the lips) with the substrate, with the thick posterior and lateral lips around the mouth directing
flow to come from the anterior direction. Singer (1978) cultured A. hemprichi on various
bacteria-rich materials. Falconi et al. (2007) fed A. hemprichi and A. viride on activated sewage
sludge, finding the worms useful in reduction of sludge volume. Nandin & Sarma (2004) found
Aeolosoma sp. to compete with planktonic daphnids for Chlorella in small laboratory containers
where Chlorella could settle out of suspension.
Guild membership
Aeolosomatidae can feed macrophagously on individual microalgae or large detritus particles
or microphagously on microbial films and small detrital particles, using the lower lip as a push
broom and a combination of ciliary motion and muscular suction to ingest its food. All species
are motile on surfaces and within interstices.
Research questions and opportunities
• Limiting food quality for small individuals is an issue that could be profitably addressed in
Aeolosoma spp. that have already been grown under laboratory conditions.
• It would be informative to know whether species from more oligotrophic locations can grow
on nutritionally more dilute food or must still specialize on rare, rich patches.
References
Falconi R, Cristiani E, Tomba G, Zaccanti F. 2007. Reduction rates and growth of two species of
Aeolosomatidae on activated sludge. Acta Hydrobiol. Sinica 31 Suppl.:166–71
Hessling R, Purschke G. 2000. Immunohistochemical (cLSM) and ultrastructural analysis
of the central nervous system and sense organs in Aeolosoma hemprichi (Annelida,
Aeolosomatidae). Zoomorphology 120:65–78
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Aeolosomatidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Kincaid W, Ruffolo JJ. 1988. Nectohelmins: A new genus of aeolosomatid oligochaete worm.
Amer. Zool. 28:9A (Abstr.)
Nandini S, Sarma S. 2004. Effect of Aeolosoma sp. (Aphanoneura: Aeolosomatidae) on the
population dynamics of selected cladoceran species. Hydrobiologia 526:157–63
Pop V. 1975. Was ist Hystricosoma chappuisi Michaelsen (Aeolosomatidae, Oligochaeta)? Mitt.
Hamburgischen zool. Mus. Inst. 72:75–8
Rouse GW. 2001. Aeolosomatidae Beddard, 1985 and Potamodrilus Lastochkin, 1935. See
Rouse & Pleijel 2001, pp. 287–9
Ruttner-Kolisko A. 1955. Rheomorpha neiswestnovae und Marinellina flagellata, zwei
phylogenetisch interessante Wurmtypen aus dem Süßwasserpsammon. Öst. zool. Z. 6:55–69
Särkkä J. 1994. Lacustrine, profundal meiobenthic oligochaetes as indicators of trophy and
organic loading. Hydrobiologia 278:231–41
Singer R. 2008. Suction-feeding in Aeolosoma (Annelida). Trans. Amer. Micros. Soc. 97:105–11
Struck TH, Purschke G. 2005. The sister group relationship of Aeolosomatidae and
Potamodrilidae (Annelida: “Polychaeta”) — a molecular phylogenetic approach based on
18S rDNA and cytochrome oxidase I. Zool. Anz. 243:281–93
Struck TH, Schult N, Kusen T, Hickman E, Bleidorn C, et al. 2007. Annelid phylogeny and the
status of Sipuncula and Echiura. BMC Evol. Biol. 7:57, 11 pp.
Alciopidae, Phyllodocida
Diversity and systematics
Alciopidae comprise about 50 species in 10 genera, only one of them monotypic. Alciopidae
are now generally included within Phyllodocidae and termed “Alciopini” by Pleijel (2001).
Molecular data support inclusion in Phyllodocidae (Halanych et al. 2007, Struck & Halanych
2010), and similarity of adult forms of alciopids and phyllodocids suggests that adaptation to
the pelagic environment was not pedomorphic (Halanych et al. 2007). Because of obvious
morphological and behavioral differences, i.e., a distinct body plan, we separate them here. Most
species are between 3 and 30 cm long, though some species are < 1 cm long.
Habitat
Alciopidae are holopelagic and widely distributed in oceanic and shelf environments. Many are
very transparent, but some forms are colored and opaque. They occur primarily in the upper
mixed layer and mid waters where their complex eyes are most useful (Halanych et al. 2007), but
some species are found in abyssal bottom boundary layers (Bühring & Chritiansen 2001).
Sensory and feeding structures
Prominent, hemispherical to spherical, image-forming eyes larger than the rest of the prostomium
are diagnostic for the group. At least one species has visual sensitivity to ultraviolet light (Torrea
candida, Wald & Rayport 1977, Johnsen 2001). A slightly raised, semicircular, densely ciliated
nuchal organ lines the dorsomedial, rear edge of each eye, and sparser tufts of what appear to
be sensory cilia are evenly dispersed in larger sections of the eye, excluding the lens (SA Rice,
Univ. Tampa, personal communication). The prostomium also carries three dorsal antennae and
two ventral palps. Anterior segments bear three to five pairs of tentacular cirri. The muscular,
eversible pharynx is large and bears papillae that may be chitinized in some species (Pleijel
2001). Dales (1955) described considerable variability in proboscis length and shape among
species, with papillae extended to form long, horn-like structures covered in mucus-secreting
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Jumars, Dorgan & Lindsay
07 November 2014
cells in some species of Alciopa, Vanadis, and Torrea. The proboscis in some species of Vanadis
and Torrea is “elongated into a slender raptorial tube” (Dales 1955).
Motility
Alciopids are strong swimmers with uniramous parapodia. Although the chaetae may be simple
or jointed, the joint is reinforced and does not seem to flex (Merz & Edwards 1998).
Illustrations
Rice (1987) provides remarkable scanning electron micrographs of anterior structures including
everted pharynges, sharp (chitinized) pharyngeal papillae, and ciliary tufts on the eyes.
Jiménez-Cueto & Suárez-Morales (2008) provide attractive and informative, stippled line
drawings of several species, showing two with everted pharynges. A striking photograph of
Vanadis sp. with it pharynx everted is posted (5 Dec. 2013) at <http://www.natgeocreative.com/
photography/1151432>.
Feeding
Studies of alciopid diets are remarkably few (Beesley et al. 2000) since Dales (1955), who
documented feeding on copepods, euphausiids, and thaliaceans. Hopkins & Torres (1989)
dissected 30 specimens of Rhynchonereella bongraini from the Weddell Sea, however, and found
25 containing diatoms and none with animal remains. The specimens dissected were only 2 - 9
mm long (mean 4 mm).
Phleger et al. (1998) studied lipids in plankton from the Elephant Island region of Antarctica
and suggested on the basis of polyunsaturated fatty acid and cholesterol contents that Vanadis
antarctica may prey on larval fishes. Bühring & Christiansen (2001) sampled abyssal
benthopelagic organisms and analyzed their lipid contents. Whereas most copepods had high
concentrations of wax esters, consistent with long-term storage of a seasonal food supply, they
found strikingly low lipid content and a dominance of membrane fatty acids in Vanadis sp. Low
lipid storage indicates that Vanadis sp. is likely feeding throughout the year, consistent with
carnivory, although concentrations of individual fatty acids were inconclusive in identifying
specific food sources.
Guild membership
We classify alciopids as macrophagous visual hunters, most of which are likely to be
carnivorous, but with some smaller members taking diatoms and other phytoplankton. They use
a muscular, eversible, generally unarmed pharynx to capture prey, primarily in the upper mixed
layer and mid waters, but some species frequent deeper bottom boundary layers. We do not
know the extent to which they are sit-and-wait predators or move more continuously.
Research questions and opportunities
• Dietary information is still lacking for most species.
• Detection distances, prey choices and hunting behaviors and success rates in still water and
in a range of turbulence intensities would be informative.
References
Bühring S I, Christiansen B. 2001. Lipids in selected abyssal benthopelagic animals: Links to the
epipelagic zone? Prog. Oceanogr. 50:369–82
Dales RP. 1955. The evolution of the pelagic alciopid and phyllodocid polychaetes. Proc. Zool.
Soc. Lond. 125:411-20
Halanych KM, Cox LN, Struck TH. 2007. A brief review of holopelagic annelids. Integr. Comp.
Biol. 47:872–9
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Alciopidae
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Hopkins TL, Torres JJ. 1989. Midwater food web in the vicinity of a marginal ice zone in the
western Weddell Sea. Deep-Sea Res. Pt. A 36:543–60
Jiménez-Cueto S, Suárez-Morales E. 2008. An account of Alciopina, Torrea, and Rhynconereella
(Polychaeta: Alciopidae) of the western Caribbean Sea. Belg. J. Zool. 138:70–80
Johnsen S. 2001). Hidden in plain sight: The ecology and physiology of organismal transparency.
Biol. Bull. 201:301–18
Merz RA, Edwards DR. 1998. Jointed chaetae—their role in locomotion and gait transitions in
polychaete worms. J. Exp. Mar. Biol. Ecol. 228:273–90
Phleger CF, Nichols PD,Virtue P. 1998. Lipids and trophodynamics of Antarctic zooplankton.
Comp. Biochem. Phys. 120:311–23
Pleijel F. 2001. Phyllodocidae Örsted 1843a. See Rouse & Pleijel 2001, pp. 132-5
Rice SA. 1987. Reproductive biology, systematics, and evolution in the polychaete Family
Alciopidae. Bull. Biol. Soc. Wash. 7:114–27
Struck TH, Halanych KM. 2010. Origins of holopelagic Typhloscolecidae and Lopadorhynchidae
within Phyllodocidae (Phyllodocida, Annelida). Zool. Scr. 39:269–75
Wald G, Rayport S. 1977. Vision in annelid worms. Science 196:1434–9
Wilson RS. 2001. Family Alciopidae. See Beesley et al. 2001, pp. 115-7
Alvinellidae, Terebelliformia
Diversity and systematics
Alvinellidae comprise about a dozen species within 2 genera. They are most closely related to
Ampharetidae and somewhat more distantly to Pectinariidae, Terebellidae and Trichobranchidae
(Zhong et al. 2011). Alvinellids are moderately large, generally tubicolous worms. Adults are
2 - 15 cm long.
Habitat
Alvinellids colonize hydrothermal vents or hydrothermally active sediments. Alvinella
pompejana is one of the first colonists of new hydrothermal vents and interacts with
hydrothermal precipitation in forming chimneys so that the hardened, parchment tubes extend
radially from the outer chimney walls. Paralvinella sulfincola shares A. pompejana’s preference
for the hot parts of vents and is frequently observed to leave its tube, in part to remain in hightemperature regions (Tunnicliffe et al. 1993). Other Paralvinella species attach to siboglinid
tubes (Desbruyères & Laubier 1991). Paralvinella bactericola inhabits bacterial mats of
hydrothermally active sediments (Desbruyères & Laubier 1991).
Sensory and feeding structures
The type species, Alvinella pompejana, is roughly 10 cm long and 1 cm in diam. and carries an
abundant, filamentous, epibiotic bacterial flora on its dorsum. Like most ampharetids, alvinellids
utilize a moderate number of buccal tentacles attached to a dorsal organ on the roof of the mouth
that are shorter than those of terebellids and are fully retractable into the mouth. These tentacles
are grooved and ciliated. Male alvinellids also have a pair of larger tentacles attached to the
ventral surface of the buccal cavity that are used in sperm transfer (Rouse 2001). The ventral
pharynx is muscular, and the buccal cavity is ciliated. It may be eversible (Rouse 2001). Lateral
pouches in the buccal cavity of A. pompejana contain rows of teeth that in transverse sections
resemble rakes and join ventrally at the rear of the buccal cavity (Saulnier-Michel et al. 1990).
They may aid in separating bacterial coatings from ingested mineral grains. The prostomium
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Jumars, Dorgan & Lindsay
07 November 2014
resembles a small hood over the buccal opening. Nuchal organs have not been described (Rouse
2001). Antennae are lacking. Four pairs of branchiae typically project from the tube.
Motility
Although most alvinellids are tube dwellers, several species of Paralvinella do not appear
to construct tubes but rather nestle in crevices among other tubes or in other rough substrata,
where they secrete copious mucus and move relatively frequently (Tunnicliffe et al. 1993).
Early reports of swimming by alvinellids (Desbruyères & Laubier 1983) have been discounted
(Desbruyères et al. 1998).
Illustrations
The original description of the type species provides remarkably detailed, whole-body ventral
and lateral views (Desbruyères & Laubier 1980, Figs. 1 & 2). Desbruyeres and Laubier (1991;
Fig. 2) show the long, spiraled tentacles of Paralvinella bactericola and the rows of denticles
along the ventral part of the everted mouth of Alvinella sp. Grelon et al. (2006, Fig. 1) present
photographs demonstrating territoriality in P. sulfincola. Video observations suggest that spacing
is effected by head-butting from nearby individuals <http://www.pmel.noaa.gov/eoi/nemo/
explorer/ashes/sulfideworm.html>. An additional close-up of this species is found at <http://
en.wikipedia.org/wiki/File:Palm_worms.jpg>. A photograph of a whole A. pompejana is posted
at <http://amex.snv.jussieu.fr/photos/Apompejana.jpg>.
Feeding
The tentacles are used to deposit feed, including on the bacterial residents of the worm tubes
(Desbruyères & Laubier 1983). Attached, filamentous bacteria on the posterior dorsal surface
of Alvinella, however, do not appear to be directly involved in their nutrition (Alyse-Danet et
al. 1986). Dissolved and particulate components of gut contents are consistent with digestion
of bacteria, leaving mineral grains, especially of elemental sulfur, to dominate in the hindgut
(Saulnier-Michel et al. 1990).
Desbruyères & Laubier (1991) suggested that P. palmiformis and pandorae can supplement
deposit feeding by collecting suspended material on their gills and funneling it to the base
of the gills, where the bolus of mucus and collected particles can be transferred to the oral
tentacles in a manner reminiscent of Spies’ (1975) observations on Flabelliderma commensalis
(Flabelligeridae). They suggested as well that the two large tentacles in P. bactericola may
be used to feed on larger suspended aggregates while the smaller tentacles engage in deposit
feeding. Observations or other kinds of evidence supporting these suggestions were not
presented.
Stable isotopic analyses among sympatric species of Paralvinella show systematic variation
in diet between species and sites and document changing diet with size in P. palmiformis but
a clear trophic dependence on chemosynthetic bacteria (Levesque et al. 2003, Bergquist et al.
2007). N and C isotopic signatures support similar dependence for P. pandorae (Bergquist
et al. 2007). A. pompejana showed high δ13C values comparable to those of the siboglinid
Riftia pachyptila, indicating strong dependence on bacteria shared by these two worms with
very different feeding modes (Desbruyères et al. 1983). Interestingly, δ13C values differed
substantially for bivalves at hydrothermal vents, indicating two very different carbon sources
(Desbruyères et al. 1983).
Guild membership
Alvinellids are tentaculate surface deposit feeders specializing on bacteria-rich aggregates,
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mats and films. In addition, some species may also suspension feed using either branchiae or
large tentacles attached to the ventral wall of the buccal cavity. We classify them as discretely
motile because even the modest amount of observation available from submersibles and video
recordings indicates that tube leaving is common in the shifting microenvironments of vent
fields. P. bactericola is infaunal in bacterial mat-covered sediments. The other alvinellid species
attach to hard substrata, including other animal tubes, near or in hydrothermally venting fluids.
The interaction of some species with precipitation of minerals in chimneys may technically make
them endolithic.
Research questions and opportunities
• Nuchal organs are so far unknown in alvinellids.
• The relative importance of suspension feeding in P. palmiformis, pandorae, and bactericola
is unknown.
• It would be interesting to know whether digestive kinetics and gut passage are speeded by
elevated temperatures experienced by some alvinellids (Chevaldonné et al. 2000).
• It is unknown whether alvinellids utilize enzyme-surfactant mixtures similar to those
produced by deposit feeders on more organically dilute sediments and how they avoid
potential problems with toxicity in their metal-rich environments (Mayer et al. 1997, Chen et
al. 2000).
References
Alayse-Danet A, Gaill F, Desbruyères D. 1986. In situ bicarbonate uptake by bacteria-Alvinella
Associations. Mar. Ecol. 7:323–40
Bergquist DC., Eckner JT, Urcuyo IA. 2007. Using stable isotopes and quantitative community
characteristics to determine a local hydrothermal vent food web. Mar. Ecol. Prog. Ser.
330:49–65
Chen Z, Mayer LM, Quétel C, Donard FX, Self RFL et al. 2000. High concentrations of
complexed metals in the guts of deposit feeders. Limnol. Oceanogr. 45:1358–67
Chevaldonné P, Fisher CR, Childress JJ, Desbruyères D, Jollivet D et al. 2000. Thermotolerance
and the ‘Pompeii worms’. Mar. Ecol. Prog. Ser. 208:93–5
Desbruyères D, Chevaldonne P, Alayse A-M, Jollivet D, Lallier FH et al. 1998. Biology and
ecology of the “Pompeii worm” (Alvinella pompejana Desbruyères and Laubier), a normal
dweller of an extreme deep-sea environment: A synthesis of current knowledge and recent
developments Deep-Sea Res. Pt. II 45:383–422
Desbruyères D, Gaill F, Laubier L, Prieur D, Rau GH. 1983. Unusual nutrition of the “Pompeii
worm” Alvinella pompejana (polychaetous annelid) from a hydrothermal vent environment:
SEM, TEM, 13C and 15N evidence. Mar. Biol. 75:201–5
Desbruyères D, Laubier L. 1980. Alvinella pompejana gen. sp. nov., Ampharetidae aberrant des
sources hydrothermales de la ride Est-Pacifique. Oceanol. Acta 3:267–74
Desbruyères D, Laubier L. 1983. Primary consumers from hydrothermal vents animal
communities. In Hydrothermal Processes at Seafloor Spreading Centers, ed. PA Rona, K
Bostrom, L Laubier, KL Smith, pp. 711–34. New York: Plenum Press
Desbruyères D, Laubier L. 1991. Systematics, phylogenhy, ecology and distribution of the
Alvinellidae (Polychaeta) from deep-sea hydrothermal vents. Ophelia Suppl. 5:31–45
Grelon D, Morineaux M, Desrosiers G, Juniper SK. 2006. Feeding and territorial behavior of
Paralvinella sulfincola, a polychaete worm at deep-sea hydrothermal vents of the northeast
Pacific Ocean. J. Exp Mar. Biol. Ecol. 329:174–86
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Alvinellidae
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Levesque C, Juniper SK, Marcus J. 2003. Food resource partitioning and competition among
alvinellid polychaetes of Juan de Fuca Ridge hydrothermal vents. Mar. Ecol. Prog. Ser.
246:173–82
Mayer LM, Schick LL, Self RFL, Jumars PA, Findlay RH et al. 1997. Digestive environments of
benthic macroinvertebrate guts: Enzymes, surfactants and dissolved organic matter. J. Mar.
Res. 55:785-812
Rouse GW. 2001. Alvinellidae Desbruyères and Laubier, 1986. See Rouse & Pleijel 2001, pp.
235–7
Saulnier-Michel C, Gaill F, Hily A, Alberic P, Cosson-Mannevy MA. 1990. Structure and
functions of the digestive tract of Alvinella pompejana, a hydrothermal vent polychaete. Can.
J. Zool. 68:722–32
Spies RB. 1975. Structure and function of the head in flabelligerid polychates. J. Morphol.
147:187-208
Tunnicliffe V, Desbruyères D. Jollivet D, Laubier L. 1993. Systematic and ecological
characteristics of Paralvinella sulfincola Desbruyères and Laubier, a new polychaete (family
Alvinellidae) from northeast Pacific hydrothermal vents. Can. J. Zool. 71:286–97
Zhadan AE, Tzetlin AB. 2002. Comparative morphology of the feeding apparatus in the
Terebellida (Annelida: Polychaeta). Cah. Biol. Mar. 43:149–64
Zhong M, Hansen B, Nesnidal M. 2011. Detecting the symplesiomorphy trap: a multigene
phylogenetic analysis of terebelliform annelids. BMC Evol. Biol. 11:369 <http://www.
biomedcentral.com/1471-2148/11/369> 15 pp.
Ampharetidae, Terebelliformia
Diversity and systematics
Ampharetidae comprise about 230 species distributed among about 62 genera, 37 of them
monotypic. Efforts have been renewed to revise generic definitions to provide more consistency
and fewer monotypic genera (Jirkov 2008, 2011, Salazar-Vallejo & Hutchings 2012), but no
consensus has been reached on the desirable revisions. At the family level, ampharetids are
closedly related to alvinellids and somewhat more distantly to pectinariids, terebellids and
trichobranchids (Zhong et al. 2011). The majority of adults are 1 - 6 cm long, although some
species can be as short as 5 mm (Rouse 2001)
Habitat
Ampharetids are tubicolous, infaunal species in muds and sands at all water depths. Although
relatively few ampharetids are adapted to low salinities and tidal emersion, those few (species
of Hobsonia, Hypania and Hypaniola) can reach high local abundances. High densities of
ampharetids are also seen in sediments at methane seeps (Thurber et al. 2013). The highest
abundances are reached in shallow shelf depths where particle fluxes are high (e.g., Buchanan
1963), but the highest species diversities are found in bathyal zones.
The anterior part of the tube is usually parallel with the sediment-water interface and may
be flush with that interface in some species but elevated as much as ten tube diameters or more
above the interface in others. The normal feeding posture holds the body axis parallel to the
sediment-water interface, ventral side down in the horizontal, anterior portion of the tube. The
tube is two to ten, but typically about three, times as long as the worm, with the posterior portion
curving downward into the sediment.
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Some ampharetids can attach to hard substrata. Zottoli (1982) described two species,
Decemunciger apalea and Endecamera palea recovered from experimentally deployed islands
of wood at bathyal depths. Amphysamytha galapagensis, in turn, attaches its tube to mineral
substrata such as lava or clam shells at hydrothermal vents (Zottoli 1983).
Sensory and feeding structures
A lobed, hood-like prostomium overlies the buccal region (Rouse 2001). It may bear a small
number of eyespots and has two lateral, comma-shaped, ridge-like nuchal organs near its
posterior edge. Feeding tentacles of ampharetids are short (relative to those of terebellids),
grooved and ciliated. They attach to the roof of the buccal cavity, into which they are fully
retractable, with the exception of two species of Noanelia for which buccal tentacles are attached
to a membrane that cannot be retracted into the mouth (Jirkov 2011), raising questions about
their placement in Ampharetidae. One or two larger tentacles (or palps) may be present with
different insertion points than the shorter ones in other genera, and this condition is sometimes
accompanied by reduction in size or even absence of the smaller tentacles (Holthe 1986, Rouse
2001). Like other Terebelliforma, ampharetids have a muscular ventral pharynx with a ciliated
buccal cavity (Zhadan & Tzetlin 2002). In Ampharete it is partly eversible (Rouse 2001).
Whereas Terebelliforma lack jaws, and most lack teeth, at least three species of ampharetids bear
teeth in radula-like arrays on the underside of a ventral pharyngeal organ that may be of use in
scraping microbial films from particles (Tzetlin 2004). All of these toothed species are small,
with adults ≤ 1 cm long. Up to 4 pairs of branchiae may be present on anterior segments. Some
species have anteriorly facing golden paleae that are similar to but considerably less pronounced
than those of pectinariids (Rouse 2001).
Internal anatomy is not well explored in Ampharetidae, but gastric diverticula are known in
Hobsonia and three other genera (Banse 1979). Gut structure is compartmentalized and diverse
(Penry & Jumars 1990).
Motility
We know of no ampharetids that are not tube builders. Ampharetids have two ways of moving.
One is by tube extension. The other is by leaving the tube. We are most familiar with two
species, Hobsonia florida and Amphicteis scaphobranchiata. When either is forced to leave the
tube it quickly burrows below the sediment surface. Some time later the single anterior tube
opening emerges on the sediment surface and is slowly extended into the normal morphology
and posture (PA Jumars, personal observations). We regard ampharetids as discretely motile.
Illustrations
Nowell et al. (1984, Fig. 1) show line drawings of the ejection of fecal pellets out of the
feeding area by Amphicteis scaphobranchiata. Mackie (1994, Fig 2a) shows a line drawing
of the position of teeth on the lower lip of Adercodon pleijeli, and more detailed drawings and
micrographs of teeth are shown in Tzetlin (2004). Line drawings of the morphology of the
buccal apparatus for Terebelliformia (Fig. 9, Zhadan and Tzetlin, 2002) illustrate hypothetical
sequences of evolutionary pathways. Jirkov (2008) provides informative line drawings
and photographs of anterior morphologies in Ampharetidae, and Stiller et al. (2013) show
photographs of Amphisamytha spp. from deep-sea vents and seeps.
Feeding
Species more than about 1 cm long are surface deposit feeders and typically bring particles to
the mouth through a combination of ciliary entrainment and transport along the tentacles plus
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muscular tentacle contraction into the mouth. The process proves highly mechanically selective
(Jumars et al. 1982). Many species rely on ambient sediment transport processes to remove fecal
pellets and resupply food. Amphicteis scaphobranchiata, which usually inhabits fine sediments
under weak currents, has evolved a behavior that enhances deposition rates to its feeding area. It
effectively maintains a sediment trap, wherein it feeds, by actively flinging its fecal pellets out of
reach of its feeding tentacles, producing a feeding pit (Nowell et al. 1984, Yager et al. 1993).
Gaston (1987) reported finding detritus in dissected guts of all 3 Ampharete arctica, 14
Anobothrus gracilis, 5 Auchenoplax crinita and 3 Melinna cristata from the U.S. mid-Atlantic
continental shelf. The species reported as M. cristata may be a closely related species (Mackie &
Pleijel 1995). Zottoli (1982) similarly found only detritus in the digestive tracts of Endecamera
palea but also found wood fragments and larvae of the shipworm Xylophaga sp. in the guts of
Decemunciger apalea. He surmised that it likely fed on fecal pellets of animals utilizing the
wood islands, on the bivalve larvae, settling detritus and fungi and bacteria colonizing the wood.
Particle selectivity has been examined in detail in Hobsonia florida. In experiments with
spherical particles, it showed peak preference for particles of about 14 µm diam. (Jumars et al.
1982, Self & Jumars 1988), preference for particles of lower specific gravity (Self & Jumars
1988), and moderate preference for protein-coated particles (Taghon 1982). It is likely that much
of this selection is mechanical (Jumars et al. 1982), but also that the peak selection on natural
particles is for somewhat larger particle sizes: smooth glass and plastic spheres have minimal
surface area per unit of weight of material and so are more difficult to pick up or retain with an
adhesive than are rougher, natural particles (Self & Jumars 1978, 1988; Guieb et al. 2004).
Post-ingestion selectivity was also observed by Self & Jumars (1978), with denser particles
being eliminated preferentially. They posited involvement of the ventral ciliated gutter. Penry
(1989) conducted a preliminary analysis of the kinematics of material transport through the gut
of Amphicteis scaphobranchiata. She found evidence for substantial axial mixing during gut
passage (which is rare in deposit feeders with tubular guts) and also for a shunt accelerating
elimination for those particles reaching the ventral ciliated gutter. This function of the ventral
ciliated gutter in ampharetids is likely facilitated by gravitational forces and therefore may
literally underlie the typical posture and tube orientation of the worms.
Juvenile Hobsonia florida < 1 cm long lack teeth but specialize on benthic diatoms
(Gallagher et al. 1990, Hentschel & Jumars 1994, Hentschel 1998) before they become large
enough to deposit feed. Zottoli (1974) described juvenile Hobsonia florida as, “feeding on
microscopic plant and animal material at about the two-chaetiger stage by forcing material
from the mud surface into the digestive tract through the action of the ventrally located buccal
mass and by cilia on the upper lip.” Similar behavior was described by Tzetlin et al. (1987,
cited in Tzetlin 2004) for juveniles of related terebellids that use a ventral pharyngeal bulb to
scrape microfouling before their tentacular apparatus fully develops. We hypothesize that teeth
in small ampharetids may be adaptations allowing ingestion of labile, high-quality diatom or
bacterial foods rather undiluted by large sediment grains. They are similar to the teeth of related
alvinellids, which appear to be used to separate bacteria from minerals. They may also be used
to puncture diatoms or to break down larger particles. Such teeth or other adaptations for highly
selective ingestion are likely to be found more widely in juveniles and pedomorphic forms of
other ampharetids. Zottoli’s (1999) observations of occasional ingestion of shipworm larvae by
8-chaetiger juveniles of Decemunciger apalea may reflect similar requirements for labile ingesta.
In his closing paragraph Oyenekan (1988) stated that it was unknown whether Melinna
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Jumars, Dorgan & Lindsay
07 November 2014
palmata is carnivorous, but he concluded that the production of the cirratulid polychaete
Caulleriella caputesocis was sufficient to support the observed production of M. palmata if it
were to have been a carnivore (cf. Oyenekan 1987). Because no evidence of carnivory in general
or on C. caputesocis was presented, we discount this suggestion until evidence is forthcoming.
Most stable isotopic studies are consistent with surface deposit feeding by ampharetids.
Populations of Amelina sp., Samytha cf. californiensis and an unidentified ampharetid
responded numerically to wood enrichments at 1670 m depth in the Santa Cruz Basin, and S. cf.
californiensis also responded to kelp enrichments. All showed slight increases in δ15N over the
ambient sediments, consistent with surface deposit feeding (Bernardino et al. 2010). Lysippe
labiata from 15 m water depth in Kongsfjorden, Spitzbergen, also showed stable N and C
signatures consistent with surface deposit feeding (Kędra et al. 2012) as did Melinna cristata
from 60 m water depth in the Gullmar Fjord, Sweden (Magnusson et al. 2003) and Ampharete
sp. from 100 m water depth in Hornsund, Spitsbergen (Sokołowski et al. 2014). Ampharete
grubei fell > 3‰ below Glycera rouxii in samples from the Bay of Biscay (Le Loc’h et al.
2008), also consistent with deposit feeding. In the Bay of Brest, Schaal et al. (2010) found
Ampharete sp. with values typical of surface deposit feeders. Hunter et al.’s (2012) δ15N values
for Ampharetidae from the oxygen minimum zone of the Arabian Sea were also consistent with
deposit feeding.
Melinna sp. showed rapid ingestion of 13C-labeled diatom detritus applied at bathyal depths
(Levin et al. 1997). Melinna at time zero in the 2-5 cm layer of sediments incorporated the
tracer, suggesting extremely rapid response, and the highest labeling was reported in Melinna
from the 5-10 cm layer after 1.5 d. Although it was captured deep in the sediments, this
individual no doubt had been surface deposit feeding. Because deposit feeders use surfactants
as well as enzymes to extract lipids from sediments (Mayer et al. 2001) and because the
hydrophobic pollutant that Magnusson et al. (2003) used was applied on the sediment surface,
it is not surprising that M. cristata showed the highest pollutant uptake among polychaetes
in 29 d incubations. Melinna palmata has been found to greatly concentrate copper in its
branchiae—to an extent that deters fish predation (Gibbs et al. 1981). Details of its acquisition
and concentration are poorly known.
In a study of intertidal and subtidal invertebrates from Ariake Sound, southern Japan,
Yokoyama et al. (2009) in an unidentified species of ampharetid found stable C and N content
indicative of purely microphytobenthic origin. Unfortunately, no information about body sizes
was given, but feeding on microphytobenthos would be consistent with feeding by juveniles or
small-bodied adults.
Carmichael et al.’s (2004) study of shallow estuaries on Cape Cod, however, gave a δ15N
value for Ampharete sp. that was anomalously high for a surface deposit feeder. One potential
explanation of occasional anomalously high δ15N values is incidental ingestion of crustacean
exuviae, settling larvae and recently settled juveniles. Feller et al. (1977) found immunological
evidence for ingestion of Corophium salmonis, Macoma balthica, Anisogammarus confervicolus
and Nereis limicola by Hobsonia florida. Among these “prey” species, only M. balthica has
larvae and juveniles small enough to have been ingested whole. The other species are likely to
have been ingested as fragments.
The original description of Amphysamytha galapagensis collected near vents reported
gut contents of detritus and bacteria (Zottoli 1983). Amphysamytha galapagensis at vents in
the Guymas Basin had stable C and N signatures consistent with detritivory (Soto 2009). A.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Jumars, Dorgan & Lindsay
07 November 2014
galapagensis on the Juan de Fuca Ridge showed very high variability in δ13C and δ15N among
individuals, suggestive of a broad range of vent and non-vent detrital sources (Bergquist et
al. 2007). Polar fatty acids have been used as biomarkers of bacterial groups in the diets of
invertebrates. On this basis, the ampharetid Amphisamytha lutzi from Mid-Atlantic Ridge
vents has been shown to feed on diverse bacterial foods including both sulfur oxidizers and
reducers (Colaço et al. 2002, 2007). (The single specimen analyzed by Colaço et al. [2002]
was erroneously labeled a chaetopterid in their Table 2.) At methane seeps, by contrast, stable
isotopic data indicated strong dependence of ampharetids on methanotrophs (Levin & Michener
2002, Carlier et al. 2010, Thurber et al. 2010) and in particular on aerobic methanotrophs
(Thurber et al. 2013). In very dense beds of ampharetids on the Hikurangi margin, New Zealand,
Sommer et al. (2010) calculated that anaerobic oxidation of methane could not produce sufficient
organic matter to support the ampharetids and suggested that organic carbon produced by aerobic
methane oxidation was the primary carbon source for these seep ampharetids.
Guild membership
Most ampharetids are microphagous infaunal, tubicolous, discretely motile, surface depositfeeders utilizing one or usually more tentacles to bring food to an unarmed (for most taxa),
ventral, muscular, ciliated pharynx. Under food-poor conditions, they may extend the tube to
reach additional feeding areas without the predation risk of leaving the tube. Juveniles and taxa
< 1 cm long may feed macrophagously on richer food materials such as diatoms, foraminiferans
or settling larvae. Incidental ingestion of animal parts, settling larvae or recently settled
juveniles is to be expected.
Research questions and opportunities
• Occasional high δ15N values remain mysterious. Possibilities include feeding on more
refractory subsurface material by depleting and removing surficial sediments or by feeding at
the bottom of the tube. Another possibility is feeding on animal detritus, such as barnacle or
copepod exuviae, or settling larvae (Zottoli 1982).
• Identification of the functions associated with the diverse and complex gut structures of
ampharetids (Penry & Jumars 1990) could provide insight into the sequencing of functions
associated with digestion and assimilation of particular foods.
• Mechanisms of metal concentration in Melinna palmata remain to be explored. Its high
copper concentrations (Gibbs et al. 1981) suggest examination of vent species for metal
contents.
References
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Bergquist DC, Eckner JT, Urcuyo IA, Cordes EE, Hourdez S, et al. 2007. Using stable isotopes
and quantitative community characteristics to determine a local hydrothermal vent food web.
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Bernardino AF, Smith CR, Baco A, Altamira I, Sumida PYG. 2010. Macrofaunal succession in
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Buchanan JB. 1963. The bottom fauna communities and their sediment relationships off the coast
of Northumberland. Oikos 14:154–75
Carlier A, Ritt B, Rodrigues CF, Sarrazin J, Olu K, et al. 2010. Heterogeneous energetic
pathways and carbon sources on deep eastern Mediterranean cold seep communities. Mar.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Ampharetidae
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Jumars, Dorgan & Lindsay
07 November 2014
Biol. 157:2545–65
Carmichael RH, Rutecki D, Annett B, Gaines E, Valiela I. 2004. Position of horseshoe crabs in
estuarine food webs: N and C stable isotopic study of foraging ranges and diet composition.
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Colaço A, Dehairs G, Desbruyères D. 2002. Nutritional relations of deep-sea hydrothermal fields
at the Mid-Atlantic Ridge: a stable isotope approach. Deep-Sea Res. Pt. I 49:395-412
Colaço A, Desbruyères D, Guezennec J. 2007. Polar lipid fatty acids as indicators of trophic
associations in a deep-sea vent system community. Mar. Ecol. 28:15–24
Feller RJ, Taghon GL, Gallagher ED, Kenney GE, Jumars PA. 1979. Immunological methods for
food-web analysis in a soft-bottom benthic community. Mar. Biol. 54:61–74
Gallagher ED, Gardner GB, Jumars PA. 1990. Competition among the pioneers in a seasonal
soft-bottom benthic succession: field experiments and analysis of the Gilpin-Ayala
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Gaston GR. 1987. Benthic Polychaeta of the Middle Atlantic Bight: feeding and distribution.
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Gibbs PE, Bryan GW, Ryan KP. 1981. Copper accumulation by the polychaete Melinna palmata:
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Guieb RA, Jumars PA, Self RFL. 2004. Adhesive-based selection by a tentacle-feeding
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Hentschel BT. 1998. Intraspecific variations in δ13C indicate ontogenetic diet changes in depositfeeding polychaetes. Ecology 79:1357–70
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
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Amphinomidae, Amphinomida
Diversity and systematics
Amphinomidae comprise about 165 species distributed among about 24 genera, 9 of them
monotypic. Painfull contact with chaetae of these “fireworms” does not involve toxic secretions
by the worms; the damage is mechanical and microbial (Eckert 1985). Sipunculans appear to
be a sister clade to Amphinomidae (Weigert et al. 2014). Borda et al. (2012) used molecular
genetics to identify subfamilial relationships. Despite some unusual anatomical features,
molecular genetics studies suggest that Archinome rosacea, found at hydrothermal vents,
belongs in Amphinomidae, not in a family by itself or in Euphrosinidae (Wiklund et al. 2008),
so Amphinomidae now includes the previous Archinomidae. More recent results revealed
that a number of different species have been lumped under this name (Borda et al. 2013).
The amphinomid body tends to be either ovoid and dorsally compressed with a large nuchal
carnuncle or elongated with a smaller caruncle. Genera with ovoid species include Bathychloeia,
Benthoscolex, Branchamphinome, Chloeia, Chloenopsis, Hipponoa, Notopygos, Parachloeia,
and Sangiria. Genera with elongate species include Amphinome, Cryptonome, Eurythoe,
Hermodice, Linopherus, Paramphinome, Pareurythoe, and Pherecardia. Both body forms tend
to be rectangular in cross section. Adults range between 0.5 and 50 cm in length (Pleijel 2001).
Habitat
Amphinomidae are epifaunal on sediments, hard bottoms, vent fields and invertebrates such
as corals, as well as infaunal in sediments—over the full range of ocean depths. Benthoscolex
cubanus inhabits the lumen of the digestive tract of a bathyal spatangoid urchin off the Bahamas
(Emson et al. 1993).
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
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Sensory and feeding structures
The prostomium bears a pair of ventral palps and a pair of dorsal antennae near its anterior and
a medial, dorsal antenna farther back. Well developed, ciliated nuchal organs usually lie at the
rear of the prostomium, on both sides of and extending onto the fleshy caruncle; the caruncle
and nuchal organs are not synonymous (Purschke 1997). Ciliary fields create remarkably rapid
flows over them (Pleijel 2001). The peristomium is reduced to lips surrounding the mouth.
Amphinomidae have a ventral, muscular pharynx with ridges for scraping off food particles (cf.
Tzetlin & Purschke 2005, Fig. 3B, Eurythoe complanata). Although the ridges appear unciliated,
E. complanata has dorsolateral ciliary folds around the outer part of the everted pharynx (Tzetlin
& Purschke 2005). The ridges may also be useful for crushing.
Motility
Amphinomids are motile. They walk on surfaces, swim and burrow (Mettam 1984, Jeffreys et
al. 2012). Burrowing species tend to be elongate (e.g., Linopherus spp., Cosentino & Giacobbe
2011, Jeffreys et al. 2012). Some elongate forms hunt in burrows or borings created by their
prey (e.g., Cryptonome, Borda et al. 2012).
Illustrations
Pleijel (2001) provides excellent orientation to anterior structures in both stippled line drawings
and micrographs. Glasby & Bailey-Brock (2001) provide striking photographs of several
shallow-water species. Jeffreys et al. (2012, Fig. 2) present photographs and video footage of
Linopherus sp. <http://www.int-res.com/articles/suppl/m470p079_supp/>, a burrowing form
that dominates hypoxic sediments of the Pakistan continental margin. Borda et al. (2013, Fig. 2)
show photographs of live Archinome spp. collected from vents and seeps. Tzetlin & Purschke
(2005, Fig. 3B) show the everted pharynx of Eurythoe complanata.
Feeding
Most studies after F&J support the classification of amphinomids as motile predators or
scavengers on the continuum of sessile and slowly moving or injured prey and carrion.
Observations of fireworms (Hermodice carunculata) feeding on fire corals and the resulting
scars on the colony support earlier suggestions of enzymatic predigestion by the everted buccal
mass (Pérez & Gomes 2012). This species appears to feed most actively on Millepora and is
most active in late afternoon (Lewis & Crooks 1996). In laboratory experiments, only small
H. carunculata individuals fed avidly on recently settled corals (Wolf & Nugues 2013). H.
carunculata also shows definite feeding preferences among gorgonian species (Vreeland &
Lasker 1989), but it apparently feeds frequently on algal remains and detritus as well (Martin &
Losada 1997, Lewis 2009). Recent field experiments revealed that H. carunculata was attracted
to decaying coral and fish more than to live coral (Wolf et al. 2014).
Barroso & Paiva (2011) found abundant foraminiferans in guts of Chloeia kudenovi
collected from bathyal depths off Brazil. A novel way of feeding primarily on foraminiferans
has evolved in Benthoscolex cubanus, which selects them from the digestive tract of its depositfeeding, spatangoid host (Emson et al. 1993). The guest’s gut contents also included occasional
fragments of Sargassum sp. and Thalassia sp. and hard parts of crustaceans, scaphopods,
polychaetes (their tubes) and sponges. The amphinomid was highly selective: None of the
14 specimens dissected contained mud, even though mud dominated gut contents of the host
(Emson et al. 1993).
Glasby & Bailey-Brock (2001) caught reef amphinomids by hook and line on carrion. Pardo
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& Amaral (2006) observed rapid chemotaxis of Eurythoe complanata to pieces of fish offered in
aquaria. Detection of prey solutes elicited raising of the anterior 1/3 of the body, opening of the
mouth and pharyngeal eversion. In the field, this posture would allow longer-range detection
and easier determination of flow direction in a bottom boundary layer. When worms reached the
fish, the lower lip was sealed around it, and the muscular pharynx was used as a pump to draw
the whole fish fragment in. Glasby & Bailey-Brock (2001) compiled evidence of carrion feeding
in the form of capture on fishhooks and hand feeding in aquaria for Chloeia flava, Eurythoe
complanata, Hermodice carunculata and Pherecardia striata.
There is evidence of more active carnivory as well. Borda et al. (2012) described or
rediscribed three species of Cryptonome associated with galleries and tunnels created by
shipworms. Gut contents were not described. More direct evidence was provided by Ward et
al. (2003) who dissected 60 specimens of Archinome rosacea (possibly A. storchi cf. Borda et
al. 2013) from the southern East Pacific Rise. They found that 70% of all observed gut content
types comprised mobile prey such as molluscs, polychaetes and crustaceans, with putative
bacterial mat material being next on the list, followed by unidentified material.
Pherecardia striata apparently is chemically attracted to injured Acanthaster individuals and
can be a significant source of their mortality by entering the body cavity through wounds made
by other predators and consuming mostly soft tissues (Glynn 1984). In laboratory feeding trials
P. striata showed strong preference for crustacean over Acanthaster remains, and gut contents
included crustacean, polychaete, mollusc, and other unidentified animal tissue, and a few
individuals examined were cannibalistic (Glynn 1984). Algae and detritus were found in greater
frequency in gut contents than were animal remains, however, indicating a tendency toward
omnivory (Glynn 1984).
Certainly the greatest departure from a typical amphinomid diet and lifestyle is reported
among members of the speciose genus Linopherus. Cosentino & Giacobbe (2011) emplaced
6.4 mm (diam.) granules of expanded fire clay in cylindrical mesh nets and buried them in the
heterogenous sediments of a coastal lagoon (dominantly coarse sand with gravel and cobbles).
Two subsets of these containers were supplemented with fish-food pellets and yeast, respectively.
Two morphs of what appeared to be L. canariensis colonized the experiments and reached densities
> 300 liter -1 in the controls and > 100 liter -1 in the high-organic, fish-food treatment and were
found at a range of sediment depths within the treatments. Cosentino & Giacobbe (2011) also
analyzed gut contents and remarked that the species was very selective in managing to avoid
ingesting both the granules and, in the ambient sediments, sand. Only organic detritus, including
remains of microalgae, was found. Guts of this same species in the Mexican Caribbean have
been reported to contain animal remains (Salazar-Vallejo 1997). Tolerance of organic-rich, lowoxygen environments is epitomized by a species of Linopherus with highly developed branchiae
that dominates the macrofauna of the oxygen minimum zone of the Pakistan continental margin
at water depths between 700 and 1100 m (Levin et al. 2009, Jeffreys et al. 2012). Burrow
openings and burrowing individuals were evident in cores, and numerical abundances exceeded
400 m-2 at 850 m. Stable isotopic signatures and gut contents as well as pulse-chase experiments
and lipid biomarkers established that Linopherus’ assimilated diet included substantial microalgal
phytodetritus, with contributions from carnivory and bacterivory (Woulds et al. 2007, Jeffreys et
al. 2012).
Stable isotope data showed 15N enrichment for Paramphinome jeffreysii from the deepsea Faroe-Shetland Channel similar to those in surface deposit feeders and much lower than
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Amphinomidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
those of predators or scavengers (Gontakaki et al. 2011). In a pulse-chase experiment, P.
jeffreysii showed rapid uptake of 13C-labeled diatoms, consistent with surface deposit feeding,
although worms were found in deeper sediments and may feed on subsurface sediments as
well (Gontakaki et al. 2011). Gontakaki et al. (2011) suggested that a shift from predation to
deposit feeding could be attributed to food limitation in the deep sea, but the richness of seasonal
phytodetrital pulses and the advantages of motility in locating rich patches probably also played
a role in the evolution of this behavior. Gaston (1987) dissected 26 individuals of P. jeffreysii
from the U.S. Mid-Atlantic Bight; all had empty guts.
There are hints from stable isotope results that some shallow-water amphinomids may
also feed low in the food web. Fedosev et al. (2014) studied a shallow-water (6 - 18 m)
sand community off southern Vietnam; unspecified amphinomids had δ15N intermediate
between sabellids and spionids and 2.9‰ below that of nepthyids. Signatures of neither
microphytobenthos nor phytoplankton were obtained, so the source of the organic matter
is difficult to infer. H. carunculata isotopic enrichments vary strongly among sites but are
consistent with omnivory but at least considerable carnivory or scavenging that increases with
worm size (Wolf et al. 2014).
Guild membership
Possibly excepting the kleptoparasitic Benthoscolex cubanus, all amphinomids so far observed in
situ or in the laboratory are motile, primarily crawling but also swimming or burrowing (Jeffreys
et al. 2012). In principle, B. cubanus is discretely motile, needing to move only when the
conveyor belt of food stops. Ovoid species are epifaunal, whereas elongate forms may burrow.
Observations since F&J have expanded diet breadth of Amphinomidae in both directions,
including more mobile prey as well as phytodetritus, although diets of individual species are
more limited. The majority of species are macrophagous carnivores or scavengers, but may
include detritus and algae in their diets. All use an unarmed, muscular, ventral, eversible
pharynx. Some Linopherus spp. and Paramphinome jeffreysii specialize on ingesting rich
detritus, but Linopherus spp. (Salazar-Vallejo 1997; Jeffreys et al. 2012), and likely P. jeffreysii
also take animal prey. It seems unlikely that any amphinomid would reject carrion from its diet.
Research questions and opportunities
• It is unknown whether Linopherus spp. utilize surfactants in the manner of deposit-feeding
polychaetes to aid in dissolution of organic matter for further digestion.
• The unusually fast chemosensing streams created by amphinomids over their nuchal organs
raise questions of detection distance of prey under varying bottom boundary-layer conditions.
• Mechanisms and behaviors of encounter and capture of motile prey remain to be described.
• It is unknown how Benthoscolex cubanus escapes damage from host digestive enzymes and
surfactants.
References
Barroso R, Paiva PC. 2010. A new deep-sea species of Chloeia (Polychaeta: Amphinomidae)
from southern Brazil. J. Mar. Biol. Ass. 91:419–23
Borda E, Kudenov JD, Bienhold C, Rouse GW. 2012. Towards a revised Amphinomidae
(Annelida, Amphinomida): description and affinities of a new genus and species from the
Nile Deep-sea Fan, Mediterranean Sea. Zool. Scr.. 41:307–25
Borda E, Kudenov JD, Chevaldonne P, Blake JA, Desbruyères D, et al. 2013. Cryptic species of
Archinome (Annelida: Amphinomida) from vents and seeps. Proc. R. Soc. B 280:20131876,
9 pp.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Amphinomidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Cosentino A, Giacobbe S. 2011. The new potential invader Linopherus canariensis (Polychaeta:
Amphinomidae) in a Mediterranean coastal lake: Colonization dynamics and morphological
remarks Mar. Pollut. Bull. 62:236–45
Eckert GJ. 1985. Absence of toxin-producing parapodial glands in amphinomid polychaetes
(fireworms). Toxicon 23:350–3
Emson RH, Young CM, Paterson GLJ. 1993. A fire worm with a sheltered life: studies of
Benthoscolex cubanus Hartman (Amphinomidae), an internal associate of the bathyal seaurchin Archeopneustes hystrix (A. Agassiz, 1880). J. Nat. Hist. 27:1013–28
Fedosov AE, Tiunov AV, Kiyashko SI, Kantor UI. 2014. Trophic diversification in the evolution
of predatory marine gastropods of the family Terebridae as inferred from stable isotope data.
Mar. Ecol. Prog. Ser. 497:143–56
Gaston GR. 1987. Benthic Polychaeta of the Middle Atlantic Bight: feeding and distribution.
Mar. Ecol. Prog. Ser. 36:251–62
Glasby CJ, Bailey-Brock J. 2001. Bait-taking fireworms (Amphinomidae: Polychaeta) and
other polychaetes. The Beagle: Records of the Museums and Art Galleries of the Northern
Territory 17:37–41
Glynn PW. 1984. An amphinomid worm predator of the crown-of-thorns sea star and general
predation on asteroids in eastern and western Pacific coral reefs. Bull. Mar. Sci. 35:54–71
Gontikaki E, Mayor DJ, Narayanaswamy BE, Witte U. 2011. Feeding strategies of deep-sea subarctic macrofauna of the Faroe-Shetland Channel: Combining natural stable isotopes and
enrichment techniques. Deep-Sea Res. Pt. I 58:160–72
Jeffreys RM, Levin LA, Lamont PA, Woulds C, Whitcraft CR, et al. 2012. Living on the edge:
single-species dominance at the Pakistan oxygen minimum zone boundary. Mar. Ecol. Prog.
Ser. 470:79–99
Levin LA, Whitcraft CR, Mendoza GF, Gonzalez JP, Cowie G. 2009. Oxygen and organic matter
thresholds for benthic faunal activity on the Pakistan margin oxygen minimum zone (700–
1100 m). Deep-Sea Res. Pt. II 56:449–71
Lewis JB, Crooks RE. 1996. Foraging cycles of the amphinomid polychaete Hermodice
carunculata preying on the calcareous hydrozoan Millepora complanata. Bull. Mar. Sci.
58:853–6
Lewis SA. 2009. The use of histology, molecular techniques, and ex situ feeding experiments
to investigate the feeding behavior of the coral reef predator Hermodice carunculata, the
bearded fireworm. MS thesis. George Mason Univ., Fairfax, VA
Martin A, Losada F. 1997. Habitos alimentarios del poliqueto anfinomido Hermodice
carunculata (Pallas), en la Isla Larga, Estado Carabobo, Venezuela. In Congresso LatinoAmericano sobre Ciências do Mar 7:140 (Resumos expandidos)
Mettam C. 1984. Functional morphology of locomotion in Chloeia (Polychaeta; Amphinomidae).
In Proc. First Internat. Polychaete Conf., ed. P.A. Hutchings, 390–400. Milson’s Point,
Sydney, N.S.W., Australia: Linnean Society of N.S.W.
Pardo EV, Amaral A. 2006. Foraging and mobility in three species of Aciculata (Annelida:
Polychaeta). Braz. J. Biol. 66:1065–72
Pérez CD, Gomes PB. 2012. First record of the fireworm Hermodice carunculata (Annelida,
Polychaeta) preying on colonies of the fire coral Millepora alcicornis (Cnidaria, Hydrozoa).
Biota Neotropica 12:217–9
Pleijel F. 2001. Amphinomida Lamarck, 1818. See Rouse & Pleijel 2001, pp. 145-50
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Amphinomidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Purschke G. 1997. Ultrastructure of nuchal organis in polychaetes (Annelida) — New results and
review. Acta Zool. 78:123–43
Salazar-Vallejo SI. 1997. Amfinómidos y euphrosínidos (Polychaeta) del Caribe Mexicano con
claves para las especias reconocidas del Gran Caribe. Rev. Biol. Trop. 45:379–90
Tzetlin A, Purschke G. 2005. Pharynx and intestine. Hydrobiologia. 535/536:199–225
Vreeland HV, Lasker HR. 1989. Selective feeding of the polychaete Hermodice carunculata
Pallas on Caribbean gorgonians. J. Exp. Mar. Biol. Ecol. 129:265–77
Ward ME, Jenkins CD, Dover CLM. 2003. Functional morphology and feeding strategy of the
hydrothermal-vent polychaete Archinome rosacea (family Archinomidae). Can. J. Zool.
81:582–90
Weigert A, Helm IC, Meyer M, Nickel B, Arendt D, et al. 2014. Illuminating the base of the
annelid tree using transcriptomics. Mol. Biol. Evol. doi: 10.1093/molbev/msu080, 11 pp.
Wiklund H, Nygren A, Pleijel F, Sundberg P. 2008. The phylogenetic relationships between
Amphinomidae, Archinomidae and Euphrosinidae (Amphinomida: Aciculata: Polychaeta),
inferred from molecular data. J. Mar. Biol. Assoc. U.K. 88:509–13
Wolf AT, Nugues MM. 2013. Predation on coral settlers by the corallivorous fireworm
Hermodice carunculata. Coral Reefs 32:227–231
Wolf AT, Nugues MM, Wild C. 2014. Distribution, food preference, and trophic position of
the corallivorous fireworm Hermodice carunculata in a Caribbean coral reef. Coral Reefs
33:1153–63
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on sea floor biological communities and their roles in sedimentary carbon cycling. Limnol.
Oceangr. 52:1698–709
Antillesomatidae, Sipuncula
Diversity and systematics
Antillesomatidae currently comprise the single species Antillesoma antillarum. The family
was created on the basis of molecular genetic data in order to avoid polyphyly (Kawauchi et al.
2012). The species is of medium size, up to 8 cm in trunk length (Kawauchi et al. 2012).
Habitat
A. antillarum bores into soft, calcareous rock, where it can reach abundances of 415 individuals
m-2 (Rice 1975). Its wide burrow terminates in a rounded, cupulate chamber (Rice 1975). It
is also found nestling in calcareous rubble (e.g., oyster beds cf. Rice et al. 1995). The species
is widely distributed from intertidal to shelf depths in tropical and subtropical waters. Cutler
(1977) reported four specimens from a grab in green clay at 520 m water depth, unusual both in
the nature of the substratum and in the bathyal depth.
Sensory and feeding structures
A stocky introvert, about one-half the diameter of the trunk, roughly equals the trunk in length.
A nuchal organ dorsal to the mouth is encircled by 30-200 digitiform tentacles > 20 times as
long as wide. Ocular tubes are present. Hooks are lacking in adults (Kawauchi et al. 2013). As
in other sipunculans, the mouth and anus are closely juxtaposed, enabling the double helical
twisting of a long gut within the trunk and setting up an ideal topology for osmotic counterflows.
Motility
We presume that boring individuals are sessile as a corollary of the boring habit; boring into into
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
rock is a slow process, so leaving an existing burrow equals nearly certain mortality. Individuals
nestling in rubble or burrowing in sediments may be discretely motile.
Illustrations
A number of photographs are available at <http://sipuncula.lifedesks.org/pages/950>.
Feeding
Rice (1976) described A. antillarum as a ciliary mucoid feeder on particles encountered by the
tentacles when they are extended above the burrow. Gut contents are mainly small particles,
consistent with suspension feeding (Rice 1975). Adults lack hooks on the introvert, and the
tentacles do not appear sufficiently robust to rub adherent material from rock surfaces.
Guild membership
Based on Rice’s (1975, 1976) descriptions, its habitat, its stocky introvert and its many long
tentacles, we conclude that A. antillarum is normally a passive suspension feeder. That is, the
ciliary currents serve to move encountered particles to the mouth but are vastly exceeded in
velocity by ambient flows (technically a mixed mode between active and passive suspension
feeding).
Research opportunities
• Suspension feeding in A. antillarum has been neither explored quantitatively in terms of
clearance rates nor placed in the context of hydrosol filtration theory. Sipunculans are
strikingly absent from reviews of suspension feeding (e.g., Riisgård & Larsen 2010).
• Motility of individuals in sediments and rubble is unknown.
References
Cutler EB. 1977. The bathyal and abyssal Sipuncula. Galathea Rept. 14:135–56
Cutler EB. 1994. The Sipuncula: Their Systematics, Biology and Evolution. Ithaca, NY: Cornell
Univ. Press
Kawauchi GY, Sharma PP, Giribet G. 2012. Sipunculan phylogeny based on six genes, with a
new classification and the descriptions of two new families. Zool. Scr. 41:186–210
Rice ME. 1975. Survey of the Sipuncula of the coral and beachrock communities of the Caribbean
Sea. In Proceedings of the International Symposium on the Biology of the Sipuncula and
Echiura, Kotor, 1970, ed. ME Rice, M Todorovic, 1:35–49. Belgrade: Naucno Delo
Rice ME. 1976. Sipunculans associated with coral communities. Micronesica 12:119–32
Rice ME, Piraino J, Reichardt HF. 1995. A survey of the Sipuncula of the Indian River Lagoon.
Bull. Mar. Sci. 57:128–135
Riisgård HU, Larsen PS. 2010. Particle capture mechanisms in suspension-feeding invertebrates.
Mar. Ecol. Prog. Ser. 418:255–93
Antonbruunidae, Nereidiformia, Phyllodocida
Diversity and systematics
Antonbruunidae comprises two species with strong resemblance to Pilargidae but uncertain
phylogeny (Glasby 1993, Pleijel 2001). Males of the type species, Antonbruunia viridis, are
dwarf but of similar morphology. Adult females are 0.6 - 1.7 cm long.
Habitat
A. viridis, was trawled from 68 - 82 m water depth in the Mozambique Channel (Hartman &
Boss 1965). A. gerdesi was taken off Concepción, Chile at depths of 843 - 846 m. Both species
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Antonbruunidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
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Jumars, Dorgan & Lindsay
07 November 2014
are known only from the mantle cavities of lucinid bivalves living in sulfidic muds.
Sensory and feeding structures
The prostomium is rounded quadrangular to trapezoidal and bears one dorso-medial and two
lateral antennae plus two anterolateral palps (Pleijel 2001). Eyes are absent, and nuchal organs
have not been described. A peristomial ring, narrow dorsally, may be complete (Pleijel 2001,
Quiroga & Sellenes 2009). A viridis carries a short, cylindrical, smooth proboscis with a
terminal ring of papillae (Pleijel 2001). Neither species has jaws or teeth.
Motility
Morphology suggests discrete motility within the mantle cavity. Whether individuals can move
between host individuals is unknown.
Illustrations
Glasby (1993, Fig. 3) provides a stippled line drawing in ventral view of the anterior morphology
of A. viridis. Quiroga & Sellenes (2009, Fig. 5, 6) provide scanning electron micrographs and
line drawings of A. gerdesi.
Feeding
No data are available on feeding.
Guild membership
We would guess that antonbruunids will be found to be discretely motile kleptoparasites or
parasites or some combination of both.
Research questions and opportunities
• Stable isotopic analysis (including the lucinid host) could be useful to distinguish
kleptoparasitism from parasitism.
References
Glasby, CJ. 1993. Family revision and cladistic analysis of the Nereidoidea (Polychaeta :
Phyllodocida). Invertebr. Taxon. 7:1551–73
Hartmann O, Boss K. 1965. Antonbruunia viridis, a new inquiline annelid with dwarf males,
inhabiting a new species of pelecypod, Lucina fosteri in Mozambique Channel. Ann. Mag.
Nat. Hist. Ser. 13, 8: 177–86
Pleijel F. 2001. Antonbruunia Hartman and Boss, 1965. See Rouse & Pleijel 2001, p. 141
Quiroga E, Sellanes J. 2009. Two new polychaete species living in the mantle cavity of
Calyptogena gallardoi (Bivalvia: Vesicomyidae) at a methane seep site off central Chile (~
36˚S). Sci. Mar. 73:399–407
Aphroditidae, Aphroditiformia
Diversity and systematics
Aphroditidae comprise about 120 species distributed among about 13 genera, five of them
monotypic. They are one of the 7 scaleworm families that constitute the Aphroditiformia
(Norlinder et al. 2012) and one of the three most deeply rooted clades of scaleworms, the other
two being Eulepethidae and a complex comprising the remaining families (Norlinder et al.
2012). There are two typical body shapes, one with a rapidly tapering posterior (e.g., Aphrodita,
Aphrogenia and Pontogenia), and one without such an abrupt taper (e.g., Laetmonice, Hutchings
& McRae 1993). Most species are 2 - 10 cm long, but as short as 1 or as long as 30 cm.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Aphroditidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Habitat
Aphroditids are found epifaunally over both hard and soft substrata and infaunally in soft
substrata at all ocean depths (deep records reviewed by Böggemann 2009).
Sensory and feeding structures
The rounded prostomium is crowded between the first pair of parapodia and bears a median
antenna and sometimes a small number of eyespots. Two ventral palps project anterolaterally.
A medial, round or oval facial tubercle overlies the region of palp insertion. The peristomium
is reduced to lips around the mouth. Nuchal organs have not received much attention but are
present in some species (Hutchings 2000).
The pharynx is axial, muscular and eversible. The literature remains opaque, however,
regarding distribution of jaws within the family and their structure. We know of no published
illustration of aphroditid jaws; they are not used diagnostically for the family or its genera.
Presence or absence of jaws has been used as a character in cladistic studies that included
Aphroditidae. They are scored as absent in Aphrodita aculeata and Palmyra aurifera (Wiklund
et al. 2005) and also in Laetmonice filicornis (Norlinder et al. 2012). In a revision of aphroditid
genera, Pettibone (1966) suggested that jaws were absent from the entire family, but later
(Pettibone 1969, 1986) described a similarity in plate-like jaws between Aphroditidae and
Eulepethidae. Baird (1865, p. 173) described aphroditid jaws as “cartilaginous, not very
distinct.” Glasby (1993) in his cladistic analysis scored the condition of aphroditid pharyngeal
armature to be unknown. Hutchings (2000, p. 119) also stated that jaws are present although
“they are irregularly shaped and less obviously grasping than those found in other scale-worm
families.” We suspect that the ambiguity is semantic and that in our terminology aphroditids lack
jaws. We also suspecty that, again in our terminology, sclerotized pharyngeal hardening may
be variably present and useful in crushing, but that jaws are absent and that McIntosh’s (1900,
p. 240) description of a pharynx “with four thickened muscular ridges representing teeth” may
be accurate. How sclerotization is distributed among aphroditids is unclear, in part for lack of
uniform terminology.
Motility
Motility in aphroditids has received little attention after Mettam’s (1971) analysis in Aphrodite
aculeata, which moves through rapid stepping of the parapodia. Parapar et al. (2013) observed
faster motion of Laetmonice producta on and into muds than over (> 0.5 cm diam.) gravel.
Illustrations
Hutchings (2000, Fig. 1.70) provides useful line drawings of characteristic features of the family.
Norlinder et al. (2012; Fig. 1) show photos of living scaleworms from diverse families, including
Aphroditidae. Parapar et al. (2013, Fig. 14) present photographs of Laetmonice producta. A
photograph of the ventral surface of Aphrodita hastata is posted at <http://seagrant.gso.uri.edu/
research/georges_bank/Species_List/Aphroditidae.htm>. An analysis of iridescence of the dorsal
felt includes several color photographs of animals moving over sediments <http://www.physics.
usyd.edu.au/theory/seamouse/aphrodita.html>. Mettam (1971, Fig. 6) shows a drawing of
parapodial walking by Aphrodita aculeata. Norlinder et al. (2012, Fig. 1) show photographs of
representatives from the 7 different families of scaleworms.
Feeding
Mettam (1980) published aquarium observations of Aphrodita aculeata that contradicted F&J’s
suggestion that aphroditids likely specialized on sessile or slowly moving prey. A. aculeata
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Aphroditidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Jumars, Dorgan & Lindsay
07 November 2014
preyed on Macoma balthica, Corophium volutator, Nephtys hombergii and Hediste diversicolor,
generally swallowing large prey head first. He described A. aculeata as unwilling to feed unless
buried and fastidious in avoiding ingestion of sediments. He also presented evidence against
maceration of ingested foods.
Stiller (1996) reported that about half of the gut contents in antarctic Laetmonice producta
producta comprised sediments and detritus, with crustaceans, polychaetes and ophiuroids making
up most of the rest. In another antarctic study, Piraino & Montiel (2001) reported 27 L. producta
with full guts out of 50 dissections with the prey being “mainly amphipods, isopods, polychaetes
(especially Flabelligeridae), but also ophiuroids and pycnogonids.” Parapar et al. (2013)
dissected 77 antarctic L. producta, with similar results, adding a priapulid to the diet list. The
case that active animals are included in the diet is convincing. Parapar et al. (2013) also reported
a lack of response by L. producta to animal prey, but their descriptions of heightened activity
in response to muds suggest that, like A. aculeata, L. producta may not feed unless buried. In
dissections, Gaston (1987) found 2 Laetmonice filicornis individuals empty; of 25 Aphrodita
hastata individuals dissected, 18 were empty, 4 held coarse sand, and 3 contained polychaetes.
Puzzling is the high reported frequency of sediment ingestion, particularly in the light of
Mettam’s (1980) contrary results. The gut structure of A. aculeata includes an abundance of
paired diverticula (Michel 1988, Fig. X.1C) as presumably do other aphroditids­—unlike anything
seen in guts of specialist deposit feeders wherein tubular structures with rapid throughput rates
are the rule (Penry & Jumars 1990). Deposit feeders show high concentrations of metals in their
gut contents, complexed with dissolved organic matter released into solution through the action
of their digestive enzymes and surfactants (Chen et al. 2000). Antarctic Laetmonice producta
contained concentrations of cadmium and copper that were slightly higher than those of other
predators but not as high as deposit feeders from the same benthic environments (Hans et al.
2011). The latter finding is consistent with an intermediate trophic status.
Stable isotopic data on aphroditids are scarce, but a single A. aculeata specimen collected
at 60 m water depth in Gullmar Fjord, Sweden, fell just below Glycera alba (Glyceridae) in
δ15N, indicative of carnivory (Magnusson et al. 2003). At 28 m water depth in the German
Bight Jennings et al. (2002) reported A. aculeata to have a higher 15N enrichment than any other
invertebrate in their extensive collection from the Silver Pit region of the central North Sea (50 80 m deep). In the Bay of Banyuls-sur-Mer, A. aculeata had a δ15N signature higher than all the
other polychaetes measured except (from highest to lowest) Scoletoma fragilis (Lumbrineridae),
Glycera celtica (Glyceridae) Polyodontes maxillosus (Acoetidae), Scoletoma impatiens
(Lumbrineridae) and Halla parthenopeia (Oenonidae), all of which are likely carnivorous.
Laetmonice hystrix at the same site, however, fell close to the characteristically more
intermediate trophic level of Nephtys sp. (Carlier et al. 2007). A. aculeata from 5 - 35 m water
depth in the Bay of Concarneau was the most highly enriched in 15N of all polychaetes reported
(Rigolet et al. 2014). In a reference Posidonia bed at 5 - 8 m water depth off Mallorca Island,
Deudero et al. (2011) found Pontogenia chrysocoma to have higher 15N enrichment than any
other polychaete, including Hilbigneris gracilis (Lumbrineridae). In a nearby bed that had been
invaded by the green alga Caulerpa, its carbon source appeared to have shifted from suspended
organic matter toward Caulerpa, and its apparent δ15N trophic level was somewhat lower as well.
In an epilithic algal bed off Corsica, an aphroditid (unidentified to species) fell close in δ15N
signature to a nereidid and below that of a syllid (Lepoint et al. 2000). Unspecified Aphroditidae
from Catalan bathyal depths fell below all Nephtys spp. in δ15N (Fanelli et al. 2011). Three
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Aphroditidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Laetmonice sp. from the Porcupine Abyssal Plain showed a range of δ15N from high values
near those of lumbrinerids to lower values closer to those of deposit feeders (Iken et al. 2001).
Thus stable isotopes generally support high to intermediate trophic positions for species of
Aphroditidae. We suspect that some past reporters of detritus feeding may have instead observed
brownish emulsions produced by lipid digestion of animal prey (Voparil et al. 2008).
Guild membership
Aphroditids are largely carnivorous and may take prey over the full range from active
macrobenthos to less mobile Foraminifera to carrion. L. producta may take in sediments in
addition, but the extent to which deposit feeding provides nutrition or is incidental in preying on
sedimentary fauna is unknown. Aphroditids can be infaunal or epifaunal. All use an eversible,
muscular, axial pharynx to feed. We tentatively classify it as unarmed.
Research questions and opportunities
• The role of deposit feeding in aphroditids remains uncertain. It would be illuminated by
measurements of surfactancy of gut fluids, digestion times, assimilation efficiencies and
assimilation rates when individuals are feeding on sediments and sediment-animal mixtures.
• Further analysis of motility and burrowing behavior would be rewarding.
• It is not apparent how aphroditids capture large, motile prey.
• The presence, geometry and function of jaws are badly in need of clarification as they are in
the sister clade Eulepethidae.
References
Baird W. 1865. Contributions towards a monograph of the species of Annelides belonging to the
Aphroditicea, containing a list of the known species, and a description of some new species
contained in the National Collection of the British Museum. J. Linn. Soc. Zool. London 8:
172–202
Böggemann M. 2009. Polychaetes (Annelida) of the abyssal SE Atlantic. Org. Divers. Evol.
9:251–428
Carlier A, Riera P, Amouroux J-M, Bodiou J-Y, Grémare A. 2007. Benthic trophic network in the
Bay of Banyuls-sur-Mer (northwest Mediterranean, France): An assessment based on stable
carbon and nitrogen isotopes analysis. Estuar. Coast. Shelf Sci. 72:1–15
Chen Z, Mayer LM, Quétel C, Donard OFX, Self RFL, et al. 2000. High concentrations of
complexed metals in the guts of deposit-feeders. Limnol. Oceanogr. 45:1358–67
Deudero S, Box A, Alós J, Arroyo NL, Marbà N. 2011. Functional changes due to invasive
species: Food web shifts at shallow Posidonia oceanica seagrass beds colonized by the alien
macroalga Caulerpa racemosa. Estuar. Coast. Shelf Sci. 93:106–16
Fanelli E, Papiol V, Cartes JE, Rumolo P, Brunet C, Sprovieri M. 2011. Food web structure of
the epibenthic and infaunal invertebrates on the Catalan slope (NW Mediterranean):Evidence
from δ13C and δ15N analysis. Deep-Sea Res. Pt. I 58:98–109
Gaston GR. 1987. Benthic Polychaeta of the Middle Atlantic Bight: feeding and distribution.
Mar. Ecol. Prog. Ser. 36:251–62
Glasby, CJ. 1993. Family revision and cladistic analysis of the Nereidoidea (Polychaeta :
Phyllodocida). Invertebr. Taxon. 7:1551–73
Hans J, Jöst C, Zauke GP. 2011. Significance and interspecific variability of accumulated trace
metal concentrations in Antarctic benthic polychaetes. Sci. Total Environ. 409:2845–51
Hutchings PA. 2000. Family Aphroditidae. See Beesley et al. 2000, pp. 117–21
Hutchings P, McRae J. 1993. The Aphroditidae (Polychaeta) from Australia, together with a
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Aphroditidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
redescription of the Aphroditidae collected during the Siboga Expedition. Rec. Aust. Mus.
45:279–363
Iken K, Brey T, Wand U, Voigt J, Junghans P. 2001. Food web structure of the benthic
community at the Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis. Prog.
Oceanogr. 50:383–405
Jennings S, Pinnegar JK, Polunin NV, Warr KJ. 2002. Linking size-based and trophic analyses of
benthic community structure. Mar. Ecol. Prog. Ser. 226:77–85
Lepoint G, Nyssen F, Gobert S, Dauby P, Bouquegneau J-M. 2000. Relative impact of a seagrass
bed and its adjacent epilithic algal community in consumer diets. Mar. Biol. 136:513–8
Magnusson K, Agrenius S, Ekelund R. 2003. Distribution of a tetrabrominated diphenyl ether
and its metabolites in soft-bottom sediment and macrofauna species. Mar. Ecol. Prog. Ser.
255:155–70
McIntosh WC. 1900. A monograph of British Annelids, Volume 1, Part 2. Polychaeta
Amphinomidae to Sigalionidae. 1:215–442. London: Ray Society
Mettam C. 1971. Functional design and evolution of the polychaete Aphrodite aculeata. J. Zool.
(Lond.) 163:489–514
Mettam C. 1980. On the feeding habits of Aphrodita aculeata and commensal polynoids. J. Mar.
Biol. Assoc. UK 60:833–34
Michel C. 1988. Intestine and digestive glands. Chapt. X. In The ultrastructure of Polychaeta.
ed. W Westheide, C0 Hermans. Microfauna Marina 1:157–75. Mainz: Akademie der
Wissenschaften und der Literatur
Norlinder E, Nygren A, Wiklund H, Pleijel F. 2012. Phylogeny of scale-worms (Aphroditiformia,
Annelida), assessed from 18SrRNA, 28SrRNA, 16SrRNA, mitochondrial cytochrome c
oxidase subunit I (COI), and morphology. Mol. Phylogen. Evol. 65:490–500
Parapar J, Moreira J, Gambi MC, Caramelo C. 2013. Morphology and biology of Laetmonice
producta producta Grube (Polychaeta: Aphroditidae) in the Bellingshausen Sea and Antarctic
Peninsula (Southern Ocean, Antarctica). Ital. J. Zool. 80:255–72
Penry DL, Jumars PA. 1990. Gut architecture, digestive constraints and feeding ecology of
deposit-feeding and carnivorous polychaetes. Oecologia 82:1–11
Pettibone MH. 1966. Heteraphrodita altoni, a new genus and species of polychaete worm
(Polychaeta, Aphroditidae) from deep water off Oregon, and a revision of the aphroditid
genera. Proc. Biol. Soc. Wash. 79:95–108
Pettibone MH. 1969. Revision of the Aphroditoid polychaetes of the Family Eulepethidae
Chamberlin (= Eulepidinae Darboux; = Pareulepidae Hartman). Smithson. Contrib. Zool.
41:1–44
Pettibone MH. 1986. Additions to the family Eulepethidae Chamberlin (Polychaeta: Smithson.
Contrib. Zool. 441:1–51
Piraino S, Montiel A. 2001. Polychaete autumn diversity and reproductive biology. In The
Expedition Antarktis XVII/3 (Easiz III) of RV “Polarstern” in 2000, ed. WE Arntz, T Brey,
Berichte Polarforsch. Meeresforsch. 402:98–103
Rigolet C, Thiébaut E, Dubois SF. 2014. Food web structures of subtidal benthic muddy habitats:
evidence of microphytobenthos contribution supported by an engineer species. Mar. Ecol.
Prog. Ser. 500:25–41
Stiller M. 1996. Verbreitung und Lebensweise der Aphroditiden und Polynoiden (Polychaeta) im
östlichen Weddellmeer und im Lazarevmeer (Antarktis) = Distribution and biology of the
Aphroditides and Polynoids (Polychaeta) in the eastern Weddell Sea and the Lazarev Sea
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Aphroditidae
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
(Antarctica). Berichte zur Polarforschung (Reports on Polar Research) 185:1-200
Voparil IM, Mayer LM, Jumars PA. 2008. Emulsions versus micelles in the digestion of lipids by
benthic invertebrates. Limnol. Oceangr. 53:387–94
Wiklund H, Nygren A, Pleijel F, Sundberg P. 2005. Phylogeny of Aphroditiformia (Polychaeta)
based on molecular and morphological data. Mol. Phylogenet. Evol. 37:494–502
Apistobranchidae
Diversity and systematics
Apistobranchidae comprise a single genus with about half a dozen species. Recent molecular
genetics results place some doubt in its placement in Canalipalpata (Zrzavý et al. 2009). The
worms are small (< 1 cm long) and fragment easily.
Habitat
Apistobranchus spp. are known only from soft sediments at shelf and slope depths, most
frequently at high latitudes (Blake 1996, Petti et al. 2007).
Sensory and feeding structures
A single pair of grooved, ciliated palps inserts dorsally just posterior to the prostomium. In
Apistobranchus tenuis, the prostomium is heavily ciliated (Wilson, 2000, Fig. 63.1a, b). Nuchal
organs are located just medial and posterior to the palp insertions (Wilson 2000, Rouse 2001).
No antennae are present. Eyes have not been reported. The pharynx is muscular and apparently
eversible, but there is some doubt whether it is axial or ventral (Rouse 2001).
Motility
There are no data on motility, but morphology and the comments of Fauchald (1977) suggest
a discretely motile existence. Petti et al. (2007) recovered no tubes in diver-collected cores; A.
glacierae does not appear to be tubicolous.
Illustrations
Informative, labeled, stippled line drawings of Apistobranchus spp. are provided by Rouse
(2001, Fig. 63.1a, b) and Wilson (2000, Fig. 1.103A after Blake 1996). Petti et al. (2007, Fig. 2,
3) provide light and scanning electron micrographs of A. glacierae.
Feeding
Fauchald (1977) observed apistobranchids (species unspecified) to feed from loosely constructed
burrows. No other direct feeding observations have been reported. They have been regarded as
deposit feeders in previous studies (e.g., Young & Rhoads 1971).
Petti et al. (2007) cited an unpublished Ph.D. dissertation (Bromberg 2004), reporting
that stable carbon isotopic signatures of antarctic A. glacieri indicated a diet of sediment and
microphytobenthos. The largest of the 2151 specimens that they examined was 7 mm long and
1 mm diam., in a size class that is unlikely to subsist on bulk deposits (e.g., Hentschel 1998).
We would predict strong selection for high-quality food items such as benthic diatoms and
concur with Petti et al. (2007) that the family remains a good target for additional observations.
Kędra et al. (2012) reported δ15N and δ13C values for A. tullbergi from Kongsfjorden, Svalbard,
collected under 15 m of water. They were consistent with values observed in other deposit
feeders.
Guild membership
Based on Fauchald’s (1977) observations, we provisionally designate apistobranchids to be
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Apistobranchidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
infaunal, discretely motile surface deposit and microphytobenthos feeders using a pair of
grooved palps, but we cannot exclude the possibility of subsurface deposit feeding in addition or
in some species. A. tenuis (Rouse 2001, Fig. 63.1) has a body plan resembling that of burrowing
cossurids, whereas A. ornatus’ more blunt prostomium and thicker palps (Wilson 2000, Fig.
1.103A) would not appear as well suited to burrowing.
Research questions and opportunities
• Additional direct observations of feeding and motility are needed.
• Assessment of the possibility of subsurface deposit feeding is needed.
References
Blake JA 1996. Family Apistobranchidae Mesnil and Caullery, 1898 In Taxonomic Atlas of the
Benthic Fauna of the Santa Maria Basin and Western Santa Barbara Channel, Vol. 6, The
Annelida. Part 3: Polychaeta: Orbiniidae to Cossuridae, ed. JA Blake, B Hilbig, PH Scott,
71-79. Santa Barbara: Santa Barbara Museum of Natural History
Bromberg S. 2004. A macrofauna bentônica da zona costeira rasa e o seu papel na trama trófica
da Enseada Martel, Baia do Almirantado (Ilha Rei George, Antártica). Ênfase para o grupo
Polychaeta (Annelida). PhD thesis, Oceanographic Institute, University of Sao Paulo, Brazil
Fauchald K. 1977. The polychaete worms. Definitions and keys to orders, families and genera.
Natural History Museum of Los Angeles County, Science Series 28:1–188
Hentschel BT. 1998. Intraspecific variations in δ13C indicate ontogenetic diet changes in depositfeeding polychaetes. Ecology 79:1357–70
Kędra M, Kuliński K, Walkusz W, Legeżyńska J. 2012. The shallow benthic food web structure
in the high Arctic does not follow seasonal changes in the surrounding environment. Estuar.
Coast. Shelf Sci. 114:183–91
Petti MAV, Nonato EF, Bromberg S, Gheller PF, Paiva PC, Corbisier TN. 2007. On the taxonomy
of Apistobranchus species (Polychaeta: Apistobranchidae) from the Antarctic. Zootaxa
1440:51–9
Rouse GW. 2001. Apistobranchus Levinsen, 1883. See Rouse & Pleijel 2001, pp. 253-255
Wilson, RS. 2000. Family Apistobranchidae. See Beesley et al. 2000, p. 190
Young DK, Rhoads DC. 1971. Animal-sediment relations in Cape Cod Bay, Massachusetts I. A
transect study. Mar. Biol. 11:242–54
Zrzavý J, Říha P, Piálek L, Janouškovec J. 2009. Phylogeny of Annelida (Lophotrochozoa): totalevidence analysis of morphology and six genes. BMC Evol. Biol. 9:189, 14 pp.
Arenicolidae
Diversity and systematics
Arenicolidae comprise about two dozen species distributed among 4 genera. The family
shows two morphotypes. About 19 species as adults are large-bodied individuals with at least
two distinct body regions (Arenicola, Arenicolides and Abarenicola). Another 4 species are
pedomorphic members of Branchiomaldane that as adults resemble juveniles of the other 3
genera. Molecular genetic analyses provisionally support two clades, the genus Abarenicola
and a clade comprising the other 3 genera (Bleidorn et al. 2005). Non-pedomorphic species
are typically 0.1 to 1 m long as adults (though in a few cases as short as 2.5 cm), whereas the
pedomorphic Branchiomaldane species are generally ≤ 4 cm long.
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Habitat
Large morphotypes typically occupy J-shaped burrows in shallow-water, silty sands.
Branchiomaldane species live more cryptically in spaces between seagrasses (Fournier & Barrie
1987), mud-filled crevices in rocky habitats (Day 1967) or in more uniform, muddy sands
(Day 1967). Some may make tubes or consolidated burrow linings (Fournier & Barrie 1987),
likely evolved as a means to direct oxygen delivery to the worm (Meyesman et al. 2005) and to
previously anaerobic sediments in front of the head shaft (Jumars et al. 1990).
Sensory and feeding appendages
Arenicolids lack head appendages. The prostomium may carry small numbers of eyespots.
According to Rouse (2001), nuchal organs are present as dorsolateral, muscular pits at the
posterior of the prostomium, but Purschke (1997) reviewed prior work and described the nuchal
organ as an unpaired, V-shaped structure. In most species the peristomium contains a pair of
statocysts (Rouse 2001). The eversible pharynx is axial, non-muscular, unciliated but often
papillated (Tzetlin and Purschke 2005). Although most of the body is aseptate, the anterior
region is separated by a gular membrane that contracts to increase hydrostatic pressure and evert
the pharynx (Wells 1952, 1954).
Motility
Arenicolids have no extensible appendages with which to reach food. They must move
themselves or subduct sediments to eat. Under conditions of favorable sediment granulometry
and sediment transport, individuals of the large forms may be relatively sedentary (discretely
motile), but in silts or where or when sediment transport is weak, large forms tend first to move
the feeding area while keeping the tail shaft place, swinging radially around the axis of the
tail shaft (e.g., Rijken 1979, Fig. 1d). The head shaft may also stay stationary, depending on
the quality of food that caves in from above as feeding continues (Rijken 1979; Retraubun et
al. 1996). Persistently poor local conditions can initiate longer-distance burrowing to a new
location. Krager & Woodin (1993) observed ~3 d residence times within the same 3 cm2 area
for Abarenicola pacifica, although spatial persistence ranged from 1-12 d. Another indication
of significant motility is the size of experimental arenicolid exclusion plots needed to assure the
absence of their effects (Volkenborn et al. 2007). The Arenicola-Abarenicola lifestyle entails
modest pumping costs, with mean flow usually focused down and into the head shaft (Toulmond
& Dejours 1994; Riisgård et al. 1996), but with frequent flow reversals (Volkenborn et al. 2010,
Woodin & Wethey 2009).
Smaller Branchiomaldane species inhabiting mucus tubes covered with sand grains, diatoms,
and spicules have been collected from sands and among algae (Fournier and Barrie 1987).
Whether these animals are more or less motile than larger arenicolids is unclear.
Illustrations
Numerous authors provide schematic diagrams of arenicolid burrows (e.g., Andresen &
Kristensen 2002, Fig. 1; Riisgård et al. 1996, Fig. 1; Wells 1966, Fig. 1). Retraubun et al.
(1996; Fig. 1) includes measurements of the dimensions of the headshaft, tailshaft, horizontal
gallery, feeding funnel, and fecal mound. The drawings by Rijken (1979; Fig. 1) show all five
different burrow types exhibited by A. marina under varying sediment and food conditions.
Rijken (1979, Plate I) also shows photographs of a feeding funnel with glass beads added to the
surface that show the narrow diameter of the feeding shaft. The contrast between the arenicolid
exclusion plot and the surrounding sediment in a photograph from Volkenborn et al. (2007; Fig.
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1b) well illustrates the impact arenicolids have on sediment topography. Pumping, burrowing,
and defecation can be seen as changes in the pressure signal near burrows and are plotted by
Volkenborn et al. (2010) and Woodin & Wethey (2009). Kermack (1955) shows extensive
drawings of the digestive and circulatory systems of A. marina as well as photographs of
dissected worms.
Feeding
Little is published of digestive anatomy or feeding in Branchiomaldane, but Arenicola marina
in 1979 was the most extensively studied polychaete species in the world regarding feeding,
and has remained so. Feeding was already reasonably well known for the larger-bodied
forms of Arenicola and Abarenicola at the time of F&J’s review because these worms feed so
prodigiously. Large arenicolids eat as much as several hundred times their body weights per
day (Taghon 1988). Two species, Arenicola marina and Abarenicola pacifica, have received
disproportionate attention since F&J. Because of their large body sizes and high abundances in
intertidal habitats, they have been common model organisms for studies of particle selectivity,
growth rates, and digestive physiology in deposit feeders; many of the findings summarized here
can be generalized to other deposit feeders.
Ingestion is selective in A. marina, with a bias toward smaller grains. Subsurface lag layers
of particles too large to ingest are conspicuous components of arenicolid habitats, but Baumfalk
(1979) documented a bias toward ingestion of smaller particles across the whole size-frequency
spectrum of ambient sediments and proposed a passive adhesion mechanism. Even when fed an
assortment of manufactured beads lacking food value, A. pacifica showed weak but statistically
significant peak preference just above 10 μm in diameter (Self & Jumars 1988). Powerful indirect
evidence of selectivity in the field is that without continual recycling of fine particles to the surface
during feeding, sands from which A. marina was excluded became muddier (Volkenborn et al.
2007). From laboratory observations on A. pacifica, Swinbanks (1981) anticipated such effects,
observing that clays are flushed out and suspended by arenicolid respiratory pumping.
Rijken (1979) found rapid growth of A. marina on a mixture of sand with two species of
bacteria, somewhat less rapid growth on a diet of sand mixed with cultured benthic diatoms, and
little or no growth on a mixture of powdered Ulva and sand. The bacterial composition offered
was unnatural, and whether the cultured diatoms matched the natural community structure
was not determined. The strength of the study is its demonstration that A. marina can grow on
either bacteria or diatoms. Andresen & Kristensen (2002) in a seasonal field study in Bregnør
Bay, Denmark, calculated from observed assimilation efficiencies that A. marina could meet its
dietary needs entirely from the combination of diatoms and bacteria during summer and fall,
but that additional dietary components accounted for about half of assimilated carbon in winter.
Mayer et al.’s (1997) analyses of digestive reagents indicated capacity for digestion of nonliving
organic matter in small particulate and adsorbed form. Microbial activity is certainly increased
in sediments affected by respiratory pumping (Reichardt 1988; Grossman & Reichardt 1991), but
whether food intake is thereby increased is less clear (Jumars et al. 1990). Holst & Zebe (1984)
observed uptake of dissolved volatile fatty acids by A. marina. We strongly suspect that this
uptake occurs via intake of water through the anus into the hindgut, where uptake of volatile fatty
acids produced by anaerobic bacterial activity is the norm not just in worms but in most animals,
including mammals (Plante et al. 1990). Riisgård & Banta (1998) reviewed diet observations
and concluded that diverse foods, including microfauna, meiofauna, and organic detritus, are
probably utilized.
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As protein concentrations of food increase from very low values, arenicolid feeding rates
increase, plateau and then decrease at the highest values (Taghon & Greene 1990; Hymel &
Plante 2000, Linton & Taghon 2000). This pattern is inconsistent with either compensatory
ingestion or a target level for assimilation rate that can be maintained—once food is rich
enough to meet the target—by decreasing ingestion rate at higher food concentrations. Neither
compensatory ingestion nor target levels are compatible with Taghon & Greene’s (1990)
observations that growth rate increases monotonically with ingested protein concentration, but
that result is expected if digestive systems operate to maximize the rate of absorption of nutrients
produced by digestion (Jumars 2000).
Digestion, transport and absorption in the guts of deposit feeders are analogous to processes
in modern washing machines in a wash-rinse cycle, except that in the animal, the reagents
(enzymes and surfactants) are apparently re-used and resorbed rather than discarded, the
solubilized and digested organic materials are absorbed, and the wash and rinse are continuous
while the animal feeds (Mayer et al. 2001). Digestive enzyme activity is highest in the ceca
at the foregut-midgut junction and in the midgut immediately behind this junction, a region
sometimes referred to as the stomach (Eberhardt 1988, A. marina; Mayer et al. 1997, A. marina
& Abarenicola vagabunda; Weston & Mayer 1998, Arenicola braziliensis). Protease activity
persisted in A. marina under starvation, and proteases exhibited little autolysis (Eberhardt 1988).
Taghon (1988) calculated that enzymatic costs in A. pacifica are a small fraction of its total
metabolic budget. Midgut fluids (of the three species mentioned parenthetically plus A. pacifica)
also exhibited high surfactancy with the surfactants maintained at concentrations above the
critical value for micelle formation, whereas pH was close to neutrality (Plante et al. 1990; Plante
& Jumars 1992; Mayer et al. 1997, 2001). Three surfactant molecules from A. marina have
been identified (Smoot et al. 2003). Rinse water is taken in through the anus. A. marina is quite
efficient at stripping and assimilating bacterial fatty acids via this wash and rinse cycle (Boon &
Haverkamp 1979, Woulds et al. 2014).
We (RFL Self & PA Jumars, unpublished), in a pulse-chase design, exposed feeding
Abarenicola pacifica to solutions containing dyes and radiotracers; these solutes first appeared
at the posterior hindgut and anterior foregut and continued toward the midgut, supporting
liquid counterflow opposing the particle path to the midgut. Controlled flow of dissolved
digestive products to absorptive sites may be one side benefit of being a slightly hyperosmotic
osmoconformer if sites of net water uptake from the gut coincide with absorptive locations
for digesta. Uptake of solutes and particles through the anus has been well documented for a
deposit-feeding holothuroid (Jaeckle & Strathmann 2013) and suggested for syllids (Ding et al.
1998). This kind of reflux is consistent with the observation of extraordinarily high dissolved
protein concentrations in the gut lumen that are capable of solubilizing metals (Chen et al. 2000).
This mode of digestion also provides a major point of entry for hydrophobic pollutants and
heavy metals into marine food webs (Weston & Mayer 1998; Chen & Mayer 1999; Weston et al.
2000). Notably little enzyme activity is observed in the feces of A. marina (Mayer et al. 2001).
It should be noted, however, that countercurrent flow of solubilized digesta is not sustainable
continuously because large, soluble, refractory molecules too large to be absorbed would
continue to accumulate.
Peak ingestion rates coincide with very short gut residence times of ingested sediments,
requiring that components to be assimilated be solubilized very quickly through the action
of surfactants and enzymes. Acceleration of both solubilization and enzymatic reaction
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at higher temperature likely explain the temperature effects observed by Hymel & Plante
(2000). Solubilization allows solutes a longer residence time for digestion and absorption
than one would expect from particle residence time in the gut. Sands are far more permeable
than muds and have less surface area for adsorption of surfactants and enzymes, so that sand
ingestion can yield a higher net profit at a higher ingestion rate than is feasible when ingesting
less permeable, chemically messier (containing higher concentrations of refractory organics)
and highly adsorptive (clay-rich) muds. Solute reflux also is more difficult in less permeable
ingesta. Assimilation of bacteria by arenicolids varies substantially across bacteria species,
and its estimation is greatly complicated by the capacity of bacteria to grow rapidly in the
hindgut (Plante et al. 1989, 1996; Plante & Jumars 1993; Plante & Mayer 1994, 1996; Plante &
Shriver 1998; Hymel & Plante 2000; Andresen & Kristensen 2002). Fluids in the gut lumen are
generally anoxic (Plante et al. 1990; Plante & Jumars 1992). A further potential complication
is the existence of intracellular digestion in arenicolids (Kermack 1955; Kaganovskaya 1979,
1983). Its dietary importance is unknown, but the India ink and carmine tracers used to
document uptake fall in size ranges similar to those of chloroplasts and their grana as well as to
bacteria. Intracellular digestion would give digestive access to particles of high food value but
digestive kinetics too slow for extracellular solubilization and hydroloysis.
Burrow structures and feeding behaviors of larger arenicolids, however, are fairly unique
among polychaetes (cf. F&J). Surface sediments arrive at the feeding depth quickly because
the region of collapse is surprisingly small in diameter (Rijken 1979), and flow reversals likely
to influence granular collapse of sediments into the feeding region are common (Volkenborn et
al. 2010). Retraubun et al. (1994) found that diatoms were subducted at concentrations similar
to those found on the surface, but large particulate detritus was concentrated in the funnel,
consistent with enhanced deposition due to slowed fluid flow in a depression. Whether enhanced
detritus actually reaches the feeding region is unclear, however, as lower quantities of detritus in
the headshaft suggested some selection against detritus in the mechanics of the collapse.
Volkenborn et al. (2010) used planar optodes to measure 2D oxygen concentration around A.
marina in sediments with different permeabilities and showed that oxygen penetration spanned
a much larger region in highly permeable sand, whereas in less permeable sediments, localized
plumes ascended into the water column above the head shaft, presumably through sedimentary
cracks. It seems likely that these mechanical differences affect feeding by altering particle
sorting, potentially limiting worms in muddier sediments to feeding on burrow walls while
enabling worms in sandier sediments greater sorting and filtering capabilities. More generally,
identities and sources of small particulate and adsorbed, nonliving organic matter in sediments
remain to be resolved. Whether a pit forms over the head shaft and what collects in it will be
affected by local details of overhead sediment transport as well as the mechanical properties of
sediments, especially their permeability and cohesion. Sediment permeability also affects the
delivery of dissolved chemical cues to burrowing arenicolids. Recent observations (Lindsay,
unpubl.) suggest that eversion of the pharynx closes off the nuchal organ of Abarenicola pacifica,
but as the pharynx is retracted, the nuchal organ is exposed and pore water is drawn toward it,
allowing the worm to “sniff” its solutes.
Arenicolids sometimes show surprisingly high δ15N, comparable to those of sympatric
Nephtys spp. or lumbrinerids (e.g., Arenicola marina, Herman et al. 2000, Kostecki et al. 2012;
Abarenicola affinis, Leduc et al. 2006). Alternatively, they may show δ15N values similar
to those of other deposit feeders (e.g., Arenicola marina, Ouisse et al. 2012). Stable carbon
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Jumars, Dorgan & Lindsay
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isotopes in these studies support a substantial contribution to diets from microphytobenthos but
do not rule out its prior transformation through a detrital and bacterial pathway. Indeed the high
variance in δ15N supports substantial variation in degrees of prior transformation.
Guild membership
F&J assigned family members to surface deposit- and suspension-feeding guilds.
Subsequent study has shown pumping rates achieved by Arenicola marina and presumably other
arenicolids to be too small for significant contribution to either nutrition or energy costs (Riisgård
et al. 1996; Riisgård & Banta 1998, who discounted the earlier results of Toulmond & Dejours
1994). Although we agree that the bulk of nutrition in the large morphotype comes from surficial
sediments, the fluid and solid mechanics, as well as the foraging risks are different in this mode
of feeding by subducting overlying sediments than in surface deposit feeding by species that
expose at least their feeding tentacles above the sediment-water interface. Moreover, this kind of
subduction depends on sediment properties; it is unlikely to succeed without a substantial sand
component. The ratio between surficial and subsurficial ingesta is sensitive to grain size and
sorting and local sediment dynamics through the angle of repose and the formation and filling
of the feeding funnel. Effectively it is subsurface deposit feeding on largely but not entirely
surficial sediments. We believe that recognizing and better understanding the peculiarities of
“funnel feeding” warrants a separate category.
Thus we classify Arenicola, Abarenicola & Arenicolides spp. as discretely motile funnel
feeders (feeding below the sediment-water interface in sand-silt mixtures but ingesting surficial
deposits along with variable amounts of subsurface sediments). More speculatively (without
evidence) we conjecture that Branchiomaldane spp. are subsurface deposit feeders. All use an
unarmed, non-muscular, eversible, axial pharynx to contact and ingest food.
Research questions and opportunities
• Even very basic feeding studies of Branchiomaldane spp. are lacking.
• Abarenicola affinis chiliensis inhabits sediments that exceed 20% organic matter by weight
(Moreno et al. 2007), two orders of magnitude more concentrated than in more typical
arenicolid habitats. Experimental studies of feeding rate versus food quality with taxa
adapted to such high organic contents could be very illuminating.
• Comparison of sedimentary food quality and microbial composition in areas where arenicolid
δ15N‰ differ should provide insights into the utility of 15N in identifying subsurface deposit
feeding.
• Large arenicolids are likely targets for studies of hypothesized links between excretory and
digestive systems through differences in water uptake from the gut lumen among gut regions.
• The relative importance of intracellular digestion and the identities of particles that enter this
pathway are unknown.
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Rijken M. 1979. Food and food uptake in Arenicola marina. Neth. J. Sea Res. 13: 406–21
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Self RFL, Jumars PA. 1988. Cross-phyletic patterns of particle selection by deposit feeders. J.
Mar. Res. 46:119–43
Smoot JC, Mayer,LM, Bock MJ, Wood PC, Findlay RH. 2003. Structures and concentrations
of surfactants in gut fluid of the marine polychaete Arenicola marina. Mar. Ecol. Prog. Ser.
258:161–9
Swinbanks DD. 1981. Sediment reworking and the biogenic formation of clay laminae by
Abarenicola pacifica. J Sediment. Petrol. 51:1137–45
Taghon GL. 1988. The benefits and costs of deposit feeding in the polychaete Abarenicola
pacifica. Limnol. Oceangr. 33:1166–75
Taghon GL, Greene RR. 1990. Effects of sediment-protein concentration on feeding and growth
rates of Abarenicola pacifica Healy et Wells (Polychaeta: Arenicolidae). J. Exp. Mar. Biol.
Ecol. 136:197–216
Toulmond A, Dejours P. 1994. Energetics of the ventilatory piston pump of the lugworm, a
deposit-feeding polychaete living in a burrow. Biol. Bull. 186:213–20
Tzetlin A, Purschke G. 2005. Pharynx and intestine. Hydrobiologia. 535/536:199–225
Volkenborn N, Hedtkamp SIC, van Beusekom JEE, Reise K. 2007. Effects of bioturbation and
bioirrigation by lugworms (Arenicola marina) on physical and chemical sediment properties
and implications for intertidal habitat succession. Estuar. Coast. Shelf Sci. 74:331–43
Volkenborn N, Polerecky L, Wethey DS, Woodin SA. 2010. Oscillatory porewater bioadvection
in marine sediments induced by hydraulic activities of Arenicola marina. Limnol. Oceanogr.
55:1231–47
Wells GP. 1952. The proboscis apparatus of Arenicola. J. Mar. Biol. Assoc. UK. 31:1–28
Wells GP. 1954. The mechanism of proboscis movement in Arenicola. Quart. J. Microsc. Sci.
95:251–70
Weston DP, Mayer LM. 1998. Comparison of in vitro digestive fluid extraction and traditional
in vivo approaches as measures of polycyclic aromatic hydrocarbon bioavailability from
sediments. Env. Tox. Chem. 17:830–40
Weston DP, Penry DL, Gulmann LK. 2000. The role of ingestion as a route of contaminant
bioaccumulation in a deposit-feeding polychaete. Arch. Environ. Contam. Toxicol. 38:
446–54
Woulds C, Middelburg JJ, Cowie GL. 2014. Alteration of organic matter during infaunal
polychaete gut passage and links to sediment organic geochemistry. Part II: Fatty acids and
aldoses. Geochim. Cosmochim. Acta 136:38–59
Aspidosiphonidae, Sipuncula
Diversity and systematics
Aspidosiphonidae currently comprise about two dozen species in a pair of genera. A third
genus, Lithacrosiphon was recently synonymized with Aspidosiphon (Kawauchi et al. 2012).
Cloeosiphon is monotypic. Trunk lengths range between 4 and 40 mm (Edmonds 2000).
Habitat
The family occurs from intertidal to abyssal depths. Members are typically nestlers in otherwise
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Jumars, Dorgan & Lindsay
07 November 2014
empty gastropod or tusk shells, foraminiferan tests, worm tubes or rock crevices. Some species
bore into limestone and other softer minerals or into algal holdfasts and seagrass scales or occupy
borings made by other species (e.g., A. muelleri in scales of Posidonia, Guidetti et al. 1997).
Sensory and feeding structures
The anterior trunk is capped by either a scleratized anal shield or a calcareous knob. The
introvert extends from the ventral surface of the anterior trunk except in C. aspergillus where it
inserts in the center of the cap (Edmonds 2000). In some Aspidosiphon spp., offset from center
is small. Eyespots are generally present as variably developed ocular tubes (Cutler 1994).
Aspidosiphon carries a middorsal nuchal organ (Edmonds 2000). Short, finger-like tentacles
encircle it. The introvert varies from one to two times the length of the trunk and bears rings of
closely packed, recurved hooks (Edmonds 2000). As in other sipunculans, the mouth and anus
are closely juxtaposed, enabling the double helical twisting of a long gut within the trunk and
setting up an ideal topology for osmotic counterflows.
Motility
Aspidosiphonidae are discretely motile, often needing to discard a shell and search for a larger
one as they grow (Murina 1984). A. jukesii pulls its adopted shell along the sediment surface
(Fisk 1983).
Illustrations
Edmonds (2000) provides informative, stippled line drawings of the two basic body plans.
Cutler (1977, Fig. 10) presents stippled line drawings illustrating the variability of the terminal
plates in the cap of C. aspergillus. Schulze et al. (2005, Fig. 1a) provide a stippled line drawing
of the external morphology of Aspidosiphon fischeri. Stolarski et al. (2001) show informative,
stippled line drawings of the ontogeny of the symbiosis between solitary corals and sipunculans.
Feeding
Published observations of feeding in this family are rare. An exception occurs among the species
of sipunculans that some solitary corals use as obligate symbionts. Such symbioses were briefly
reviewed by Stolarski et al. (2001) and date back to the Cretaceous Period. The coral settles
on a gastropod shell already occupied by the sipunculan and leaves one or more openings for
the sipunculan as it overgrows the shell. Fisk (1981) cited in Fisk (1983) observed A. jukesii
to ingest sand < 500 µm diam by extending its introvert into the sediment, and he determined
a gut residence time of 24 to 48 h for ingested sediments—unusually long for deposit feeders,
especially those feeding on sands.
Murina (1984) placed members of Aspidosiphon in either of two feeding categories.
Roughly ¼ of the species, especially those living in shells and tests, were considered deposit
feeders. The rest were considered endolithic, scraping detritus from the substratum with papillae
and hooks on the introvert. Blake (1994) regarded A. zinni as a subsurface deposit feeder based
on its vertical distribution in layered cores. Of 139 individuals collected at slope depths off
North Carolina, 53% were in the top 2 cm, 46% in the next 3 cm and 1% in the 5-10 cm layer.
Also based on layered cores, Faresi et al. (2012) considered A. muelleri a surface deposit feeder.
A photograph of 2 A. muelleri individuals pulling along commensal corals (credited to C. Mitel
at < http://doris.ffessm.fr/>) shows trailing surface sediments cleared of organic material. This
information seems to conflict with Fig. 4D and D’ of Morton & Salvador (2009) showing A.
muelleri feeding > 2 cm below the sediment-water interface from the larger opening of a buried
serpulid (Ditrupa arietina) tube. It may be useful to note that the use of the tube, with its smaller
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Jumars, Dorgan & Lindsay
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opening above the sediment-water interface (likely for respiratory ventilation) could cause most
individuals to fall in the surface layer of sediments when cores are sectioned—even if the species
normally feeds below the surface.
A. muelleri from the Bay of Banyuls-sur-Mer (Carlier et al. 2007) and from the Catalan slope
(Fanelli et al. 2011) had δ15N values consistent with surface deposit feeding. Specimens from 15
- 35 m water depth in the Bay of Concarneau in winter were close in δ15N to those of Hilbigneris
gracilis (Lumbrineridae, Rigolet et al. 2014); levels suggest inclusion of animals or subsurface
deposit in the diet. The same species collected in seagrass beds around Mallorca Island,
showed enrichments that varied from levels seen in other surface deposit feeders to levels seen
in lumbrinerids (Deudero et al. 2014); scraping with hooks may entail a degree of associated
omnivory that varies with habitat.
Guild membership
Based on the limited direct observations, the presence of hooks on the introvert, stable isotopic
data, we suggest that most aspidosiphonids are surface deposit feeders and (or) scrapers of
surface coatings from solid interfaces. Off-axis placement of the introvert would seem a
disadvantage in burrowing, and the hardened cap would seem a useful protective device for
operating near the sediment-water interface in non-shell occupiers or as something like an
operculum in shell occupiers. Shell occupiers may utilize subsurface sediments within reach.
Sediment dwellers appear to be discretely motile, whereas endolithic species may be sessile.
Research opportunities
• Direct laboratory and field observations of feeding are still rare. Nocturnal, red-light
observations would appear especially worthwhile. The long gut residence time reported by
Fisk (1983) when surface deposit feeding on sand suggests that A. jukesii may also scrape
richer food from its shell.
• Biomechanical analysis of the direction of burrowing forces resulting from the shape and
orientation of the occupied shell resisting the pull of the generally off-center introvert would
be informative regarding the potential to subsurface deposit feed.
• Additional stable isotope measurements, gut residence time estimates, and digestive enzyme
and surfactant assays would be useful.
References
Blake JA. 1994. Vertical distribution of benthic infauna in continental slope sediments off Cape
Lookout, North Carolina. Deep-Sea Res. Pt. II. 41:919–27
Carlier A, Riera P, Amouroux J-M, Bodiou J-Y, Grémare A. 2007. Benthic trophic network in the
Bay of Banyuls-sur-Mer (northwest Mediterranean, France): An assessment based on stable
carbon and nitrogen isotopes analysis. Estuar. Coast. Shelf Sci. 72:1–15
Cutler EB. 1977. The bathyal and abyssal Sipuncula. Galathea Rept. 14:135–56
Cutler EB. 1994. The Sipuncula: Their Systematics, Biology and Evolution. Ithaca, NY: Cornell
Univ. Press
Deudero S, Box A, Vázquez-Luis M, Arroyo NL. 2014. Benthic community responses to
macroalgae invasions in seagrass beds: Diversity, isotopic niche and food web structure at
community level. Estuar. Coast. Shelf Sci. 142:12–22
Edmonds SM. 2000. Phylum Sipuncula. See Beesley et al. 2000, pp. 375–400
Fanelli E, Papiol V, Cartes JE, Rumolo P, Brunet C, Sprovieri M. 2011. Food web structure of the
epibenthic and infaunal invertebrates on the Catalan slope (NW Mediterranean): Evidence
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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from δ13C and δ15N analysis. Deep-Sea Res. Pt. I. 58:98–109
Faresi L, Bettoso N, Aleffi IF. 2012. Vertical distribution of soft bottom macrozoobenthos in the
Gulf of Trieste (northern Adriatic Sea). Ann. Ser. Hist. Nat. 22:123–32
Fisk DA. 1981. Studies of two free-living corals and their common sipunculan associate at
Wistari Reef (Great Barrier Reef). MS thesis. Univ. Queensland, Australia
Fisk DA. 1983. Free-living corals: distributions according to plant cover, sediments,
hydrodynamics, depth and biological factors. Mar. Biol. 74:287–94
Guidetti P, Bussotti S, Gambi MC, Lorenti M. 1997. Invertebrate borers in Posidonia oceanica
scales: relationship between their distribution and lepidochronological parameters. Aquat.
Bot. 58:151–64
Kawauchi GY, Sharma PP, Giribet G. 2012. Sipunculan phylogeny based on six genes, with a
new classification and the descriptions of two new families. Zool. Scr. 41:186–210
Murina G-V. 1984. Ecology of Sipuncula. Mar. Ecol. Prog. Ser. 17:1–7
Rigolet C, Thiébaut E, Dubois SF. 2014. Food web structures of subtidal benthic muddy habitats:
evidence of microphytobenthos contribution supported by an engineer species. Mar. Ecol.
Prog. Ser. 500:25–41
Stolarski J, Zibrowius H, Loser H. 2001. Antiquity of the scleractinian-sipunculan symbiosis.
Acta Palaeontol. Pol. 46:309–30
Asteriomyzostomatidae, Myzostomida
Diversity and systematics
We rely on the comprehensive review and revision by Grygier (2000) for the family definition.
The more recent family-level revision by Summers & Rouse (2014) left this family unchanged.
Asteriomyzostomatidae are known from two species of Asteriomyzostomum (Grygier 2000).
Individuals are flattened, oval disks up to 6 mm long and 8.5 mm wide (Grygier 2000).
Habitat
Both species live in seastars at shelf to shallow bathyal depths (Wheeler 1905). A. asteriae is
known from the pyloric caeca of two species of Sclerasterias in the Mediterranean, whereas A.
fisheri occupies the body cavity of Tosia leptoceramus off southern California (Wheeler 1905).
Sensory and feeding structures
The mouth is ventral, as are unpaired, papilliform, eversible lateral (sensory) organs (Grygier
2000). Salivary glands inside the mouth precede a pharyngeal muscle bulb. The gut opens into
two principal pairs of diverticula, each with five main branches (Grygier 2000). A protrusible
pharynx is lacking.
Motility
Individuals appear to retain modest, discrete motility in the reference frame of the host (within
the host gut or coelom).
Illustrations
Grygier (2000, Fig. 2.17) provides line drawings of basic ventral external morphology and
a sagital section of internal morphology for A. asteriae. Wheeler (1905, Fig. A) provides a
detailed ventral view as a charcoal drawing of A. fisheri.
Feeding
Where the animal feeds is better known than its food. A. asteriae may be kleptoparastic,
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Jumars, Dorgan & Lindsay
07 November 2014
parasitic, or both, whereas A. fisheri is parasitic on coelomic contents of its host.
Guild membership
We classify A. asteriae as a kleptoparasite and A. fisheri as a parasite and assume that both are
discretely motile.
Research opportunities
• The extent to which A. asteriae relies on digestive products versus unhydrolyzed food or
digestive tissues of its host is unknown.
• Energy costs to the hosts from the parasitism are unknown.
• Mechanisms structuring host specificity remain poorly known.
References
Grygier MJ. 2000. Class Myzostomida. See Beesley et al. 2000, pp. 297–329
Summers MM, Rouse GW. 2014. Phylogeny of Myzostomida (Annelida) and their relationships
with echinoderm hosts. BMC Evol. Biol. 14:170, 15 pp.
Wheeler WM. 1905. A new Myzostoma, parasitic in a starfish. Biol. Bull. 8:75–8
Asteromyzostomatidae, Myzostomida
Diversity and systematics
We rely on the comprehensive review and revision by Grygier (2000) for the family definition.
The more recent family-level revision by Summers & Rouse (2014) left this family unchanged.
Asteriomyzostomatidae are known from the single genus Asteromyzostomum. Three species are
described from the Russian Arctic, and a pair of unnamed species are known from the Antarctic
and Atlantic (Grygier 2000), respectively. Individuals are somewhat flattened, irregularly lobate
ovoids or rectangles up to about 5 mm long and 15 mm wide (Grygier 2000).
Habitat
All species appear to be ectoparasitic on seastars. Each of the three Russian Arctic species is
known from a separate species of seastar (Grygier 2000). Collections come from shelf and
bathyal depths.
Sensory and feeding structures
The mouth is ventral, and the pharyngeal muscle bulb penetrates the integument of the
host. Circumoral tentacles restrain the muscle bulb from being pulled out. Some pharyngeal
protrusion accompanied initial penetration of the host, but pharyngeal protrusion and retraction
do not occur afterward. One or more pairs of chemo- and mechanosensory lateral organs are
present. A single pair of highly branching gut diverticula is present (Grygier 2000).
Motility
Individuals appear to be sessile in the reference frame of the host.
Illustrations
Grygier (2000) provides a line drawing (Fig. 2.18) of a cross section of internal morphology
through the widest part of the body of A. witjasi and a photograph of a whole specimen of an
unnamed species from McMurdo Sound.
Feeding
Asteromyzostomum spp. are restricted to feeding on coelomic contents of their hosts.
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Asteromyzostomatidae
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Guild membership
We classify Asteromyzostomum spp. as sessile ectoparasites.
Research opportunities
• Energy costs to the host from the parasitism are unknown.
References
Grygier MJ. 2000. Class Myzostomida. See Beesley et al. 2000, pp. 297–329
Summers MM, Rouse GW. 2014. Phylogeny of Myzostomida (Annelida) and their relationships
with echinoderm hosts. BMC Evol. Biol. 14:170, 15 pp.
Bonelliidae, Echiura
Diversity and systematics
Bonelliidae comprises about 65 species distributed among 26 genera, 9 of them monotypic
and none with as many as 10 species. Provisional molecular phylogenetic results suggest that
Bonelliidae and Ikedidae are sister clades (Goto et al. 2013). Recent morphological, cladistic
analyses that include internal characters support convergent evolution of bifid probosces within
the family (Lehrke 2011). Bonelliids are sexually dimorphic, with dwarf males dependent on
females for nutrition (Edmonds 2000). Our analysis treats female feeding traits only. The trunk
in most species is 2 - 10 cm long.
Habitat
Bonelliidae inhabit soft and mixed sediments as well as crevices in hard bottoms, often
occupying burrows made by other animals. They occur from intertidal to hadal depths.
Sensory and feeding structures
The proboscis is bifid in the type genus and in many other bonelliids. Animals are very light
sensitive (Jaccarini & Schembri 1977b), but eyespots are absent in adults. Sensory cells may
be concentrated dorsally at the point of proboscis branching (dorsal being a morphological term
referring to the side opposite the ventral nerve chord). Echiurans probe sediments with the
dorsal side of the proboscis downward. The proboscis is ciliated ventrally and in some species
on the anterior edges and anterior dorsal surfaces near the edges of the two branches (Jaccarini
& Schembri 1977a, 1979). The ciliated surface faces upward. Dorsal, leading-edge cilia are
morphologically different from the ventral cilia used for food gathering and are used in proboscis
extension (Jaccarini & Schembri 1977a). Proboscis shape is highly variable among deep-sea
species, with the proximal portion highly modified in some species into a funnel, massive lips, a
collar, or a tunnel (DattaGupta 1981, Edmonds 2000). Bonelliid probosces are highly extensible,
in Bonellia viridis to lengths up to 1.5 m (Edmonds 2000). Bonelliids have long, convoluted guts
characteristic of echiurans and a siphon tube that connects the anterior midgut with the posterior
midgut. Paired anal sacs may open into the hindgut through either one or two ducts (Lehrke
2011). Anal sacs in Bonelliidae can be sac like or tubular; rarely they are absent (Lehrke 2011).
Motility
As frequent occupants of burrows made by other organisms, some shallow-water bonelliids
are discretely motile by peristaltic burrowing or moving slowly over the sediment surface with
a combination of muscular and ciliary motions (Jaccarini & Schembri 1977a, b, c). B. viridis
lives in at least four distinct burrow structures formed initially by other species (Schembri &
Jaccarini 1978). Bonelliids are among the least motile echiurans, however, compensated by the
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Jumars, Dorgan & Lindsay
07 November 2014
most extensible introverts. Extensive symbionts attest to the stability of some bonelliid burrows
(Nickell et al. 1995). Hughes et al. (1999) observed that specific ejecta mounds of Maxmuelleria
lankesteri at 13 - 15 m water depth in Loch Sween, Argyll, Scotland, remained active and
spatially stable for the full 15 mo of their study. Feeding sites at the presumed other end of the
burrow were often occluded by sediments. By contrast, based on the appearance of new feeding
sites and ejection mounds in bottom photographs, Bett et al. (1995) reported apparent movement
of a putative echiuran at 4600 m water depth on the Cape Verde Abyssal Plain approximately
every 10 wk. Hughes et al. (1999) suggested that M. lankesteri could remain sedentary because
of its high local food supply rates. M. lankesteri appears unusual among echiurans in being
unable to reburrow, specimens surviving for 2 - 3 mo in mud-containing aquaria without
reburrowing (Nickell et al. 1995). Although it may be nearly sessile, we assume that it could
move its burrow laterally if its burrow were collapsed by neighbors or by physical processes and
thus regard it as discretely motile, albeit toward the sedentary end of the spectrum.
Bonellia viridis has an open body cavity that enables peristaltic movement using waves
traveling either in or opposed to the direction of forward movement. Schembri & Jaccarini
(1977) described peristaltic waves with a short contracted region and large dilated region
traveling from the anterior to posterior of the worm to irrigate the burrow. B. viridis alternates
direction of peristaltic waves to move forward and backward in the burrow and was observed
to turn around in a glass tube by first everting the proboscis, likely to reduce the body volume,
and to retract the proboscis only after the turn was completed (Schembri & Jaccarini 1977).
Having an open body cavity facilitates alternating between forward and backward movements
and rotating within or squeezing through tight spaces, advantageous for an animal that
primarily utilizes already-made burrows. Peristaltic movements are very similar to those of
Scalibregmatidae (Elder 1973), which share a similar body aspect ratio and an open body cavity. Burrows of M. lankesteri extended deep into the sediment and were topped with mounds
of sediment. M. lankesteri constructed a long-lived burrow that could reach 80 cm into the
sediment and be > 1 m long. The bottoms of the burrows were nearly horizontal, and only one
opening was observed in resin casts; the opening from which the worm fed was funnel shaped
and paired with a mound of ejected sediment up to 20 cm high, but the funnel was often filled
with sediments and not always evident (Nickell et al. 1995).
Illustrations
With line drawings and photographs DattaGupta (1981) displays some of the morphological
diversity in deep-sea bonelliid probosces. Fig. 2 in Jaccarini & Schembri (1997c) is an
informatively labeled line drawing of B. viridis that has often been reproduced. Their Fig. 5 is
a simple time series of particle pickup and transport at and near the tentacle tip, and their Fig. 7
shows loci of particle rejection. Ohta (1984) provides striking photographs of bonelliid feeding
traces at bathyal and abyssal depths. A remarkable photograph of three B. viridis individuals
feeding on the sediment surface is available at <http://tolweb.org/Echiura/2524/2008.01.09>.
They appear to have swept up dark, surficial detritus, leaving behind a clean sand trail.
Feeding
By far the most information on feeding and motility in Bonelliidae comes from observations
and experiments on Bonellia viridis, collected under water 3 - 6 m deep off Malta, and on
Maxmuelleria lankesteri from 11 - 15 m water depths in Loch Sween, Scotland. In the former
species, particles were picked up at the proboscis tips, which were used like scoops while the
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Jumars, Dorgan & Lindsay
07 November 2014
tip of the proboscis curled upward with respect to the sediment-water interface (but downward
with respect to the ventral nerve chord), and the powerful cilia on the proboscis tip entrained
particles into the gutter formed by the upward-curled (into the water column) sides of the
proboscis (Jaccarini & Schembri 1977a). That is, the normal posture of the proboscis is to hold
the anatomically ventral side upward. Small particles (< 100 μm diam.) were picked up purely
by ciliary entrainment, whereas larger particles were grasped, pincers like, by the muscular sides
of the proboscis tips. Particle rejection was concentrated at the junction of the two proboscis
tips, at more proximal contractions along the proboscis, and just before the mouth (Jaccarini
& Schembri 1977a; Fig. 7). Sediment collection was described for M. lankesteri from in situ
video observations in Loch Sween, Scotland, at 11-12 m depth; the proboscis extended radially
away from the burrow, skimming off the top layer of sediments (Hughes et al. 1993). Proboscis
extension rate had a mean speed of 2.6 cm min-1; retraction was ≥ 30 times faster; the animal
limited its exposure risk when not picking up particles. The bulk of the sediment collected
on the proboscis was then pulled back into the burrow by muscular retraction of the proboscis
rather than by ciliary motion (Jaccarini & Schembri 1977b). Hughes et al. (1993) concluded that
sediments were further processed within the safety of the burrow.
Sediments were expelled from the mounded burrow opening of M. lankesteri as either
fine clouds of suspended material or as a dense slurry in a gravity flow down the sides of the
mound (Hughes et al. 1993). The relative contributions of feces, pseudofeces and sweepings
from burrow maintenance to these ventings could not be discerned. From a video analysis,
however, Hughes et al. (1996) estimated that M. lankesteri redistributed about 13 g dry wt. d-1
of sediments on the sediment surface and incorporated about 0.9 g d-1 as feces into its burrow
lining. We suspect that coprophagy accounted at least in part for the imbalance seen by Hughes
et al. (1996) in burrow intake versus output of sediments, in which case an imbalance would
still exist even if both ends of the putatively U-shaped burrow Hughes et al. 1996, Fig. 4) could
be clearly identified. Moreover Hughes et al. (1999) saw a biphasic relationship between diver
measurements of ejection rates over 48 h taken once a month and labile organic content of
surficial sediments during that month. Up to about the point where 58% of total combustible
organic carbon was labile, M. lankesteri maintained a roughly constant ejection rate of about 5.7
g dry wt. d-1 of sediments. Above that threshold, however, ejection rates increased sharply to
about 17 g d-1 when the labile fraction reached 0.73. This pattern is consistent with caching (and
replacement of existing cache) when food quality merits.
Smith et al. (1986) described mounds roughly 10 cm high and 30 cm in diameter composed
largely of fecal pellets, probably made by Prometor benthophila, under 1240 m of water in the
Santa Catalina Basin. It appeared to use the same feeding area at one end of a U-shaped burrow
but to move the mounded end around. The resulting feeding pit could become as large as 1 m
diam. and 10 cm deep.
Feeding activity of B. viridis was primarily crepuscular and nocturnal (Jaccarini & Schembri
1977c), and M. lankesteri also proved to be nocturnal (Hughes et al. 1993). On sand cleaned
of most of its organic matter, B. viridis showed little feeding activity (Jaccarini et al. 1977a). A
few particles were picked up, but most (except a small residuum of the smallest particles) were
rejected prior to reaching the mouth. When B. viridis individuals were simultaneously presented
control microscope slides without food value and experimental slides covered with Isochrysis
in different portions of their potential feeding area, worms spent significantly more time feeding
on the enriched slides. M. lankesteri was more reluctant than B. viridis to keep its proboscis
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
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Jumars, Dorgan & Lindsay
07 November 2014
above the sediment-water interface. Typical individuals fed only every other night (Hughes et
al. 1993). Feeding bouts lasted about 10 min, but were sometimes curtailed by contact with
epifauna. Median number of bouts per individual per night was 9, without apparent periodicity.
Individuals did not regularly space their feeding around the circumference of the burrow opening
but rather showed clearly non-random preference for some locations.
Ohta (1984) photographed star-shaped feeding traces of putative bonelliids at bathyal and
abyssal depths and identified a very tight relationship between the length-to-width ratio of
the radial traces and the maximum number of traces. He pointed out the way that these two
parameters combine to determine gain and efficiency of gain (by restricting double coverage) per
stroke. A consequence is that an individual able to recognize its prior recent traces (e.g., through
chemosensing) could follow a simple algorithm to feed efficiently around the burrow opening
on areas that had not been harvested recently. Jumars (1993) provided an explicit formula to
calculate the area left unharvested by n evenly spaced radial traces of a given aspect ratio.
Kershaw et al. (1984) identified burrows thought to belong to M. lankesteri and found fecal
pellets characteristic of this species lining both the entrance funnel and the posterior portion
of cored burrows. Jumars et al. (1990) suggested that echiurans lining their burrows with, or
making mounds of, fecal pellets may be caching food of moderate to high quality and controlling
microbial community structure by providing inocula and nitrogen as pellets pass their distinctive
anal sacs. Alternate feeding on cached resources and unpelletized surface sediments might help
explain the infrequent feeding in these echiurans compared with other surface deposit feeders.
B. viridis is known to harbor blue-green bacteria in its integument (Kawaguti 1971). M.
lankesteri harbors rod-shaped bacteria (McKenzie & Hughes 1999). Whether these bacteria play
any role in nutrition in either echiuran is unknown.
Guild membership
We characterize bonelliids as surface deposit feeders with the potential to cache food of moderate
to high residual value in the form of fecal pellets. How much such caching affects the energy
budget remains to be determined. All feed with an extensible, muscular, ciliated, proboscis. We
judge them to be discretely motile.
Research questions and opportunities
• Gut residence times of inert tracer particles would be informative.
• Does radial trace length vary with food quality and quantity, with bonelliid nutritional status,
and with predation risk?
• Does the anal sac provide inocula of bacteria that remain active in fecal mounds and fecal
burrow linings? How important is such caching to the energy budget?
• Prospecting floras of bonelliid guts, anal sacs, integuments and burrows might be rewarding.
• How frequently do individuals move burrows or move to a new burrow?
• Functions of the modified proboscises often found in deep-sea species are unknown.
References
Bett BJ, Rice AL, Thurston MH. 1995. A quantitative photographic survey of ‘Spoke-Burrow’
Type Lebensspuren on the Cape Verde Abyssal Plain. Int. Rev. Ges. Hydrobiol. 80:153–70
DattaGupta AK. 1981. Atlantic echiurans. Part I. Report on twenty-two species of deep-sea
echiurans of the North and the South Atlantic Ocean. Bull. Mus. Natn. Hist, Nat., Paris, 4e
sér., 3 section A: 353–78
Edmonds SM. 2000. Phylum Echiura. See Beesley et al. 2000, pp. 353–74
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Jumars, Dorgan & Lindsay
07 November 2014
Goto R, Okamoto T, Ishikawa H, Hamamura Y, Kato M. 2013. Molecular phylogeny of echiuran
worms (Phylum: Annelida) reveals evolutionary pattern of feeding mode and sexual
dimorphism. PLoS ONE 8:e56809. 6 pp.
Hughes DJ, Ansell AD, Atkinson RJA. 1996. Sediment bioturbation by the echiuran worm
Maxmuelleria lankesteri (Herdman) and its consequences for radionuclide dispersal in Irish
Sea sediments. J. Exp. Mar. Biol. Ecol. 195:203–20
Hughes DJ, Ansell AD, Atkinson RJA, Nickell LA. 1993. Underwater television observations of
surface activity of the echiuran worm Maxmuelleria lankesteri (Echiura: Bonelliidae). J. Nat.
Hist. 27:219–48
Hughes DJ, Atkinson RJA, Ansell AD. 1999. The annual cycle of sediment turnover by the
echiuran worm Maxmuelleria lankesteri (Herdman) in a Scottish sea loch. J. Exp. Mar. Biol.
Ecol. 23:209–23
Jaccarini V, Schembri PJ. 1977a. Feeding and particle selection in the echiuran worm Bonellia
viridis Rolando (Echiura: Bonelliidae). J. Exp. Mar. Biol. Ecol. 28:163–81
Jaccarini V, Schembri PJ. 1977b. Locomotory and other movements of the proboscis of Bonellia
viridis (Echiura, Bonelliidae). J. Zool. 182:467–76
Jaccarini V, Schembri PJ. 1977c. Locomotory and other movements of the trunk of Bonellia
viridis (Echiura, Bonelliidae). J. Zool. 182:477–94
Jumars PA. 1993. Gourmands of mud: diet selection in marine deposit feeders. In Diet Selection:
An Interdisciplinary Approach to Foraging Behaviour, ed. RN Hughes, 7:124–56. Oxford:
Blackwell Scientific
Jumars PA, Mayer LM, Deming JW, Baross JA, Wheatcroft RA. 1990. Deep-sea deposit-feeding
strategies suggested by environmental and feeding constraints. Philos. T. R. Soc. Lond. A
331:85–101
Kawaguti S. 1971. Blue-green algae in echiuroid worms. In: Aspects of the Biology of Symbiosis,
ed. TC Cheng TC, pp. 265–73. Baltimore: University Park Press
Kershaw PJ, Swift DJ, Pentreath R J, Lovett MB. 1984. The incorporation of plutonium,
americium and curium into the Irish Sea seabed by biological activity. Sci. Total Environ.
40:61–81
Lehrke J. 2011. Phylogeny of Echiura (Annelida, Polychaeta) inferred from morphological
and molecular data-implications for character evolution. PhD thesis. Friedrich-WilhelmsUniversität, Bonn
McKenzie JD, Hughes DJ. 1999. Integument of Maxmuelleria lankesteri (Echiura), with notes
on bacterial symbionts and possible evidence of viral activity. Invertebr. Biol. 118:296–309
Nickell LA, Atkinson RJA, Hughes DJ, Ansell AD, Smith CJ. 1995. Burrow morphology of the
echiuran worm Maxmuelleria lankesteri (Echiura: Bonelliidae), and a brief review of burrow
structure and related ecology of the Echiura. J. Nat. Hist. 29:871–85
Ohta S. 1984. Star-shaped feeding traces produced by echiuran worms on the deep-sea floor of
the Bay of Bengal. Deep-Sea Res. Pt. A 1:1415–32
Schembri PJ, Jaccarini V. 1977. Locomotory and other movements of the trunk of Bonellia
viridis (Echiura, Bonelliidae). J. Zool. 182:477–94
Schembri PJ, Jaccarini V. 1978. Some aspects of the ecology of the echiuran worm Bonellia
viridis and associated infauna. Mar. Biol. 47: 55–61
Smith CR, Jumars PA, DeMaster DJ. 1986. In situ studies of megafaunal mounds indicate rapid
sediment turnover and community response at the deep-sea floor. Nature. 323:251–3
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A57
Capitellidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Capitellidae
Diversity and systematics
Capitellidae comprise approximately 180 species distributed among about 49 genera, 24 of them
monospecific. They are closely related to echiurans and clitellids (Struck et al. 2011). The body
is usually very thin compared to its length. Adult lengths range from < 1 to about 30 cm.
Habitat
Capitellids are found in sediments and microbial mats at all water depths. A few commensal
species occur in other materials or inside other animal tubes.
Sensory and feeding structures
The prostomium is often short, blunt and roughly conical, but with many variations. One or
more pairs of dorsal eyespots may be present near the posterior of the prostomium. Paired,
eversible nuchal organs are usually located dorsally between the prostomium and peristomium,
forming distinct pits when retracted. The peristomial ring completely encircles the head (Rouse
2001). Capitellids feed by everting and retracting a non-muscular, non-ciliated, often papillated,
axial or dorsal pharynx (Saulnier-Michel 1992, Boyle & Seaver 2009).
A thin accessory intestine runs ventral to, and connects with, the main intestine in
Notomastus latericeus (Eisig 1887) and has also been described in Capitella jonesi (Eckelbarger
& Grassle 1982) and teleta (Eckelbarger et al. 1984), the latter formerly known as Capitella
sp. I (cf. Blake et al. 2009). Functions of this accessory intestine and whether it is common
throughout Capitellidae remain unknown.
Motility
Lacking extensible appendages, capitellids move to eat, and most species burrow in muddy
sediments. Some species feed below the surface and utilize the same tail shaft leading up to the
sediment surface for extended periods. Some species form mucus-lined burrows or tubes that
may be retained on a sieve. As noted by F&J, tube building can vary ontogenetically.
Illustrations
Rouse (2001) provides informative, stippled line drawings of anterior structures. Blake et al.
(2009, Fig. 1) provide definitive, stippled line drawings of the famously opportunistic Capitella
teleta, formerly and variously known as Capitella sp. I and Capitella capitata.
Feeding
With exceptions noted by F&J, possibly Abyssocapitella commensalis that dwells in
pogonophoran tubes (Buzhinskaja & Smirnov 2000), and Capitella ovincola that lives in squid
egg capsules (Zeidberg et al. 2011), most capitellids appear to be subsurface deposit feeders.
A. commensalis may feed on deposits within the tube, but its food source is not yet clear. C.
ovincola has a mutualistic relationship with the squid, Doryteuthis (= Loligo) opalescens, eating
the egg capsule matrix rather than the paralarvae and increasing hatching rates for the squid eggs
(Zeidberg et al. 2011).
Capitella spp. package ingested sediments into characteristic, prolate spheroidal pellets in
the foregut, generally visible through the body wall. C. teleta carries a median number of about
26 such spheroids in its gut at any one time, and pellet weight scales as worm volume to the 0.70
power; this value indicates that smaller worms carry relatively larger pellets (Forbes & Lopez
1987). These pellets when released are sites of high bacterial activity (Wu et al. 2003). Tracer
experiments show feeding by these small worms to be concentrated between 1 - 2 cm below the
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Jumars, Dorgan & Lindsay
07 November 2014
sediment-water interface, with some feeding activity extending > 3 cm (Salen-Picard et al. 1994).
Once released, in some settings C. teleta pellets can remain intact for surprisingly long periods
(20 yr half-life cf. Gallagher & Keay 1998). Gaston (1987), based on 15 individuals of each
species dissected, classed Mediomastus californiensis and Notomastus latericeus as subsurface
feeders on detritus. Fuller et al. (1988) found the highest pellet output for Mediomastus ambiseta
between midnight and early morning and the lowest in the period before midnight. Wheatcroft et
al. (1998) observed decreasing pellet production rates in this species with increasing crowding.
Contrary to F&J’s expectations of selection for the smallest particles sizes, both Capitella
sp. and Barantolla americana showed strong selection for intermediate sizes (≈ 10 µm diam.)
in subsurface deposit feeding (Self & Jumars 1988). Both showed some, but not statistically
significant, selection for lower particle specific gravity. Capitella teleta also showed strong
selection for particle size, both when it fed from subsurface sediments and when it turned around
in its tube and fed at the surface (Horng & Taghon 1999, Tsutsumi et al. 2005). The Capitella sp.
that Dauer (1980) dissected (possibly C. teleta) appeared to have selectively ingested diatoms.
Mediomastus ambiseta’s gut contents showed selection for particles below ambient median
grain size (Dauer 1980). In mesocosm and field aggregations of M. ambiseta, pelletized surface
sediments were enriched in organic matter but depleted in bacteria. In the deeper feeding zone,
organic matter was depleted but bacterial growth was enhanced (Hughes 1996).
Heteromastus filiformis appeared somewhat less selective for sizes of particles ingested
(Cadée 1979), but appeared able to select fine particles richer in organic carbon and protein than
the average present in the feeding zone (Neira & Höpner 1994). This species also concentrated
clay grains in its burrow lining through mechanisms that remain to be determined (Zorn et al.
2010). H. filiformis appeared to have unusually low assimilation efficiencies for bacteria, benthic
microalgae and organic detritus (Clough & Lopez 1993).
Because C. teleta has been in culture more than three decades and has become a model
opportunist, an unusual amount of work has been done on its feeding and growth rates. It is ≤
24 mm long as an adult (Blake et al. 2009), apparently small enough to be affected by resource
competition with several meiofaunal species (Alongi & Tenore 1985). Feeding rates showed a
Q10 of 2.49 with short-term changes in temperature in the 15 - 25˚C range, a somewhat stronger
dependence than seen in the average biochemical process (Forbes & Lopez 1987). Adult and
juvenile growth rates both were strongly affected at O2 tensions < 25 mm Hg, but adult growth
rates were more sensitive to bulk food quality than were juvenile growth rates (Forbes & Lopez
1990a). Reducing salinity lowered growth rates by reducing feeding rates (Pechenik et al. 2000).
Peak individual growth rates were seen at worm body volumes of about 2 mm3 (Forbes & Lopez
1990b). Adult growth rates were more sensitive than juvenile growth rates to food type and
ration, with high diatom concentrations yielding high growth rates (Marsh et al. 1989). Both
organic nitrogen content and digestively available caloric content of detritus determined growth
rates (Tenore 1981). Settling larvae chose sediments with higher quality food (low carbohydrate/
protein ratios, Thiyagarajan et al. 2005). When fed red seaweed detritus, C. teleta growth slowed
dramatically if only large particles (150 - 250 µm) were available (Phillips & Tenore 1984).
Capitella raised for 3 mo on Spartina detritus, Gracilaria detritus or Gerber’s mixed cereal
had δ13C values enriched over its food source by 0.8, 2.1 and 0.2‰, respectively (Haines
& Montague 1989). Stable isotopic data for field-collected capitellids usually showed δ15N
values slightly higher than or roughly equal to those of sympatric surface deposit feeders (e.g.,
Notomastus fragilis, Herman et al. 2000; Notomastus sp., Kikuchi & Wada 1996J; Capitella
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
sp., Levin et al. 2006; Heteromastus filiformis & Notomastus latericeus, Dubois et al. 2007;
Heteromastus sp. & Capitella sp., Kanaya et al. 2007; Notomastus latericeus, Bode et al.
2013; Capitellidae, Iken et al. 2001). In the Bay of Banyuls-sur-Mer, however, δ15N levels
were markedly elevated in Notomastus sp. over levels seen in other deposit feeders except
Macroclymene santanderensis (Maldanidae, Carlier et al. 2007). Similarly, in the Kitakami
River estuary (Honshu Island, Japan), Notomastus sp. showed δ15N levels 5 - 6‰ above those
of its putative sedimentary food (Doi et al. 2005). The high values may be associated with this
species feeding up to 20 cm below the sediment surface on anoxic muds (cf. Kikuchi & Wada
1996, who also found high values of δ15N in Notomastus sp. from the lower Nanakita River
estuary, Honshu Island).
At New Zealand cold seeps, some capitellids had δ13C signatures indicating strong
dependence on methane-derived carbon (Thurber et al. 2010). In the vicinity of cold seeps
northwest of Norway, capitellids showed large variance in dependence on methane-derived
carbon and had δ15N values slightly lower at seeps than in the surrounding community. At arctic
hydrothermal vents, capitellids varied in apparent dependence on vent microbes (highly variable
δ13C) but appeared to stay at about the same trophic level as indicated by δ15N (Sweetman et
al. 2013). Capitella from oil-influenced sediments showed evidence of obtaining part of their
nutrition from oil-based pathways (Spies et al. 1989, Kiyashko et al. 2001). In laboratory
experiments, Capitella teleta incorporated carbon fixed by sulfide-oxidizing bacteria and showed
stimulated growth (Tsutsumi et al. 2001). Closely related species of Capitella, however, differed
in body sizes, growth rates and sensitivities to both hypoxia and sulfide exposure (Gamenick et
al. 1998, Méndez et al. 2001), so it is unclear how well these results for C. teleta generalize.
Guild membership
Evidence supports motile, subsurface deposit feeding in most species. C. teleta and probably
other species also ingest some surficial sediments. C. ovincola, however, feeds on squid egg
capsules as it burrows through them. Abyssocapitella commensalis has motility limited by
residence inside its host’s tube, and its diet is unknown. All species utilize a non-muscular,
eversible, unciliated, axial or dorsal pharynx to contact and ingest food.
Research questions and opportunities
• Functions of the accessory gut remain to be identified and quantified.
• Foregut formation of pellets implies inclusion of digestive enzymes in them at that location.
Testing that idea and whether the membrane surrounding pellets is semi-permeable (e.g.,
retaining large molecules like enzymes but permeable to digestive products) would be
interesting. Does the membrane play any mechanical role by shrinking?
• Lab and field experiments are in order to decipher how some capitellids in some places
become so enriched in 15N.
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Bode A, Fernández C, Mompeán C, Parra S, Rozada F, et al. 2014. Differential processing of
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A60
Capitellidae
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doi: 10.1146/annurev-marine-010814-020007
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Jumars, Dorgan & Lindsay
07 November 2014
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methane use by New Zealand cold seep benthos. Mar. Geol. 272:260–9
Tsutsumi H, Taniguchi A, Sakamoto N. 2005. Feeding and burrowing behaviors of a depositfeeding capitellid polychaete, Capitella sp. I. Benthos Res. 60:51–8
Tsutsumi H, Wainright S, Montani S, Saga M, Ichihara S, Kogure K. 2001. Exploitation of
a chemosynthetic food resource by the polychaete Capitella sp. I. Mar. Ecol. Prog. Ser.
216:119–27
Wheatcroft RA, Starczak VR, Butman CA. 1998. The impact of population abundance on the
deposit-feeding rate of a cosmopolitan polychaete worm. Limnol. Oceanogr. 43:1948–53
Wu SS, Tsutsumi H, Tsukamoto K, Kogure K, Ohwada K, Wada M. 2003. Visualization of the
respiring bacteria in sediments inhabited by Capitella sp. 1. Fish. Sci. 69:170–5
Zeidberg LD, Isaac G, Widmer CL, Neumeister H, Gilly WF. 2011. Egg capsule hatch rate and
incubation duration of the California market squid, Doryteuthis (= Loligo) opalescens:
insights from laboratory manipulations. Mar. Ecol. 32:468–79
Zorn ME, Gingras MK, Pemberton SG. 2010. Variation in burrow-wall micromorphologies
of select intertidal invertebrates along the Pacific northwest coast, U.S.A.: Behavioral and
diagenetic implications. Palaios 25:59–72
Chaetopteridae, Spionida
Diversity and systematics
Chaetopteridae comprise about 65 species fairly evenly divided among 4 genera. We
accept Nishi’s (1999) reassignment of the formerly monotypic Sasekumaria selangora to
Mesochaetopterus. Chaetopteridae are basal within Annelida (Weigert et al. 2014), and
morphological similarity to Spionida (Rouse & Fauchald 1997) appears to be convergent.(Zrzavý
et al. 2009, Rousset et al. 2007, Struck 2011, Struck et al. 2011). At the species level, the idea
that the well-studied C. variopedatus is a single, cosmopolitan species had long been questioned
on morphological grounds and has been rejected on molecular genetic evidence (Osborn et al.
2007, Martin et al. 2008), but descriptions and ranges of valid species remain to be worked
out. At the generic level, preliminary phylogeny found that Spiochaetopterus nested within
Phyllochaetopterus (Osborn et al. 2007). Taxonomic revision thus is needed at multiple levels.
Chaetopteridae follow one of three body plans. Tube-dwelling Chaetopterus spp. display
characteristic, strong regionalization of body structures including flap-like chaetigers for active
pumping and palps too short to reach out of the tube. Neotenous C. pugaporcinus is roughly
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spherical and 1 - 2 cm in diameter. The three other chaetopterid genera contain tube dwellers
with more moderate regionalization of body structures and a pair of palps that can be extended
from the tube. Mesochaetopterus is intermediate between Chaetopterus and the other two genera
in morphology, e.g, body size, relative palp length, and number of mucus bags (Barnes 1965).
Most species are of moderate size, of order 10 cm long, but Phyllochaetopterus gigas and P.
major reach 30 cm (Nishi & Rouse 2014).
Habitat
Although the majority of species come from shelf and shallower depths, chaetopterids extend
to abyssal hydrothermal vent sites (Fabri et al. 2011). P. gigas was found with the baleen of a
whale fall at 3000 m water depth. The sole planktonic species occupies bathyal depths (Osborn
et al. 2007). All others are tubicolous and infaunal in sediments or epifaunal on hard substrata.
U- or J-shaped tubes of Chaetopterus have two openings to the water side of the sediment-water
or rock-water interface, whereas those of other benthic genera have only one opening into the
water column and can extend deep into the sediment (e.g., > 1 m for Mesochaetopterus taylori in
False Bay, San Juan Islands) in a straight, branched or J-shaped geometry.
Sensory and feeding structures
The small, rounded prostomium bears no antennae but may carry one or two pairs of eye spots.
A single pair of grooved, ciliated palps inserts dorsally at the anterior of the peristomium. Just
behind them, a little more medial, and covering about the same area as palp insertion can be a
pair of ciliated nuchal organs (Wilson 2000), but they are absent in Chaetopterus spp. (Rouse
2001). Dales (1962) described the mouth region of Chaetopterus as a simple tube lacking a
proboscis, but more detailed descriptions are lacking.
Motility
Chaetopterus pugaporcinus is neutrally buoyant and passively motile in weak, midwater
currents. The other species are tubicolous and do not appear able to move from their settlement
sites. They enlarge rather than replace tubes as they grow.
Illustrations
Martin et al. (2008) present a photograph of helical coiling by the palps of M. rogeri in situ
in apparently passive suspension-feeding mode (their Fig. 3A, B). Barnes’ (1964, 1965)
comparative studies of feeding and tube building in chaetopterids contain many informative line
drawings. Nishi’s (1999, Fig. 5) photograph depicts the perforations that permeate the buried
end of the tube in M. selangolus. Osborn et al. (2007) provide several informative photographs
and drawings of the family’s sole planktonic species. Nishi & Rouse (2014) provide remarkable
in situ photographs of P. gigas. They and the supplemental video archived with the journal
article show deposit feeding with the palps extended to the seafloor.
Feeding
No major changes in understanding of feeding by tube-dwelling Chaetopterus have ensued
since F&J: Chaetopterus spp. are active, mucus-net suspension feeders. Flood & Fiala-Médioni
(1982) quantified the spacing of mucus filaments in the bag of C. cf. variopedatus from the
northwest Mediterranean to be roughly ½ by ¾ μm. Mucus nets, however, through direct
interception also capture particles substantially smaller than their nominal mesh sizes (Sutherland
et al. 2010). Particle capture efficiency for C. cf. variopedatus from Sweden was lower than
expected from this mesh size, with only 90% efficiency for particles > 1 μm and only ~ 50%
efficiency for 0.5 μm particles (Jørgensen et al. 1984). It is possible that worms from these two
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locations are different species or that mesh size may vary with body size. C. cf. variopedatus
from the west coast of Sweden maintained a large pressure drop to keep a high flow rate through
the net, but, even so, pumping costs constituted only a modest fraction (~ 4%) of its total energy
expenditure (Riisgård 1989). C. aduncus is unusual in the genus in having a J- rather than a
U-shaped tube, but the dynamics of pumping may not be greatly affected because this species
lives attached to hard substrata, with both tube openings in bottom water (Nishi et al. 2009).
No doubt the most startling chaetopterid finding since F&J is the discovery of a midwater,
neutrally buoyant, planktonic species, Chaetopterus pugaporcinus (Osborn et al. 2007), that
generates no feeding current but instead spins and ingests a mucous web; the process can be
continuous. This method of trapping plankton and detritus is more reminiscent of thecosome
pteropod feeding (e.g., Silver & Bruland 1981) than of feeding in any other polychaete. The
dominant mechanism of particle encounter appears to be gravitational deposition. For the
moment, C. pugaporcinus is a solitary morphotype. It secretes no tube.
Large palps and J-shaped, branching or straight tubes with one buried end characterize
the genera Phyllochaetopterus and Spiochaetopterus, that have similar body plans and do not
appear to be genetically distinct (Osborn et al. 2007). At hydrothermal vent sites, however,
both tube openings may be above the sediment-water interface, supported by attachment to hard
substrata or to other tubes (Fabri et al. 2011). Barnes (1964) in his masterful analysis of mucus
bag feeding in S. oculatus did not present specimens with any substantial horizontal velocities
(normal to the tube opening) or any surfaces from which to deposit feed. Under the conditions
he provided, S. oculatus actively suspension fed similar to Chaetopterus but using numerous
smaller mucus bags to capture particles and pumping water through the tube with cilia rather
than piston-like pumping with modified segments. When horizontal flows and bottom deposits
were presented, S. oculatus used its large palps to suspension and deposit feed and was well
able to deal with oscillatory flows like those produced under surface waves (Turner & Miller
1991, Miller et al. 1992). Horizontal flux of high-quality, particulate organic matter stimulated
suspension feeding in this species (Bock & Miller 1996, 1997). Passive suspension feeding
involves helical coiling of the palps (Turner & Miller 1991) that appears homologous with the
suspension-feeding behavior of some spionids (Taghon et al. 1980, Shimeta 2009). Barnes
(1965) described feeding by Phyllochaetopterus socialis, which, like S. oculatus is smaller
than most Chaetopterus and Mesochaetopterus species. It produces numerous mucus bags and
pumps water through ciliated notopodial rings. P. socialis fed using mucus bags in still water,
but also produced a mucus rope that extended into the overlying water to suspension feed and
used its palps, even in still water, to feed (Barnes 1965). Palp extension beyond the tube in a
Phyllochaetopterus sp. was observed in video recordings by Fabri et al. (2011) near abyssal
hydrothermal vents; prior observations of such behavior are illustrated in F&J (their Fig. 5).
Nishi & Rouse (2014) observed similar extension in P. gigas associated with a whale fall at 3000
m water depth in Monterey Canyon. Deposit feeding was resolved in photographs and video
recordings. It is not known whether the species suspension feeds.
Feeding is less well understood in Mesochaetopterus, which is intermediate in body size
and morphology between Chaetopterus and the other two genera. Mesochaetopterus taylori
maintains a parchment, sand-coated tube that extends to or above the sediment surface at one
end and is buried at the other. Populations vary greatly in sediment depth of the buried end,
which is perforated, allowing pumping of water through one or two mucus bags and out into the
surrounding sediments (Sendall et al. 1995). We suspect that the regional variation corresponds
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with permeability of the sediments in which the tube terminates. The tube is extended by using
chaetae to cut an opening and excavating the adjacent sediment, some of which is transported in
a mucus bag to the open end of the tube (Sendall et al. 1995). Given the length of these tubes
and the even greater friction involved in pumping through the perforations and surrounding
sediments, reported flow velocities are surprisingly large (0.25 - 0.50 cm s-1; Sendall et al. 1995),
comparable to those in C. cf. variopedatus (Riisgård 1989). Flow resistance is overcome in M.
taylori by peristaltic pumping (Sendall et al. 1995). Both Ranzanides (= Mesochaetopterus)
sagittaria and M. taylori fed using mucus nets in still-water, laboratory experiments (Barnes
1965, Sendall et al. 1995), but M. taylori was observed to deposit feed with its large palps in tide
pools at low tide (Busby & Plante 2007). Martin et al. (2008) described helical coiling of the
palps of M. rogeri extending into the bottom boundary layer (their Fig. 3A, B) similar to that of
Spiochaetopterus oculatus, indicating that it also passively suspension feeds.
Although all chaetopterids thus can be classified as potential suspension feeders, the
mechanisms differ among genera and, at least for Mesochaetopterus, under different flow
conditions. Mucus-net feeding differs from palp feeding in that it captures particles of
smaller sizes, results in higher clearance efficiencies, and incurs higher energetic costs. It is
interesting to note that the larger Chaetopterus spp. pump water through tubes, a process much
less expensive for larger-diameter tubes; for a given pressure gradient, volumetric flow rate
varies with diameter to the 4th power, so costs for a given volumetric flow rate are inversely
proportional to 4th power of diameter. Smaller Phyllochaetopterus and Spiochaetopterus under
natural conditions appear to feed primarily with palps; Mesochaetopterus has been described
using both feeding modes and is of intermediate size.
Some shallow-water chaetopterids have shown stable isotopic and fatty acid signatures
consistent with feeding on phytoplankton (Chaetopterus cautus, Kharlamenko et al. 2008, Ishihi
& Yokoyama 2010; Mesochaetopterus sp., Yokoyama et al. 2009). Corbisier et al. (2006) found
that shallow-water Brazilian Spiochaetopterus nonatoi had an isotopic signature consistent with
being a primary consumer but did not provide stable isotopic signatures of local phytoplankton
distinct from seston. Løkken (2013) obtained similar results for a Spiochaetopterus sp. from ~
270 m water depth in Isfjorden, Svalbard. 13C depletion in Phyllochaetopterus socialis near the
sulfide horizon in a hypoxic, Mediterranean, submarine cave (Abbiati et al. 1994, Southward et
al. 1996) and in Phyllochaetopterus sp. from the Mid Atlantic Ridge (Fabri et al. 2011), however,
suggested a bacterial diet. Likewise the generally low δ15N trophic level of chaetopterids at
arctic hydrothermal vents (Sweetman et al. 2013) also suggested a bacterial diet. Colaço et al.
(2002) reported stable isotopic content of a single putative chaetopterid from the Logatchev vent
field on the Mid Atlantic Ridge, but that specimen appears instead to have been the ampharetid
Amphisamytha lutzi (our impression from their comments at the bottom of p. 403).
Guild membership
C. pugaporcinus is a motile (planktonic), passive suspension feeder; given its geometry and
low turbulence intensities in mid waters, the dominant mechanism of encounter is likely
gravitational deposition onto its mucous web. Other Chaetopterus spp. are obligate, active,
benthic suspension feeders pumping water through a mucus filter. Species in the other genera are
functional active, benthic suspension feeders using mucus filters, functional passive suspension
feeders using palps projecting from the tube, and functional surface deposit feeders with those
palps. Soft-sediment species are infaunal, but some species attach to hard substrata including
tubes of other animals and of conspecifics.
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Research questions and opportunities
• Does layer permeability determine the sediment depth to which chaetopterid tubes with a
single surface opening are built?
• Do the varying pressures that short-wavelength surface waves produce inhibit mucus-bag
feeding in species with variable feeding modes?
• For species that both actively and passively suspension feed, does the proportion of time
spent in active suspension feeding depend on tube inside diameter and thus vary as an
individual grows?
• Is active suspension feeding substantially more energetically expensive in species bearing
one perforated tube end than it is in Chaetopterus?
• In the three genera with two suspension-feeding and one deposit-feeding mode, what
environmental factors determine fraction of time spent in each feeding mode?
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Chrysopetalidae, Phyllodocida
Diversity and systematics
Chrysopetalidae comprise about 80 species distributed among 27 genera, 14 of them monotypic.
They now include members of the former families Calmyzidae (1 sp.) and Nautiliniellidae (~ 20
spp.) that proved to be highly derived chrysopetalids (Aguado et al. 2013).
Free-living Chrysopetalidae, characterized by golden paleal notochaetae (Fauchald & Rouse
1997), fall into two morphotypes, medium-to-large versus small worms (the latter mostly <
1 cm long). The latter include Acanthopale, Dysponetus, Pseudodysponetus and Vigtorniella
that appear in need of revision for lack of monophyly (Olivier et al. 2012). The also small,
commensal species in Subfamily Calamyzinae (that comprise the former families Calmyzidae
and Nautiliniellidae, as short as 5 mm) also need generic revision to produce monophyletic
groupings (Aguado et al. 2013). The striking paleae of free-living chrysopetalids and their
similarity to features of Canadia and Wiwaxia in the Burgess shale generated a great deal of
interest in many aspects of the family for a time, but the relationship does not appear to be close
(Eibye-Jacobsen 2004).
Habitat
Members of the large, free-living morphotype are primarily epibenthic, whereas the small,
free-living morphotype is associated with a variety of substrata (Olivier et al. 2012). The forms
with paleae are most abundant in tropical, shallow waters, but some species are bathyal and
abyssal (Watson Russell 1991). Calamyzinae are either ectoparasitic on ampharetids (monotypic
Calamyzas cf. Aguado et al. 2013) or commensal in the branchial cavities of bivalves that rely on
chemosyntetic bacterial symbionts (the remaining genera). Hence the bivalve commensals are
restricted to environments containing reduced inorganic compounds and oxygen.
Sensory and feeding structures
In the free-living forms, the prostomium is rectangular to rounded. Its anterior bears a pair of
dorsal antennae and a pair of ventral palps. Farther back on the prostomium, up to two pairs of
eyespots may be present, and a single medial antenna is found (Pleijel 2001). Nuchal organs
are (Watson Russell 2000) variable in morphology at the rear of the prostomium as an ovoid
caruncle (Chrysopetalum), a half-moon-shaped nuchal fold (Paleanotus, Treptopale, Arichlidon
& Paleaequor), a thickened ridge (Bhawania) or a pair of ciliated dorsolateral patches (Pleijel
2001). They are apparently absent in Vigtorniella (Dahlgren et al. 2004, Wiklund et al. 2009).
A peristomium is not evident dorsally and is likely restricted to lips around the mouth. The
lower lip projects. The pharynx is muscular and axial. A single (left-right) pair of lateral,
opposed stylets usually tips the everted pharynges of both large and small, free-living forms.
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07 November 2014
Some variability exists among small-bodied species, however. Small individuals of Vigtorniella
flokati carry a pair of hinged stylets whose orientation is difficult to discern from their dissected
structure, but large individuals lack stylets entirely, unusual among Chrysopetalidae, and
suggestive that this species may be an outlier in feeding strategy (Dahlgren et al. 2004). V.
zaikai’s plate-like teeth (Kisseleva 1992) are consistent with feeding on bacterial mats. A distal
ring of papillae may be present on the everted pharynx (Pleijel 2001).
Calamyzinae may lack a median antenna, the paired antennae or the paired palps. Eyes are
absent, and nuchal organs are unknown. The pharynx is axial but not yet described in detail.
Stylets are absent (Pleijel 2001).
Motility
Predators of sessile bivalves, such as Strepternos didymopyton (below), must be motile as must
scavenging species, but direct information on motility in situ is lacking. Wiklund et al. (2009)
observed that Vigtorniella ardabilia was able to move inside bones burrowed by Osedax spp.,
suggesting refuge from predation. Calamyzinae clearly have limited motility; it is not known
whether they change host individuals as adults.
Illustrations
Perkins (1985) provides line drawings of several free-living species from shallow water.
Böggemann (2009) provides photographs and line drawings of several free-living species from
deep water. Dahlgren et al. (2004) provide remarkable photographs of Vigtorniella flokati.
Aguado & Rouse (2011) provide informative photographs and drawings of several genera and
species of bivalve commensals.
Feeding
Epibenthic forms appear to be largely carnivores or scavengers, as stated by F&J, “but might also
be semi-parasitic, feeding, for example, on other invertebrates or algae, possibly piercing and
sucking food material with their muscular eversible proboscis and the terminal stylet-like pair of
jaws” [simply pair of stylets in our terminology] (Böggemann 2009). Very few explicit predatorprey relations have been established for these larger species, however. One exception is Watson
Russell’s (1991) description of Strepternos didymopyton from among the collection of Turner
(1978) who observed that “crysoptellid [sic.], hesionid and polynoid worms were often found
between the valves, obviously feeding on the [wood-boring bivalve] Xylophaga” in her deepsea colonization experiments with wood. The pair of ornamented stylets illustrated by Watson
Russell (1991, p. 291) appears well suited to extracting boring bivalves from their shells. Watson
Russell (2000) also reported finding algal material in the guts of Paleanotus and Treptopale spp.
collected from foliaceous and coralline algae in shallow water.
The small Vigtorniella ardabilia feeds on bacterial mats beneath fish farms and around
whale falls (Wiklund et al. 2009). Wicklund et al. (2009) observed aquarium specimens of V.
ardabilia to feed on bone-dwelling, white, giant, filamentous, sulphide-feeding bacteria, using
their unarmed, eversible pharynges to package the mat into pellets for ingestion. V. zaikai’s
concentration at the oxic-anoxic interface in the Black Sea (Zaika & Sergeeva 2012) and its
plate-like teeth (Kisseleva 1992) suggest a similar diet, but the apparent lack of stylets in adult
V. flokati and oddly articulated stylets in juveniles (Dahlgren et al. 2004) suggest an unusual
diet. Dense clusters of the large worms (up to 4 cm long) hang from the undersides of whale
remains. Dahlgren et al. (2004) suggested that they may be osmotrophic on dissolved material
leaking from the remains, but the geometry of diffusion and advection around such large worms
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makes us doubt this suggestion. Ingestion of bacterially degraded tissue or energy-dense oil
droplets seeping from the remains that are rapidly absorbed and therefore quickly absent from
gut contents seems more likely to explain the match of overhang microhabitat and worm. High
worm abundance argues for high energy density in their food.
Stable isotope data for V. flokati indicate that nutrients are obtained from whale tissue
(Dahlgren et al. 2004). 13C and 15N data were consistent with a parasitic lifestyle for commensal
Vesicomyicola trifurcatus on bivalves, but sulfur isotopic data differed substantially, suggesting
an additional food source for the worm (Van Dover et al. 2003; Dreyer et al. 2004). Juveniles
of clam commensals have been observed to displace clam gill filaments, but no tissue necrosis
is evident (Mills et al. 2005). Becker et al. (2013) collected gill commensals from Calyptogena
spp. and Bathymodiolus heckerae, finding similar δ13C and δ34S values in the hosts and
commensals. δ15N in the commensals, however, ranged from very similar, implying simple
kleptoparasitism, to nearly a trophic level higher for the commensals, suggesting parasitism. As
Becker et al. (2013) point out, however, it is possible that the commensals are feeding on bivalve
secretions rather than their tissues.
Guild membership
We tentatively classify stylet-bearing species as predators; stylets would not appear to be very
useful for obligate scavengers. V. flokati is a scavenger as an adult. Calamyzas amphictenicola
is clearly an ectoparasite. The remaining members of Calamyzinae are parasites, kleptoparasites
or more likely a bit of both.
Research opportunities
• No feeding observations are available for Acanthopale, Dysponetus, or Pseudodysponetus.
• Provision of tracer-containing whale oil under an overhang of (or near) whale remains could
be revealing regarding the diet of V. flokati.
• Stable isotopic data for any of the large, free-living forms are lacking.
References
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annelids, Nautiliniellidae and Calamyzidae (Phyllodocida, Annelida), are a clade of derived
chrysopetalid polychaetes. Cladistics 29:610–28
Aguado MT, Rouse GW. 2011. Nautiliniellidae (Annelida) from Costa Rican cold seeps and a
western Pacific hydrothermal vent, with description of four new species. Syst. Biodivers.
9:109–31
Böggemann M. 2009. Polychaetes (Annelida) of the abyssal SE Atlantic. Org. Divers. Evol.
9:251–428
Dahlgren TG, Glover AG, Baco A, Smith CR. 2004. Fauna of whale falls: systematics and
ecology of a new polychaete (Annelida: Chrysopetalidae) from the deep Pacific Ocean.
Deep-Sea Res. Pt. I 51:1873–87
Dreyer J, Miura T, Van Dover CL. 2004. Vesicomyicola trifurcatus, a new genus and species of
commensal polychaete (Annelida: Polychaeta: Nautiliniellidae) found in deep-sea clams
from the Blake Ridge cold seep. Proc. Biol. Soc. Wash. 117:106–13
Eibye-Jacobsen D. 2004. A reevaluation of Wiwaxia and the polychaetes of the Burgess Shale.
Lethaia 37:317–35
Fauchald K, Rouse G. 1997. Polychaete systematics: past and present. Zool Scr. 26:71–138
Kisseleva MI. 1992. New genus and species of the family Chrysopetalidae (Polychaeta) from the
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Black Sea. Zool. Journ. 71:128–32
Mills AM, Ward ME, Heyl TP, Van Dover CL. 2005. Parasitism as a potential contributor to
massive clam mortality at the Blake Ridge diapir methane-hydrate seep. J. Mar. Biol. Assoc.
UK. 85:1489–97
Olivier F, Lana P, Oliveira V, Worsfold T. 2012. Dysponetus joeli sp. nov. (Polychaeta:
Chrysopetalidae) from the north-east Atlantic, with a cladistic analysis of the genus and a
key to species. J. Mar. Biol. Ass. UK. 92:989–96
Perkins TH. 1985. Chrysopetalum, Bhawania and two new genera of Chrysopetalidae
(Polychaeta), principally from Florida. Proc. Biol. Soc. Wash. 98:856–915
Pleijel F. 2001. Chrysopetalidae Ehlers, 1864. See Rouse & Pleijel 2001, pp. 89–90
Turner RD. 1978. Wood, mollusks, and deep-sea food chains. Bull. Am. Malacol. Union, Inc.
1977:13–9
Van Dover CL, Aharon P, Bernhard JM, Caylor E, Doerries M, et al. 2003. Blake Ridge methane
seeps: characterization of a soft-sediment, chemosynthetically based ecosystem. Deep-Sea
Res. Pt. I 50:281–300
Watson Russell C. 1991. Strepternos didymopyton Watson Russell in Bhaud & Cazaux, 1987
(Polychaeta: Chrysopetalidae) from experimental wooden panels in deep waters of the
western North Atlantic. Ophelia Suppl. 5:283–94
Watson Russell C. 2000. Family Chrysopetalidae. See Beesley et al. 2000, pp. 121–5
Wiklund H, Glover AG, Johannessen PJ, Dahlgren TG. 2009. Cryptic speciation at organic-rich
marine habitats: a new bacteriovore annelid from whale-fall and fish farms in the north-east
Atlantic. Zool. J. Linn. Soc. 155:774–85
Zaika V, Sergeeva N. 2012. Deep-water benthic polychaetes (Vigtorniella zaikai and Protodrilus
sp.) in the Black Sea as indicators of the hydrogen sulfide zone boundary. Vestnik Zoologii
46:e19–e27
Cirratulidae, Cirratuliformia, Terebellida
Diversity and systematics
Cirratulidae comprise about 240 species distributed among 17 genera, 6 of them monotypic.
Inclusion of Flabelligeridae and Ctenodrilidae in Cirratuliformia based on morphological
similarities has been supported by molecular data (Zrzavý et al. 2009; Struck et al, 2011). Recent
molecular evidence suggests that Siboglinidae and Orbiniidae are sister clades to Cirratuliformia
(Weigert et al. 2014). Generic definitions in Cirratulidae have undergone major revision, and
many new species have been described since F&J. With Raricirrus and Pseudocirratulus
removed from Cirratulidae (Petersen & George 1991, Petersen 1994), all genera are currently
discriminated by number and location of ciliated, grooved, dorsal feeding tentacles (either two or
a larger number) and details of their simple chaetae. There are three basic morphotypes: sessile
tube dwellers that live doubled over; muscular, dorsoventrally flattened forms with crowded
abdominal segments; and, species with moniliform midsections and muscular front and back
ends. Here we focus primarily on distinctions among morphotypes rather than on number of
palps or generic definitions. Cirratulidae remain problematic in systematics, but pragmatic
benthic ecologists have arguably benefitted from the system of filing species into genera based on
chaetal characters. We concur with Dean & Blake (2009), however, that—with the exception of
Dodecaceria—the bitentaculate genera of cirratulids are very unlikely to be found monophyletic
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when molecular genetic approaches are applied. Morphotypes cross generic boundaries freely,
and generic names give little insight into feeding guild assignments. Adults range from < 1 to
about 20 cm long.
Habitat
Cirratulids are ubiquitous in soft sediments and dominate many deep-sea macrofaunal
communities numerically. Dodecaceria spp. are also frequent community members on hard
substrata and among macrophytes in shallow water. Some species such as Cirratulus cirratus
live nestled against rocks (Flattely 1916), and Cirriformia moorei is common in heterogeneous
muds with small boulders (KM Dorgan, pers. obs.). More unusual habitats include external
surfaces of sponges (Crozier 1963) and cavities in bones of dead whales (Taboada et al. 2012).
Sensory and feeding structures
Most cirratulids bear a pointed or rounded, roughly conical prostomium. Lateral (usually) or
dorsolateral nuchal organs are present as pits, slits, notches or patches at the posterior of the
prostomium, usually above and usually just anterior to (Blake 2006, Doner & Blake 2006,
Dean & Blake 2009), sometimes just posterior to (Taboada et al. 2012), and sometimes nearly
directly above (Dean & Blake 2007) the mouth. A small number of eyespots may be present but
may not persist in adults. The unarmed, ventral pharynx is eversible as a buccal bulb. Dales
(1962) pointed out similarity between the tongue-like buccal apparatus of cirratulids and of the
meiofaunal Ctenodrilus; molecular data further support a close relationship (Zrzavý et al. 2009).
In bipalpate species, the palps (sometimes called tentacles) insert at the rear of the peristomium.
In species with > 2 palps, they originate on more posterior chaetigers. Species of the following
genera bear more than two feeding palps or tentacles: Cirratulus, Cirriformia, Fauvelicirratulus,
Protocirrineris, and Timarete. All of their numerous segments are muscular and much shorter
than wide. Aphelochaeta, Caulleriella, Chaetozone, Dodecaceria, Monticellina and Tharyx
contain the bipalpate cirratulids, which have more varied morphologies. In other genera, palps
insert dorsally and (or) dorsolaterally, but in Dodecaceria they are lateral.
Motility
Of the bipalpate genera, Dodecaceria has the most consistent lifestyle. Dodecaceria spp.
secrete a mucus whose constituents mineralize to produce a fibrous calcite/aragonite tube that
microscopically bears greater resemblance to stromatolites than to the tubes and shells of other
animals (Fischer et al. 2000). D. carolinae can bore galleries into limestone as well as form
tubes; its typical posture is folded over with both ends protruding from a single opening, and up
to three individuals can occupy a single tube (Aguilar-Camacho & Salazar-Vallejo 2011). D.
meridiana does not appear to bore and in the laboratory will build its calcareous tube in sand,
also adopting the folded-over posture typical of Dodecaceria (Elías & Rivero 2009).
Most unusual are Monticellina species that agglutinate mudballs projecting above the
sediment-water interface (Jumars 1975, M. luticastella; Levin & Edesa 1997, M. sp.). M.
luticastella has a short, blunt peristomium that appears more useful for plugging the opening
of the helical chamber that the worm inhabits than for burrowing. The animal is very weakly
muscularized except for the peristomium and pygidium and lives bent 180˚ over itself, like
Dodecaceria, with both prostomium and pygidium near the mudball entrance (Jumars 1975).
Levin & Edesa (1997) observed a species of Aphelochaeta that built similar concretions. We
tentatively judge the mudball-making species and all Dodecaceria spp. to be sessile.
We consider the remainder of cirratulids to be motile or discretely motile burrowers. Worms
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extend burrows in muds by fracture using peristaltic expansions with the hydrostatic skeleton
to apply dorsoventral forces to burrow walls (Che & Dorgan, 2010a). Cirratulus, Cirriformia,
and Fauvelicirratulus contain some of the largest cirratulids, which tend to be most ovoid or
rectangular in cross section (e.g., Çinar & Petersen 2011) as expected of animals that burrow
by fracture through mud (Dorgan et al. 2006). Worms with this body plan can burrow either
forward or backward (Che & Dorgan 2010a, b, Cirriformia moorei). Protocirrineris and
Timarete contain some smaller species that are often found in groups (Petersen 1991). Smaller
burrowers, such as Timarete punctata (illustrated in Çinar 2007), must be blunter than larger
species to produce the forces necessary to fracture muds (Che & Dorgan 2010a). Observations
of Cirriformia moorei in ant farms and preliminary data of C. moorei burrowing in small
calorimetry chambers filled with mud indicate that worms alternate burrowing with stationary
periods, with burrowing periods ~ 45 min to 1 h followed by sedentary periods of varied lengths
(Dorgan, unpublished observations). Prolonged pauses in burrowing sometimes occurred
near the sediment-water interface with gills extended close to the sediment surface, but also
frequently occurred at depth in ant farms where worms had no apparent access to oxygenated
water. Physiological measurements in Cirriformia moorei implied that burrowing incurs
relatively low cost per unit of time (Dorgan et al. 2011).
Illustrations
Che & Dorgan (2010a, b) provide photographs of forward and backward burrowing, respectively,
by Cirriformia moorei in gelatin. Taken together, Blake (2006), Doner & Blake 2006, Blake &
Dean (2009), and Taboada et al. (2012) through stippled line drawings and scanning electron
micrographs give a good impression of the diversity in shapes and locations of cirratulid nuchal
organs and of anterior morphology in general. Levin and Edesa (1997) show photographs of
mudballs (Fig. 2) and a drawing of the posture of Monticellina sp. (Fig. 5).
Feeding
Although F&J suggested based on the assumed limitations of tentaculate feeding that cirratulids
are surface deposit feeders, evidence suggests that subsurface feeding may be common among
burrowing cirratulids. Larger cirratulids with short, muscular segments and more than two
palps are mostly active burrowers with the head generally held below the sediment-water
interface, although one or more feeding palps may reach the interface (Ronan 1977, Cirriformia
spirabrancha; Shull & Yasuda 2001, C. grandis; Pardo & Amaral 2004, C. filigera). Although
feeding tentacles have been drawn as extending dispersely through the sediment and resting
on the surface to feed (Pardo & Amaral 2004, Shull &Yasuda 2001), tentacles and gills of C.
moorei burrowing through gelatin by fracture extend straight back, filling the lateral edges of
the crack-shaped burrow, and when worms back up, the palps and gills both extend anteriorly
into the previously formed crack (Che & Dorgan, 2010a). We have observed C. moorei in
the field oriented head up with palps and gills extending above the head in a compact region
roughly the diameter of the worm, consistent with feeding on burrow walls. C. grandis from a
Massachusetts estuary had a δ15N similar to that of other deposit feeders (Martinetto et al. 2006),
giving no reason to doubt its source of nutrition.
Feeding by C. grandis produces net downward movement of particles from the surface, and
contrary to expectation in F&J even the largest species show particle size preference (Shull &
Yasuda 2001). Selection experiments presenting a range of glass bead sizes have been done
with Cirriformia grandis (Shull & Yasuda 2001) and more recently with multitentaculate
Timarete hawaiensis and bitentaculate Aphelochaeta honouliuli (Magalhães & Bailey-Brock,
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in manuscript). All three species selected beads in the smallest size category presented. We
caution, however, that peak selection among glass bead sizes may underestimate the modal size
of sediment grains ingested (Guieb et al. 2004). Magalhães & Bailey-Brock (in manuscript)
were also able to observe transfer of particles from the palps to the mouth in T. hawaiensis.
Beads were dropped from the palps near the head of the animal onto the surrounding substratum
and then picked up and ingested by inversion of the pharynx. They noted that in specimens
with all the feeding palps ablated, particle collection continued with branchiae, but that
particle retention was less efficient than when particles were handled by palps. Weidhase et al.
(2014) grew and maintained a population of Cirratulus cf. cirratus > 3 yr on a weekly diet of
zooplankton processed to use as food for corals.
Whereas most cirratulids deposit and detritus feed, Cirratulus balaenophilus occupies
csavities in whale bones and may feed on bacterial films (Taboada et al. 2012). Dark, prolate
spheroidal pellets are evident in the posterior guts of the worms (Fig. 2 of Taboada et al. 2012),
suggesting that the worm feeds on some combination of microbial films and particles that
sediment into and onto the porous bone matrix.
Most Dodecaceria spp. live in hard substrata in shallow water and feed on detrital particles
within reach of their tubes. Flow dynamics and their posture would appear to admit both deposit
and suspension feeding, but the latter has not been reported. Besides ingesting detritus, D.
berkeley individuals devoured all the abalone juveniles within reach ≤ 24 h after their settlement
(Naylor & McShane 1997).
The other bipalpate genera are more heterogeneous in morphologies and lifestyles. The type
species of Aphelochaeta, A. monilaris, has moniliform abdominal segments, but the head and tail
are muscular. Analogy has been drawn to a long train, which requires an engine at the rear if it
is to go backward; pushing backward would derail middle cars or buckle moniliform segments
of a long train or worm, respectively (Jumars et al. 2007). Several other Aphelochaeta species
resemble the body plan of burrowing Cirriformia species, with abdominal segments much
wider than long, and often carry a dorsal crest (e.g., Doner & Blake 2009) that may be useful in
enhancing tensile stresses orthogonal to the cracking plane in burrowing. Aphelochaeta marioni
is the best studied species of the genus and is in the group with moniliform abdominal segments.
Farke (1979) observed it in the laboratory to be a very active burrower that can be reared on
phytoplankton. He noted that it depletes surficial sediments of fine particles, implying the same
kind of particle selectivity and net downward transport seen by Shull & Yasuda (2001). Isotopic
tracer studies, ordination analyses of community structure and manipulative experiments show
A. marioni to be a specialist on benthic diatoms in intertidal habitats (Herman et al. 2000, Van
Colen et al. 2010, Weerman et al. 2011), but it also thrives on organic-rich detritus of various
types (e.g., Tomassetti & Porrello 2005, Brito et al. 2009). A. marioni accumulates unusually
high, whole-body concentrations of arsenic, even in unpolluted environments (Gibbs et al. 1983,
Fattorini et al. 2005, Waring & Mahrer 2005).
There are few observations of life habits or feeding in Caulleriella. In basic body plan its
species belong to the group with crowded (much wider than long) abdominal setigers. Mud
dwellers may be somewhat ovoid in cross section (e.g., Magalhães & Bailey-Brock 2013,
Caulleriella cordiformia), but members of the genus typically have large spaces between notoand neuropodia, and sand dwellers are more circular in cross section (Dean & Blake 2007). A
groove of unknown function may be present midventrally (Doner & Blake 2006, C. cordiformia;
Elías & Rivero 2008, C. bremecae & C. galeanoi) or mid dorsally (Dean & Blake 2007, C.
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moralesensis). Most species appear to deposit feed, but C. galeanoi, a species so far known
only from aquaria supplied with seawater from the intertidal, is a herbivore on Vaucheria sp., a
filamentous yellow-green alga (Elías & Rivero 2008). Under 1 cm long, this species likely is too
small to subsist on the dilute resources used by deposit feeders.
Chaetozone also belongs in the group with crowded abdominal segments, but its posterior
segments are accordion shaped, thinnest between segments and widest at the cincture of spines,
tapering gradually to the pygidium (Chambers 2000). Posterior segments may be mildly
moniliform. The type species, C. setosa, in the Bay of Brest reaches peak densities in sediments
that are 10 - 11% organic matter by weight (Hily 1987). In a stable isotopic study of the food
web in Canada Basin, Iken et al.(2005) found bathyal C. setosa to have a 13C signature closer
to that of fresh phytodetritus than did any other species of polychaete, providing evidence of
selective surface deposit feeding. Similarly, Chaetozone cf. setosa from 100 m water depth in
Hornsund, Spitsbergen, was less enriched in 15N than the other surface deposit feeder reported,
Ampharete sp. (Ampharetidae, Sokołowski et al. 2014). The manner of deployment of the
prominent spines during burrowing has not been observed. In preserved specimens they usually
project orthogonal to the axis of the worm, but even a slight inclination to the body axis could
bias forward or backward progress as the accordion is stretched and compressed. The epidermis
appears tautly stretched over the proximal portion of the spines, suggesting that they might
act (tent-pole like) to help the worm resist elastic rebound of the sediment without resorting
to the maintenance of high internal hydrostatic pressure. Cinctures of spines are developed to
extraordinary degree in the bathyal species, C. palaea (Blake 2006).
Whereas most cirratulids have a simple, tubular gut, sometimes with some helical coiling
or zig-zagging in the posterior half of the body to accommodate a gut somewhat longer than
the body, C. brunnea has a distinctive, enlarged stomach roughly one-third of the distance
from the prostomium to the pygidium. Just behind the stomach, ingested sediments are formed
into spherical pellets that pass backward, one per segment (Blake 2006), in a manner highly
reminiscent of Capitella spp. Not all Chaetozone spp. live in sediments. One species, C. nr.
corona, lives as a homochromic commensal on the sponge Microciona prolifera. Apparently
a detritivore, it surrounds itself with “used” detritus that it collects from the sponge’s surface
(Crozier 1963).
Various generic revisions have depopulated the ranks of Tharyx, leaving few recent studies
to cite. Most remaining Tharyx spp. appear to belong to the group of cirratulids with crowded
abdominal setigers, but at least two species, T. tumulosa (Magalhães & Bailey-Brock 2013)
and T. kirkegaardi (Blake 1991) have moniliform segments in their midsections. Bolam (2011)
reported that a species of Tharyx showed weak ability to survive burial, but the lack of species
identification limits the information gain from that observation. T. acutus from a Massachusetts
estuary had a δ15N signature similar to other deposit feeders (Martinetto et al. 2006).
Monticellina species can have either crowded or moniliform segments, and they display even
greater variety in body plans than species of Aphelochaeta. Most have muscular anterior and
posterior segments that appear well suited to burrowing (Blake 1996, Dean & Blake2009). Three
species (M. cryptica, M. elongata & M. giribeti) from shallow-water sands have peristomia that
are longer (relative to width) than those of mud-dwelling species (Dean & Blake 2009); this
morphological difference may reflect adaptation to media with different mechanical properties.
Whereas most shallow-water cirratulids appear to concentrate near the sediment-water
interface, Monticellina baptisteae at bathyal depths does not, with over two-thirds of individuals
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recovered > 2 cm below the sediment-water interface (Blake 1994). This species dominates
shelf communities off the northeastern U.S. as well, including Georges Bank (Blake 1991). It
has about 100 chaetigers and a notably expanded and muscular thorax with conspicuous ventral
glands and a posterior that is muscular and rectangular in cross section,with the middle segments
somewhat moniliform (Blake 1991), suggesting that it burrows well both forward and backward.
The mudball-inhabiting M. luticastella by contrast is a highly specialized surface deposit feeder,
with > 80% of its body volume occupied by the gut (Penry & Jumars 1990).
Contrary to F&J, there do appear to be subsurface deposit feeders among the cirratulids,
including the most common slope species in the western Atlantic, M. baptisteae (Blake 1991,
1994). Based on labeling experiments, surface deposit-feeding cirratulids appear to be among
the first and most selective to ingest fresh phytodetritus arriving in deep water (Levin et al. 1999,
Aberle & Witte 2003, Iken et al. 2005, Sweetman & Witte 2008, Hunter et al. 2012). At the
same time, there are subsurface-dwelling and -feeding individuals with signatures isotopically
distinct from surface deposit-feeding forms (Witte et al. 2003, Gontikaki et al. 2011). Without
this isotopic information it would be difficult to discredit the idea that all cirratulids are
surface feeders, but that some succeed in retracting or digging further into tubes or burrows
before samples can be vertically sectioned. Recently Cosentino (2013) documented some
deep burrowing (> 10 cm) by both Caulleriella bioculata and Cirriformia tentaculata. More
surprisingly, she documented such deep burrowing as well by juveniles of an unknown cirratulid
species into an artificial substratum.
Guild membership
We provisionally classify Dodecaceria and mudball-constructing cirratulid species as
sessile, surface deposit feeders, although we would not be surprised to find some capacity in
Dodecaceria to suspension feed passively. Rock- and crevice-nestling cirratulids (F&J) may
be discretely motile surface deposit feeders or detritivores by virtue of locating in microhabitats
with large fluxes of particulate material.
We suspect most species of cirratulids to be motile deposit feeders over a depth range
of several centimeters that includes the sediment-water interface and to feed from both the
sediment-water interface and their burrow walls. This behavior has been documented, however,
for only a few species of Cirriformia. Absent species-specific observations, a sensible default
may be to classify non-mudball-building, soft-sediment cirratulids as 50% surface and 50%
subsurface deposit feeders. In some species, however, the depth range of burrowing may not
usually include the sediment-water interface. Monticellina baptistae is such a specialist on
deeper deposits (100% subsurface). A few cirratulids do not deposit feed but have specialized
on a richer diet by occupying a particular habitat (Cirratulus balaenophilus in whale bones) or
feeding herbivorously at the sediment-water or rock-water interface (Caulleriella galeanoi) or
detritivorously on sloughed sponge detritus (Chaetozone. nr. corona).
Research questions and opportunities
• Do Dodecaceria spp. suspension feed?
• How do burrowing and feeding habits of moniliform species differ from those with short
chaetigers? Do they differ in gut volumes, assimilation efficiencies or gut residence times?
• How are spine cinctures deployed in burrowing Chaetozone?
• Do the vertically burrowing cirratulids in water depths where visual predators operate feed
preferentially at the sediment-water interface at night, and deeper during the day?
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A77
Cirratulidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
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Cirratulidae
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Dorgan KM, Jumars PA, Boudreau BP, Johnson BD. 2006. Macrofaunal burrowing: The medium
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Jumars, Dorgan & Lindsay
07 November 2014
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to POM enrichment: an in-situ experimental study. Mar. Ecol. Prog. Ser. 251:27–36
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Cossuridae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Cossuridae
Diversity and systematics
Cossuridae comprises about two dozen species in the single genus Cossura. We follow Read’s
(2000) opinion that other named genera in the family are junior synonyms. Cossura spp.
are relatively long and skinny, with most species > 1 but < 5 cm long. Their position within
annelids is still uncertain. Several authors have found close relation with Scalibregmatidae and
Opheliidae (Rouse & Fauchald 1997, Bleidorn 2005, Rousset et al. 2007), but a more recent
assessment suggests closer affiliation with Paraonidae and Fauveliopsidae (Zrzavý et al. 2009).
Habitat
Cossurids are eurybathic in soft sediments. They are prominent members of many bathyal
communities and can be numerical dominants in organic-rich settings (e.g., Gaston 1985,
Wheatcroft 2006, Sellanes et al. 2007, Levin et al. 2009). In bathyal settings it is not unusual to
have more than one abundant species of Cossura, with evidence of vertical stratification in their
distributions within the sediments (Jumars 1978, Blake 1994).
Sensory and feeding structures
Cossurids have muscular anteriors, a prostomium tapering to a sharp or rounded tip or extended
laterally as horns (Liñero-Arana & Díaz-Díaz 2010), a distinct peristomium comprising two
complete rings, and a single, mid-dorsal tentacle, thought to serve primarily in respiration and
not feeding (Rouse 2001). Eyes are absent, but lateral nuchal organs are present as ciliated pits
or grooves at the posterior of the prostomium. Tzetlin (1994) and Purschke & Tzetlin (1996)
illuminated the simple, muscular, axial pharynx, lacking dorsolateral folds. When everted it is
tipped by buccal tentacles having the appearance and approximate number of “tentacles” of two
to four, clasped, miniature, fuzzy (heavily ciliated) gloves. Whereas buccal tentacles of Armandia
(Opheliidae) have considerable coelomic space and presumably are inflated by hydrostatic
pressure, buccal tentacles of Cossura are muscular with little coelomic space (Tzetlin & Zhadan
2009). Juveniles have unbranched, very heavily ciliated pharynges (Zhadan et al. 2012).
Motility
We infer from morphology and depth distribution that cossurids are motile. They cannot reach
much food without moving. They have a muscular anterior anatomy consistent with burrowing
by fracture. Lateral horns when present (i.e., Liñero-Arana & Díaz-Díaz 2010, C. ginesi) are
consistent with energy-efficient crack extension through side-to-side motion (Dorgan et al. 2008).
Although not as balanced in robustness as the front and back ends of moniliform cirratulids, a
somewhat muscular hind end also suggests some backward burrowing capability (cf. Jumars et
al. 2007, Che & Dorgan 2010).
Illustrations
Rouse (2001) provides informative stippled line drawings and scanning electron micrographs of
cossurid morphology. Zhadan et al. (2012) provide remarkable scanning electron micrographs
including the buccal tentacles and nuchal organs in their redescription of C. pygodactyla.
Feeding
So far as we can tell, no one has reported observations of a live cossurid feeding. In bathyal
and shallow-water specimens we have observed (PA Jumars, unpublished) sediments in the
gut lumen through the body wall. Others have made similar observations on shallow-water
specimens (Liñero-Arana & Díaz-Díaz 2010). Tzetlin (1994) illustrated a hypothetical cossurid
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Cossuridae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
surface deposit feeding with its oral tentacles as it extended from a burrow onto the sedimentwater interface. Subsequent advances in understanding of fracture mechanics in sediments
(Dorgan et al. 2006; Jumars et al. 2007) and reported depth-frequency distributions of cossurids
in sediments (Jumars 1978, Blake 1994, Gutiérrez et al. 2000, Wheatcroft 2006) make us
confident that cossurids rarely feed at the sediment-water interface but instead use the tentacles
to “mop up” particles from fractured surfaces when they propagate cracks in the act of burrowing
through sediments, but direct evidence is still lacking.
Kędra et al. (2012) reported a δ15N value for a single individual of C. longocirrata from
Kongsfjorden, Svalbard, collected under 15 m of water. It was consistent with values observed
in other deposit feeders, slightly higher than a pectinariid and orbiniids but lower than cirratulids
and an ampharetid. Supporting δ13C data indicate similar carbon sources across these taxa. An
indication of the value of additional stable isotopic data is the other single datum (again one
worm) provided by Levin et al. (2009) from a currently inactive hydrothermally produced sulfide
deposit at Manus Basin (1430–1634 m water depth) near, Papua, New Guinea. Cossura sp. had
δ15N nearly 12‰ higher than Heteromastus sp. (Capitellidae) at the same site without much
difference in δ13C. Cossura sp. from a hydrothermal vent field in the Costa Rican margin, by
contrast was highly depleted in 13C, suggesting feeding on organic matter produced by aerobic
methanotrophs (Levin et al. 2012). Cossura spp. are prevalent in oxygen minimum zones,
making the reasons for the high variances among species and locations all the more interesting.
Microbial transformations and selectivity of food and feeding depths are likely to underlie
the huge differences, but details, possible alternative explanations, and data from additional
specimens and sediment depths are still lacking.
Guild membership
We conjecture that cossurids are motile, subsurface deposit feeders using their short but muscular
oral tentacles to free and ingest sediments from their burrow walls.
Research opportunities
• Any direct feeding observations would be the first.
• Deep burrowing in oxygen-poor sediments suggests an interesting respiratory physiology.
• Use of a muscular pharynx in deposit feeding is somewhat unusual, suggesting a comparison
in selectivity and diet with other burrowing species.
• Additional stable isotope data would be informative.
• The hypothesis that deeper-dwelling (in the sediments) cossurids show higher 15N
enrichments could be tested, e.g., at the sites studied by Jumars (1978) and Blake (1994).
References
Blake JA. 1994. Vertical distribution of benthic infauna in continental slope sediments off Cape
Lookout, North Carolina. Deep-Sea Res., Pt. II 41:919–27
Bleidorn C. 2005. Phylogenetic relationships and evolution of Orbiniidae (Annelida, Polychaeta)
based on molecular data. Zool. J. Linn. Soc. 144:59–73
Che J, Dorgan KM. 2010. Mechanics and kinematics of backward burrowing by the polychaete
Cirriformia moorei. J. Exp. Biol. 213:4272–7
Dorgan KM, Arwade SR, Jumars PA. 2008. Worms as wedges: Effects of sediment mechanics on
burrowing behavior. J. Mar. Res. 66:219-54
Dorgan KM, Jumars PA, Johnson BD, Boudreau BP. 2006. Macrofaunal burrowing: the medium
is the message. Oceanogr. Mar. Biol. Ann. Rev. 44:85–121
Gaston GR. 1985. Effects of hypoxia on macrobenthos of the inner shelf off Cameron, Louisiana.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Estuar. Coast. Shelf Sci. 20:603–13
Gutiérrez D, Gallardo VA, Mayor S, Neira C, Vásquez C, et al. 2000. Effects of dissolved
oxygen and fresh organic matter on the bioturbation potential of macrofauna in sublittoral
sediments off Central Chile during the 1997/1998 El Niño. Mar. Ecol. Prog. Ser. 202:81–99
Jumars, P.A. 1978. Spatial autocorrelation with RUM (Remote Underwater Manipulator):
vertical and horizontal structure of a bathyal benthic community. Deep-Sea Res. 25:589–604
Kędra M, Kuliński K, Walkusz W, Legeżyńska J. 2012. The shallow benthic food web structure
in the high Arctic does not follow seasonal changes in the surrounding environment. Estuar.
Coast. Shelf Sci. 114:183–91
Levin LA, Mendoza GF, Konotchick T, Lee R. 2009. Macrobenthos community structure and
trophic relationships within active and inactive Pacific hydrothermal sediments. Deep-Sea
Res., Pt. II 56:1632–48
Levin LA, Orphan VJ, Rouse GW, Rathburn AE, Ussler W, et al. 2012. A hydrothermal seep on
the Costa Rica margin: middle ground in a continuum of reducing ecosystems. Proc. Roy.
Soc. B doi:rspb20120205
Liñero-Arana I, Díaz-Díaz Ó. 2010. A new species of Cossuridae (Annelida: Polychaeta) from
Venezuela. Interciencia-Caracas 35:789–92
Purschke G, Tzetlin AB. 1996. Dorsolateral ciliary folds in the polychaete foregut: structure,
prevalence and phylogenetic significance. Acta Zool. 77:33–49
Read GB. 2000. Taxonomy and distribution of a new Cossura species (Annelida: Polychaeta:
Cossuridae) from New Zealand. Proc. Biol. Soc. Wash. 113:1096–110
Rouse GW. 2001. Cossuridae Day, 1963. See Rouse & Pleijel 2001, pp. 46–8
Rouse GW, Fauchald K. 1997. Cladistics and polychaetes. Zool. Scr. 26:139-204
Rousset V, Pleijel F, Rouse GW, Erséus C, Siddall ME. 2007. A molecular phylogeny of annelids.
Cladistics 23:41–63
Sellanes J, Quiroga E, Neira C, Gutiérrez D. 2007. Changes of macrobenthos composition under
different ENSO cycle conditions on the continental shelf off central Chile. Cont. Shelf Res.
27:1002–16
Tzetlin AB. 1994. Fine morphology of the feeding apparatus of Cossura sp. (Polychaeta,
Cossuridae) from the White Sea. Mém. Mus. Natl. Hist. Nat., Sér. A Zool. 162:137–43
Tzetlin A, Zhadan A. 2009. Morphological variation of axial non-muscular proboscis types in the
Polychaeta. Zoosymposia 2:415–27
Wheatcroft RA. 2006. Time-series measurements of macrobenthos abundance and sediment
bioturbation intensity on a flood-dominated shelf. Prog. Oceanogr. 71:88–122
Zhadan AE, Vortsepneva EV, Tzetlin, AB. 2012. Redescription and biology of Cossura
pygodactylata Jones, 1956 (Polychaeta: Cossuridae) in the White Sea. Invertebr. Zool. 9:11525
Zrzavý J, Říha P, Piálek L, Janouškovec J. 2009. Phylogeny of Annelida (Lophotrochozoa): totalevidence analysis of morphology and six genes. BMC Evol. Biol. 9:189, 14 pp.
Ctenodrilidae, Cirratuliformia, Terebellida
Diversity and systematics
Ctenodrilidae comprises 3 genera with 3 species each. Genera correspond with morphotypes.
Long considered related to Cirratulidae, recent molecular analyses have placed Ctenodrilids
within Cirratulidae (Rousset et al. 2007) or polyphyletic within Cirratulidae and Opheliidae
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
(Bleidorn et al. 2003), indicating that taxonomic revision is needed. Inclusion within
Cirratulidae would indicate a secondary loss of feeding tentacles and a change in feeding
behavior and likely diet in these small-bodied (possibly progenetic) worms. Hence we find it
more convenient to deal with Ctenodrilidae as a separate family. Members of Ctenodrilus are
grub like and generally < 5 mm long. Raphidrilus spp. are more elongate (larger in ratio of
length to diameter), tend to taper toward the rear and be most muscular in the head region, but
are still quite small (< 7 mm long). Raricirrus spp. are the longest of the ctenodrilids, 0.7 to 1.7
cm long as adults (Petersen & George 1991, Dean 1995), have a moniliform midsection and a
very muscular hind end. R. beryli is the largest known species.
Habitat
Predictably, as small worms, they are found in organically enriched environments, including
marine oil fields (e.g., ME Petersen & George 1991, Raricirrus beryli), near sewage outfalls
(Magalhães et al. 2011, Raphidrilus hawaiiensis), on an experimental whale fall at 125 m water
depth in Kosterfjord, Sweden (JM Petersen et al. 2012, R. beryli) and in experimental deep-sea
enrichments placed in the vicinity of mud volcanoes in the Gulf of Cádiz (Cunha et al. 2013, R.
beryli). Specifically, R. beryli was found on wood enrichments at water depths of 300 and about
1,000 m and on alfalfa enrichments at the latter depth.
Sensory and feeding structures
Ctenodrilids lack appendages and eyespots on their rounded, conical prostomia. A pair of lateral
nuchal organs in the form of pits or slits are located at the rear of the prostomium in Ctenodrilus
and Raphidrilus, but are more variable in Raricirrus, being larger, more complex and more
exposed in Raricirrus beryli (Petersen & George 1991). Rouse (2001) indicated that the
peristomium forms a complete ring, not just the lip region surrounding the mouth. As is typical
with small worms, the pharynx is ventral (Purschke 1988). The lower lip is eversible.
Motility
We classify ctenodrilids as motile. They lack appendages with which to forage at any substantial
distance without moving.
Illustrations
Magalhães et al. (2011) provide an effective combination of line drawings and light and
electron micrographs to show the sensory and feeding structures of Raphidrilus harperi and R.
hawaiiensis, including several depictions of the everted lower lip. Purschke (1988) provides
much more detailed illustrations of the pharyngeal morphology and ultrastructure in Ctenodrilus
serratus. A simple light micrograph in Westheide et al. (2003, Fig. 1) effectively displays the
grub-like shape typical of this genus. Petersen & George (1991) with line drawings and scanning
electron micrographs document the morphology of 2 spp. of Raricirrus.
Feeding
Moore (1991) examined gut contents of Raricirrus beryli in an oil field and found this species
to select sand grains larger than the local median grain size. Moore (1991) suggested that it is
a subsurface feeder. We suspect that it is highly selective for organic coatings on those grains
(e.g., diatoms) and thus most likely to be found near the sediment-water interface. R. beryli
reported from a whale fall by Petersen et al. (2012) was incorrectly classified as a terebellid. All
nine specimens probed after multiple rinses had sulfur-oxidizing symbionts closely related to
those found in vent mussels (Petersen et al. 2012), but their role, if any, in nutrition is not clear.
Raphidrilus hawaiiensis reached its highest reported densities on the invasive alga Gracilaria
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Ctenodrilidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
salicornia (Magalhães et al. 2011), perhaps grazing on epiphytes.
Guild membership
We tentatively classify ctenodrilids as highly selective feeders on microbial films and rich
organic detritus. Based on morphology and references in F&J, we suspect that Ctenodrilus spp.
are primarily epibenthic on a variety of substrata. Based on the information in Magalhães et al.
(2011) and Monticellini (1910) we suggest that Raphidrilus spp. can be epifaunal, interstitial or
may have modest ability to burrow forward. Raricirrus spp. may be more adept at burrowing
both forward and especially backward, and the largest individuals may be able to deposit feed.
Research opportunities
• Ctenodrilids as opportunists may be relatively easy to culture for experiments on growth
efficiency on various substrates.
• The observation of sand ingestion suggests experiments with growth efficiency on sediments
of varying grain sizes but similar food qualities.
• Sizes and habitats suggest that it would be informative to test Raricirrus beryli with a variety
of methods for ontogentic diet shifts (e.g., Hentschel 1998a, b)
References
Bleidorn C, Vogt L, Bartolomaeus T. 2003. New insights into polychaete phylogeny (Annelida)
inferred from 18S rDNA sequences. Mol. Phylogenet. Evol. 29:279–88
Cunha MR, Matos FL, Génio L, Hilário A, Moura CJ, et al. 2013. Are organic falls bridging
reduced environments in the deep sea? - Results from colonization experiments in the Gulf
of Cádiz PLoS ONE 8:e76688, 17 pp.
Dean HK. 1995. A new species of Raricirrus (Polychaeta: Ctenodrilidae) from wood collected in
the Tongue of the Ocean, Virgin Islands. Proc. Biol. Soc. Wash. 108:169–79
Hentschel BT. 1998a. Spectrofluorometric quantification of neutral and polar lipids suggests a
food-related recruitment bottleneck for juveniles of a deposit-feeding polychaete population.
Limnol. Oceanogr. 43:543–9
Hentschel BT. 1998b. Intraspecific variations in δ13C indicate ontogenetic diet changes in
deposit-feeding polychaetes. Ecology 79:1357–70
Magalhães WF, Bailey-Brock JH, Davenport JS. 2011. On the genus Raphidrilus Monticelli,
1910 (Polychaeta: Ctenodrilidae) with description of two new species. Zootaxa 2804:1–14
Monticelli, F. S. 1910. Raphidrilus nemasoma Montic. Nuovo Ctendorilide del Golfo di Napoli.
Revisione de’ Ctenodrilidi. Archivio Zoologico, pubblicato sotto gli auspicii della Unione
Zoologica Italiana 4:401–36
Moore DC. 1991. Raricirrus beryli Petersen & George (Ctenodrilidae): A new polychaete
indicator species for hydrocarbon polluted sediments. Ophelia Suppl. 5:477–86
Petersen JM, Wentrup C, Verna C, Knittel K, Dubilier N. 2012. Origins and evolutionary
flexibility of chemosynthetic symbionts from deep-sea animals. Biol. Bull. 223:123–37
Petersen ME, George JD. 1991. A new species of Raricirrus from northern Europe with notes on
its biology and a dicussion of the affinities of the genus (Polychaeta: Ctenodrilidae). Ophelia
Suppl. 5:185–208
Purschke G. 1988. Anatomy and ultrastructure of ventral pharyngeal organs and their
phylogenetic importance in Polychaeta (Annelida). Zoomorphology 108:119–35
Rouse GW. 2001. Ctenodrilidae Kennel, 1882. See Rouse & Pleijel 2001, pp. 216–9
Rousset V, Pleijel F, Rouse GW, Erséus C, Siddall ME. 2007. A molecular phylogeny of annelids.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A85
Ctenodrilidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Cladistics 23:41–63
Westheide W, Haß-Cordes E, Krabusch M, Müller M. 2003. Ctenodrilus serratus (Polychaeta:
Ctenodrilidae) is a truly amphi-atlantic meiofauna species—evidence from molecular data.
Mar. Biol. 142:637–42
Dinophilidae
Diversity and systematics
Dinophilidae are very small worms (< 0.5 mm long), formerly termed archiannelids. To date
they comprise 1 species of Apharyngtus, 10 of Dinophilus, and 4 of Trilobodrilus. Dinophilids
are assumed to have a progenetic origin, but with uncertain phylogenetic placement. They
have most often been suspected to be progenetic dorvilleids as detailed by Eibye-Jacobsen &
Kristensen (1994), an opinion shared in the most recent polychaete textbooks (Pleijel 2000,
Paxton 2001), but not universally held (Struck 2006). Molecular methods, however, have failed
to show an affiliation with Dorvilleidae (Struck et al. 2002, 2005; Zrzavý et al. 2009).
Habitat
Dinophilids have been found in sands and muds and among algae, but most frequently as
interstitial members of beach faunas. We are unaware of any deep-water records.
Sensory and feeding structures
Head appendages are absent. Shallow nuchal organs are present on the anterior (Purschke 1997).
A pair of eyespots may be present. The ventral pharynx is muscular and eversible in most
species in Dinophilus and Trilobodrilus. It is similar in orientation and geometry in Apharyngtus
but neither muscular nor eversible (Rieger & Rieger 1975). Jaws and teeth are lacking in all
three genera (Eibye-Jacobson & Kristensen 1994).
Motility
Dinophilids move by ciliary gliding.
Illustrations
Rieger & Rieger (1975, Fig. 1, 2) provide informative stippled line drawings of the anterior of
Trilobodrilus in dorsal and lateral views. Line drawings of two species of Dinophilus are found
at <http://species-identification.org/>
Feeding
More recent publications do not alter the generalizations in F&J that dinophilids use a tonguelike, eversible pharynx to feed on bacteria, protozoans, unicellular algae, and detritus, but
virtually all the published information to date comes from the genus Dinophilus. D. gyrocilatus
can be reared on a wide variety of diets, from spinach to fish food (Prevedelli & Simonini 2001),
but natural Dinophilus diets comprise high-food-value microbiota such as diatoms (Jennings &
Donworth 1986, D. taeniatus). D. gyrocilatus has been widely used in toxicity testing, and there
may be some dietary information in the observation that it is susceptible to dinoflagellate toxins
(Simonini et al. 2011). Little is published on diets in the other two genera, Trilobodrilus and
Apharyngtus.
Guild membership
Dinophilids are motile specialists on microbial films, diatoms, other protists and rich detritus
on which they feed with an unarmed pharynx that (except in Apharyngtus) is muscular and
eversible.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Dinophilidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Research opportunities
• No feeding information appears to be available for Apharyngtus or Trilobodrilus.
• Variation in pharyngeal morphology makes a comparison of feeding between Apharyngtus
and the other genera particularly interesting.
• The ability to culture some species makes investigation of nutritional requirements much
more feasible.
References
Eibye-Jacobsen D, Kristensen RM. 1994. A new genus and species of Dorvilleidae (Annelida,
Polychaeta) from Bermuda, with a phylogenetic analysis of Dorvilleidae, Iphitimidae and
Dinophilidae. Zool. Scr. 23:107–31
Jennings JB, Donworth PJ. 1986. Observations on the life cycle and nutrition of Dinophilus
taeniatus Harmer 1889 (Annelida: Polychaeta). Ophelia 25:119–37
Paxton H. 2001. Family Dorvilleidae. See Beesley et al. 2001, pp. 91–4
Pleijel F. 2000. Dorvilleidae Chamberlin, 1919. See Rouse & Pleijel 2000, pp. 158–159
Prevedelli D, Simonini R. 2001. Effects of diet and laboratory rearing on demography of
Dinophilus gyrociliatus (Polychaeta: Dinophilidae). Mar. Biol. 139:929–35
Purschke G. 1997. Ultrastructure of nuchal organs in polychaetes (Annelida)—new results and
review. Acta Zool. 78:123–43
Rieger RM, Rieger GE. 1975. Fine structure of the pharyngeal bulb in Trilobodrilus and its
phylogenetic significance within Archiannelida. Tissue Cell 7:267-79
Simonini R, Orlandi M, Abbate M. 2011. Is the toxic dinoflagellate Ostreopsis cf. ovata harmful
to Mediterranean benthic invertebrates? Evidences from ecotoxicological tests with the
polychaete Dinophilus gyrociliatus. Mar. Environ. Res. 72:230–3
Struck TH. 2006. Progenetic species in polychaetes (Annelida) and problems assessing their
phylogenetic affiliation. Integr. Comp. Biol. 46:558–68
Struck, TH, Halanych KM, Purschke G. 2005. Dinophilidae (Annelida) is most likely not a
progenetic Eunicida: Evidence from 18S and 28S rDNA. Mol. Phylogen. Evol. 37:619–23
Struck TH, Westheide W, Purschke G. 2002. Progenesis in Eunicida (‘‘Polychaeta,’’ Annelida)—
separate evolutionary events? Evidence from molecular data. Mol. Phylogen. Evol. 25:
190–9
Zrzavý J, Říha P, Piálek L, Janouškovec J. 2009. Phylogeny of Annelida (Lophotrochozoa): totalevidence analysis of morphology and six genes. BMC Evol. Biol. 9:189, 14 pp.
Diurodrilidae
Diversity and systematics
Diurodrilidae comprise 6 species in the genus Diurodrilus with adults < 0.5 mm long. They
are former archiannelids that, like dinophilids, have sometimes been grouped with dorvilleids
(Pleijel 2001), or more generally with eunicidans (Paxton 2000). Detailed anatomical
study raised questions about their membership in Class Polychaeta and even in Phylum
Annelida. They lack chaetae, parapodia, and segmentation. Numerous anatomical features
(e.g., the nervous system) differ from (other) annelids (Worsaae & Rouse 2008). Analysis of
mitochondrial genomes, however, points to a basal position in Annelida and is compatible with a
progenetic origin of the family (Golombek et al. 2013).
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Diurodrilidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Habitat
Diurodrilids are typically interstitial in beach sands.
Sensory and feeding structures
The prostomium is divided by two annular constrictions into three sections that precede the
peristomium. Head appendages and nuchal organs are absent; sensory ciliophores in the anterior
region likely serve a similar function but are not true nuchal organs (Worsaae & Rouse 2008). A
muscular, ventral, pharyngeal bulb is present. A prepharyngeal gland lies anterior to the mouth,
and two salivary glands lie behind it. Diurodrilids carry numerous (presumably mechano- and
chemo-) sensory cilia (Kristensen & Niilonen 1982, Paxton 2000).
Motility
Diurodrilids move by ciliary gliding, and they have head and “toe” adhesive glands (Worsaae &
Rouse 2008). Species exhibit distinct zonations on sandy beaches; differences in adhesive organ
morphology are consistent with species distributions (Villora-Moreno 1996).
Illustrations
Kristensen & Niilonen (1982) provide extensive and informative stippled line drawings and
photographs of Diurodrilus westheidei. External morphology and internal anatomy are well
documented in drawings and micrographs of Diurodrilus spp. by Worsaae & Rouse (2008).
Feeding
Diurodrilus westheidei feeds by using prostomial ciliophores “as a broom to collect small detrital
particles” (Kristensen & Niilonen 1982), an observation repeated for an Australian D. sp. & D.
subterraneus by Worsaae & Rouse (2008). Chandrasekhara Rao & Ganapati (1968) suggested
that the diet of D. minimus & D. benazzi also includes bacteria and small protists.
Guild membership
Diurodrilids are motile specialists on microbial films, diatoms, other protists and rich detritus.
Research opportunities
• Potential differences in feeding behaviors among habitats have not been explored.
• Selectivity and effectiveness of ciliophores in guiding feeding on a variety of potential foods
remain to be determined.
References
Chandrasekhara Rao G, Ganapati PN. 1968. On some archiannelids from the beach sands of
Waltair Coast. Proc Indian Acad. Sci., Sect. B 67:24–30
Golombek A, Tobergte S, Nesnidal MP, Purschke G, Struck TH. 2013. Mitochondrial genomes to
the rescue—Diurodrilidae in the myzostomid trap. Mol. Phylogenet. Evol. 68:312–26
Kristensen RM, Niilonen T. 1982. Structural studies on Diurodrilus Remane (Diurodrilidae fam.
n.), with description of Diurodrilus westheidei sp. n. from the Arctic interstitial meiobenthos,
W. Greenland Zool. Scr. 11:1–12
Paxton H. 2000. Family Dorvilleidae. See Beesley et al. 2001, pp. 91–4
Pleijel F. 2001. Dorvilleidae Chamberlin, 1919. See Rouse & Pleijel 2001, pp. 158–9
Villora-Moreno S. 1996. Ecology and distribution of the Diurodrilidae (Polychaeta), with
redescription of Diurodrilus benazzii. Cah. Biol. Mar. 37:99–108
Worsaae K, Rouse GW. 2008. Is Diurodrilus an annelid? J. Morphol. 269:1426–55
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Dorvilleidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Dorvilleidae, Eunicida
Diversity and systematics
The number of genera in Dorvilleidae has more than doubled since F&J (Eibye-Jacobson &
Kristensen 1994), and known species now number about 200. Of 37 genera, over half are
monotypic, with only 5 comprising 10 or more species. Members of Ophryotrocha, the most
speciose and ubiquitous genus, are surprisingly closely related to Iphitime, which was previously
in a separate family (Heggøy et al. 2007). Ophryotrocha is paraphyletic, Iphitime, Palpiphitime
and Exallopus falling within the Ophryotrocha clade (Wiklund et al. 2012). Palpiphitime has
been made a junior synonym of Ophryotrocha (Wiklund et al. 2012), with further revisions
anticipated. Contrary to previous conclusions based on jaw morphology, dorvilleids do not
appear to be a basal group in Eunicida (Struck et al. 2006). They range in length from 250 µm
(Eibye-Jacobson & Kristensen 1994 ) up to about 10 cm (Paxton 2000).
Habitat
Small dorvilleids have long been associated with sewage and other organic-rich settings (e.g.,
Gray et al. 1979, Reish 1980, Cardell et al. 1999). In an ordination of communities surrounding
the historical White’s Point sewage outfall off Los Angeles, Smith & Greene (1976, their Fig.
8) noted that an unidentified dorvilleid was by far the most strongly associated invertebrate with
high organic nitrogen and sulfide levels in the sediments. It thus is not surprising that dorvilleids
are prominent members of oxygen minimum-zone (Levin 2003), cold-seep (e.g., Vanreusel
et al. 2009, Thurber et al. 2010), whale-fall (Smith & Baco 2003), wood-fall (Wiklund et al.
2012), hydrocarbon-seep (Robinson et al. 2004), and hydrothermal-vent (e.g., Grassle 1986)
communities. Dorvilleids demonstrate unusual tolerance of sulfides (Levin et al. 2013).
In enrichment experiments with macroalgae and wood at 1670 m depth in the Santa Cruz
Basin, Bernardino et al. (2010) noted two species of Ophryotrocha responding in ≤ 0.5 yr, the
population response lasting ≥ 5.5 yr, with one specializing on resulting bacterial mats and the
other on degradation products of wood. A species of Parougia also showed a response to the
wood enrichment. Molecular genetic analyses suggest that dorvilleids invaded organically rich
environments at least four times (Thornhill et al. 2012). An undescribed bathyal species of
Ophryotrocha lives on bathyal sea pens (Mercier et al. 2014)
Sensory and feeding structures
The prostomium is generally rounded, and carries a pair of articulated or unarticulated antennae
dorsally and a pair of palps ventrally. Palps often terminate in a distinct palpode. Antennae or
palps or both may be reduced or absent in some taxa. A pair of eyespots may be present near the
rear of the prostomium. Meiodorvillea spp. have a more pear-shaped prostomium and reduced
antennae and palps in apparent adaptation for burrowing. Dorvilleid nuchal organs are unevenly
known because many species descriptions have avoided mention of them (e.g., Jumars 1974,
Wiklund et al. 2012). Most common are a pair of shallow grooves or pits located dorsolaterally
at the rear of the prostomium, but in some taxa four such shallow depressions may be present
(Pleijel 2001, Paxton & Åkesson 2010). At least four species have a dorsal, medial nuchal
papilla posterior to the antennae (Pettibone 1961). Nuchal organs may be absent (Paxton 2009).
Paxton (1980) briefly reviewed jaw growth and replacement in polychaetes, touching on
dorvilleids. The jaws and teeth of dorvilleids have attracted particular attention due to their
resemblance to scolecodonts found most often in shales indicative of hypoxic environments of
the past (e.g., Courtinat & Howlett 1990). Purschke (1987) studied the jaws of Ophryotrocha
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Dorvilleidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
gracilis and Protodorvillea kefersteini and described replacement of the maxillary plates in
the former. Orensanz (1990) mapped the terminology most often used for fossil jaws onto
the terminology used for modern dorvilleids. Macnoughton et al. (2010, 2011) refined the
terminology further for modern worms and noted substantial variation among species in
whether jaw parts grow by accretion or replacement, even in very closely related species. Many
dorvilleid maxillae appear well suited as a pair of jaws to rasp and retrieve filamentous mat
material when the pharynx retracts and jaws close. Jaws are absent in Apodotrocha but present
in the similarly diminutive Neotenotrocha. Ophryotrocha lipscombae has jaws more typical of
other Eunicida than of Dorvilleidae (Lu & Fauchald 2000).
Motility
Tube building is the exception among dorvilleids but is known from at least three species
of Ophryotrocha. O. cosmetandra produces simple, single, mucous tubes that initially are
fragile but become more parchment like as they age (Oug 1990, his Fig. 5). O. socialis lives
gregariously in—and homes to—branching mucous tube networks that it secretes and continually
modifies (Ockelmann & Åkesson 1990). Paxton & Davey (2010) described mounds of radiating
O shieldsi tubes under fish pens. Mounds were typically 30 cm but could reach 1 m diam.
Aggregations of tubes are likely important in supplying oxygen and removing sulfide (e.g.,
Fenchel 1996). Tube building is also known in Iphitime paguri (Høisaeter & Samuelsen 2006).
The majority of dorvilleids are motile, although we cannot dismiss the possibility of sitand-wait predation being used by some taxa. Most appear from morphology best adapted
to epifaunal or interstitial existence, but members of Meiodorvillea appear to be adapted for
burrowing and show subsurface maxima in abundance when cores are sectioned (Jumars
1978, Blake 1994). Small forms, such as Ophryotrocha spp., use ciliary gliding. The smallest
dorvilleids, in Apodotrocha and Neotenotrocha, move almost entirely that way. Dorvillea
bermudensis when well fed crawled over the substratum but when starved increased its
frequency of swimming (Åkesson & Rice 1992).
Illustrations
Tzetlin & Purschke (2005, Fig. 10F) provide a striking scanning electron micrograph of everted
jaws in Protodorvillea kefersteni. Wiklund et al. (2012) show informative drawings and
micrographs of several Ophryotrocha spp. Macnoughton et al. (2010, 2011) use micrographs to
document ontogenetic change in jaws of Ophryotrocha spp. Levin et al. (2013, Fig. 4) provide
photographs of eight species of dorvilleids from methane seeps. Photographs of Dorvillea
australis at <http://www.annelida.net/nz/Polychaeta/Family/Dorvilleidae/dorvillea-australiensisPic.htm> reveal the typical curved posture in which large dorvilleids hold their palps.
Feeding
Small dorvilleids feed on algal, animal, and bacterial material, with all species likely facultative
carnivores. As with other small polychaetes, they may feed macrophagously or microphagously.
In an oversight, F&J suggested in a table designation (BMJ) that Meiodorvillea spp. were
subsurface deposit feeders. They intended to convey the burrowing habit supported by data on
vertical distribution (Jumars 1978, Blake 1994) but had no indication of deposit feeding in this
genus. We strongly doubt that these small animals could subsist on a diet substantially diluted
by mineral grains. Additional species have been cultured since F&J, but the diversity of items
that serve as food, from frozen spinach to carrion (e.g., Ockelmann & Åkesson 1990) give little
indication of diets in situ. Ophyrotrocha socialis, isolated from a laboratory flowing seawater
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Dorvilleidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
system, showed this dietary breadth but responded most strongly to mysid shrimp remains; it
was generally a nocturnal feeder except when this stimulus was provided during daylight. O.
cosmetandra appeared to feed on greenish or brownish detritus in the field (Oug 1990). O.
labronica when fed on Tetramin™ (a commercial fish food) spawned more frequently than when
fed on spinach or cereal (Prevedelli & Vandini 1998). An undescribed bathyal Ophryotrocha sp.
was found on sea pens and could be reared to reproductive stages on their soft tissues and those
of soft corals; sediments were also ingested (Mercier et al. 2014). The smallest dorvilleids were
observed to graze bacterial films from sand grains or air-water interfaces (Eibye-Jacobson &
Kristensen 1994).
Glasby (1984) dissected several large Dorvillea australis from a variety of shallow-water
locations in western, southern and eastern Australia and reported one individual with a large
amount of coralline red algae, several with unidentifiable macroalgae, several with unidentifiable
animal remains, and none with sediments in their guts. In several smaller specimens of
Schistomeringos loveni from sandy bottoms near Sydney, however, he found a mixture of
sediment and detrital material in the posterior section of the gut. Gaston (1987) in bottom
samples from the U.S. Mid-Atlantic Bight dissected 17 Schistomeringos caeca individuals and
found detritus in all of them and a foram in one; 28 Protodorvillea minuta individuals were
empty, and 1 contained forams; 5 P. gaspeensis were empty. Of 12 P. kefersteini individuals, 11
were empty, and one contained a peracarid.
With the inclusion of Iphitime in Dorvilleaidae (Eibye-Jacobson & Kristensen 1994, Wiklund
et al. 2009), the family now contains commensals, most of which live in the branchial cavities
of brachyuran crabs (de Paiva & Nonato 1991, Høisaeter & Samuelson 2006). Diets of Iphitime
spp. are unknown, but host gill tissues show no signs of injury (de Paiva & Nonato 1991). The
monotypic Veneriserva pygoclava lives in the coelom of Aphrodita longipalpa and Laetmonice
producta and is presumed to be parasitic (Rossi 1984, Micaletto et al. 2002). Most hosts contain
a single V. pygoclava and no more than six (Micaletto et al. 2002), and evidence of impact on
reproductive status of the host is so far negative (Micaletto et al. 2002, 2003; Parapar et al.
2013). V. pygodactyla retains what appears to be a functional gut and a morphology very similar
to Parophryotrocha and Ophryotrocha (Eibye-Jacobsen & Kristensen 1994).
Where stable isotopic signatures are available, mostly from vent and seep fields, dorvilleids
often plot near the lowest values in both δ13C and δ15N for any invertebrates, indicating a diet
rich in chemosynthetic bacteria (Levin et al. 2000, a single Dorvillea sp.; Bergquist et al. 2007,
19 pooled Ophryotrocha globopalpata; Decker & Olu 2010, 10 pooled, unidentified dorvilleids)
and consistent with grazing on microbial mats. Thurber et al. (2012) raised O. labronica through
an entire life cycle on two strains of Euryarchaeota in the laboratory, obtaining growth rates
as high as those on bacterial or eukaryotic diets. The lipids unique to these prokaryote strains
were not incorporated in worm tissues. By contrast, an endolithic species of Dorvillea collected
from the continental margin of Costa Rica and dorvilleids from sediments around California and
Oregon methane seeps incorporated fatty acids unique to anaerobic, methane-oxidizing Archaea
(Thurber et al. 2012). These findings suggest that some of the high diversity of dorvilleids
around vents and seeps may be due to dietary specialization on particular prokaryotes. There is
substantial diversity in dietary sources and trophic levels among dorvilleid species collected from
methane seeps (including feeding on phytodetritus), as determined by δ13C and δ15N (Thornhill
et al. 2012; Levin et al. 2013).
Further experiments with O. labronica raised them on spinach, rice, pure cultures of
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Dorvilleidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
eubacteria or of Euryarchaeota (Thurber 2014) and examined both ∆15N and fatty acid contents.
Results are quite disconcerting regarding the reliability of trophic inference from field-collected
specimens. The worms were in general more depleted in 15N than their foods, and food source
had little effect on worm fatty acid profiles. In the absence of documentation about the fed diets,
the observed fatty acid profiles in the worms would have been attributed to a phytoplankton diet.
Stable isotopic data on dorvilleids away from seeps and vents are rare. Iken et al. (2005)
reported values for a single specimen of Dorvillea cf. rudolphi from the Amundsen Gulf in the
Canada Basin at 625 m water depth. It was less enriched in 15N than a goniadid, nephtyid or
nereidid but more enriched than Chaetozone setosa (Cirratulidae), Prionospio sp. (Spionidae)
or Ophelina cylindricaudata (Opheliidae). Its δ15N was comparable to those of a capitellid
and Terebellides stroemii (Trichobranchidae). We suspect that it had a diet of surficial
phytodetritus plus protist and animal tissues, but this stable isotope datum is also compatible
with subsurface deposit feeding. Kiyasho et al. (2001) provided some 13C evidence of utilization
by Schistomeringos japonica (4 specimens) of carbon originating from oil pollution. Three
dorvilleid species from deep-sea, wood enrichment sites had higher δ15N than expected of
animals feeding directly on sediments, suggesting contributions from scavenging or predation on
animals with more direct dependence on the enrichments (Bernardino et al. 2010).
Guild membership
We find little evidence to change F&J’s suggestion that all dorvilleids may feed carnivorously,
given the opportunity, but that many if not all could survive on a diet of macro- or microalgae
or concentrations of bacteria (filamentous or otherwise). Jaws that can rasp and grasp give most
species the potential to be microphagous or macrophagous. Tubicolous species are discretely
motile. We tentatively classify non-tubicolous, free-living species as motile, though it is possible
that some are sit-and-wait predators and thus also discretely motile. Dorvilleids are commonly
found nestled against or under stones and in rubble or borings of calcareous substrata (to which
they may contribute cf. Hutchings & Peyrot-Clausade 1988), so sit-and-wait predation along
with opportunistic feeding on drift algae seems highly likely.
Research opportunities
• Stable isotopic measurements could clarify whether Iphitime spp. are parasitic or, like
Histriobdellidae, primarily graze the microflora that fouls gill surfaces of the host.
• Variability in stable isotope data among individuals within a population would be useful in
determining intraspecific diet variability.
• Lipid analyses could narrow the estimates of realized diets, with caveats that lipid analysis
has not always proven reliable (Thurber 2014).
• Estimates of motility (frequencies and distances moved) in the field, especially for larger
species, would illuminate potential diets.
• The frequency with which larger species (> 1 cm long) burrow into soft sediments is poorly
known.
References
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and quantitative community characteristics to determine a local hydrothermal vent food web.
Mar. Ecol. Prog. Ser. 330:49–65
Bernardino AF, Smith CR, Baco A, Altamira I, Sumida PYG. 2010. Macrofaunal succession in
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Dorvilleidae
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
sediments around kelp and wood falls in the deep NE Pacific and community overlap with
other reducing habitats. Deep-Sea Res. Pt. I 57:708–23
Blake JA. 1994. Vertical distribution of benthic infauna in continental slope sediments off Cape
Lookout, North Carolina. Deep-Sea Res. Pt. II 41:919–27
Cardell MJ, Sardà R, Romero J. 1999. Spatial changes in sublittoral soft-bottom polychaete
assemblages due to river inputs and sewage discharges. Acta Oecol. 20:343–51
Courtinat B, Howlett P. 1990. Dorvilleids and arabellids (Annelida) as indicators of dysaerobic
events in well-laminated non-bioturbated deposits of the French Mesozoic. Palaeogeogr.
Palaeoclimatol. Palaeoecol. 80:145–51
de Paiva PC, Nonalo EF. 1991. On the genus Iphitime (Polychaeta: Iphitimidae) and description
of Iphitime sartorae sp. nov. a commensal of Brachyuran crabs. Ophelia 34:209–15
Decker C, Olu K. 2010. Does macrofaunal nutrition vary among habitats at the Hakon Mosby
mud volcano? Cah. Biol. Mar. 51:361–7
Eibye-Jacobsen D, Kristensen RM. 1994. A new genus and species of Dorvilleidae (Annelida,
Polychaeta) from Bermuda, with a phylogenetic analysis of Dorvilleidae, Iphitimidae and
Dinophilidae. Zool. Scr. 23:107–31
Fenchel T. 1996. Worm burrows and oxic microniches in marine sediments. 1. Spatial and
temporal scales. Mar. Biol. 127:289–95
Gaston GR. 1987. Benthic Polychaeta of the Middle Atlantic Bight: feeding and distribution.
Mar. Ecol. Prog. Ser. 36:251–62
Glasby CJ. 1984. A review of Dorvillea and Schistomeringos (Annelida: Polychaeta) chiefly
from southern and eastern Australia with a description of a new species of Schistomeringos.
In Proceedings of the First International Polychaete Conference, Sydney, Australia, ed. PA
Hutchings, pp. 98–11. Sydney: Linnean Society of New South Wales
Grassle JF. 1986. The ecology of deep-sea hydrothermal vent communities. Adv. Mar. Biol.
23:301–62
Gray JS, Waldichuk M, Newton AJ, Berry RJ, Holden AV, Pearson TH. 1979. Pollution-induced
Changes in populations [and discussion]. Phil.Trans. Roy. Soc. B: Biol. Sci. 286:545–61
Høisæter T, Samuelsen TJ. 2006. Taxonomic and biological notes on a species of Iphitime
(Polychaeta, Eunicida) associated with Pagurus prideaux from western Norway. Mar. Biol.
Res. 2:333–54
Hutchings PA, Peyrot-Clausade M. 1988. Macro-infaunal boring communities of Porites: A
biogeographical comparison. In Proceedings of the 6th International Coral Reef Symposium,
Townsville, Australia. ed. JH Choat, D Barnes, MA Borovitzka, 3: 263–7. Townsville:
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Iken K, Bluhm BA, Gradinger R. 2005. Food web structure in the high Arctic Canada Basin:
evidence from 13C and 15N analysis. Polar Biol. 28:238–49
Jumars PA. 1974. A generic revision of the Dorvilleidae (Polychaeta), with six new species from
the deep North Pacific. Zool. J. Linn. Soc. 54:101–35
Jumars PA. 1978. Spatial autocorrelation with RUM (Remote Underwater Manipulator): vertical
and horizontal structure of a bathyal benthic community. Deep-Sea Res. 25:589-604
Kiyashko SI, Fadeeva NP, Fadeev VI. 2001. Petroleum hydrocarbons as a source of organic
carbon for the benthic macrofauna of polluted marine habitats as assayed by the 13C/12C ratio
analysis. Dokl. Biol. Sci. 381:535–7
Kvalø Heggøy K, Schander C, Åkesson B. 2007. The phylogeny of the annelid genus
Ophryotrocha (Dorvilleidae). Mar. Biol. Res. 3:412–20
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Levin LA. 2003. Oxygen minimum zone benthos: adaptation and community response to
hypoxia. Oceanogr. Mar. Biol. Ann. Rev. 41:1–45
Levin LA, Ziebis W, Mendoza GF, Bertics VJ, Washington T, et al. 2013. Ecological release and
niche partitioning under stress: Lessons from dorvilleid polychaetes in sulfidic sediments at
methane seeps. Deep-Sea Res. Pt. II. 92:214–33
Lu H, Fauchald K. 2000. Ophryotrocha lipscombae, a new species and a possible connection
between ctenognath and labidognath-prionognath eunicean worms (Polychaeta). Proc. Biol.
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Macnaughton MO, Eibye-Jacobsen D, Worsaae K. 2011. Comparative studies of jaw
morphology and ontogeny in two species of asexually reproducing Dorvilleidae (Annelida).
Zool. Anz. 250:134–42
Macnaughton MO, Worsaae K, Eibye-Jacobsen D. 2010. Jaw morphology and ontogeny in five
species of Ophryotrocha. J. Morphol. 271:324-39
Mercier A, Baillon S, Hamel JF. 2014. Life history and seasonal breeding of the deep-sea annelid
Ophryotrocha sp.(Polychaeta: Dorvelleidae). Deep-Sea Res. Pt. I 91:27–35
Micaletto G, Gambi MC, Cantone G. 2002. A new record of the endosymbiont polychaete
Veneriserva (Dorvilleidae), with description of a new sub-species, and relationships with its
host Laetmonice producta (Polychaeta: Aphroditidae) in Southern Ocean waters (Antarctica).
Mar. Biol. 141:691–8
Micaletto G, Gambi MC, Piraino S. 2003. Observations on population structure and reproductive
features of Laetmonice producta Grube (Polychaeta, Aphroditidae) in Antarctic waters. Polar
Biol. 26:327–33
Ockelmann KW, Åkesson B. 1990. Ophryotrocha socialis n. sp., a link between two groups of
simultaneous hermaphrodites within the genus (Polychaeta, Dorvilleidae). Ophelia 31:145–
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Orensanz JM. 1990. The eunicemorph polychaete annelids from Antarctic and Subantarctic
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Washington, D.C.: American Geophysical Union
Oug E. 1990. Morphology, reproduction, and development of a new species of Ophryotrocha
(Polychaeta: Dorvilleidae) with strong sexual dimorphism. Sarsia 75:191–201
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producta producta Grube (Polychaeta: Aphroditidae) in the Bellingshausen Sea and Antarctic
Peninsula (Southern Ocean, Antarctica). Ital. J. Zool. 80:255–72
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Paxton H. 2000. Family Dorvilleidae. See Beesley et al. 2000, pp. 91–4
Paxton H. 2009. A New Species of Palpiphitime (Annelida: Dorvilleidae) from Western Canada
Proc. Biol. Soc. Wash. 122:26–31
Paxton H, Davey A. 2010. A new species of Ophryotrocha (Annelida: Dorvilleidae) associated
with fish farming at Macquarie Harbour, Tasmania, Australia. Zootaxa 2509:53–61
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of the Dorvilleidae. Proc. Biol. Soc. Wash. 74:167–86
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phylogenetic importance in Polychaeta (Annelida). IV. The pharynx and jaws of the
Dorvilleidae. Acta Zool. 68:83–105
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Dorvilleidae
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
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with the emendation of the family Iphitimidae. Bull. S. Calif. Acad. Sci. 83:163–6
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Thurber AR. 2014. Diet-dependent incorporation of biomarkers: implications for foodweb studies using stable isotope and fatty acid analyses with special application to
chemosynthetic environments. Mar. Ecol. doi:10.1111/maec.12192, in press
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methane use by New Zealand cold seep benthos. Mar. Geol. 272:260–9
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for food webs and biogeochemical cycling. ISME J. 6:1602–12
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seep ecosystems along the European margins. Oceanography 22:110–27
Wiklund H, Altamira IV, Glover AG, Smith CR, Baco AR, Dahlgren TG. 2012. Systematics and
biodiversity of Ophryotrocha (Annelida, Dorvilleidae) with descriptions of six new species
from deep-sea whale-fall and wood-fall habitats in the north-east Pacific. Syst. Biodiv.
10:243–59
Wiklund H, Glover AG, Dahlgren TG. 2009. Three new species of Ophryotrocha (Annelida:
Dorvilleidae) from a whale-fall in the north-east Atlantic. Zootaxa 2228:43–56
Echiuridae, Echiurida
Diversity and systematics
Affinities of Echiurus have been questioned since Nishikawa (2002) proposed Ikedidae as a
junior synonym of Echiuridae. Especially for our purposes here of assigning feeding guilds, the
more recent reassignments of genera by Goto et al. (2013) to families based on molecular genetic
evidence appears more orderly. Reverting to the view held by Edmonds (2000) and many of his
predecessors, Goto et al. (2013) regarded Echiurus as the only genus in Echiuridae, known from
4 well accepted species and 1 additional species whose status is less certain. WoRMS does not
yet reflect this view. Echiuridae is a sister clade to Urechidae, with which it shares anal chaetae
(Goto et al. 2013). Molecular data place Echiurida sister to Capitellidae within Annelida (Struck
et al. 2011). Adult trunk lengths in Echiuridae range from about 3 to 30 cm.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Habitat
Echiurus spp. burrow in soft sediments from intertidal to at least bathyal depths (Galil & Goren
1994), mostly in cold waters. Gallardo et al. (1977) reported individual abundances up to 2600
m-2 of E. antarcticus as early colonists of volcanic deposits around Deception Island, Antarctica.
Sensory and feeding structures
The proboscis may range from short and spatulate to long and nearly tubular. Ventral cilia and
muscular movements are used to transport particles to the mouth. Two ventral swellings on the
proboscis in front of the mouth are regions of particle sorting (Edmonds 2000). Echiurids lack
other anterior appendages, and their sensory organs are poorly known. Echiurids have long,
convoluted guts characteristic of echiurans and possess a siphon tube that connects the anterior
midgut with the posterior midgut. The gut of E. echiurus about 10 times as long as the trunk.
Paired, tubular anal sacs open into the hindgut through separate ducts (Lehrke 2011).
Motility
Gislén (1940) reviewed past work on E. echiurus and incorporated his own extensive
observations. The worm swims by twisting the whole body into a spiral. It is also able to move
slowly on the sediment surface through a combination of peristalsis and anchoring with its anal
chaetae. During the digging of a new burrow, its proboscis lies dorsal to and against the body
pointing backward, and the part of the anterior trunk bearing two stout chaetae is first to enter the
sediments. The worm normally lies ventral side upward in the bottom of a broad, flat-bottomed,
U-shaped burrow, but the posterior end of the burrow is often filled with loose sediments until
hydraulically cleared by peristaltic pumping. In this orientation, the numerous anal chaetae do
not contact the roof of the burrow but are effective for traction with the lower wall.
Illustrations
Goto et al. (2013) present color photographs of 12 species of echiurans, including E. echiurus.
Edmonds (2000, Fig. 4.11) provides a line drawing of E. echiurus.
Feeding
In E. echiurus, the proboscis enters sediments at a shallow angle, with its ciliated, anatomically
ventral, ciliated side up, and the cilia transport particles back toward the mouth; extension is a
jerky motion (Gislén 1940, Nyholm & Bornö 1969). Two ventral swellings in front of the mouth
are used to reject some large particles (Gislén 1940, Nyholm & Bornö 1969). The proboscis
spends little time on clean sand, but digs out lumps of sediment in areas with an organic surface
film. By successive extension and ciliary transport of particles, a fully extended proboscis is
filled with sediment; it is then rolled into a semi-enclosed tube and withdrawn by muscular
contractions into the burrow. Extension lasted 1 - 4 min whereas contraction took only 2 - 4 s
(Gislén 1940). The process left distinct radial tracks that were avoided in subsequent extensions.
No matter the proboscis direction, the ventral side remained upward, enabled by twisting of
the base of the proboscis up to 180˚. Occasionally during extension, E. echiurus would roll
up its proboscis, transferring particles adherent to the dorsal surface to the ciliated ventral side
(Nyholm & Bornö 1969). Ingesta were formed into distinct pellets before leaving the esophagus;
pelletized ingesta differed little in appearance from foregut to hindgut except that ingested
diatoms were thoroughly digested (Gislén 1940). At a given time the gut could contain up to
about 540 pellets (Gislén 1940).
Feeding bouts were separated by a few days. In aquaria, Gislén (1940) described bouts of
fecal ejection from the burrow, separated by several days with none. This long period made
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Gislén (1940) suspect temporary pellet storage in the burrow. This suspicion has been confirmed
in resin casts (Ditadi 1983). Gislén (1940) dyed particles and first observed them back at the
sediment surface 4.5 d after ingestion. It is unknown how long they might have been stored in
the burrow before being ejected. Nyholm & Bornö (1969) repeated the experiment but dissected
individuals at known times after ingestion. They found that it took 4 h for marked particles
to reach the start of the midgut. Such long particle residence times are unusual among other
deposit-feeding polychaetes.
Investigators, beginning with Gislén (1940), have consistently found mildly alkaline
conditions in the guts of Echiurus echiurus. Bornö (1971) found proteolytic activity in
E. echiurus that showed a broad optimum around pH 10. It included strong tryptic, some
dipeptidase, but no chymotryptic activity. Mayer et al. (2001) found a slightly basic pH (8.6)
and esterase activities in the gut of E. echiurus that exceeded those of other deposit feeders by an
order of magnitude. Esterase activity was quantified against a butyrate substrate, suggesting very
active short-chain fatty acid digestion. Chen et al. (2002) found a midgut pH of 8.4 in the same
species. Long residence times and alkaline pH are uncharacteristic of deposit feeders in either
other Polychaeta or in Echinodermata (Mayer et al. 1997).
We were able to find only one δ13C measurement for Echiurus spp., done by McConnaughey
& McRoy (1979) on a single Echiurus echiurus alaskensis. It indicated mixed eelgrass and
phytoplankton carbon sources.
Guild membership
We regard Echiurus spp. as discretely motile surface deposit feeders using an unarmed proboscis.
Storage of pellets in the burrow has been documented; we interpret it to include some caching,
though its quantitative importance in the diet is unknown. Echiurids may supplement their
nutrition with sediments settling into the burrow and with subsurface sediments lining the
burrow.
Research opportunities
• Stable isotope measurements are scarce for Echiurus.
• Particle selection experiments apparenly have not been carried out.
• How the spines are used in burrowing remains to be determined.
• Additional gut residence time and assimilation efficiency measurements would be profitable
to test the hypothesis that—through long residence time, high enzymatic activity, basic pH,
and perhaps re-ingestion of feces—high assimilation efficiencies are achieved.
• Fatty acid digestion and uptake studies appear promising (Mayer et al. 2001).
• Experimental introduction of tracers falling into the burrow would be useful to test the
hypothesis that Echiurus spp. use this source of nutrition on a diel cycle to supplement
nocturnal surface deposit feeding.
• Functions of the anal sacs and siphon tubes are poorly known. The sacs are well positioned
to provide reduced N and microbial inocula to fecal pellets that will be cached. Some
capitellids and deposit-feeding echinoderms also carry siphons.
References
Bornö C. 1971. Proteolytic enzymes of Echiurus echiurus pallas. Comp. Biochem. Physiol. Pt. B
38: 507–12
Chen Z, Mayer LM, Weston DP, Bock MJ, Jumars PA. 2002. Inhibition of digestive enzyme
activities by copper in the guts of various marine benthic invertebrates. Environ. Toxicol.
Chem. 21:1243–48
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Echiuridae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Ditadi ASF. 1983. On the burrows of echiuran worms (Echiura): a survey. Bol. Zool.
(Universidade de São Paulo) 7:21–36
Edmonds SJ. 2000.Phylum Echiura. See Beesley et al. 2000, pp. 353–74
Galil BS, Goren M. 1994. The deep sea Levantine Fauna.-New records and rare occurrences.
Senck. Marit. 25:41–52
Gallardo VA, Castillo JG, Retamal MA, Yañez A, Moyano HI,Hermosilla JG. 1977. Quantitative
studies on the soft-bottom macrobenthic animal communities of shallow Antarctic bays. In
Llano GA (ed) Adaptations within Antarctic ecosystems, ed. GA Llano, 361–87. Houston:
Gulf Publications
Gislén T. 1940. Investigations on the ecology of Echiurus. Lunds Universitets Årsskrift 36:1–36
Goto R, Okamoto T, Ishikawa H, Hamamura Y, Kato M. 2013. Molecular phylogeny of echiuran
worms (Phylum: Annelida) reveals evolutionary pattern of feeding mode and sexual
dimorphism. PLoS ONE 8:e56809, 6 pp.
Mayer LM, Jumars PA, Bock MJ, Vetter YA, Schmidt JL. 2001. Two roads to sparagmos:
Extracellular digestion of sedimentary food by bacterial inoculation versus deposit-feeding.
In Organism–Sediment Interactions, ed. JY Aller, SA Woodin, RC Aller, 335–47. Columbia:
Univ. South Carolina Press
Mayer LM, Schick L, Self RFL, Jumars PA, Findlay R, et al. 1997. Digestive environments of
benthic macroinvertebrate guts: enzymes, surfactants and dissolved organic matter. J. Mar.
Res. 55:785–812
Nishikawa T. 2002. Comments on the Taxonomic Status of Ikeda taenioides (Ikeda, 1904) with
some amendments in the classification of the Phylum Echiura. Zool. Sci. 19:1175–80
Nyholm K-G, Bornö C. 1969. The food uptake of Echiurus echiurus Pallas. Zool. Bidrag
Uppsala. 38:249–54
Eenymeenymyzostomatidae, Myzostomida
Diversity and systematics
Eenymeenymyzostomatidae was recently erected (Summers & Rouse 2014) for what was
previously known as Myzostoma cirripedium. Adults are 2 - 5 mm long (Fedotov 1938).
The species inserts into the phylogeny much more basally than members of the remaining
Myzostomatidae, and together Myzostomatidae and Pulvinomyzostomidae form a sister clade
to Eenymeenymyzostomatidae (Summers & Rouse 2014). Summers & Rouse (2014) suspected
that as many as 10 potential congeners may be reassigned to Eenymeenymyzostoma when
molecular genetic data become available. Based on morphological similarity with some other
species of Myzostomida, potential congeners include M. wyvillethomsoni, wheeleri, and ingolfi.
All these animals are a few millimeters long as adults and cluster together because they are
relatively long and oval and share a common arrangement of parapodial cirri (Grygier 1990).
Habitat
E. cirripedium infests deep-water metacrinine, stalked crinoids near the Philippines and
Moluccas (as do M. wyvillethomsoni and wheeleri according to Grygier 1990).
Sensory and feeding structures
The morphology of E. cirripedium is reasonably well known from early studies (Fedotov 1938),
and gives us no reason to differentiate basic sensory and feeding structures from better known
species of Myzostoma. We caution that addition of species to Eenymeenymyzostoma may
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
allow finer distinctions. The following descriptions are collected largely from Grygier (2000)
and based heavily on studies of M. cirriferum, whose phylogenetic position is relatively basal
within Myzostoma in the analysis by Summers & Rouse (2014). Eyes and nuchal organs are
absent. Some but not all patches of external cilia are apparently sensory (Eekhaut & Jangoux
1993a). Sucker-like lateral organs, found near the lateral margins of the animal, are mechanoand chemosensory (Eekhaut & Jangoux 1993b). The anterior of the body is apparently reduced
to a retractile, muscular proboscis through which the unciliated, axial pharynx extends (Eekhaut
et al. 1995). The proboscis retracts into a cavity or sheath. The basal muscle bulb of the pharynx
undergoes peristaltic contractions that carry food from the mouth to the stomach (Eekhaut et al.
1995). The stomach opens into paired, branching caeca and is followed by a thin and relatively
short intestine.
Motility
E. cirripedium is assumed from morphology to be discretely motile.
Illustrations
Illustrations of E. cirripedium appear limited to a drawing in ventral view in the original
description (von Graff 1885) and some drawings of tissue sections (Fedotov 1938).
Feeding
E. cirripedium is assumed to feed kleptoparasitically.
Guild membership
Eenymeenymyzostoma cirripedium is a discretely motile kleptoparasite using an unarmed,
protrusible proboscis to feed on particles from the ambulacral grooves of its crinoid host.
Research opportunities
• Energy costs to the host from the (klepto)parasitism are unknown.
• The species affords an opportunity to run experiments on selective ingestion by presenting
visually recognizable particles to the host and video recording food passage upstream, at the
location of the myzostome, and downstream to test for selective ingestion. This design is
reminiscent of classic experiments on food choice by birds from items passing on a conveyor
belt (e.g., Krebs et al. 1977).
References
Eeckhaut I, Dochy B, Jangoux M. 1995. Functional morphology of the introvert and digestive
system of Myzostoma cirriferum (Myzostomida). Acta Zool. 76:307–15
Eeckhaut I, Jangoux M. 1993a. Life cycle and mode of infestation of Myzostoma cirriferum
(Annelida): a symbiotic myzostomid of the comatulid crinoid Antedon bifida
(Echinodermata). Dis. Aquat. Organ. 15:207–17
Eeckhaut I, Jangoux M. 1993b. Integument and epidermal sensory structures of Myzostoma
cirriferum (Myzostomida). Zoomorphology 113:33–45
Fedotov DM. 1938. Spezialisation und Degradation im Körperbau der Myzostomiden in
Abhängigkeit von der Lebensweise. Acta Zool. 19:353–85
Grygier M.J. 1990. Distribution of Indo-Pacific Myzostoma and host specificity of comatulidassociated Myzostomida. Bull. Mar. Sci. 47:182–91
Grygier MJ. 2000. Class Myzostomida. See Beesley et al. 2000, pp. 297–329
Krebs JR, Erichsen JT, Webber MI, Charnov EL. 1977. Optimal prey selection in the great tit
(Parus major). Anim. Behav. 25:30–8
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Eenymeenymyzostomatidae
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Jumars, Dorgan & Lindsay
07 November 2014
Summers MM, Rouse GW. 2014. Phylogeny of Myzostomida (Annelida) and their relationships
with echinoderm hosts. BMC Evol. Biol. 14:170, 15 pp.
von Graff L. 1885. Description of a new species of Myzostoma. Trans. Linn. Soc. Lond., 2nd ser.,
Zool. 2:444–6, plate LII, Fig. 19
Endomyzostomatidae, Myzostomida
Diversity and systematics
Based on molecular genetic data, Summers & Rouse (2014) recently removed Contramyzostoma
and Mycomyzostoma from Endomyzostomatidae, leaving only 14 species of Endomyzostoma.
The body of Endomyzostoma spp. is a circular disc 2 - 11 mm in diameter, but is often folded
into a more three-dimensional bean shape within the gall or cyst (Grygier 2000).
Habitat
All species inhabit soft cysts on feather stars or hard galls on stalked crinoids. Galls comprise
enlarged and deformed crinoid ossicles, whereas cysts are fleshy. One or usually two openings
are present. The proboscis protrudes through one opening for feeding.
Sensory and feeding structures
A muscle-bulb-containing pharynx or proboscis is protrusible through an anterior mouth in
Endomyzostoma spp. Most species lack lateral organs (Grygier 2000). The stomach epithelium
is ciliated.
Motility
Individuals are sessile in the reference frame of the host.
Illustrations
Grygier (2000) provides line drawings of external and internal morphology. Eeckhaut &
Lanterbecq (2005, Fig. 1J) presents a color photography of E. tenuispinum. Summers et al.
(2014) show color photographs of two new species.
Feeding
Endomyzostoma spp. are kleptoparasitic on food diverted from the ambulacral grooves of their
crinoid hosts (Grygier 2000, Summers & Rouse 2014).
Guild membership
We classify Endomyzostoma spp. as sessile kleptoparasites with food sources as noted in the
previous sentence and obtained through a muscular, protrusible pharynx.
Research opportunities
• Energy costs to the host from the (klepto)parasitism are unknown.
• There is an analogy between classic choice experiments done with conveyor-belt delivery
of potential prey to great tits (Krebs et al. 1977) and the opportunity to observe prey choice
from the stream of particles carried past kleptoparasites in the crinoid ambulacral groove.
How selective are the kleptoparasites and for what items?
References
Eeckhaut I, Lanterbecq D. 2005. Myzostomida: a review of the phylogeny and ultrastructure.
Hydrobiologia 535/536:253–75
Grygier MJ. 2000. Class Myzostomida. See Beesley et al. 2000, pp. 297–329
Krebs JR, Erichsen JT, Webber MI, Charnov EL. 1977. Optimal prey selection in the Great Tit
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Jumars, Dorgan & Lindsay
07 November 2014
(Parus major). Anim. Behav. 25:30–8
Summers MM, Al-Hakim I, Rouse GW. 2014. Turbo-taxonomy: 21 new species of Myzostomida
(Annelida). Zootaxa 3873:301–44
Summers MM, Rouse GW. 2014. Phylogeny of Myzostomida (Annelida) and their relationships
with echinoderm hosts. BMC Evol. Biol. 14:170, 15 pp.
Eulepethidae, Aphroditiformia
Diversity and systematics
Eulepethidae is a small family of scaleworms (21 species in 6 genera; Woolley & Wilson 2011).
The family is deeply rooted, with Aphroditidae and a large group containing the remaining 5
scaleworm families as sister clades (Wiklund et al. 2005, Norlinder et al. 2012). Most species
are 3 - 8 cm long (Pettibone 1969).
Habitat
Most Eulepethidae burrow in soft sediments, ranging from the intertidal to 800 m water depth.
Most occur at low latitudes. Burrowing species in cross section have the nearly rectangular
shape expected of strong burrowers in mud. Two species are thought to inhabit tubes of other
species: Grubeulepis geayi commensal with Acoetes malanonota (Day 1962), and G. malayensis
in empty tubes of Mesochaetopterus selangorus (Nishi 2001).
Sensory and feeding structures
Two short antennae are inserted anteroventrally on the prostomium. The third is anterodorsal,
with a pair of elongate palps ventral. A variable number of eyes may be present but hidden by
the second segment (Pettibone 1969). Nuchal organs are present as dorsolateral, club-shaped
appendages between the prostomium and the first segment. Eulepethids are equipped with an
eversible pharynx tipped with terminal papillae. The pharynx is armed by what are described
as two pairs of plate-like jaws. We are quite certain that in our terminology there is either one
pair of jaws or, at the other extreme, there are four regions of sclerotization on the inside of the
pharynx. The same uncertainty persists with the sister group Aphroditidae.
Motility
No studies of motility have been published, but eulepethids are thought to be motile burrowers
(Pettibone 1969). The two tube-dwelling species, however, are likely to be discretely motile, sitand-wait predators.
Illustrations
Pettibone (1969) and Woolley & Wilson (2011) provide line drawings that together illustrate the
morphology and diversity of the family.
Feeding
The burrowing Eulepethidae are assumed to be predators. Both commensals may be sit-and-wait
predators, or G. geayi may scavenge scraps from its host as a kleptoparasite. For no species have
diets or feeding behaviors been described. The gut bears numerous diverticula (Darboux 1899).
Guild membership
The burrowing species are assumed to be motile, though sit-and-wait predation is possible. The
commensals are assumed to sit and wait and so are classified as discretely motile. On the basis
of poorly known jaw morphology alone we assign them to be carnivorous.
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Eulepethidae
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Jumars, Dorgan & Lindsay
07 November 2014
Research opportunities
• Any feeding information would be valuable, including gut contents, direct observations, lipid
tracers and stable isotopes.
• Likewise any information on movement frequencies and distances would be useful.
• The geometry and function of jaws are badly in need of clarification as they are in the sister
clade Aphroditidae
References
Darboux JG. 1899. Recherches sur les Aphroditiens. Travaux de l’Institut de Zoologie de
l’Université de Montpellier et de la Station Maritime (Zoologique) de Cette 6:1–276
Day JH. 1962. Polychaeta from several localities in the western Indian Ocean. Proc. Zool. Soc.
Lond. 139: 627–56
Nishi E. 2001. A new species of scaleworm, Grubeulepis malayensis (Annelida: Polychaeta:
Eulepethidae), from Morib Beach, Malaysia, living in chaetopterid tubes. Species Divers.
6:1–9
Norlinder E, Nygren A, Wiklund H, Pleijel F. 2012. Phylogeny of scale-worms (Aphroditiformia,
Annelida), assessed from 18SrRNA, 28SrRNA, 16SrRNA, mitochondrial cytochrome c
oxidase subunit I (COI), and morphology. Mol. Phylogen. Evol. 65:490–500
Pettibone, M.H. 1969. Revision of the aphroditoid polychaetes of the Family Eulepethidae
Chamberlin (= Eulepedinae Darboux = Pareulepidae Hartman). Smithsonian Contrib. Zool.
41:1–44
Wiklund H, Nygren A, Pleijel F, Sundberg P. 2005. Phylogeny of Aphroditiformia (Polychaeta)
based on molecular and morphological data. Mol. Phylogenet. Evol. 37:494–502
Eunicidae, Eunicida
Diversity and systematics
Eunicidae are speciose (~ 400 spp.), particularly within the genus Eunice (~ 250 spp.). Of nine
genera, only one is monotypic. Early genetic data had suggested that Eunicidae are polyphyletic,
Onuphidae falling within the eunicid clade and commonly studied Marphysa more closely
related to onuphids than to other eunicids (Struck et al. 2006). More extensive data, however,
support the monophyly of both Eunicidae and Onuphidae as well as the need for generic revision
(Zanol et al. 2010, 2014). Species range from slightly less than 1 cm to 6 m long (Fauchald
1992). In coral rubble, they often display impressive, iridescent colors, intimidating jaw
structures, and a wide array of behaviors.
Since F&J, a great deal of feeding information has been recorded under the name Marphysa
sanguinea. Hutchings & Karageorgopoulos (2003) discovered, however, that several species
had been lumped under this name. They distinguished a new species, M. mullawa, known in
Australia to fishermen as the “bloodworm” (used in the U.S. for Glycera spp.) and valuable
enough to for substantial aquaculture interest. Taxonomic identities of species previously
referred to M. sanguinea remain confused because of the large number of morphologically
similar species (Glasby & Hutchings 2010) and because of realized potential for anthropogenic
introduction (Hutchings et al. 2012). For species previously referred to M. sanguinea (type
locality: Cornwall, England), in most cases there is insufficient information to assign clear
species identity. Therefore we provide locality information by author.
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Jumars, Dorgan & Lindsay
07 November 2014
Habitat
M. cf. sanguinea burrows in oxygen-poor muds and rock and coral crevices and has a respiratory
physiology indicative of chronic exposure to low oxygen levels (Weber et al. 1978; N. Carolina
intertidal mud). Numerous eunicids are associated with corals, although the nature of those
associations is not always clear. Tubicolous commensals E. marianae and E. kristiani are known
to alter the growth forms of black corals (Molodtsova & Budaeva 2007). Eunicids are also well
known to bore into coral skeletons, where their jaws leave tooth marks (e.g., Hutchings 2008),
but the difficulty of sampling and the fact that many of the boring individuals are juveniles
makes unraveling the relationships difficult. It is problematic, for example, to distinguish borers
that make openings in coral from nestlers that use existing ones. On the basis of gut contents
(sand-sized fragments digested to a smooth, thick mud posteriorly) Ebbs (1966) confirmed
E. schemacephala to be a major borer in Floridian Montastrea. MacGeachy & Stearn (1976)
found E. schmacephala, E. mutilata and E. kinbergi in holes in Barbados Montastrea but were
noncommittal as to boring versus nestling. Pepe (1985) identified E. aphroditois, E. filamentosa
and Palolo siciliensis in coral rubble on both sides of the Isthmus of Panama. At Enewetak
Atoll Highsmith (1981) collected Lysidice collaris, Nematonereis unicornis, E. siciliensis, E.
antennata and E. sustralensis from the corals Favia pallida, Goniastrea retiformis, and Porites
lutea, noting that N. unicornis was small enough to move freely through the pores of P. lutea.
Sensory and feeding structures
The prostomium is bilobed or entire, and often shorter than the peristomium. The peristomium
is often thin and dorsally located, leaving room below for jaw eversion. Eyes when present
are a dorsal pair near the rear of the prostomium (Fauchald 1992). Five head appendages are
typical, but are variably reduced or lost in some species. They insert dorsally between the
prostomium and peristomium. They were usually termed antennae until Orrhage (1995) on the
basis of innervation labeled the most lateral pair as palps. Nuchal organs have not been regularly
described in this family but are often present as a pair of dorso-lateral, ciliated ridges covered by
the overhang of the peristomium over the prostomium. This overhang is sometimes termed the
nuchal fold (Fauchald 1992).
Eunicidae have a ventral, muscular proboscis with elaborate, articulated jaws that have
received considerable attention by taxonomists. Recently settled M. cf. sanguinea lose their
jaws, passing them through the intestine and secreting a new set (Prevedelli et al. 2007, Venice
lagoon). Molting of jaws occurs several times in M. fauchaldi, with jaws becoming more pincerlike in adults, in contrast to the transition in the onuphid, Diopatra aciculata, from juvenile jaws
similar to M. fauchaldi to more saw-like adult jaws (Paxton & Eriksson 2012). Resemblance to
lumbrinerid jaws appears to be convergent (Struck et al. 2006).
Motility
Eunicidae crawl and burrow, with tube building being highly variable among eunicid species
and life stages (Fauchald 1992). E. magellanica from Patagonia builds conspicuous tubes fouled
by sessile invertebrates. Its gut contents are similar to this fouling fauna, and in some parts of
its South American range it is associated with Macrocystis holdfasts (Orensanz 1990). Some
eunicid tubes are very complex. E. impex from Jervis Bay makes a “trunk” of up to 20 parallel
tubes that project from the sediment before each tube branches as many as 11 times to form a
colonial “tree” (Jacoby et al. 1995). E. metatropos from western Australia produces zig-zagging
branches (Hanley 1986). Several species of Eunice bore through coral, creating tunnel systems
up to 10 cm deep, likely using the mandibles to mechanically bore (MacGeachy & Stern 1976).
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Jumars, Dorgan & Lindsay
07 November 2014
Other Eunice species build tubes along spines of black corals (Molodtsova & Budaeva 2007).
E. norvegica builds a whitish-gray, paper-like tube only slightly longer than the worm,
with several openings, and attaches it to coral branches that may eventually overgrow the tube
(Winsnes 1989). Juvenile M. cf. sanguinea secrete a mucryus tube upon first settlement. Tube
dwelling, with attachment to shells and serpulid tubes, persists through development to about
27 mm body length before adult musculature suffices for burrowing (Prevedelli et al. 2007,
Venice lagoon). In aquaria E. pennata became sedentary after building a tube-tunnel complex,
wheras E. dubitata burrowed more deeply and continuously (Winsnes 1989). E. pennata would
temporarily store food in its tunnel while it foraged for more.
Illustrations
The video and image of E. aphroditois at <http://www.wired.com/wiredscience/2013/09/absurdcreature-of-the-week-bobbit-worm/> are both remarkable as is its cover photo on Beesley et al.
(2000). Paxton (2009) shows SEM and light microscope images of jaws of Eunicidae as well as
other Eunicida. Gambi et al. (2003) show an image of Lysidice cf. ninetta boring in the seagrass
Thalassia testudinum.
Feeding
Although the noted images and video of E. aphroditois clearly illustrate sit-and-wait predation,
the diets of Eunicidae, described as varied by F&J, have expanded to include an even broader
range of possible food items. Marphysa cf. sanguinea surface deposit feeds by extending
part of the body out of the mucus tube (small juveniles) or burrow (large juveniles and adults)
onto the sediment surface (Fig. 6 in Onozato et al. 2010; Yoro tidal flat off Tokyo Bay), and
surface deposit feeding is confirmed via the heavy burden of polycyclic aromatic hydrocarbons
contained in their fecal pellets (Onozato et al. 1010; Nishigaki et al. 2013, also Yoro tidal flat).
It is a candidate for multispecies aquaculture because it grows well on fish wastes (Parandavar
& Kim 2014). Gut contents show high prevalence of Ulva, Enteromorpha, Fucus vesiculosus
and fine sediments with benthic microalgae (Castro 1993 cited in Garcês & Pereira 2011,
Sado estuary, Portugal). In feeding experiments with sediments from which all macrofauna
had been sieved and most meiofauna eliminated by heat treatment, juveniles grew faster at all
experimental salinities when the diet was supplemented with Ulva lattuca, although the effect
of the supplement was not large (Garcês & Pereira 2011). Juveniles were highly territorial and
often cannibalistic (Garcês & Pereira 2011). Meat extracts were more effective than filamentous
algae in accelerating growth (Prevedelli 1994). Gaston (1987) on the basis of gut contents and
unspecified information on burrowing depth of animals collected in Smith-McIntyre grabs from
the Mid-Atlantic Bight of the US continental shelf classified four eunicid species as subsurface
deposit-feeding detritivores: E. antennata, E. pennata, E. vittata and Marphysa bellii.
Evidence of herbivory includes macroalgae, encrusting algae, and angiosperms. Pardo &
Amaral (2006) in laboratory experiments found Marphysa formosa from São Sebastião Brazil
to be exclusively herbivorous on algae, avoiding ingestion of invertebrates. Antoniadou &
Chintiroglou (2006) observed Lysidice ninetta from the northern Agean Sea to feed primarily
on encrusting algae (e.g., Jania sp., Ceramium sp.). Perhaps most remarkable is the complex
of species that bore into and consume the scales (remains of the bases of former leaves) of
Posidonia oceanica. As Gambi (2002) pointed out, this tissue has very low nitrogen content
and comprises abundant, lignified, structural carbohydrates. She found four species of eunicid
borers in the scales. The two dominants were L. ninetta and L. collaris, with many plants having
2 - 4 worms per rhizome at 11 and 28 m water depths off Ischia. A few Nematonereis unicornis
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Jumars, Dorgan & Lindsay
07 November 2014
and Marphysa fallax were also found in the scales. Gambi et al. (2003) identified similar boring
into the seagrass Thalassia testudinum by N. cf. unicornis, L. cf. ninetta and L. cf. collaris in
the Mexican Caribbean. Cigliano et al. (2003) identified cellulase (ß-1,4Glucanase) localized in
the intestines of both of the boring Lysidice species in the Mediterranean. Cellulase activity in
eunicids is otherwise known only from E. aphroditois (Yokoe & Yasumasu 1964). That finding
is somewhat surprising because E. aphroditois is clearly a sit-and-wait, nocturnal predator as an
adult, although it will also take algae (Steene 2000); it is more mobile as a juvenile (Day 1967).
In coarser, encrusted sediments off the Island of Ustica, L. ninetta was found in abundance,
but only within rhodoliths. Gut contents included coralline algae, macroalgae, foraminiferans,
diatoms and Posidonia detritus. Less common were Bryozoa, calcareous spicules and sporangia
(Castriota et al. 2003).
Gut contents in specimens from Scottish sea lochs led Pearson (1971) to classify E. pennata
as a carnivore, and Desière (1967, NE Atlantic) described M. bellii as carnivorous. What Saraç
et al. (1998, Bribie Island, Queensland) called M. sanginuea we assume was M. mullawa. This
species appeared overtly carnivorous and grew well for them on squid meal in a carrageenan or
alginate gel.
Winsnes (1989) maintained E. pennata and E. dubitata from Oslofjord in aquaria on a diet
of the mussel, Modiolus modiolus. He also examined gut contents of field-collected E. pennata,
finding gastropod shells, foraminiferans and ophiuroid fragments. In addition, Winsnes (1989)
noted that a specimen of E. norvegica, a commensal with the coral Lophelia pertusa, was
found with nemerteans in its pharynx. Mortensen (2001) subsequently studied these species in
aquaria and observed E. norvegica to “steal” food from the coral but also to clean the polyps of
sediment particles and promote skeletal growth local to the tube. Mueller et al. (2013) quantified
the interaction by feeding corals with attached worms as well as individual corals and worms
isolated in separate aquaria on diets of small-celled phytoplankton and Artemia that were labeled
with stable isotopes of carbon and nitrogen. Food assimilation by E. norvegica more than
doubled in the presence of the coral, and calcification by the coral increased up to four times in
the association. E. norvegica has also been found on the gills of horse mackerel and suggested
to be parasitic (Saglam & Sarieyyupoglu 2008), although whether those specimens are the same
species as the coral-dwelling E. norvegica is questionable.
On marl beds in the shallow (mean depth 8 m) Bay of Brest, Grall et al. (2006) used stable
carbon and nitrogen isotopes to estimate trophic levels of macrofauna collected in grabs. Stable
nitrogen values clearly identified Marphysa cf. sanguinea, Lysidice ninetta and Marphysa
bellii as carnivores. Nematonereis unicornis and Eunice harassii were slightly less enriched,
falling between the other eunicids and the more clearly deposit-feeding species Eupolymnia
nebulosa (Terebellidae) and Notomastus latericeus (Capitellidae) in 15N enrichment. In Poole
Bay (southern England) Lysidice ninetta, Guerin (2009) also reported 15N enrichment consistent
with carnivory. In Posidonia beds at 5 - 8 m off Mallorca Island, Deudero et al. (2011, 2014)
reported δ15N in Eunice vittata consistent with carnivory—although less enriched than sympatric
lumbrinerids and oenonids and thus also consistent with a degree of omnivory. Although
Deudero et al. (2014) classified Lysidice ninetta as a herbivore, its 15N enrichment was entirely
comparable to those of sympatric lumbrinerids, suggesting selective assimilation of the fouling
fauna on the encrusting algae that dominate its gut contents.
Guild membership
Many eunicids are discretely motile, residing in tubes or burrows in sediments, in or on corals
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Jumars, Dorgan & Lindsay
07 November 2014
or other hard substrata, or nestling among rubble. There is likely a broad range in motility
from nearly sessile tube dwellers to fully motile crawlers. Most are macrophagous, including
carnivory on prey of varied motility, carrion feeding, and herbivory on both macroalgae and
angiosperms. E. pennata has some capacity for short-term caching. Some eunicids are deposit
feeders, either on surface or subsurface sediments, but we suspect that they take advantage of
any rich prey items near their burrows, and we do not know whether deposit feeding alone would
support growth or gamete production.
Research opportunities
• Taxonomic revision is needed to determine the degree of omnivory within species or
populations, especially of Marphysa cf. sanguinea.
• Relationships with corals are poorly understood; stable isotope data would be helpful.
• It would be interesting to know whether deposit-feeding eunicids utilize surfactants in
digestion and to know their rates of growth and maturation on a sediment diet.
References
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different algal growth forms. Helgol. Mar. Res. 60:39–49
Beesley PL, Ross GJ, Glasby CJ, eds. 2000. Fauna of Australia, Vol. 4A, Polychaetes and Allies:
The Southern Synthesis. Canberra: CSIRO Publishing
Castriota L, Gambi MC, Zupo V, Sunseri G. 2003. Structure and trophic ecology of a population
of Lysidice ninetta (Polychaeta) associated to rhodoliths off the Island of Ustica (Southern
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Cigliano M, Manini E, Gambi MC. 2003. First data on cellulolytic enzyme activity in polychaete
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Garcês JP, Pereira J. 2010. Effect of salinity on survival and growth of Marphysa sanguinea
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
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Jumars, Dorgan & Lindsay
07 November 2014
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Guerin AJ. 2009. Marine communities of North Sea offshore platforms, and the use of stable
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Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Washington, D.C.: American Geophysical Union
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Euphrosinidae, Amphinomida
Diversity and systematics
Transfer of Archinome to Amphinomidae (Wicklund et al. 2008) left about 60 species in
Euphrosinidae, all but a few of them in the type genus Euphrosine. Euphrosinidae are small
animals typically a few centimeters long, and nearly as wide.
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Habitat
Euphrosinids are widespread on soft and mixed bottoms, including high latitudes and the deep
sea. Some species are found frequently on sponges. They appear to be primarily epifaunal.
Sensory and feeding structures
The prostomium is reduced to a narrow ridge, and the peristomium to lips around the mouth.
A small pair of lateral antennae projects ventrally. Palps are lacking. Eyes are often present
just lateral to and near the leading edge of the well developed caruncle. Caruncles are support
structures for complex nuchal organs. In Euphrosinidae, the caruncle bears a median keel, three
pairs of longitudinal folds, eight longitudinal, ciliated ridges and a short, medial nuchal cirrus
(Hutchings 2000). Euphrosinids scrape and engulf prey with an eversible, ventral, hypertrophied
pharynx bearing a thickened, ridged cuticle (Hutchings 2000).
Motility
No explicit data on motility have been published. The only prey so far identified are sessile or
slowly moving (F&J).
Illustrations
Hutchings (2000) provides informatively labeled line drawings of anterior structures in an
unidentified euphrosinid in both dorsal and ventral views.
Feeding
F&J cited evidence of feeding on sponges and foraminiferans. We know of no additional direct
observations of ingested diet or additional gut content analyses, but there are at least three more
recent studies that provide some information on diet. Würzberg et al. (2011) dredged samples
from the Weddell and Lazarev Seas at 600 - 5337 m. They sorted polychaetes to the family
level and analyzed their lipids. The five euphrosinid individuals analyzed had lipid signatures
indicative of feeding on foraminiferans, consistent with deep-sea results from the North Atlantic
(F&J).
Grall et al. (2006) in samples from marl beds in the shallow (mean depth 8 m) Bay of Brest
reported δ13C and δ15N values in Euphrosine foliosa characteristic of feeding near the base of
the food web on phytoplankton detritus and considered it a sponge grazer, clustering in stable
isotope values near deposit feeders. Among the polychaetes in their study, only the terebellid
Eupolymnia nebulosa had a lower apparent δ15N. Feeding on sponges is consistent with F&J,
although the possibility of detritus feeding cannot be eliminated on stable isotopic evidence.
Somewhat more ambiguous were the results of Beviss-Challinor & Field (1982), who
reported uptake results with radioactively labeled Artemia eggs and nauplii, Dunaliella cells and
kelp detritus, with these three items presented in separate experiments. Euphrosine capensis
showed substantial uptake of all three foods in incubations as short as 1 h, suggesting that not all
euphrosinids may be carnivorous or detritivorous all of the time.
Guild membership
Euphrosinids were considered exclusively carnivorous by F&J. We would be surprised neither
by additional evidence showing some species at some times to feed on non-animal, relatively
labile materials (phytodetritus and macroalgal detritus) nor by evidence of some species feeding
on more mobile prey.
Research opportunities
• Gut content analysis of additional species would be worthwhile.
• Lipid markers could provide insight into a diet source of phytodetritus versus sponge tissue.
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• There appear to be no direct observations of behavior published (motility or feeding) after
F&J.
References
Beviss-Challinor H, Field JG. 1982. Analysis of a benthic community food web using
isotopically labelled potential food. Mar. Ecol. Prog. Ser. 9:223–30
Grall J, Le Loc’h F, Guyonnet B, Riera P. 2006. Community structure and food web based on
stable isotopes (δ15N and δ13C) analysis of a North Eastern Atlantic maerl bed. J. Exp. Mar.
Biol. Ecol. 338:1–15
Hutchings PA. 2000. Family Euphrosinidae. See Beesley et al. 2000, pp. 110–2
Wiklund H, Nygren A, Pleijel F, Sundberg P. 2008. The phylogenetic relationships between
Amphinomidae, Archinomidae and Euphrosinidae (Amphinomida: Aciculata: Polychaeta),
inferred from molecular data. J. Mar. Biol. Ass. UK 88:509–13
Würzberg L, Peters J, Schüller M, Brandt A. 2011. Diet insights of deep-sea polychaetes derived
from fatty acid analyses. Deep-Sea Res. Pt. II 58:153–62
Fabriciidae, Sabellida
Diversity and systematics
Fabriciidae were recently removed from Sabellidae because molecular evidence showed them
to be more closely related to serpulids than to the remaining Sabellidae (Kupriyanova & Rouse
2008). Fabriciidae comprise about 83 species in 21 genera, 11 of them monotypic and only 3
with > 9 species. Fabriciids are diminutive, adults ranging from 0.85 to 10 mm long (Huang et
al. 2011).
Habitat
Contrary to statements by Huang et al. (2011), Fabriciidae are common at all ocean depths,
including the deep sea (e.g., Hessler & Jumars 1974, Jumars 1975, Blake 1994, Hilbig & Blake
2006, Wilmsen & Schüller 2011) and can be found building tubes both on hard and in soft
substrata. They can be extremely abundant in shallow marine and lotic fresh waters. They
recently have been reported from mud volcanoes in Lake Baikal (Zemskaya et al 2012).
Sensory and feeding structures
The prostomium in fabriciids is transformed into a tentacular crown, each half homologous
with a palp in other polychaete groups (Orrhage 1980) and comprising a number of radioles. A
radiole rises from the branchial lobe and holds laterally paired, cylindrical pinnules. Pinnules
bear long, laterofrontal ciliary bands that bias particle motion toward a wider band of mucuscoated frontal (oral side of the pinnule) cilia that continue onto the trunk, which is rooted in
the branchial lobes that converge in a U on the peristomial mouth. Paired nuchal organs are
located in pits dorsal to the mouth. The mouth, in reference to the ventral nerve chord, is also
ventral. Most genera of Fabriciidae have three radioles on each side, but species of Manayunkia
and Monroika africana have only two (Huang et al. 2011). In those species ventral filamentous
appendages insert just below the dorsal lip and are characteristically used in deposit feeding
(Lewis 1968). Fabriciola spp. have three pairs of radioles plus ventral filamentous appendages,
and Augeneriella spp. bear three pairs of radioles plus a pair of branching, ventral, filamentous
appendages (Fitzhugh 1989). Fabricinuda rosaelenae also bears three pairs of radioles but
bears one pair of ventral (non-branching) filamentous appendages (López & Rodríguez 2008).
The identity and orientation of pinnules can be confusing in Fabriciidae, not least because
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07 November 2014
radioles in these diminutive worms can in some species be the same size as the pinnules in larger
sabellids (Fitzhugh 1989; Bick 2004). Capa et al. (2011) indicated that ventral filamentous
appendages are present in at least some of Augeneriella, Fabriciola, Fabricinuda, Manayunkia,
Pseudofabriciola, and in genus A of Fitzhugh (1989). Genus A has been more recently named
Echinofabricia by Huang et al. (2011) and enlarged by Giangrande et al. (2013). Eyespots may
be present both on the peristomium and the pygidium, indicative backward movement (with the
pygidium in front).
Motility
Discrete motility has been reported from aquarium observations (F&J). Malakusas et al. (2013)
experimented with erosion of M. aestuarina. Shear velocities ≥ 3 cm s-1 were needed to initiate
physical transport of the worms because worms burrowed and secreted copious mucus, avoiding
shear stresses. Mortality was low for eroded worms; they recovered quickly upon reaching more
tranquil conditions.
Illustrations
Fitzhugh (1989) provides informative line drawings of several fabriciids and contrasting
drawings of sabellids. Huang et al. (2011) provide attractive and informative light and scanning
eletron micrographs of a few fabriciids.
Feeding
Whereas the systematics literature on Fabriciidae has been voluminous, new feeding information
has been scarce. By far the most new information has been obtained on Manayunkia aestuarina,
which was already one of the best studied Fabriciidae (Lewis 1968). Taghon (1982) ran particle
choice experiments with glass beads deployed for 15-30 min on the sediment surface in shallow,
sandflat tidepools at low tide and assayed gut contents afterward. From a sediment that was 42%
beads of 13 - 20 µm diam. (by number), with the remainder being beads 20 - 44 µm diam., M.
aestuarina showed highly significant selection for the smaller beads, but 35% of ingested beads
nevertheless were the larger ones. These results indicate that M. aestuarina is able to take large
particles compared to those most frequently ingested by Sabellidae and Serpulidae, and they also
corroborate that it can deposit feed as there were no suspended beads in the experiment.
M. aestuarina has also come under close scrutiny as an obligate intermediate host for
myxosporean parasites that infect juvenile salmon (Wilson et al. 2008). Although most of
the known intermediate hosts for tetractinomyxon actinospores are polychaetes known to
suspension feed (as a potential means to encounter the spores), a single known host (Nephasoma
diaphanes corrugatum) is a deposit-feeding member of Golfingiidae (Køie 2002), so the mode
of infection (deposit or suspension feeding) in M. aestuarina is not known. Successful rearing
of M. aestuarina was achieved by providing moving water and Kent Marine, Inc., Micro-Vert
Invertebrate Food ™ three times a week; powdered yeast as an alternative caused excessive
bacterial growth (Willson et al. 2010). In the Rogue River system, M. aestuarina preferred
slowly flowing but not stagnant habitats and was most abundant where flows decelerated into
reservoirs (Stocking 2006). At those locations, where turbulent resuspension abruptly ceased,
near-bed suspended loads and deposition rates would both be expected to be high.
Lewis (1968) made an interesting distinction that is worth revisiting. He recognized three
feeding modes in M. aestuarina: deposit feeding with what are now called ventral filamentous
appendages, secondary suspension feeding on material resuspended by the activity of the
ventral filamentous appendages, and primary suspension feeding on material suspended by
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Jumars, Dorgan & Lindsay
07 November 2014
other processes. F&J also described a second mode of deposit feeding wherein the worm trails
mucus behind the branchial crown as it moves, pygidium first, along the sediment surface,
before ingesting the mucus with its embedded sediment contents. Lewis (1968) also studied
Fabricia sabella and observed only suspension feeding by ciliary means. Riisgård & Nielsen
(2006) confirmed that Fabricia stellaris feeds by downstream ciliary capture as do Sabellariidae:
Laterofrontal cilia on the pinnules detect particles, catch up with them as they pass laterally, and
convey them into the frontal (downstream) ciliary band.
Galván et al. (2008) studied saltmarsh mudflat and creek-wall infauna, including Manayunkia
aestuarina and Fabricia sabella. 15N data supported a primary diet of suspended particulate
organic material for both species. The second highest food source for F. sabella was Spartina
spp. (detritus that could have been suspended or deposited) whereas M. aestuarina showed
greater dependence on microphytobenthos. Repeated enrichment of sedimentary primary
producers in 15N also supported a greater importance of suspended material to both species.
Although relatively little of these non-suspended sources reached either fabriciid, M. aestuarina
was more than twice as enriched after three weeks as F. sabella, consistent with some deposit
feeding in M. aestuarina. Tissue digestions of both fabriciids (n = 3 in both cases) revealed
frustules of pennate and centric diatoms.
One of us (PA Jumars, unpublished) has observed even species of Serpulidae and Sabellidae
to bend over and sweep the sediment surface when starved of suspended material in an aquarium
and so do not doubt that more mobile and far smaller fabriciids can do the same, but the more
interesting question is the extent to which this behavior occurs in the natural environment.
Whereas some taxa can use only one feeding mode at a time, M. aestuarina can simultaneously
suspension and deposit feed. It appears uniquely adapted by size, motility and appendages to
locate in the lee of flow obstructions in the bottom boundary layer where materials selectively
deposit and attached eddies cause recirculation of suspended materials. This microhabitat
preference would explain its tight spatial association with larger tube builders (Eckman 1979).
Due to their small sizes, we expect fabriciids to be highly selective for labile foods. This
expectation is met in the diatoms reported in the specimens of M. aestuarina and F. sabella
examined by Galván et al. (2008). It appears contradictory to the results of Taghon (1982), but
those individuals were given Hobson’s choice: Eat glass beads (a particle with which there is no
evolutionary experience) or eat nothing.
Guild membership
Fabricia sabella and F. stellaris appear to be obligate suspension feeders. We conjecture that
other species without ventral filamentous appendages will also be found to feed primarily from
suspension. We conjecture that species with ventral filaments will obtain some but < 50% of
their nutrition from surface deposits. That conjecture is based on the relative sizes of the radioles
and filaments and the relative organic richness of suspended versus deposited particles.
Research questions and opportunities
• Fabriciids are good candidates for measurement of clearance rates and observation of
encounter mechanisms in small flow cells (e.g., Marcos & Stocker 2006).
• There is a clear need for experiments to evaluate the importance of suspension versus deposit
feeding in Fabriciidae and to compare multiple species with and without ventral filamentous
appendages in a range of natural flow settings.
• It would be particularly interesting to know the foods eaten by deep-sea species.
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Jumars, Dorgan & Lindsay
07 November 2014
References
Bick A. 2004. Redescription of Pseudoaugeneriella nigra (Langerhans, 1880), new combination
(Polychaeta, Sabellidae), with remarks on some characters of Fabriciinae. Zool. Anz. 243:53–
63
Blake JA. 1994. Vertical distribution of benthic infauna in continental slope sediments off Cape
Lookout, North Carolina. Deep-Sea Res. Pt. II 41:919–27
Capa M, Hutchings P, Teresa Aguado M, Bott NJ. 2011. Phylogeny of Sabellidae (Annelida)
and relationships with other taxa inferred from morphology and multiple genes. Cladistics
27:449–69
Eckman JE. 1979. Small-scale patterns and processes in a soft-substratum benthic community. J.
Mar. Res. 37: 437–57
Fitzhugh K. 1989. A systematic revision of the Sabellidae-Caobangiidae-Sabellongidae complex
(Annelida, Polychaeta). Bull. Am. Mus. Nat. Hist. 192:1–104
Galván K, Fleeger JW, Fry B. 2008. Stable isotope addition reveals dietary importance of
phytoplankton and microphytobenthos to saltmarsh infauna. Mar. Ecol. Prog. Ser. 359:37–49
Giangrande A, Licciano M, Castelli A. 2013. The genus Echinofabricia (Annelida: Fabriciidae)
in the Mediterranean Sea with the description of E. rousei sp. nov. J. Mar. Biol. Ass. UK
93:1773–6
Hessler RR, Jumars PA. 1974. Abyssal community analysis from replicate box cores in the
central North Pacific. Deep-Sea Res. 21:185–209
Hilbig B, Blake JA. 2006. Deep-sea polychaete communities in the northeast Pacific Ocean off
the Gulf of the Farallones, California. Bull. Mar. Sci. 78:243–69
Huang D, Fitzhugh K, Rouse GW. 2011. Inference of phylogenetic relationships within
Fabriciidae (Sabellida, Annelida) using molecular and morphological data. Cladistics
27:356–79
Jumars PA. 1975. Environmental grain and polychaete species’ diversity in a bathyal benthic
community. Mar. Biol. 30:253–66
Køie M. 2002. Spirorchid [sic.] and serpulid polychaetes are candidates as invertebrate hosts for
Myxozoa. Folia Parasit. 49:160–2
Lewis DB. 1968. Feeding and tube-building in the Fabriciinae (Annelida, Polychaeta). Proc.
Linn. Soc. Lond. 179:37–49
López E, Rodríguez CT. 2008. A new species of Fabricinuda Fitzhugh, 1990 (Fabriciinae:
Sabellidae: Polychaeta) from the Caribbean, with an emendation of the genus. J. Nat. Hist.
42:1937–49
Malakauskas DM, Willson SJ, Wilzbach MA, Som NA. 2013. Flow variation and substrate
type affect dislodgement of the freshwater polychaete, Manayunkia speciosa. Freshw. Sci.
32:862–73
Marcos [first author has only one name], Stocker R. 2006. Microorganisms in vortices: a
microfluidic setup. Limnol. Oceanogr. Meth. 4:392–8
Orrhage L. 1980. On the structure and homologues of the anterior end of the polychaete families
Sabellidae and Serpulidae. Zoomorphology 96:113–68
Riisgård HU, Nielsen C. 2006. Feeding mechanism of the polychaete Sabellaria alveolata
revisited: comment on Dubois et al. (2005). Mar. Ecol. Prog. Ser. 328:295–305
Stocking RW. 2006. Distribution of Ceratomyxa shasta (Myxozoa) and habitat preference of the
polychaete host, Manayunkia speciosa, in the Klamath River. MS thesis. Oregon State Univ.,
Corvallis
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Taghon GL. 1982. Optimal foraging by deposit-feeding invertebrates: roles of particle size and
organic coating. Oecologia 52:295–304
Willson SJ, Wilzbach MA, Malakauskas DM, Cummins KW. 2010. Lab rearing of a freshwater
polychaete (Manayunkia speciosa, Sabellidae) host for salmon pathogens. Northwest Sci.
84:183–91
Wilmsen E, Schüller M. 2011. Diversity and distribution of Polychaeta in deep Antarctic and
Subantarctic waters along the Greenwich meridian. Deep-Sea Res. Pt. II 58:2004–12
Zemskaya TI, Sitnikova TY, Kiyashko SI, Kalmychkov, GV, Pogodaeva TV, et al. 2012. Faunal
communities at sites of gas- and oil-bearing fluids in Lake Baikal. Geo-Mar. Lett. 32:437–51
Fauveliopsidae, Cirratuliformia
Diversity and systematics
Fauveliopsidae comprise about two dozen species distributed between two genera, Fauveliopsis
and Lauberiopsis. Their nearest relatives have been difficult to identify on either morphological
or molecular genetic grounds with hints that they may or may not include Sternaspidae,
Flabelligeridae and sipunculans (Struck et al. 2007, Zrzavý et al. 2009; Zhadan & Atroshchenko
2010, Purschke 2011). Body sizes are small, with adult lengths ranging from about 1 mm
(Nuñez et al. 1997) to 2 cm (Zhadan & Astroshchenko 2010).
Habitat
Fauveliopsids are regular members of soft-bottom abyssal and bathyal communities, where they
are frequently found in tubes, shells and tests of other organisms. A few species are found in
shallower waters, where they tend to be interstitial (Riser 1987, Nuñez et al. 1997).
Sensory and feeding structures
Fauveliopsids lack head appendages. The anterior is retractable, in common with some
Flabelligeridae, the monotypic Poeobidae and all sipunculans, although Zhadan & Atroshchenko
(2010) found that only the prostomium and peristomium of Laubieriopsis sp. from the North Sea
form the introvert and suggest that the introvert is not homologous with those of flabelligerids
(which include the first segment as well). In a number of species, nuchal organs are a pair of
densely ciliated, flat, dorsolateral tufts at the rear of the prostomium in (Riser 1987, L. arenicola;
Purschke 1997, 2011, F. cf. adriatica; Petersen 2000, L. cabiochi). Petersen (2000) considered
this state to be common to all members of the family. In L. norvegica, however, nuchal organs
are ciliated pits in roughly the same location (Zhadan & Atroshchenko 2010). Just medial to the
nuchal organs are a pair of ocellar tubes resembling structures in sipunculans (Purschke 2011).
The ventral mouth opening has dorsolateral ciliary folds but lacks a ventral pharyngeal organ
(Zhadan & Atroshchenko 2010).
Motility
Very little is known about motility in fauveliopsids, but their use of tubes, tests and shells
produced by other organisms suggests that motility is limited despite their lack of extensible
feeding appendages, a puzzling situation.
Illustrations
Purschke (2011) and Thiel et al. (2011) taken together provide good orientation to the
morphologies of this family. Purschke (1997, Fig. 2L) provides an electron micrograph of an
anterior view of F. cf. adriatica with nuchal organs in the form of densely ciliated, flat tufts.
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Jumars, Dorgan & Lindsay
07 November 2014
Feeding
Gaston (1987) reported finding detritus in 8 dissected individuals of a Fauveliopsis sp. Blake &
Petersen reported that their largest specimens of F. glabra (c. 1 cm long) contained fine silt and
a few larger particles including forminiferans. Thiel et al. (2011) similarly found that F. confusa
frequently had sediment grains in its gut and inferred a diet of bacteria and detritus. Würzberg
et al. (2011) dredged samples from the Weddell and Lazarev Seas at 600-5337 m. They sorted
polychaetes to the family level and analyzed their lipids. The three fauveliopsids assayed
showed lipids characteristic of fresh diatom detritus.
Fauveliopsis jameoaquensis is a shallow-water, interstitial species in coarse sand and lapilli
in dimly lit, igneous caves that has only 10 setigers and does not exceed 1.3 mm in length
(Nuñez et al. 1997). Brito et al. (2009) referred to F. jameoaquensis as an omnivore but did not
specify the nature of the evidence. We expect a species this small to specialize on ingesting
labile, digestively rewarding items such as diatoms.
Guild membership
On the basis of this scant evidence we infer that small fauveliopsids specialize on rich detritus
and live diatoms and that larger species (> 1 cm long) may deposit feed as adults. We tentatively
list them as motile as did F&J, largely due to the lack of extensible feeding appendages. Most
of the species we have recovered from deep-sea samples have been found in the uppermost layer
of vertically sectioned cores, but we very tentatively classify them as subsurface detritivores or
deposit feeders as did F&J and Gaston (1987).
Research opportunities
• Stable 15N data and additional gut contents analyses would be useful for identifying trophic
levels of feeding as would time-versus-uptake data with stable-isotope-labeled substrates.
• Motility and feeding depth merit quantification.
References
Blake JA, Petersen ME. 2000. Family Fauveliopsidae Hartman, 1971. In Taxonomic Atlas of the
Benthic Fauna of the Santa Maria Basin and the Western Santa Barbara Channel ed. JA
Blake, B Hilbig, P Valentich, PH Scott, 7:31–45. Santa Barbara, CA: Santa Barbara Mus.
Nat. Hist.
Brito MC, Martínez A, Núñez J. 2009. Changes in the stygobiont polychaete community of the
Jameos del Agua, Lanzarote, as a result of bioturbation by the echiurid Bonellia viridis. Mar.
Biodiv. 39:183–7
Gaston GR. 1987. Benthic Polychaeta of the Middle Atlantic Bight: feeding and distribution.
Mar. Ecol. Prog. Ser. 36:251–62
Núñez J, Ocaña O, del Carmen Brito M. 1997. Two new species (Polychaeta: Fauveliopsidae
and Nerillidae) and other polychaetes from the marine lagoon cave of Jameos del Agua,
Lanzarote (Canary Islands). Bull. Mar. Sci. 60:252–60
Petersen ME. 2000. A new genus of Fauveliopsidae (Annelida:Polychaeta), with a review of its
species and redescription of some described taxa. Bull. Mar. Sci. 67:491–515
Purschke G. 1997. Ultrastructure of nuchal organs in polychaetes (Annelida)—new results and
review. Acta Zool. 78: 123–43
Purschke G. 2011. Sipunculid-like ocellar tubes in a polychaete, Fauveliopsis cf. adriatica
(Annelida, Fauveliopsidae): implications for eye evolution. Invertebr. Biol. 130:115–28
Riser NW. 1987. A new interstitial polychaete (Family Fauveliopsidae) from the shallow subtidal
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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of New Zealand with observations on related species. Bull. Biol. Soc. Wash. 7:211–6
Struck TH, Schult N, Kusen T, Hickman E, Bleidorn C, et al. 2007. Annelid phylogeny and the
status of Sipuncula and Echiura. BMC Evol. Biol. 7:57, 11 pp.
Thiel D, Purschke G, Böggemann M. 2011. Abyssal Fauveliopsidae (Annelida) from the south
east Atlantic. J. Nat. Hist. 45:923–37
Würzberg L, Peters J, Schüller M, Brandt A. 2011. Diet insights of deep-sea polychaetes derived
from fatty acid analyses. Deep-Sea Res. Pt. II 58:153–62
Zhadan AE, Atroshchenko MM. 2010. The morphology of Laubieriopsis sp. (Polychaeta,
Fauveliopsidae) and the position of fauveliopsids in the polychaete system. Biology Bull.
37:876–85
Zrzavý J, Říha1 P, Piálek L, Janouškovec J. Phylogeny of Annelida (Lophotrochozoa): totalevidence analysis of morphology and six genes. BMC Evol. Biol. 9:189 14 pp.
Flabelligeridae, Cirratuliformia
Diversity and systematics
Flabelligeridae comprise about 150 species distributed among 22 genera, 7 of them monotypic.
The family is undergoing extensive analysis and revision on the basis of both morphology
(Salazar-Vallejo et al. 2008) and molecular genetics (Osborn & Rouse 2011). On a molecular
genetic basis, both Buskiella (a senior synonym of Flota cf. Salazar-Vallejo & Zhadan 2007)
and Poeobius fall within Flabelligeridae but in different clades, indicating evolution of pelagic
forms at least twice (Osborn & Rouse 2008). Although we expect Poeobius to be placed in
Flabelligeridae, we give its details under Poeobidae. Flabelligeridae appear most closely related
to Acrocirridae (Osborn & Rouse 2011). Non-pelagic genera have been extensively revised
(Salazar-Vallejo 2012a, b; 2013). Adult lengths range from a diminutive 5 mm up to 22 cm
(Rouse 2001). General appearance is often dominated by a gelatinous tunic that may or may
not be smooth, may or may not allow numerous papillae to project through, and may or may not
carry a tightly adhering layer of sediments. Morphologies can vary substantially even within
genera, but two end members are frequent: short fusiform species lacking cephalic cages (e.g.,
Brada spp.) and elongate, anteriorly inflated species usually with a cephalic cage (e.g., many
Pherusa spp.) that occupy a blind-ended burrow in a J shape with the posterior end of the worm
folded over and pointed toward the burrowing opening.
Habitat
Flabelligerids are common but rarely abundant. They are found on and in both hard and soft
substrata at all ocean depths. Some benthic species nestle under rocks, some bore into loess
underlying dense coralline algal crusts and appear capable of lining their burrows with aragonite
(Amor 1994, Hutchings 2000), some are commensal on echinoderms, and many burrow in sand
or mud. They do not construct tubes. Buskiella spp. are pelagic in deep water, but observations
of living specimens are scarce, preserved specimens are often only fragments, and their
distribution between bottom boundary layers and mid waters is not well known (Salazar-Vallejo
& Zhadan 2007). The sole exception is the report by Robison et al. (2010) that Buskiella vitjasi
feeds both in the bottom boundary layer and in mid waters above.
Sensory and feeding structures
Anterior appendages are best viewed head on (F&J, Fig. 9). The prostomium is reduced to a
longitudinal, caruncle-like dorsal ridge that may bear up to 4 eyes. Head on, it appears centrally
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located and nose like. It is flanked by one pair of ciliated, grooved palps inserted just above
cheek-like lateral lips that themselves flank the mouth. The locations of palp scars make
them often resemble eyes in a face (Spies 1975). Below the mouth is a chin-like lower lip. A
generally smaller upper lip may be visible (Filippova et al. 2003). Limits of the peristomium
are not apparent. The upper half of the “face” is occupied by a few to scores of filamentous
branchiae. A pair of ciliated nuchal organs curve along the sides of the prostomium to the
insertions of the palps and the closest branchiae to them. In many species the head can retract,
flexing anterior chaetae into a protective, forward-extending, cephalic cage. Individuals have a
ventral pharynx with dorsolateral ciliary folds and a bulbous muscle (Purschke & Tzetlin 1996).
Motility
F&J listed flabelligerids as either discretely motile or motile, the latter based on a description by
Rasmussen (1973) of motility of Flabelligera affinis, an epifaunal form. The species certainly
falls at the more mobile end of the spectrum, but it may not meet our criterion of needing to
move to feed, especially if it finds itself in a high-flux microenvironment. We regard all benthic
flabelligerids as discretely motile. Many shallow-water, benthic species are most active at night,
and it is not unusual to catch individuals in the water column then (PA Jumars, pers. obs.). In
laboratory aquaria with Pherusa affinis, burrows often remained in one location for weeks.
Individuals removed from sediments quickly reburrow, but a well developed burrow system is
not evident for P. affinis for several days (PA Jumars, pers. obs.). Robison et al. (2010) listed
Buskiella vitjasi has well developed swimming chaetae (Osborn & Rouse 2008, Fig. 1).
Illustrations
The head-on stippled line drawings by Spies (1975) give a good idea of the variety of
flabelligerids, as do the color photographs by Salazar-Vallejo (2012a, b; 2013).
Feeding
Few observations or experiments with identified, individual, benthic flabelligerid species have
been reported since F&J, and observations on behavior of the short, fusiform species are absent.
Beviss-Challinor & Field (1982), however, reported results for an unidentified Pherusa sp. and
other members of a kelp holdfast community in South Africa exposed separately to radioactively
labeled Artemia eggs and nauplii and to labeled kelp detritus. Pherusa sp. took up label from
both. Beviss-Challinor & Field (1982) inferred that the Pherusa must have taken up label
from feces of a carnivore that was included in the experiment with Artemia, but we suspect
instead that it ingested the eggs, and possibly even some nauplii, directly. We have observed
few detritivores or deposit feeders to reject non-motile parcels of protein and lipid that are in
a suitable particle size category for ingestion. Amor (1994) reported an intertidal, endolithic
Pherusa sp. from Argentina using the chaetae of its cephalic cage to filter particles from the
water and then transporting them to the mouth with its palps. Robison et al. (2010) indicated
that Buskiella vitjasi is a predator in the BBL and mid waters above but indicated neither the
observations that led them to this conclusion nor whether their observations indicated sit-andwait or more mobile predation.
At both cold seeps (Levin et al. 2000) and hot vents (Decker & Olu 2010), stable isotopic
content suggests little or no dietary dependence on chemosynthetic bacteria among flabelligerids.
They apparently depend on photosynthetically produced detritus in most settings. Würzberg et
al. (2011) dredged samples from the Weddell and Lazarev Seas at 600 - 5337 m. They sorted
polychaetes to the family level and analyzed lipids. The two flabelligerids sampled had lipid
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contents consistent with feeding on fresh phytodetritus. Two species of Brada from the Chukchi
Sea, however, while showing δ13C consistent with a phytoplankton source, had δ15N signatures
comparable to lumbrinerids at the same station, suggesting an animal or microbially modified
diet. We suspect the latter. Brada spp. are short and fusiform and lack a cephalic cage. Two
individuals of Pherusa plumosa from 180 –182 m water depth in Isfjorden, Svalbard, had δ15N
substantially below values for Polynoidae at the same site (Løkken 2013), suggesting more
ordinary deposit feeding. Although the authors without explanation classified it as a carnivore on
invertebrates, Pherusa eruca collected from seagrass beds around Mallorca Island also showed
15
N consistent with surface deposit feeding (Deudero et al. 2014).
Guild membership
We regard soft-sediment, benthic flabelligerids to be discretely motile, moving on the sediment
surface and even into the water, primarily at night. Species boring into hard substrata and
producing blind-ending burrows typically have a long, thin posterior indicative of a folded-over
posture in the burrow (e.g., Amor 1994) and the may be functionally sessile. We base opinion
regarding soft-sediment species on evidence in F&J, our own aquarium observations of Pherusa
spp. and field capture of Pherusa spp. in shallow-water plankton nets and emergence traps. We
regard species > 1 cm long as tentaculate surface deposit feeders with some capability to select
more nutritious material or obtain it from their hosts (F&J) but suspect that smaller species
specialize on richer detritus. We tentatively list Buskiella spp. as discretely motile (buoyancyadjusting and perhaps more actively pursuing) predators based on the report by Robison et al.
(2010) but have no indication of prey identity.
Research opportunities
• Direct observations of feeding on small, fusiform species would be rewarding.
• Additional δ15N measurements and pulse-chase experiments with labeled substrates would be
informative.
• Quantitative tests of Spies’ (1975) suggestion of feeding on seston entrained by respiratory
currents are in order.
• More data on motility and feeding by pelagic forms would be informative as would
quantitative motility data on benthic forms.
References
Amor A. 1994. Ecology of Pherusa sp.(Polychaeta, Flabelligeridae). Mémoir. Mus. Natl. Hist.
162:339–46
Beviss-Challinor MH, Field JG. 1982. Analysis of a benthic community food web using
isotopically labeled potential food. Mar. Ecol. Prog. Ser. 9:223–30
Decker C, Olu K. 2010. Does macrofaunal nutrition vary among habitats at the Hakon Mosby
mud volcano? Cah. Biol. Mar. 51:361–7
Deudero S, Box A, Vázquez-Luis M, Arroyo NL. 2014. Benthic community responses to
macroalgae invasions in seagrass beds: Diversity, isotopic niche and food web structure at
community level. Estuar. Coast. Shelf Sci. 142:12–22
Filippova AV, Tzetlin AB, Purschke G. 2003. Morphology and ultrastructure of the anterior
end of Diplocirrus longisetosus Marenzeller, 1890 (Flabelligeridae, Polychaeta, Annelida).
Hydrobiologia 496:215–23
Hutchings PA. 2000. Family Flabelligeridae. See Beesley et al. 2000, pp. 215–8
Levin LA, James DW, Martin CM, Rathburn AE, Harris LH, Michener RH. 2000. Do methane
seeps support distinct macrofaunal assemblages? Observations on community structure and
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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nutrition from the northern California slope and shelf. Mar. Ecol. Prog. Ser. 208:21–39
Løkken, TS. 2013. Carbon source and trophic structure along a depth gradient in Isfjorden,
Svalbard. MS thesis. University of Tromsø
Osborn KJ, Rouse GW. 2008. Multiple origins of pelagicism within Flabelligeridae (Annelida).
Mol. Phylogenet. Evol. 49:386–92
Osborn KJ, Rouse GW. 2011. Phylogenetics of Acrocirridae and Flabelligeridae (Cirratuliformia,
Annelida). Zool. Scr. 40:204–9
Rasmussen E. 1973. Systematics and ecology of the Isefjord marine fauna (Denmark) with a
survey of the eelgrass (Zostera) vegetation and its communities. Ophelia 11:1-507
Robison BH, Sherlock RE, Reisenbichler KR. 2010. The bathypelagic community of Monterey
Canyon. Deep-Sea Res., Pt. II 57:1551–6
Rouse GW. 2001. Flabelligeridae Saint-Joseph, 1894. See Rouse & Pleijel 2001, pp. 223–5
Salazar-Vallejo SI. 2012a. Revision of Flabelligera Sars, 1829 (Polychaeta: Flabelligeridae).
Zootaxa 3203:1–64
Salazar-Vallejo SI. 2012b. Revision of Trophoniella Hartman, 1959 (Polychaeta, Flabelligeridae).
Zoosystema 34:453–519
Salazar-Vallejo SI. 2013. Revision of Therochaeta Chamberlin, 1919 (Polychaeta:
Flabelligeridae). Zoosystema 35:227–63
Salazar-Vallejo SI, Carrera-Parra LF, Fauchald K. 2008. Phylogenetic affinities of the
Flabelligeridae (Annelida, Polychaeta). J. Zool. Syst. Evol. Res. 46:203–15
Salazar-Vallejo SI, Zhadan AE. 2007. Revision of Buskiella McIntosh, 1885 (including Flota
Hartman, 1967), and description of its trifid organ (Polychaeta, Flotidae). Invertebr. Zool.
4:65–82
Spies RB. 1975. Structure and function of the head in flabelligerid polychaetes. J. Morphol.
147:187–207
Würzberg L, Peters J, Schüller M, Brandt A. 2011. Diet insights of deep-sea polychaetes derived
from fatty acid analyses. Deep-Sea Res. Pt. II 58:153–62
Glyceridae, Glyceriformia
Diversity and systematics
Glyceridae comprise about 90 species in 4 genera, 2 of them monotypic. The vast majority of
species are in the type genus, Glycera. The family was last revised by Böggemann (2002) who
reviewed 172 named species and subspecies, largely based on type material, and concluded
that only 42 species were valid (36 Glycera, 1 Glycerella and 1 Hemipodia). Recent molecular
analyses have suggested that cryptic species of Glycera may abound (Schüller 2011). Molecular
genetics and morphology place the family sister to Goniadidae within Phyllodocida (Zrzavý
et al.2009, Struck et al. 2011). Less expectedly, molecular genetics also show affinities to
Lumbrineridae and Onuphidae (Rousset et al. 2007, Struck et al. 2011). Lengths range from
about 1 to 60 cm.
Habitat
Glycerids are found in soft and mixed sediments and rubble at all water depths (Böggemann
2002). They are also known from shipworm burrows in wood experimentally deployed on the
bathyal seafloor (Böggemann et al. 2011). Glycerids are most abundant in shallow water.
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Sensory and feeding structures
A typically conical prostomium terminates with two pairs of short appendages, one dorsolateral
and the other ventrolateral, that appear to serve primarily mechanosensory functions. The ventral
pair is more nearly terminal. The prostomium consists of multiple rings, all but the first and last
bearing cilia (Böggemann 2002). The diameter of the worm may increase gradually or abruptly
at the posterior of the prostomium. Eyes are not known in adults. Nuchal organs have not been
detailed in most early descriptions, but a pair of bulbous, eversible, lateral nuchal organs midway
along the prostomium are described in Glycera convoluta (Purschke 1997); in G. unicornis
they occur in the posteriormost annulus of the prostomium (Böggemann & Fiege 2001). The
peristomium is reduced, but the worm’s entire aspect is dominated by an extraordinarily long,
muscular, axial, eversible pharynx tipped with four hollow, venomous fangs equally spaced
around the opening of the everted pharynx. The mouthward-curving fangs contain a copperbased mineral that increases their hardness and stiffness, giving them a resistance to abrasion
almost as great as vertebrate tooth enamel (Lichtenegger et al. 2002). The pharynx also bears
varied papillae that appear to have mechanosensory function (Böggemann et al. 2000).
Motility
Glycerids can be discretely motile, setting up a gallery of connected burrows through which they
hunt overpassing epifauna (Ockelman & Vahl 1970). Adults move around in the water column
at night, not only in breeding seasons (Dean 1978), but in feeding terms we share Böggemann’s
(2002) doubt that continual movement is common. The great reach of the everted pharynx seems
well suited to sit-and-wait predation. The pharynx is also used in burrowing and, unlike most
other burrowers studied so far, exerts much greater tensile stresses on the burrowing medium
than the minimum to propagate a crack (Murphy & Dorgan 2011). Large G. dibranchiata exert
sufficient force to produce unstable fracture (shattering) of gelatin (Murphy & Dorgan 2011).
Potential reasons for excess force production include an ability to liquefy sands and to crack
through toughened tube and burrow walls of prey.
Illustrations
Böggemann’s (2002) revision gives comprehensive line drawings and scanning electron
micrographs. The small subset of species similarly illustrated in Böggemann & Fiege (2001)
gives a good impression of the variety of head shapes. Murphy & Dorgan (2011) show images
and supplementary videos of Hemipodus simplex burrowing in gelatin.
Feeding
Gaston (1987) dissected 15 G. capitata, 29 G. dibranchiata, 6 G. robusta and 5 Hemipodus
roseus individuals from the Mid-Atlantic Bight. Most were empty, but, in this same order of
species the following numbers of individuals had the following gut contents: none; 5 with coarse
sand and one each with an amphipod and a polychaete; none; and, 1 with coarse sand.
In an entirely different approach to understanding diets, Voparil et al. (2008) examined lipid
digestion in freshly collected G. dibranchiata from the intertidal of midcoast Maine, finding
that it produced emulsions with droplet sizes up to 25 µm diam. This digestive mode for lipids
differs dramatically from the micellar surfactants used by deposit feeders to scavenge scarcer
hydrophobic components from sediments. As Voparil et al. (2008) noted, such emulsions would
be difficult to digest and transport to absorptive sites through a fine-grained sediment. These
findings imply that if indeed some glycerids deposit feed on muds they are unlikely to digest
animal prey at the same time. G. dibranchiata was listed by F&J as a species consistently
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observed to detritus feed. Voparil et al. (2008) saw no evidence, however, of any detritus or
sediment ingestion in the specimens they dissected. Ambrose’s (1984) manipulative field and lab
experiments, also in midcoast Maine, had results consistent with predation by G. dibranchiata
at a level that affected community composition, strongly indicating significant predation by
this species on Alitta virens or an effective flight response by the latter. We are unaware of any
documentation of detritus feeding in glycerids after F&J.
Ambrose’s (1984) and Voparil’s (2008) results for G. dibranchiata conflict with F&J’s
conclusion that this species is a detritivore and that glycerid species fall cleanly into detritivore
or carnivore categories. Sanders et al. (1962) accepted Klawe & Dickey’s (1957) conclusion
that the species is a detritivore, but Sanders et al. (1962) presented no evidence for detritivory.
On the contrary, of 19 individuals they dissected, 17 were empty, 1 had only sand, and the other
had sand and abundant polychaete chaetae. Klawe & Dickey (1957), in turn, based skepticism
of carnivory on their and prior workers’ inabilities to elicit predation by presenting potential
prey. Ockelmann & Vahl (1970) clearly showed for Glycera alba that construction of a burrow
network and detection of fluid oscillations (vibrations) was prerequisite for predatory strikes,
casting doubt on the value of negative predation results absent both a normal predator domicile
and moving prey.
Hartman (1950) expressed skepticism that fangs with secretory glands were of use to
detritivores, but at the time venom secretion had not been documented. When F&J drew their
conclusions, studies of the venom were just beginning (e.g., Michel & Keil 1975). Subsequent
characterizations have been much more specific regarding mode of action (e.g., Bon et al.
1985, Meunier et al. 2002). Very recently, von Reumont et al. (2014) applied transcriptomics
to venom gland cells of Glycera dibranchiata, G. fallax and G. tridactyla and identified coding
for precursors in 20 known toxin classes. Böggemann (2002) in the most recent review of the
family reflects the trajectory of the evidence since F&J toward carnivory in glycerids as the
norm. We strongly suspect that most of the reports of detrital gut contents in F&J were based
on the unusual appearance of animal remains in the guts of glycerids. The active lipid digestion
system in these animals quickly turns prey remains into a brown, pasty emulsion (Voparil et al.
2008), highlighting semantic difficulties surrounding the term “detritus feeding.”
Stable isotopic analyses have been more frequent since F&J than have other feeding studies
on glycerids. Le Loc’h et al. (2008) sampled largely distinct mud and sand communities on the
continental shelf of the Bay of Biscay. G. rouxii was common to both and showed the highest
enrichment of any polychaete in 15N, confirming its predatory status. Similar results have been
seen for: G. rouxii in the Iroise Sea, Western Brittany (Bodin et al. 2008); G. alba, G. celtica and
G. unicornis from the Bay of Banyuls-sur-Mer (Carlier et al. (2007); G. alba from 60 m water
depth in the Gullmar Fjord, Sweden (Magnusson et al. 2003); G. tridactyla from an intertidal
site in Arachon Bay (Schaal et al. 2008), from Brest Harbor (Schaal et al. 2010), from seagrass
beds near Roscoff (Ouisse et al. 2012), and from the intertidal zone of the east coast of South
Africa between the Mgazi and Mgazana estuaries (Bezuidenhout 2010); G. macintoshi and G.
nicobarica from Ariake Sound, southern Japan (Yokoyama et al. 2005, 2009); Glycera spp. from
Pleasant Bay, Cape Cod (Carmichael et al. 2004); and, Glycera sp. from St. Lucia estuary, South
Africa (Govender et al. 2011), from shallow water in the Bay of A Coruña, NW Spain (Bode
et al. 2014) and from seagrass beds in Dong-dae Bay, North Korea (Ha et al. 2014). Because
other potential prey were largely unsampled, in our view Ha et al. (2014) do not provide strong
support for their suggestion that Glycera sp. feeds on meiofauna. Sampaio et al. (2010) found
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Jumars, Dorgan & Lindsay
07 November 2014
Glycera sp. to have reduced enrichment in the immediate vicinity of a pair of sewage outfalls off
Lisbon, Portugal, but the sediment isotopic signature was also depressed by the outfall, thus still
supporting the trophic position of Glycera sp. as a predator. In the Mondego estuary, Portugal,
G. tridactyla and its prey apparently integrated over modest seasonal changes in signatures of
particulate organic inputs to show no seasonal change in enrichment (Baeta et al. 2009a, b). In
two tributaries to Waquoit Bay on Cape Cod, G. americana’s enrichment reflected that of the
ambient sediments and its predatory status (Martinetto et al. 2006). In a slow succession from
new cold seep to background community in the Gulf of Mexico, G. tesselata’s enrichment
tracked gradual increase in isotopic enrichment toward later successional stages less dependent
on methane (Cordes et al. 2010).
Carlier et al. (2009), however, found significant small-scale variation in the apparent trophic
level of G. alba within the Salces-Leucate Lagoon on the Mediterranean coast. In the southern
basin it had similar enrichment to the other Glycera results quoted above, but in the northern
basin it appeared to feed considerably lower in the food web. G. tridactyla from an oyster
culture site the Bay of Veys, Normandy, also was less enriched in 15N than expected of a predator
(Dubois et al. 2007). The same was true of a Glycera sp. from some locations off the coast of
Portugal (Sampaio 2010) and another Glycera sp. from the Godaviri estuary in the Bay of Bengal
(Sarma et al. 2012). Fedosev et al. (2014) studied a shallow-water (6 - 18 m) sand community
off southern Vietnam; unspecified glycerids had δ15N equal to that of spionids and near that of
sabellids, but neither microphytobenthos nor phytoplankton values were measured. Some of this
variability among locations and species likely is due to differences in trophic level of glycerid
prey, but an alternative explanation is feeding on rich patches of microphytobenthos.
Guild membership
Glycera alba is clearly a sit-and-wait (discretely motile) predator (Ockelmann & Vahl 1970).
Some glycerids may be more motile and thus better at encountering sessile prey. We are
unconvinced by the published evidence that detritus is the primary food source of any glycerid.
Sand is not infrequently reported from gut contents, leaving open the possibility that it is taken
along with lipid- and protein-rich materials such as diatoms or bacterial films or foraminiferans
from which the feeding devices of glycerids have little ability to separate sediment grains;
inclusion of sand presents little digestive difficulty. Mixing of mud with rich food resources
presents substantial digestive difficulties and is less likely. Motile epifaunal or infaunal hunting
appears feasible among glycerids but has not been documented.
Research questions and opportunities
• Motility data on both glycerids and their ingested prey would inform.
• Stable isotopic and lipid tracer data on populations of glycerids thought to detritus feed
would be useful, especially if combined with analysis of gut contents.
• Lipid analysis of putative detritus in gut contents could be informative.
• Is it possible to elicit growth in any glycerid on a detrital diet?
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Golfingiidae, Sipuncula
Diversity and systematics
As recently redefined by Kawauchi et al. (2012), Golfingiidae comprises about 80 species
distributed among seven genera, one of them monotypic (containing only Phascolopsis gouldii).
They are small to medium in size, with trunk lengths of 1 - 20 cm (Kawauchi et al. 2012). The
family constitutes a clade most closely related to a second clade containing all other families
of sipunculans except Sipunculidae. Relations to other polychaete families have been unclear
because sipunculans appear to be fairly basal in the polychaete tree (Dordel et al. 2010; Struck et
al. 2011), but recent molecular analysis showed Sipuncula to be sister to Amphinomidae (Weigert
et al. 2014).
Habitat
Golfingiids occupy the full range of ocean depths. Most burrow in sand and mud, although
sediment-filled crevices in rocks, reefs and rubble may be used, especially by suspension-feeding
forms (e.g., Awati & Pradhan 1935). In shallow water they can reach abundances of 4 × 103 m-2
(Rice et al. 1983) and be important components of benthic carbon budgets (e.g., Rodhouse &
Roden 1987). They can reach abundances of 3 × 102 m-2 in bathyal locations where steep slopes
cause high fluxes of particulate material (Thompson 1980). Romero-Wetzel (1987) reported
finding surface burrow openings as dense as 1.1 × 104 m-2 in cores from the Vöring Plateau on
the Norwegian continental slope, likely created by Nephasoma lilljeborgi, although only 4 × 102
individuals m-2 with trunk lengths of 3 - 20 mm and diameters of 0.2 - 0.5 mm were recovered
from the cores. A few burrows extended ≥ 50 cm into the sediment. Romero-Wetzel (1987)
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inferred that an individual worm probably occupied about 20 burrows; Shields & Kędra (2009),
in a follow-up study identified four Nephasoma spp. in the region but N. lilljeborgi as largely
responsible for the dense burrow networks. Wolff (1979) reported Nephasoma schuettei from
burrows, likely made by other organisms, in deep-sea wood fragments. N. eremita is found in
cold waters at deep shelf and shallow bathyal depths (Hobson et al. 2002).
Sensory and feeding structures
Golfingia, Nephasoma, Phascolion, Themiste, Thysanocardia and Golfingia spp. bear prominent,
bulbous, dorsal nuchal organs aboral to the circle of oral feeding tentacles. Eyespots are
generally present as variably developed ocular tubes (Cutler 1994). In Thysanocardia spp., a
secondary set of tentacles may encircle the nuchal organ (Adrianov et al. 2006), and the introvert
is somewhat longer than the trunk. In Themiste and Thysanocardia spp., the oral surface of the
tentacles is grooved and heavily ciliated (Pilger 1982, Adrianov et al. 2006). Thysanocardia
tentacles are filiform and carry both lateral and aboral cilia (Maiorova & Adrianov 2005). In
Themiste, the oral tentacles branch from either 4 or 6 stems in adults, and the introvert is not
as long as the trunk (Cutler 1994). There is some confusion about ciliation on the pinnules of
Themiste lageniformis. Although they are sparse and aboral, and lateral tufts are evident in Fig.
2B of Pilger (1982), Maiorova & Adrianov (2005, p. 26) concluded that they were absent.
The reaches and tentacle structures of the remaining golfingiids are highly variable (Cutler
1994): Tentacle structure is highly variable among Golfingia spp., but the introvert is usually
shorter than the trunk. In Phascolion, the introvert varies from ½ to 4 times trunk length, and
tentacle structure is highly variable. According to species descriptions in Stephen & Edmonds
(1972) as well as in Cutler (1994), Phascolion lutense has ≤ 16 tentacles, reflecting the original
description of the species. There appears to be an error on p. 115 of Cutler (1994) where he
included P. lutense in a group of species lacking tentacles and having < 10 lobes. Onchnesoma
spp. sport < 10 tentacles; they may be highly reduced or entirely absent, and the introvert is much
longer than the trunk. Nephasoma spp. may also have reduced tentacles; introverts are as long as
or shorter than the trunk. Phascolopsis gouldii has an introvert about 1/3 trunk length, tipped with
abundant tentacles. As in other sipunculans, the mouth and anus are closely juxtaposed, enabling
the double helical twisting of a long gut within the trunk and setting up an ideal topology for
osmotic counterflows.
Motility
The kind of investment in burrow structure seen in Nephasoma lilljeborgi suggests limited,
discrete motility primarily through burrowing. All golfingiids appear to retain the ability to
burrow if placed on the sediment surface. This kind of reburial has been studied in particular in
Themiste hennahi (Pebbles & Fox 1933, Tarifeño 1975) and is accomplished by arching the body
to give the introvert a downward component of motion into the sediment, taking advantage of
the weight of the body and larger rocks and sediment grains to help direct the force downward
(Tarifeño 1975). Murina (1984) regarded most Phascolion and certain Golfingia species to
shelter in shells, tests and tubes of other organisms and was of the opinion that they “usually
move very little.” Contrary to that suggestion, field-observed specimens of P. strombus appeared
to move relatively frequently, with grooves from dragging of the shell visible behind most
specimens even though the introvert rarely was seen on the sediment surface (G. Hampson, pers.
commun. of diving observations).
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07 November 2014
Illustrations
Rice (1993, Figs. 17, 19, 21) provides informative drawings of anterior structures of Nephasoma
pelucidum, Phascolion cryptum, and Phascolosoma nigrescens, in the latter two cases including
the nuchal organs. Gage (1968, Fig. 1) presents a very informative drawing summarizing the
feeding geometry of P. strombus and its respiratory currents through the snail shells that it
utilizes. The high diversity of feeding structures among Golfingiidae can be appreciated from the
line drawings in Stephen & Edmonds (1972) and in Cutler (1994).
Feeding
Murina (1984) reviewed sipunculan feeding modes and placed them in 4 categories, 3 of which
are found in Golfingiidae. The only category missing from Golfingiidae comprises worms that
bore or nestle in hard substrata and use introvert hooks to scrape food from surrounding surfaces.
Themiste and Thysanocardia appear primarily to suspension feed with an as yet undescribed,
mucociliary mechanism. They and Antillesoma antillarum (Antillesomatidae) are the only
known suspension feeders among sipunculans, with possible addition of a species of Sipuncula
(Thomsen & Flach 1997). In one of the earliest quantitative studies of feeding in golfingiids,
Peebles & Fox (1933) worked with the species now known as Themiste hennahi. They made the
interesting observation that worms brought in from the field often had guts packed with sand but
that worms kept in the laboratory rarely ingested any. The animals were collected from strongly
wave-swept environments where sand is frequently resuspended, whereas no such resuspension
occurs in typical aquaria. In the laboratory, worms could be induced to ingest deposited sand and
tracer charcoal particles, however, by adding blood serum or egg albumin. These experiments
demonstrated a functional ability to deposit feed, and Peebles & Fox (1933) suggested based on
their observations that the species can feed above, on and beneath the sediment-water interface
if rich food is present there and absent from other locations. Awati & Pradhan (1935) studied the
species now known as Themiste lageniformis and observed that it suspension fed with cilia on
sand, organic debris microorganisms and meiofauna.
Murina (1984) considered species that utilize shells and tests (most Phascolion and certain
Golfingia spp.) as a relatively uniform trophic group that are mostly epifaunal and engage in
surface deposit feeding. Murina (1984) also noted that deep-sea P. lutense (redescribed by
Murina 1957) built its own thick, gray, silt tubes from which it surface deposit fed with well
developed tentacles on detritus. At least some species in this group, however, are subsurface
deposit feeders. P. strombus is a shallow-burrowing subsurface deposit feeder that occasionally
surface deposit feeds (Hampson 1964, Gage 1968). It usually occupies snail shells and
maintains an incurrent siphon opening to the sediment-water interface, probing the sediment
in all directions, including downward, as far as its siphon will reach, a few centimeters in adult
specimens, before moving to a new location by burrowing with its introvert and pulling the shell
along (Gage 1968, Fig. 1). Dolbeth et al. (2009) also classified P. strombus at shelf depths off
southern Portugal as a subsurface deposit feeder but gave no reference or independent evidence.
In the third of the feeding modes used by Golfingiidae, Murina (1984) considered
Phascolopsis gouldii, all Onchnesoma spp. and most Golfingia spp. to be “burrowing and
swallowing forms” that burrowed more continuously. Nephasoma spp. were separated out from
Golfingia subsequently but belong to this feeding category. Thompson (1980) studied what is
now known as Nephasoma (Nephasoma) wodjanizkii wodjanizkii collected from bathyal basins
off southern California (moved from Golfingia but part of this third feeding mode). Specimens
had trunk lengths of 7 - 36 mm and diameters of 0.5 - 3 mm; introverts reached 6 - 7 times
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Jumars, Dorgan & Lindsay
07 November 2014
trunk length and were tipped by 4 - 8 small, digitate tentacles. Gut contents were reported as
fine, particulate material flocculated with clay-sized (< 4 µm) mineral particles. Average loss
on ignition of the excised gut contents of three individuals was a stunning 48%, indicating great
selectivity (in contrast to Thompson’s 1980 conclusion), likely for recently deposited organic
aggregates. In 50 particles from three individuals, mean mineral particle size ingested was 7.5
µm, somwhat larger than mean ambient particle size of 2.7 µm. Smith et al. (1998) reported
this same species collected 2 m from a whale skeleton at 1240 m in the Santa Catalina Basin off
southern California.
Graf (1989) associated the burrows studied by Romero-Wetzel (1987) with high subsurface
microbial activity at very short intervals after deposition of a large pulse of Calanus finmarchicus
fecal pellets. Jumars et al. (1990), based in part on an x-radiograph implicating a sipunculan
in caching material from upwelling-generated blooms, suggested that sipunculans in regions of
highly episodic inputs of high-quality organic matter could benefit from this practice. Although
the introvert of N. lilljeborgi is short, multiple burrow openings per individual give access to
substantial surface area at the sediment-water interface and multiply the burrow surface area
available for caching. Shields & Kędra (2009) estimated that with its roughly 6 mm long
introvert and the observed burrow density, N. lilljeborgi could reach 100% of the sediment
surface. Caching implies burrow maintenance and return to stored resources and so is not
compatible with ideas of more or less continuous burrowing.
Thorsen (1957) suggested that Golfingia procerum pokes its introvert into Aphrodite aculeata
and sucks out coelomic fluids. We concur with Cutler (1994) in discounting this feeding mode
in Golfingia and suspect the observations to have resulted from trawl damage to the sea mice and
accidental juxtapositions with probing or burrowing introverts.
Studies of digestion in golfingiids have been few. Brown et al. (1982) documented the
presence of a chymotrypsin-like protease in the luminal fluids of Phascolopsis gouldii. Midgut
pH was mildly basic (7.8). In laboratory incubations, Golfingia sp. from the Kattegat showed no
significant effect on diatom spore viability due to gut passage and hence probably no nutritional
gain (Hansen & Josefson 2004). We presume that this Golfingia sp. did not utilize a shell or test
because the authors described careful washing of the animal before the feeding experiment.
In stable isotopic studies, Golfingia vulgaris from the Bay of Brest showed δ15N intermediate
between those of nereidids and terebellids at the same site (Schaal et al. 2010). In stable isotopic
studies, Golfingia margaritacea from the Chukchi shelf showed δ15N 2.5‰ above unidentified
Sabellidae and 2‰ below Nephtys sp. Its δ13C was also consistent with surface and perhaps
subsurface deposit feeding (Feder et al. 2011). This species has an introvert < ½ trunk length,
tipped with abundant tentacles (Cutler 1994). The species is bipolar and may also avail itself of
caching. Stable isotopic composition of P. gouldii collected in the intertidal zone of Ny Ålesund,
Svalbard—in summer—indicated that it fed primarily on primary production from ice algae and
at a trophic level similar to that of suspension-feeding sabellids (McMahon et al. 2008). This
result is most compatible with surface deposit feeding (perhaps including caching).
Under the North Water Polynya, Nephasoma eremita had a 13C content consistent with
feeding on organic matter derived from ice algae but showed 15N enrichment by 7‰ over the ice
algae, equivalent to that of Phyllodoce mucosa and only 2‰ less than Lumbrineris sp. (Hobson
et al. 2002). Alternative (and again not mutually exclusive) interpretations include some
carnivory and digestion of refractory or otherwise highly microbially modified detritus.
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Jumars, Dorgan & Lindsay
07 November 2014
Guild membership
We tentatively classify Themiste and Thysanocardia spp. as ciliary suspension feeders. We
suspect that members of both genera will be found to use downstream collecting (Riisgård
et al. 2000). P. lutense may surface deposit feed. We believe that the remaining golfingiids
either surface deposit feed and cache (Nephasoma spp. and Phascolopsis gouldii) or subsurface
deposit feed (Phascolion strombus and likely other species). All golfingiids appear to be
discretely motile. We suspect that species with relatively few and short tentacles will be found to
subsurface deposit feed, but that suggestion needs to be tested.
Research questions and opportunities
• Suspension feeding in Themiste and Thysanocardia has neither been explored quantitatively
in terms of clearance rates nor placed in the context of hydrosol filtration theory. Sipunculans
are strikingly absent from reviews of suspension feeding (e.g., Riisgård & Larsen 2010).
• If Phascolopsis gouldii is found to cache ice-algal-derived material, its intertidal access could
permit useful experimental assessment of bacterial competitors or mutualists affecting that
resource.
• The family presents abundant opportunities to associate introvert length and tentacle structure
with more finely resolved feeding guilds.
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07 November 2014
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Goniadidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
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Jumars, Dorgan & Lindsay
07 November 2014
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Goniadidae, Glyceriformia
Diversity and systematics
Goniadidae comprises about 100 named species in about a dozen genera, 4 of them monotypic
(WoRMS). The most recent family revision, however, found only 63 valid species (Böggemann
2005). Molecular genetics and cladistics place the family closest to Glyceridae and close
to other Phyllodocida (Zrzavý et al. 2009, Struck et al. 2011), but less expectedly molecular
genetics also show affinities with Lumbrineridae and Onuphidae (Rousset et al. 2007, Struck et
al. 2011). A putative whole goniadid in the fossil record dates back to the Carboniferous Period,
and goniadid fangs are well known from the Triassic (Böggemann 2005). Adults can range from
1 to 76 cm long (Pettibone 1963).
Habitat
Goniadids occur at all water depths on and in both hard and soft bottoms. They are most
abundant in shallow water.
Sensory and feeding structures
A generally conical prostomium terminates in four small antennae, the ventral pair more
nearly terminal. A small number of eyespots may be present. A pair of lateral nuchal organs is
generally present near the rear of the prostomium. When everted, the axial pharynx is tipped
by two opposing, lateral sets of grasping teeth, smaller than glycerid fangs, and often by a
more complete circlet of even smaller teeth. Only Goniada amacrognatha lacks the larger,
opposed, grasping fangs (Böggemann 2005). The external surface of the everted pharynx
bears numerous, and in some species diverse, scleratized papillae (also called pharyngeal teeth)
that point backward. Larger, hardened chevrons may also be present laterally, also pointing
backward—up to 80 in number. Silberstein (1987) suggested that chevrons are used for purchase
on the inside of the prey tube. Papillae in Glycinde polygnatha are hook shaped and typically
have subterminal pores through which secretions exude (Silberstein 1987). In our terminology
they are pharyngeal hooks. Hooks and chevrons may both be useful in holding position while
extracting prey, ratcheting prey inward during pharyngeal inversion and gaining frictional
purchase during burrowing. Compositions of the secretions and their toxic, lubricating, adhesive
or hydrolytic activities are unknown.
Motility
Mattson (1981) made basic observations of Goniada maculata burrowing and searching
behaviors and concluded, consistent with its diet, that it is a motile predator that does not build
a permanent burrow or gallery. In aquaria, Glycinde polygnatha initially formed a U-shaped
burrow and then added secondary branches, lining them with a tough mucus that persisted
for several weeks after the worm was removed. Worms were not observed to leave burrows
(Silberstein 1987).
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Goniadidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Illustrations
Silberstein (1987) provides several informative line drawings of goniadid pharynges in various
states of eversion and an electron micrograph of a doomed prey’s eye view of an oncoming, fully
everted pharynx tipped by dorsolateral fangs. Smith et al. (1995) display pharyngeal armature of
Glycinde armigera in informative line drawings and scanning electron micrographs. Böggemann
(2005) masterfully displays the full range of goniadid morphology in both line drawings and
micrographs.
Feeding
Several studies on gut contents, as well as stable isotope data, have supported the classification
of Goniadidae as carnivores, with some less conclusive hints at a broader diet. Dauer (1980)
dissected 20 Glycinde sp. from a sandy intertidal zone in Florida; 15 were empty. The other
5 each contained numerous small fecal pellets. Because of the large fraction of specimens
with empty guts, Dauer (1980) considered these results inconclusive as to principal diet in
this population. Mattson (1981) dissected 130 specimens of Goniada maculata and found 24
with food remains including spionids, orbiniids, cirratulids, maldanids, capitellids and a single
individual terebellid and scalibregmatid. He found very little incidental ingestion of sediments.
Gaston (1987) dissected 114 Goniadella gracilis individuals of which 12 held undigested and
unidentified food, and 7 held forams. Of 18 Goniada brunnea individuals, 17 were empty and
the other held a peracarid. Four Goniada maculata individuals, and 2 each of G. norvegica and
G. teres were empty.
Silberstein (1987) dissected 370 individuals of Glycinde polygnatha and found gut contents
in 100 of them. Of the individuals that contained prey, 86% held tubicolous polychaetes, and
47% contained spionids. Tubicolous worms, primarily spionids, were more prevalent among
the gut contents than in the ambient community as a whole. Prey were swallowed head first.
Only one ‘motile’ polychaete, Nephtys sp., was a major prey item, but only for juvenile G.
polygnatha. The tube-dwelling Owenia collaris was underrepresented in gut contents relative to
its availability, and Silberstein (1987) suggested that its tube, which is highly flexible and durable
and narrows to a conical tip at the opening, may be more difficult for the proboscis to enter and
maneuver in than the simple cylindrical tubes of spionids. “Sand grains or other extraneous
materials were rarely found in gut contents” (Silberstein 1987, p. 9). In experiments, individuals
consumed about one spionid every 2 d, presumably within reach of one of the burrow branches.
Silberstein (1987) also dissected several Glycinde armiger and reported that they contained
polychaete chaetae. He hypothesized that goniadids with exceptionally long pharynges and well
developed chevrons would be found to specialize on tubicolous species.
Stable isotopic signatures of goniadids have also been consistent with a carnivorous lifestyle
(Tucker et al. 1999, Goniadidae; Magnusson et al. 2003, Goniada maculata; Yoshino et al. 2006,
Goniadidae;McLeod et al. 2010, Goniadidae and Glyceridae combined; Bergamino et al. 2011,
Hemipodus olivieri). Where goniadids and glycerids have both been analyzed, goniadids usually
have shown slightly higher δ15N values.
Guild membership
Goniadids apparently can be (motile) roaming predators without burrow galleries (e.g., Goniada
maculata) or be discretely motile burrow dwellers (e.g., Glycinde polygnatha) using an eversible
pharynx armed with grasping fangs in most species. It is interesting that the presence of tubebuilding polychaetes in the gut is unreliable as an indicator of whether the predator species is
motile or discretely motile.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Research questions and opportunities
• Hypothetical functions of the papillae, chevrons and papillae secretions remain to be tested
experimentally.
• Predator motility and its consequences for prey selection are unknown for most species.
• It would be interesting to compare behaviors and diets between Goniada amacrognatha and
species that do carry opposed fangs.
References
Bergamino L, Lercari D, Defeo O. 2011. Food web structure of sandy beaches: temporal and
spatial variation using stable isotope analysis. Estuar. Coast. Shelf Sci. 91:536–43
Böggemann M. 2005. Revision of the Goniadidae (Annelida, Polychaeta). Abh. Naturwiss. Ver.
Hamburg (NF) 39:1–354
Böggemann M. 2009. Polychaetes (Annelida) of the abyssal SE Atlantic. Org. Divers. Evol.
9:251–428
Dauer DM. 1980. Population dynamics of the polychaetous annelids of an intertidal habitat of
upper old Tampa Bay, Florida. Int. Rev. Ges. Hydrobio. 65:461–87
Gaston GR. 1987. Benthic Polychaeta of the Middle Atlantic Bight: feeding and distribution.
Mar. Ecol. Prog. Ser. 36:251–62
Magnusson K, Agrenius S, Ekelund R. 2003. Distribution of a tetrabrominated diphenyl ether
and its metabolites in soft-bottom sediment and macrofauna species. Mar. Ecol. Prog. Ser.
255:155–70
Mattson, S. 1981. Burrowing and feeding of Goniada maculata. Sarsia 66:49–51
McLeod RJ, Wing SR, Skiltona JF. 2010. High incidence of invertebrate–chemoautotroph
symbioses in benthic communities of the New Zealand fjords. Limnol. Oceanogr. 55:2097–
106
Pettibone MH. 1963. Marine polychaete worms of the New England region. I. Aphroditidae
through Trochochaetidae. Bull. US Nat. Mus. 227:1-356
Rousset V, Pleijel F, Rouse GW, Erséus C, Siddall ME. 2007. A molecular phylogeny of annelids.
Cladistics 23:41–63
Silberstein M. 1987. Feeding ecology of the polychaete worm, Glycinde polygnatha Hartman
1950, an infaunal predator, with notes on life history. MS thesis. San José, CA: San José
State Univ.
Struck TH, Paul C, Hill N, Hartmann S, Hösel C, et al. 2011. Phylogenomic analyses unravel
annelid evolution. Nature. 470:95–8
Tucker J, Sheats N, Giblin AE, Hopkinson CS, Montoya JP. 1999. Using stable isotopes to trace
sewage-derived material through Boston Harbor and Massachusetts Bay. Mar. Env. Res.
48:353–75
Yoshino K, Miyasaka H, Kawamura Y, Gengai-Kato M, Okuda N, et al. 2006. Sand banks
contribute to the production of coastal waters by making a habitat for benthic microalgae in
the sublittoral zone: food web analyses in Aki-Nada using stable isotopes. Plankton Benthos
Res. 1:155–63
Zrzavý J, Říha P, Piálek L, Janouškovec J. 2009. Phylogeny of Annelida (Lophotrochozoa): totalevidence analysis of morphology and six genes. BMC Evol. Biol. 9:189, 14 pp.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Hartmaniellidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Hartmaniellidae, Eunicida
Diversity and systematics
Hartmaniellidae to date comprise 3 species in a single genus: Hartmaniella erecta, H.
tuleaerensis, and an unnamed species. The latter 2 have been redescribed, to the extent
possible, by Carerra-Parra (2003). Due to fragmentation, lengths are not well known but
appear to be ≤ 1 cm, with diameters of order 1 mm. Hartmaniella was initially thought to be
within Lumbrineridae, but its jaw structures place it closer to taxa known only from the fossil
record (Orensanz 1990). The match of jaw structure to fossil taxa is remarkable in its detail
(Szaniawski & Imajima 1996).
Habitat
Specimens were dredged from deep shelf depths.
Sensory and feeding structures
A rounded prostomium precedes a pair of peristomial rings and projects over the mouth opening.
The anterior peristomial ring projects as lateral lappets over the rear of the prostomium, covering
small, ciliated, pad-like nuchal organs (Fauchald & Rouse 1997). Head appendages are absent,
as are eyes. Individuals carry a pair of jaws, including elongate mandibles and an arrangement
of maxillary plates unique among living Eunicida.
Motility
Morphology suggests motility or discrete motility.
Illustrations
Carerra-Parra (2003, Figs. 1 & 2) displays photographs and line drawings of two of the three
species in the family, including their jaw structures. Szaniawski & Imajima (1996, Fig. 1) give
line drawings of jaw structures of both H. erecta and a fossil species of Eunicida, showing
striking similarity. Rouse (2001) provides stippled line drawings of both ventral and dorsal
views of H. erecta as well as its jaw structures.
Feeding
The small size of the animal and the jaws that it carries imply a rich diet, but no observations of
jaw operation, feeding or gut contents have been published. Kinematics and dynamics of jaw
operation are unknown, but it is interesting to speculate that the superficially orbiniid-like, dorsal
displacement of mid-body dorsal cirri may function to resist backward and upward motion of this
small worm during pharyngeal eversion.
Guild membership
Size and jaw morphology suggest predation on meiofauna. We tentatively consider members of
the family to be motile.
Research opportunities
• Direct evidence of diet and motility is lacking.
• The outward-facing, lateral spur on the mandibles of Hartmaniella spp. begs for functional
analysis that would give insight into fossil taxa as well.
References
Carrera-Parra LF. 2013. Redescription of Hartmaniella tulearensis n. comb. (Amoureux,
1978) with comments on Hartmaniella sp. and affinities of the family (Polychaeta:
Hartmaniellidae). J. Nat. Hist. 37:49–55
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Hartmaniellidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Fauchald K, Rouse GW. 1997. Polychaete systematics: Past and present. Zool. Scr. 26:71–138
Orensanz JM. 1990. The eunicemorph polychaete annelids from Antarctic and Subantarctic
seas: With addenda to the Eunicemorpha of Argentina, Chile, New Zealand, Australia, and
the southern Indian Ocean. In Biology of the Antarctic Seas, ed. LS Kornicker 21:1–183.
Washington, D.C.: American Geophysical Union
Rouse GW. 2001. Hartmaniellidae Imajima, 1977. See Rouse & Pleijel 2001, pp. 158–9
Szaniawski H, Imajima M. 1996. Hartmaniellidae—living fossils among polychaetes. Acta
Palaeontol. Pol. 41:111–25
Hesionidae, Nereidiformia, Phyllodocida
Diversity and systematics
Hesionidae were revised by Pleijel (1998), who recognized about 130 spp. in 31 genera. Pleijel
(1998) excluded Hesionides and Micropthalmus. Molecular data support this removal (Struck
2006). We caution that F&J treated these two genera under Hesionidae; we treat them briefly
under Pilargidae. Excluding Hesionides and Micropthalmus, WoRMS lists about 150 species in
35 genera, 15 of them monotypic.
Morphology has been used to infer close relationship of Hesionidae with Nereididae and
Chrysopetalidae (Pleijel & Dahlgren 1998). Hesionidae clearly belong in Phyllodocida, but their
high intrafamilial diversity has made their accurate molecular genetic placement among other
Phyllodocida difficult (Zrzavý et al. 2009). Pleijel’s (1998) cladistic analysis of morphology
suggested that several genera needed revision. Ruta et al.’s (2007) molecular genetic analysis
underscored this conclusion. Nereimyra has recently been revised (Pleijel et al. 2012). Adults
range from a few millimeters to about 7 cm long.
Habitat
Few if any oxic or suboxic, benthic habitats lack hesionids. They can be abundant on
microbial mat communities at hydrothermal sites (Bernardino et al. 2012) and hydrocarbon
seeps (Robinson et al. 2004). Vrijenhoekia balaenophila colonizes whale bones (Pleijel et al.
2009). At least one hesionid species metamorphoses in the under-ice community before older
juveniles apparently drop to the seabed (Carey & Montagna 1982). The ‘ice worm’ Hesiocaeca
methanicola creates evenly spaced, shallow burrows in both exposed and shallowly buried
methane hydrates (Desbruyères & Toulmond 1998).
Sensory and feeding structures
A pair of ventrolateral palps, homologous with those of other Phyllodocida (Orrhage 1996), is
present except in Hesione, wherein only vestigial innervation remains. Palps are reduced in
Wesenbergia. A pair of dorsolateral antennae is present, usually relatively far toward the anterior
of the prostomium. A medial antenna is variably present across species and life stages and is
usually farther toward the rear of the prostomium. A pair of nuchal organs in the form of ciliated
bands outline the posterior dorsolateral edges of the prostomium, often resembling teddy-bear
ears; in some species they nearly meet at the dorsal midline. A pair of black, red or orange eyes
may be present. Although most hesionids feed with unarmed, axial, eversible pharynges, diverse
hardened structures are scattered through the family (Pleijel 1998). Syllidia spp. in Pleijel
(1998) carry two toothed, lateral plates and a conical medial ventral tooth (Pleijel 1998, Rizzo &
Salazar-Vallejo 2014). The plates are not hinged, but their toothed surfaces are opposable and
appear capable of macerating or crushing food between them and against the ventral, conical
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Hesionidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
tooth (Fig. 3 of Rizzo & Salazar-Vallejo 2014, the ventral tooth being termed a stylet). Leocrates
chinensis carries small stylets (Pleijel 1998, Fig. 8). The inner surface of the pharynx itself may
be scleratized (Pleijel et al. 2008). Nereimyra punctata carries a pair of blunt teeth at the ends of
hinged jaws (Fig. 16A in Pleijel 1998) that appear potentially useful for crushing, but whether the
two blunt surfaces come all the way together when the pharynx retracts is not clear. Members of
this genus also bear a pair of lip glands, pad-like secretory structures situated on each side of the
mouth opening (Pleijel 1998).
Motility
General morphology suggests motility or discrete motility. Oxydromus pugettensis and O.
flexuosus are epibenthic and motile, whereas Nereimyra punctata constructs a burrow gallery and
is discretely motile as a sit-and-wait predator. For most species, the category they belong in is
unknown. Likewise, information on whether species are infaunal or epifaunal is scant.
Illustrations
Pleijel et al. (2008) present in situ color photographs of Vrijenhoekia balaenophila among
Osedax individuals on a whale bone; they also show scanning electron micrographs and
line drawings of this newly described species. Pleijel (1998) presents a large collection
of micrographs and line drawings that give a good idea of the extensive morphological
variation among species of the family. Desbruyères & Toulmond (1998) present stunning in
situ photographs together with scanning electron micrographs and stippled line drawings of
Hesiocaeca methanicola. An array of excellent illustrations of hesionids is posted at <http://
tolweb.org/Hesionidae/>.
Feeding
From combinations of laboratory observations and experiments with analyses of gut contents
in field-collected specimens, feeding biologies of three hesionid species are relatively well
known: Oxydromus pugettensis, O. flexuosus, and Nereimyra punctata. Shaffer (1979) dissected
gut contents or observed feces from 150 field-collected O. pugettensis and ran feeding trials in
laboratory aquaria. Harpacticoid copepods strongly dominated gut contents of field-collected
specimens, but a wide variety of motile and tubicolous polychaetes were also taken in both the
field and laboratory. The previous sentence also summarizes results of Oug’s (1980) analysis of
feces from 55 and gut contents from 262 O. flexuosus, although tubicolous species, in particular
spionids, were more common in the diet of O. flexuosus than of O. pugettensis. Both Oxydromus
species are epifaunal and move deliberately over the sediment surface, pausing when prey are
detected—likely to increase mechanosensory sensitivity­by reducing self “noise”—and then
using the information to vector into position before pharyngeal eversion.
N. punctata by contrast is infaunal, building a burrow gallery with multiple openings at the
sediment surface, usually connected to a deeper, more vertical, central burrow. N. punctata
extends tentacular cirri from burrow openings and ambushes prey that intersect its burrow
network (Oug 1980). Despite its burrowing habit and jaws, pellet contents of 68 field-collected
specimens of N. punctata were remarkably similar to those of O. flexuosus from the same habitat
(Oug 1980). This similarity suggests that both species depend primarily on prey motion for
encounter, explaining diet similarity and harpacticoid dominance of gut contents, but move
themselves or their burrow structures sufficiently frequently to encounter some tubicolous prey.
Both Shaffer (1979) and Oug (1980) remarked that their study species avoided bulk ingestion
of sediments and macroalgal fragments. Oug (1980) indeed reported regurgitation of sediments
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
ingested during predation attempts. Individual diatoms and diatom chains were occasionally
swallowed. Unlike polynoids, glycerids and goniadids, whose guts are most often found
empty, guts of the field-collected hesionids were typically partially filled with multiple items,
reflecting the relatively small size and high abundance of benthic harpacticoids and other prey.
Mechanosensing and chemosensing were used by all three species. Oug (1980) demonstrated
strikes at inanimate objects when moved, and both Shaffer (1979) and Oug (1980) observed
scavenging on dead animals, demonstrating that either sensory modality alone could suffice,
even though they are generally used in concert. Absence of gut contents in 8 specimens of a
Gyptis sp. (Gaston 1987) suggests that some other hesionids may be predatory on larger, rarer
species. Dauer (1980) dissected 30 Gyptis vittata from a sandy intertidal site in Florida; 24
were empty. The remainder each contained 3 - 10 sand grains and traces of finer sediment. He
considered these results inconclusive regarding the diet of the species at this location.
Blake (1975) observed late nectochaetes and six-setiger juveniles of O. pugettensis to feed on
diatoms (the only food offered). Carey & Montagna (1982) reported settlement of hesionids into
the community of arctic, under-ice algae. Snelgrove et al. (1994) found mass settlement of N.
punctata into diatom-enriched settlement trays at 900 m off St. Croix, with only roughly half as
many settlers into trays enriched with ground Sargassum. Diatoms may serve both as food and
as “bait” for meiofauna toward which diets turn from diatoms as hesionids mature.
Stable isotopic signatures of Hesiospina vestimentifera at hydrothermal vents suggest
feeding on microbial mats or on meiofauna that do. This hesionid had δ13C slightly lower than
Paralvinella from the same environment and δ15N only 1.6 to 2.4‰ higher and much more
variable, suggesting diet diversity across the 3 specimens analyzed and less direct dependence
on microbial production than observed in Paralvinella (Bergquist et al. 2007). Hesiocaeca
methanicola inhabiting methane hydrates in the bathyal zone of the northern Gulf of Mexico had
stable isotopic signatures at first thought to be indicative of direct feeding on methane-oxidizing
bacteria; no internal symbionts were evident, and the gut was complete (Fisher et al. 2000). The
regular spacing of burrows suggested local enhancement of microbial food production through
enhanced surface area via burrow structure and thinning of the diffusive boundary layer via
respiratory ventilation. Additional studies in nearby locations over a wider range of water depths
showed a substantially wider diversity in stable isotope signatures, all consistent with feeding on
local bacteria, but not on a single metabolic type of bacteria (Becker et al. 2013).
Isotopic analyses of hesionids have also been done on specimens collected from coldwater coral mounds (van Oevelen et al. 2009). In this study, biofilm had an unusual definition
including mobile meiofauna and polychaetes as well as fouling prokaryotes and eukaryotes on
dead coral surfaces. Although how this layer was sampled went undescribed, hesionid δ15N
values were consistent with direct feeding on this community. We seriously doubt the authors’
unsupported suggestion that hesionids are suspension and deposit feeders. The pumping action
during prey ingestion described by Shaffer (1979) is not of sufficient capacity (volume per time)
to permit suspension feeding. The authors (van Oevelen et al. 2009) appear to have been misled
by the data-sparse vagueness of F&J’s familial summary for Hesionidae.
Guild membership
Ophiodromus flexuosus and O. pugettensis are motile carnivores using unarmed, eversible
pharynges. Nereimyra punctata is a discretely motile sit-and-wait predator with a similarly
unarmed pharynx. These observations support F&J’s conjecture that most large hesionids would
be found to be carnivorous. Two large hesionids (about 2 cm long), however, are supported
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Jumars, Dorgan & Lindsay
07 November 2014
by microbial production, perhaps very directly (Hesiospina vestimentifera and Hesiocaeca
methanicola). Most hesionid species are likely to fall into motile or discretely motile categories.
Pleijel (1998) listed hesionid species known to have jaw armature. How the structures are
deployed and on what foods is unknown. Small hesionids can be expected to feed on rich
foods but are not necessarily carnivorous, with diatoms and microbial mats as non-animal foods
already known to be consumed by some species.
Research opportunities
• Form and function remain to be linked for species with pharyngeal armature.
• Diet and motility are unknown for most species.
• Ontogenetic shifts in diet would be interesting to explore further in this group.
References
Becker EL, Cordes EE, Macko SA, Lee RW, Fisher CR. 2013. Using stable isotope compositions
of animal tissues to infer trophic interactions in Gulf of Mexico lower slope seep
communities. PLoS ONE 8:e74459, 16 pp.
Bergquist DC., Eckner JT, Urcuyo IA. 2007. Using stable isotopes and quantitative community
characteristics to determine a local hydrothermal vent food web. Mar. Ecol. Prog. Ser.
330:49–65
Bernardino AF, Levin LA, Thurber AR, Smith CR. 2012. Comparative composition, diversity
and trophic ecology of sediment macrofauna at vents, seeps and organic falls. PLoS ONE
7:e33515, 17 pp.
Blake JA. 1975. The larval development of Polychaeta from the northern California coast. III
Eighteen species of Errantia. Ophelia 14:23–84
Carey AC, Montagna PA. 1982. Arctic sea ice fauna1 assemblage: first approach to description
and source of the underice meiofauna. Mar. Ecol. Prog. Ser. 8:1–8
Dauer DM. 1980. Population dynamics of the polychaetous annelids of an intertidal habitat of
upper old Tampa Bay, Florida. Int. Rev. Ges. Hydrobio. 65:461–87
Debruyères D, Toulmond A. 1998. A new species of hesionid worm, Hesiocaeca methanicola
sp. nov. (Polychaeta: Hesionidae), living in ice-like methane hydrates in the deep Gulf of
Mexico. Cah. Biol. Mar. 39:93–8
Fisher CR, MacDonald IR, Sassen R, Young CM, Macko SA, et al. 2000. Methane ice worms:
Hesiocaeca methanicola colonizing fossil fuel reserves. Naturwissenschaften 87:184–7
Orrhage L. 1996. On the microanatomy of the brain and the innervation and homologues of the
cephalic appendages of Hesionidae and Syllidae (Polychaeta). Acta Zool. 77:137–51
Oug E. 1980. On feeding and behaviour of Ophiodromus flexuosus and Nereimyra puncatata.
Ophelia 19:175–91
Pleijel F. 1998. Phylogeny and classification of Hesionidae (Polychaeta). Zool. Scr. 27:89–163
Pleijel F. 2001. Hesionidae Grube, 1850. See Rouse & Pleijel 2000, pp. 91–3
Pleijel F, Dahlgren TG. 1998. Position and delineation of Chrysopetalidae and Hesionidae
(Annelida, Polychaeta, Phyllodocida). Cladistics 14:129–50
Pleijel F, Rouse GW, Nygren A. 2012. A revision of Nereimyra (Psamathini, Hesionidae,
Aciculata, Annelida). Zool. J. Linn. Soc. 164:36–51
Pleijel F, Rouse GW, Ruta C, Wiklund H, Nygren A. 2008. Vrijenhoekia balaenophila, a new
hesionid polychaete from a whale fall off California. Zool. J. Linn. Soc. 152:625–34
Rizzo AE, Salazar-Vallejo SI. 2014. Hesionidae Grube, 1850 (Annelida: Polychaeta) from southsoutheastern Brazil, with descriptions of four new species. Zootaxa 3856:267–91
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Robinson CA, Bernhard JM, Levin LA, Mendoza GF, Blanks JK. 2004. Surficial hydrocarbon
seep infauna from the Blake Ridge (Atlantic Ocean, 2150 m) and the Gulf of Mexico (690–
2240 m). Mar. Ecol. 25:313–36
Ruta C, Nygren A, Rousset V, Sundberg P, Tillier A, et al. 2007. Phylogeny of Hesionidae
(Aciculata, Polychaeta), assessed from morphology, 18S rDNA, 28S rDNA, 16S rDNA and
COI. Zool. Scr. 36:99–107
Shaffer PL. 1979. The feeding biology of Podarke pugettensis. Biol. Bull. 156:343–55
Snelgrove PVR, Grassle JF, Petrecca RF. 1994. Macrofaunal response to artificial enrichments
and depressions in a deep-sea habitat. J. Mar. Res. 52:345–69
van Oevelen D, Duineveld G, Lavaleye M, Mienis F Soetaert K, et al. 2009. The cold-water
coral community as a hot spot for carbon cycling on continental margins: A food-web
analysis from Rockall Bank (northeast Atlantic). Limnol. Oceanogr. 54:1829–44
Zrzavý J, Říha1 P, Piálek L, Janouškovec J. 2009. Phylogeny of Annelida (Lophotrochozoa):
total-evidence analysis of morphology and six genes. BMC Evol. Biol. 9:189 14 pp.
Histriobdellidae, Eunicida
Diversity and systematics
Histriobdellidae is a small family of small Eunicida (< 2 mm long as adults) whose members live
commensally in branchial chambers or on carapaces of crustaceans. Histriobdella and Dayus
are monotypic, whereas Stratiodrilus contains about a dozen species. The case for placing them
within Eunicida is fairly strong (Struck et al. 2006, Rousset et al. 2007), though far from airtight
(Paxton 2009, Zrzavý et al. 2009). They are considered to be closely related to Oenonidae based
on similarity in jaw morphology, but molecular data are lacking (Paxton 2009). Their habits
were reviewed by Martin & Britayev (1998).
Habitat
All known histriobdellids inhabit crustacean hosts. H. homari inhabits Homarus branchial
chambers, and S. spp. inhabit branchial chambers of crayfish in the southern hemisphere. D.
cirolanae inhabits a South African isopod.
Sensory and feeding structures
The prostomium is frontally rounded and fused to the peristomium. Eyes are lacking. To
our knowledge, nuchal organs have not been described. A frontal pair of ventrolateral palps
is present as is a median antenna and a dorsolateral pair of antennae (Paxton 2000). Paired,
retractile, lateroventral locomotor appendages on the prostomium bear adhesive glands on
their distal ends (Steiner & Amaral 1999). Histriobdellid morphologies, including posterior
attachment structures with adhesive glands, are highly modified for attaching to hosts (Martin
& Britayev 1998). In common with other eunicidan families, Histriobdellidae have ventral,
muscularized pharynges, ventral mandibles and dorsal maxillae.
Jennings and Gelder (1976) examined the jaw structure and function of Histriobdella homari
and described the movement of the mandible and maxillae during operation of the pharyngeal
apparatus. The curvature of the carriers on the maxillae matches the mandible curvature such
that the carriers slide backward and forward along the mandibles. Contractions of carrier
retractor muscles, that extend from the ventral bulb of the posterior muscular organ to the carrier,
slide the maxillae back along the mandibles. Inelastic fibers attach the carriers to a long, narrow
“dorsal rod” that attaches to the maxillae and extends down along the mandible. The anterior
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
end of the dorsal rod is pulled posteriorly with the carriers while the posterior end is held in place
by several other muscles, bending the dorsal rod. Relaxation of the carrier retractor muscles (and
several other muscles) releases the dorsal rod to straighten, extending the maxillae anterior to the
mandibles. Jennings and Gelder (1976) noted that the histriobdellid proboscis differs from other
eunicids in having articulated maxillae, in possessing a more elaborate carrier capable of anterior
and posterior movement along the mandibles, and in using a dorsal rod, the latter not known in
any other taxa.
Motility
Rouse (2001) described crawling of histriobdellids in what resembles the “walk of Charlie
Chaplin.” Histriobdella homari uses a duo-gland adhesive system to “walk” with two posterior,
foot-like appendages over the gills of its lobster host. The ultrastructure of these foot-like
appendages is similar to the duo-gland adhesive systems used by Saccocirrus and other
meiofauna (Gelder & Tyler 1986).
Illustrations
Jennings and Gelder (1976) include images and drawings of whole Histriobdella homari as
well as details of pharyngeal morphology and jaw function. Gelder and Tyler (1986) show
photographs of H. homari with stained (and oddly named) viscous glands at the anterior and
posterior. Steiner & Amaral (1999) give line drawings of members of the other two genera.
They are strikingly similar in overall appearance to members of the type genus.
Feeding
Jennings and Gelder (1976) examined gut contents of over 100 Histriobdella homari, which lives
in the branchial chambers of two species of lobsters, and found microflora, comprising bacteria
(including cyanobacteria) and green algae in proportions similar to those of their environment.
No microfauna or host tissues were found. Similarly, Stratiodrilus novaehollandiae was shown
through feeding experiments that included presentation of host tissue and associated fauna and
microflora and through gut content analyses to feed only on microflora lining the host crayfish’s
gill filaments and branchial chamber walls (Cannon & Jennings 1987). H. homarus also grazes
fouling organisms from lobster eggs (Brattey & Campbell 1985). No published data indicate
that histriobdellids consume host tissues (Martin & Britayev 1998). The diet of the isopod
commensal is unknown.
Feeding behavior of H. homari was described by Jennings and Gelder (1976, p. 509) as
scraping with the maxillae during proboscis eversion. Then, during retraction, “the toothed
surfaces of the first maxillae and the ridged surfaces of the second, third, and fourth maxillae
draw the food, rake-like, across the serrated margins of the mandibles and detach it from its
substratum.” Alternately, the proboscis remains extended “while the first maxillae operate
independently, rapidly opposing their toothed surfaces and detaching the longer filamentous food
organisms.”
Guild membership
Although commensal, histriobdellids appear to be herbivores or scrapers of labile fouling
material rather than parasites. They are motile, crawling with posterior appendages containing
duo-gland adhesive organs.
Research opportunities
• Stable isotopic data on histriobdellids and their hosts could be informative.
• Quantitative data on motility within or between host individuals would be the first.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
• Phylogenetic position within Eunicida remains uncertain.
References
Brattey J, Campbell A. 1985. Occurrence of Histriobdella homari (Annelida: Polychaeta) on the
American lobster in the Canadian Maritimes. Can. J. Zool. 63:392–5
Cannon LRG, Jennings JB. 1987. Occurrence and nutritional relationships of four ectosymbiotes
of the freshwater crayfish Cherax dispar Riek and Cherax punctatus Clark (Crustacea :
Decapoda) in Queensland. Austr. J. Mar. Fresh. Res. 38:419–27
Gelder SR, Tyler S. 1986. Anatomical and cytochemical studies on the adhesive organs of
the ectosymbiont Histriobdella homari (Annelida: Polychaeta). Trans. Am. Microsc. Soc.
105:348–56
Jennings JB, Gelder SR. 1976. Observations on the feeding mechanism, diet and digestive
physiology of Histriobdella homari van Beneden 1958: An aberrant polychaete symbiotic
with North American and European lobsters. Biol. Bull. 151:489–517
Martin D, Britayev TA. 1998. Symbiotic polychaetes: Review of known species. Oceanogr. Mar.
Biol. Ann. Rev. 36:217–340
Paxton H. 2000. Family Histriobdellidae. See Beesley et al. 2000, pp. 105–6
Paxton H. 2009. Phylogeny of Eunicida (Annelida) based on morphology of jaws. Zoosymposia
2:241–64
Rouse GW. 2001. Histriobdellidae Vaillant, 1890. See Rouse & Pleijel 2001, pp. 160–3
Rousset V, Pleijel F, Rouse GW, Erséus C, Siddall ME. 2007. A molecular phylogeny of annelids.
Cladistics 23:41–63
Steiner TM, Amaral CZ. 1999. The family Histriobdellidae (Annelida, Polychaeta) including
descriptions of two new species from Brazil and a new genus. Contrib. Zool. 68:95–108
Struck TH, Purschke G, Halanych KM. 2006. Phylogeny of Eunicida (Annelida) and exploring
data congruence using a partition addition bootstrap alteration (PABA) approach. Syst. Biol.
55:1-20
Zrzavý J, Říha1 P, Piálek L, Janouškovec J. 2009. Phylogeny of Annelida (Lophotrochozoa):
total-evidence analysis of morphology and six genes. BMC Evol. Biol. 9:189, 14 pp.
Ichthyotomidae, Eunicida
Diversity and systematics
Ichthyotomus sanguinarius is the only member of this family. It is thought, based on jaw
structure and ventral palps, to belong to Eunicida (Glasby 1993) and can reach a length of 1 cm
(Pleijel 2001).
Habitat
The species is known only from the fins of three species of eels. F&J incorrectly classified it as
a gill parasite. Culurgioni et al. (2006) added additional records of occurrence on conger eels to
those listed by Martin & Britayev (1998).
Sensory and feeding structures
The prostomium of I. sanguinarius bears a pair of indistinct, ventrolateral palps, a rudimentary,
anteriorly inserted, median antenna and small, dorsolaterally inserted, paired antennae. A pair
of small eyes with lenses is present, and lateral nuchal organs are suspected (Pleijel 2001). The
species attaches to its host with a pair of specialized, tong-like jaws surrounded by a suction-cuplike oral cone at the end of its muscular, axial pharynx.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Motility
Frequency of movement once first attached to a host is unknown. Details of host finding are also
unknown.
Illustrations
There appears to be only a single set of drawings of the anterior and jaws of this species dating
back to the original species description. They are reproduced as Fig. 20C in Martin & Britayev
(1998).
Feeding
I. sanguinarius is a blood-feeding parasite attaching to the fins of its hosts. The ontogeny of
infection is not known.
Guild membership
I. sanguinarius is a discretely motile carnivore using jaws to pierce and attach to host fins.
Research questions and opportunities
• Behaviors of host finding and attachment remain to be resolved.
• How this species came to be parasitic on three eel species that are not particularly closely
related is an interesting question.
References
Culurgioni J, D’Amico V, Coluccia E, Mulas A, Figus V. 2006. Metazoan parasite fauna of
conger eel Conger conger L. from Sardinian waters (Italy). Ittopatologia 3:253–61
Glasby CJ. 1993. Family revision and cladistic analysis of the Nereidoidea (Polychaeta:
Phyllodocida) Invertebr. Taxon. 7:1551–73
Martin D, Britayev TA. 1998. Symbiotic polychaetes: Review of known species. Oceanogr. Mar.
Biol. Ann. Rev. 36:217–340
Pleijel F. 2001. Ichthyotomus Eisig, 1906. See Rouse & Pleijel 2001, pp. 115–6
Ikedidae, Echiura
Diversity and systematics
Ikedidae contains the single genus Ikeda with two named species. It is a sister group to
Bonelliidae (Goto et al. 2013). I. taenioides can reach trunk lengths of 40 cm and diameters
of 2 - 3 cm, but a highly extended proboscis can measure 1.5 m long × 1.5 cm wide (Edmonds
2000). WoRMS lists I. pirotansis as uncertain in status, but there is at least one additional,
undescribed species of Ikeda from shallow water of Ishigaki Island, Japan (Goto et al. 2013) and
likely another from shallow water in Victoria, Australia (Lehrke 2011). As there is behavioral
information on I. pirotansis (some under its prior name of Prashadus pirotansis before the
generic synonomy by Nishikawa 2002), we provide a summary as I. pirotansis pending further
clarification. Hughes & Crisp (1976) reported I. pirotansis to reach trunk lengths of 60 cm.
Habitat
I. taenioides was described from the intertidal zone to about 13 m water depth in sand and firm
mud near the Misaki Marine Biological Station between Tokyo Bay and Sagami Bay. The
burrow excavated in the intertidal zone extended vertically 70 - 90 cm. Most of the burrows
originally excavated were 2 cm in diameter except near the bottom terminus, where they widened
to 4 - 5 cm. Sides of the burrow were made smooth by a mucus coating and were rusty reddish,
presumably from precipitation of oxidized iron (Ikeda 1907).
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
I. pirotensis was described from an intertidal mudflat of Pirotan Island, Gulf of Kutch, India.
Hughes & Crisp (1976) redescribed the species based on new material from Saudi Arabia and
Kuwait. Hornby (2005) made observations at several intertidal locations near Abu Dhabi.
Sensory and feeding structures
The distal end of the spatulate proboscis in I. taenoides is rounded and moves from side to side
as it is extended (Ikeda 1907). Nuchal organs and eyes are not known in Ikeda. Ikeda spp.
have long, convoluted guts characteristic of echiurans and possess a siphon tube that connects
the anterior midgut with the posterior midgut. They have terminal, tubular anal sacs that open
separately into the hindgut (Lehrke 2011).
Motility
Iron oxide precipitation in the burrow of I. taenioides suggests that it is occupied and oxidized
long enough to imply discrete motility. The burrow of I. pirotansis can be > 1 m deep (Hughes
& Crisp 1976) and shows variable mounding at the burrow opening dependent on sediment type
(steeper in muds than in sands; Hornby 2005).
Illustrations
Edmonds (2000, Fig. 4.19) provides a stippled line drawing of a whole I. taenoides in ventral
view and photographs of extended probosces of a southern Australian Ikeda sp. (Plates 11.5,
11.6). Goto et al. (2013, Fig. 1K, L) present photographs of the extended probosces of I.
taenoides and an undescribed Ikeda sp. Hornby (2005) provides photographs of extended
probosces of I. pirotansis over saturated sediments at low tide.
Feeding
I. taenoides extends the proboscis from the burrow; the trunk is not visible during feeding (Ikeda
1907). I. taenoides pelletizes ingested food into small rods even before it leaves the esophagus
(Ikeda 1907). I. pirotansis also pelletizes its ingesta far forward in the digestive tract (Menon &
DattaGupta 1962). Its pellets are prolate spheroidal and about 3 mm long (Hornby 2005).
I. pirotansis showed strong tidal periodicity in its feeding, beginning to feed on the outgoing
tide when about 10 cm of overlying water remained and continuing to feed over saturated
sediments upon emersion (Hughes & Crisp 1976, Hornby 2005). By the time that the flood
tide arrived, feeding had ceased (Hughes & Crisp 1976). Hornby (2005) noted that a feeding
proboscis was seen at low tide in association with only a very small proportion (≤ 0.05) of the I.
pirotansis burrows and that probosces avoided patches of sand covered with filamentous algae.
Guild membership
We tentatively classify Ikeda spp. as discretely motile, surface deposit feeders utilizing a highly
extensible proboscis.
Research questions and opportunities
• No quantitative data on motility, feeding rates, feeding frequencies or feeding selectivities are
available.
• It is unknown whether fecal pellets are cached and reingested.
• Do anal sacs harbor specific bacteria that could be gardened in a cache of pellets?
• Feeding during emersion brings forces of surface tension into play that likely affect abilities
to pick up sediments and to sort them.
• Functions of the midgut siphon and anal sacs are poorly known. Gut siphons are also known
from some capitellids and deposit-feeding echinoderms.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
References
Goto R, Okamoto T, Ishikawa H, Hamamura Y, Kato M. 2013. Molecular phylogeny of echiuran
worms (Phylum: Annelida) reveals evolutionary pattern of feeding mode and sexual
dimorphism. PLoS ONE 8:e56809, 6 pp.
Edmonds SJ. 2000. Phylum Echiura. See Beesley et al. 2000, pp. 353–74
Hornby RJ. 2005. An intertidal spoon worm (Phylum Echiura) in the United Arab Emirates:
occurrence, distribution, taxonomy and ecology. Tribulus 15:3–8
Hughes RN, Crisp DJ. 1976. A further description of the echiuran Prashadus pirotansis. J. Zool.
Lond. 180: 233–42
Ikeda I. 1907. On three new and remarkable species of echiuroids (Bonellia miyajimai,
Thalassema taenioides, T. elegans). J. Coll. Sci. Imp. Univ. Tokyo 21:1–64
Lehrke J. 2011. Phylogeny of Echiura (Annelida, Polychaeta) inferred from morphological and
molecular data—implications for character evolution. PhD thesis. Friedrich-WilhelmsUniversität, Bonn
Menon PKB, A.K. DattaGupta AK. 1962. On a new species of Ikedosoma (Echiuridae). Ann.
Mag. Nat. Hist. (Ser. 13) 5:305–9
Nishikawa T. 2002. Comments on the taxonomic status of lkeda taenioides (Ikeda, 1904) with
some amendments in the classification of the phylum Echiura. Zool. Sci. 19:1175–80
Iospilidae, phyllodocida
Diversity and systematics
After the synonymy of Paraiospilus (Orensanz & Ramírez 1973, using the spelling variant
Pariospilus), Iospilidae contains 2 species in each of 2 genera: Iospilus phalacroides and I.
affinis, typically < 1 cm long; and, Phalacrophorus pictus and P. uniformis that each can reach 2
cm in length.
Habitat
Iospilids are most abundant in the upper mixed layer but can be caught in mid waters (e.g.,
Fernández-Álamo 2006, Jiménez-Cueto et al. 2006, Tovar-Faro et al. 2013).
Sensory and feeding structures
A single pair of anterior appendages is present on the prostomium ventrolaterally, thought to be
palps or possibly antennae. Boundaries of the peristomium are uncertain. A single pair of lensed
eyes may be present; nuchal organs have not been found (Pleijel 2001). Both species of Iospilus
feed with unarmed pharynges. Phalacrophorus spp. are presumed to capture prey with a pair of
laterally opposed fangs at the end of the everted pharynx.
Motility
I. phalacroides feeds on non-motile prey so likely is motile. It is not known whether
Phalacrophorus spp. are ambush predators or more motile hunters.
Illustrations
Tovar-Faro et al. (2013, Fig. 3) provide line drawings of the fangs in Phalacrophorus uniformis
in both retracted and everted postures of the pharynx. Druzhkov et al. (2000, Fig. 1 & 2) show
stippled line drawings of the retracted fangs of Phalacrophorus pictus borealis. Uschakov
(1972, Plate XXII, 1 & 3) shows inverted and everted positions of fangs in subspecies of P.
pictus. Jiménez-Cueto et al. (2006, Fig. 3A) present a micrograph of the anterior end of P.
uniformis in ventral view and a stippled line drawing of P. uniformis (Fig. 4B), both showing
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
the retracted jaws. Plate III, Figs. 1, 2 of Orensanz & Ramírez (1973) show retracted jaws of
both Phalacrophorus spp., and Fig. 4 shows the fangs at the tip of the everted pharynx of P.
pictus. The two fangs appear attached to substantial muscles at their bases but are not strongly
articulated with one another so do not constitute jaws in our terminology.
Feeding
Day (1967) indicated that I. phalacroides feeds on diatoms, a conclusion supported by its
positive covariation in abundance with them (Fernández-Álamo & SanVicente-Añorve 2005).
Carnivory by Phalacrophorus spp. has not been disputed, but prey taxa have not been identified.
Guild membership
We tentatively list I. phalacroides as a motile herbivore on diatoms and suspect the same of
I. affinis based on body size and lack of pharyngeal armature. We would not be surprised
to find Iospilus spp. feeding on other microalgae or heterotrophic protists. We guess that
Phalacrophorus spp. are discretely motile, ambush predators because the parapodia and chaetae
do not suggest powerful swimming.
Research questions and opportunities
• Data on motility are lacking.
• Data on prey of Phalacrophorus spp. are lacking.
• It would be interesting to know the sensory modalities and behaviors used by I. phalacroides
(and perhaps I. affinis) to encounter and capture microalgae.
References
Day JH. 1967. A Monograph on the Polychaeta of South Africa. Part 1. Errantia. London:
British Museum of Natural History
Druzhkov NV, Marasaeva EF, Druzhkova EI, Båmstedt U. 2000. New records of the carnivorous
pelagic polychaete, Phalacrophorus pictus borealis Reibisch, 1895 in the Arctic Ocean.
Sarsia 85:467–9
Fernández-Álamo MA, SanVicente-Añorve L. 2005. Holoplanktonic polychaetes from the Gulf
of Tehuantepec, Mexico. Cah. Biol. Mar. 46:227–39
Jiménez-Cueto S, Suárez-Morales E, Salazar-Vallejo SI. 2006. Iospilids (Polychaeta: Iospilidae)
from the northwest Caribbean Sea, with observations on reproductive structures. Zootaxa
1211:53–68
Orensanz JMA, Ramírez FC. 1973. Taxonomía y distribuciónde los poliquetos pelágicos del
atlántico sudoccidental. Boletín–Instituto de Biología Marina 21:1-86.
Pleijel F. 2001. Iospilidae Bergström, 1914. See Rouse & Pleijel 2001, p. 121
Tovar-Faro B, Leocádio M, de Paiva PC. 2013. Distribution of Iospilidae (Annelida) along the
eastern Brazilian coast (from Bahia to Rio de Janeiro). Lat. Am. J. Aquat. Res. 41: 323–34
Uschakov PV. 1972. Polychaeta 1. Polychaetes of the suborder Phyllodociformia of the Polar
Basin and the northwestern part of the Pacific. Fauna SSSR 102:1–271
Iphionidae, Aphroditiformia
Diversity and systematics
Iphionidae comprise 7 species in the genus Iphione and 2 in Thermiphione. Previously part
of a subfamily within Polynoidae, these taxa were elevated to familial status because of their
molecular genetic distinctiveness (Norlinder et al. 2012). They are somewhat more closely
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Jumars, Dorgan & Lindsay
07 November 2014
related to Polynoidae and Acoetidae than to other scaleworms (Norlinder et al. 2012). The body
is a sturdy hemispheroid 2 to 3 times as long as wide. Adults are typically 1 - 3 cm long.
Habitat
Iphione spp. are epifaunal on diverse substrata from intertidal to shelf depths (Pettibone 1986,
Imajima 2005). They may occur at 525 - 600 m water depth on the Reykjanes Ridge (Copley
et al. 1996). Thermiphione is known from hydrothermal vent fields on the East Pacific Rise
(Hartman-Schröder 1992) and in the North Fiji Basin (Miura 1994) at depths of 1750 - 2800 m.
Sensory and feeding structures
Sensory structures are abundant and crowded to face forward on and around a small, bilobed
prostomium that is partially fused with the first segment and withdrawn into segments 2 - 4,
directing the mouth forward. Iphionids have a pair of lateral antennae and a medial facial
tubercle but lack a medial antenna, although an occipital papilla is present. Two ventral palps
are fused to the first segment. Two pairs of eyes may be present. An unpaired nuchal organ is
present as a hemispheroidal or more rectangular mound medially atop the second segment and
projecting over the rear of the prostomium (Pettibone 1986). The peristomium is limited to a
small lip region. The axial, muscular pharynx is eversible and carries one pair of parrot-beaklike jaws, with two large teeth on each jaw of the pair. In the confusing jargon often applied to
scaleworms, the structure is called “four jaws” or “two pairs of jaws.” The single pair of jaws (in
our terminology) is strongly articulated and is associated with what may be venom glands (Wolf
1986). The everted pharynx is tipped with a circlet of papillae.
Motility
Storch (1967) described Iphione muricata as very chiton like. It attached firmly to hard reef
substrata and attached even more firmly rather than fled when disturbed. The ventral surface
lacked grooves and conformed to the shape of the substratum; its muscles were able to create
suction on flat surfaces. The animal was sessile during daylight and typically moved only a
few centimeters at night. It was apparently limited to an awkward and slow parapodial motion.
Iphione sp. was described in the caption of Plate 3.5 by Hutchings (2001) as an active carnivore,
so not all Iphione spp. are as sedentary as I. muricata.
Illustrations
Pettibone (1986) provides line drawings of several species of Iphione. Hutchings (2000, Pl. 3.5,
attributed to R. Steene) provides a color photograph of a probable Iphione sp.
Feeding
We know of no published data on feeding behavior or prey preferences but presume on the basis
of jaw morphology and analogy with better known scaleworms that iphionids are predators.
Guild membership
We tentatively conjecture that members of the family range from discretely motile, sit-and-wait
predators (based on Storch’s 1976 description of motility), to more actively hunting, motile
predators (based on Hutchings’ 2000 caption). All use a pair of jaws.
Research opportunities
• Any data on feeding would be the first.
• Quantitative data on motility would be useful.
• Compositions of secretions from the jaw glands are unknown.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Iphionidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
References
Copley JTP. Tyler PA, Sheader M, Murton BJ, German CR. 1996. Megafauna from sublittoral to
abyssal depths along the Mid-Atlantic Ridge south of Iceland. Oceanol. Acta 19:549–59
Hartmann-Schröder G. 1992. Zur Polychaetenfauna in rezenten hydrothermalen
Komplexmassivsulfiderzen (‘Schwarze Raucher’) am Ostpazifischen Rücken bei 21˚30’S.
Helgoländ. Wiss Meer. 46: 389–403
Hutchings PA. 2000. Family Polynoidae. See Beesley et al. 2000, pp. 152–7
Miura T. 1994. Two new scale-worms (Polynoidae: Polychaeta) from the Lau back-arc and north
Fiji basins, South Pacific Ocean. Proc. Biol. Soc. Wash. 107:532–43
Norlinder E, Nygren A, Wiklund H, Pleijel F. 2012. Phylogeny of scale-worms (Aphroditiformia,
Annelida), assessed from 18SrRNA, 28SrRNA, 16SrRNA, mitochondrial cytochrome c
oxidase subunit I (COI), and morphology. Mol. Phylogen. Evol. 65:490–500
Pettibone MH. 1986. Review of the Iphioninae (Polychaeta: Polynoidae) and revision of Iphione
cimex Quatrefages, Gattyana deludens Fauvel, and Harmothoe iphionelloides Johnson
(Harmothoinae). Smithsonian Contrib. Zool. 428:1–43
Storch V. 1967. Iphione muricata (Savigny), ein den chitonen ähnlicher Lebensformtyp unter den
Polychaeten. Kieler Meeresforsch. 23:148–55
Wolf PS. 1986. A new genus and species of interstitial Sigalionidae and a report on the presence
of venom glands in some scale-worm families (Annelida: polychaeta). Proc. Biol. Soc. Wash.
99:79–83
Lacydoniidae, Glyceriformia, Phyllodocida
Diversity and systematics
Lacydoniidae are known from the single genus, Lacydonia, that currently contains 10 species.
Böggemann (2009) reviewed recent revisions of the family. In molecular genetic analyses
among the Phyllodocidae, he found Lacydoniidae to be closest to Paralacydoniidae and distant
from Nereididae, Sphaerodoridae and Goniadidae. Adults are < 1 cm long and as short as 2 mm.
Habitat
Lacydoniids are collected from intertidal to abyssal depths, primarily on soft sediments
(Böggemann 2009).
Sensory and feeding structures
The prostomium tends to be hemispherical. It bears two ventrolateral palps, two dorsolateral
antennae and one medial antenna. A pair of dorsolateral eyespots may be present about midway
along the prostomium. Nuchal organs are dorsolateral, ciliated slits just behind the prostomium
(Böggemann 2009). The muscular, axial pharynx is unarmed with hard parts but carries a
distinctive pair of lateral proboscis glands of unknown function.
Motility
We know of no data on motility in the family.
Illustrations
Pleijel & Fauchald (1993, Figs. 1 & 2) present line drawings of the anteriors of both L. oculata
and L. miranda in both dorsal and ventral views. Böggemann (2009, Figs. 67 - 69) presents
similar drawings as well as scanning electron micrographs of L. papillata. Pleijel (2001)
presents informative stippled line drawings of L. miranda and revealing micrographs of an
unidentified Lacydonia sp., including details of its nuchal organs.
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Lacydoniidae
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doi: 10.1146/annurev-marine-010814-020007
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Jumars, Dorgan & Lindsay
07 November 2014
Feeding
Lacydoniids are assumed to be carnivorous or omnivorous (Böggemann 2009), but no specific
food items have been identified.
Guild membership
We tentatively list lacydoniids as motile carnivores, likely on meiofauna, based on morphology
alone.
Research questions and opportunities
• Data on both motility and diet are lacking.
References
Böggemann M. 2009. Polychaetes (Annelida) of the abyssal SE Atlantic. Org. Divers. Evol.
9:251–428
Pleijel F. 2001. Lacydonia Marion, 1874. See Rouse & Pleijel 2001, pp. 117–8
Pleijel F, Fauchald K. 1993. Scalispinigeraoculata Hartman, 1967 (Scalibregmatidae:
Polychaeta): Senior synonym of Lacydonia antarctica (Lacydoniidae) Hartmann-Schröder &
Rosenfeldt, 1988. Proc. Biol. Soc. Wash. 106:673–7
Laetmonectidae, Terebellida (?)
Diversity and systematics
The monotypic family is known only from the type and original description (Buzhinskaya 1986).
Additional specimens may prove it to be a terebellid (cf. Fauchald & Rouse 1997).
Habitat
The species is known only from the type locality in the Gulf of Aden, Indian Ocean.
Sensory and feeding structures
These structures have not been analyzed.
Motility
Live specimens have not been observed.
Illustrations
The only illustrations are in the original description.
Feeding
Feeding biology of the species is unknown.
Guild membership
We presume that it is a tentaculate deposit feeder and guess from its lack of uncini that it is a
discretely motile, burrowing form.
Research questions and opportunities
• Any data on feeding or motility would be the first.
References
Buzhinskaya GN. 1986. Laetmonecticus nigrum gen. et sp. n. (Laetmonectidae fam. n.,
Polychaeta) from the Gulf of Aden. Zool. Zh. 65:1258–61
Fauchald K, Rouse GW. 1997. Polychaete systematics: Past and present. Zool. Scr. 26:71– 138
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Longosomatidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Longosomatidae, Spioniformia
Diversity and systematics
The family is known from about 7 species in the genus Heterospio (Bochert & Zettler 2009).
Lengths are difficult to estimate because most specimens are fragmented, but are of order 1 cm
and up to 5 cm. Anterior segments are small and crowded, but mid-abdomen segments are very
elongate. They are followed by a bulbous posterior.
Habitat
Longosomatids are known from shelf to abyssal depths in soft sediments. Most species have
been found between 50 and 1500 m. They are rare.
Sensory and feeding structures
The rounded conical prostomium lacks appendages. Dorsolateral nuchal organs are present
at the posterior of the prostomium as deep, ciliated grooves. The peristomium is a complete
ring. The presence or absence of palps on it has been controversial, however, because most
specimens have been recovered without palps, and palp scars may have been confused with the
nuchal organs (Parapar et al. 2014). Recent attempts to locate palp scars by scanning electron
microscopy have failed (Bochert & Zettler 2009, Parapar et al. 2014).
Motility
Live specimens have not been observed, but the bulbous posterior and diminutive head region
suggest that longosomatids may burrow backward more often than forward. Borowski (1994)
reported finding a mucoid sheath on one specimen of H. peruana, suggestive of tube building,
but it may be a burrow lining instead. He also remarked that the unusual, swollen posterior
section of the body was usually recovered from sediments > 10 cm below the sediment-water
interface and that all specimens were recovered 5 - 20 cm below the sediment-water interface.
Illustrations
Parapar et al. (2014) provide informative line drawings and scanning electron micrographs of
the anterior and elongate middle segments. Borowski (1994) provides informative stippled line
drawings of the posterior end as well.
Feeding
Published feeding information is lacking.
Guild membership
Any feeding assignment is speculative. We suspect from the depth distribution data in sediments
and the swollen posterior that Longosomatidae are subsurface deposit feeders. If they lack palps
motility would seem essential. If palps are present, discrete motility is likely, with potential
functional similarities to subsurface deposit feeding cirratulids.
Research opportunities
• Definitive information on the presence or absence of palps is needed.
• If live specimens could be obtained it would be interesting to compare burrowing in a
longosomatid with burrowing in Chaetozone (Cirratulidae) that also have cinctures of spines
to test the hypothesis that spine posture is controlled to ratchet burrowing directionally.
• Any feeding information would be the first. A likely target of such studies is Marlborough
Sounds, New Zealand, where in sediments that were < 10% sand, longosomatids were among
the most frequently collected polychaetes (Estcourt 1967). Although due to difficulties in
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Longosomatidae
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Jumars, Dorgan & Lindsay
07 November 2014
sieving no abundance estimates were made, Heterospio sp. was found at a wide range of
depths < 60 m.
• The expanded rear may be an adaptation enabling burrowing in particularly stiff muds.
References
Bochert R, Zettler ML. 2009. A new species of Heterospio (Polychaeta, Longosomatidae) from
offshore Angola. Zool. Sci. 26:735–7
Borowski C. 1994. New records of Longosomatidae (Heterospionidae) (Annelida, Polychaeta)
from the abyssal Southeast Pacific wtth the description of Heterospio peruana sp.n. and
general remarks on the family. Mitt. Hamb. Zool. Mus. lnst. 92:129–44
Estcourt IN. 1967. Distribution and association of benthic invertebrates in a sheltered water soft
bottom environment (Marlborough Sounds, New Zealand). N. Z. J. Mar. Fresh. Res. 1:352–
70
Parapar J, Aguirrezabalaga F, Moreira J. 2014. First record of Longosomatidae (Annelida:
Polychaeta) from Iceland with a worldwide review of diagnostic characters of the family. J.
Nat. Hist. 48:983–98
Lopadorrhynchidae, Phyllodocida
Diversity and systematics
Molecular data indicate that Lopadorrhynchidae (spelled with a double r according to WoRMS)
fall within Phyllodocidae and should be synonymized (Struck & Halanych 2010), but we treat
them separately because of morphological and behavioral differences. They are closely related
to Typhloscolecidae and Alciopidae, also treated separately here but part of Phyllodocidae
(Struck & Halanych 2010). They comprise about 19 species in 5 genera, 2 of them monotypic,
and range in length from a few millimeters to several centimeters (Pleijel 2001).
Habitat
Lopadorrhynchidae are holopelagic and concentrate in the upper mixed layer but also extend into
mid waters.
Sensory and feeding structures
The prostomium is smoothly rounded to nearly rectangular, with a pair of dorsolateral antennae
and a pair of ventrolateral palps. The latter are usually slightly smaller. Eyes are present as a
single, lensed pair or absent. Nuchal organs are present as a lateral pair of ciliated knobs that
may be eversible (Pleijel 2001). A peristomium is difficult to delineate. The axial pharynx is
not well known but is unarmed in some taxa (Pleijel 2001). Members of the genus Pelagobia
have been described as carrying a pair of diminutive mandibles (Orensanz & Ramirez 1973) or
two hooks (Uschakov 1972, cited in Pleijel 2001 as stylet-like hooks). In our terminology, these
teeth are fangs or stylets; there are no hinged jaws. Neither teeth nor jaws have been described
in other genera of the family. Large, mucus-producing glands open into the base of the pharynx
(Dales 1955). The gut is a straight tube, consistent with a nutrient-rich diet. Lopadorrhynchids
have elongate parapodia for swimming (cf. Fig. 1B of Halanych et al. 2007).
Motility
Parapodia and chaetae are modified for swimming. The balance between sit-and-wait versus
cruising predation is unknown.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Illustrations
Uschakov (1972, Plate XXI, 2a, b) provides line drawings of the fangs (described as hooks)
of Pelagobia longicirrata seen both through the body wall and excised. Orensanz & Ramirez
(1973, Plate II, Fig. 5) provide a line drawing of a single tooth and its muscle bulb from the same
nominal species; it looks more stylet like. Sardá et al. (2009, Fig. 5F) provide a light micrograph
of a single tooth that looks intermediate in curvature between the other two sets of depictions.
Feeding
Contrary to both inference in F&J and confident assertion by Day (1967), not all holopelagic
lopadorrhynchids are carnivorous. Indeed, the only abundant gut content data yet published are
for Pelagobia longicirrata, and they clearly show it to be herbivorous on microalgae. Hopkins
(1985) dissected 144 specimens 2.2 - 4.5 mm long from Gerlache Strait but found identifiable
gut contents in only 12: 10 with phytoplankton debris, 3 with recognizable diatoms, 3 with
Euphausia superba debris, and 1 with coelenterate material. Of 50 individuals 3.5 - 5.5 mm
long from McMurdo Sound dissected by Hopkins (1987), all 44 with identifiable gut contents
contained Nitzchia spp., 23 contained Chaetoceros spp., 11 contained Coscinodiscinae, and
3 contained peridinian dinoflagellates. Hopkins & Torres (1989) dissected an additional 30
individuals 1.5 - 6.6 mm long from the Weddell Sea and found 26 to contain diatoms and 1 to
contain an ostracod.
Hopkins (1985) also dissected 19 individuals of Maupasia caeca 2.4 -13.0 mm long. He
found identifiable gut contents in only 3: 2 with phytoplankton detritus, 1 with a Corethron
sp. (diatom), and 1 with protozoan remains. These results, with most guts empty, are
more ambiguous regarding herbivory versus carnivory. Hopkins (1985) suggested that the
phytoplankton might be the result of incidental ingestion of herbivorous, gelatinous plankton.
Guild membership
We tentatively characterize lopadorrynchids as motile herbivores on microalgae and predators
on other small protists and animals using either armed or unarmed pharynges. The degree of
motility (range between cruising and sit-and-wait predation) is not known.
Research questions and opportunities
• The fangs in Pelagobia would appear to have limited utility in feeding on microalgae. We
suspect that the phytoplankton-containing diet is supplemented with animal prey. Stable
isotopic data would be informative in testing this hypothesis.
• Live observations would be useful in understanding the cues and methods used to detect and
capture phytoplankton and other organisms.
References
Dales RP. 1955. The evolution of the pelagic alciopid and phyllodocid polychaetes. Proc. Zool.
Soc. Lond. 125:411–20
Day JH. 1967. A Monograph on the Polychaeta of South Africa. Part 1. Errantia. London:
British Museum of Natural History
Halanych KM, Cox LN, Struck TH. 2007. A brief review of holopelagic annelids. Integr. Comp.
Biol. 47:872–9
Hopkins TL. 1985. Food web of an Antarctic midwater ecosystem. Mar. Biol. 89:197–212
Hopkins TL. 1987. Midwater food web in McMurdo Sound, Ross Sea, Antarctica. Mar. Biol.
96:93–106
Hopkins TL, Torres JJ. 1987. Midwater food web in the vicinity of a marginal ice zone in the
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doi: 10.1146/annurev-marine-010814-020007
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Jumars, Dorgan & Lindsay
07 November 2014
western Weddell Sea. Deep-Sea Res. 36:543–60
Orensanz JMA, Ramírez FC. 1973. Taxonomía y distribuciónde los poliquetos pelágicos del
atlántico sudoccidental. Boletín–Instituto de Biología Marina 21:1–86
Pleijel F. 2001. Lopadorhynchidae Claparède, 1868. See Rouse & Pleijel 2001, pp. 119–20
Sardá R, Gil J, Taboada S, & Gili J. 200). Polychaete species captured in sediment traps moored
in northwestern Mediterranean submarine canyons. Zool. J. Linn. Soc. 155:1-21
Struck TH, Halanych KM. 2010. Origins of holopelagic Typhloscolecidae and Lopadorhynchidae
within Phyllodocidae (Phyllodocida, Annelida). Zool. Scr. 39:269–75
Uschakov PV. 1972. Polychaeta 1. Polychaetes of the suborder Phyllodociformia of the Polar
Basin and the northwestern part of the Pacific. Fauna SSSR 102:1–271
Lumbrineridae, Eunicida
Diversity and systematics
Lumbrineridae comprise over 300 species in about two dozen genera, 5 of them monotypic.
Over half of all species are in the genus Lumbrineris. They are medium long to long (most adult
individuals 5 cm to 1 m) but can be very slender. They resemble Oenonidae externally, but their
jaws differ substantially. Molecular genetic analysis suggests that Lumbrineridae are basal in
eunicidan phylogeny (Struck 2006).
Habitat
Most lumbrinerids burrow in sands and muds, although some live on rocky bottoms and among
algal holdfasts (Pleijel 2001). Ayyagari & Kondamudi (2014) recently described an unusual
association of Lumbrineris latreilli, normally free living in sediments, found among the spines
of a rock-burrowing sea urchin in the intertidal. Stabili et al. found several specimens of L.
cf. latreilli burrowed within the large mucus envelope surrounding Myxicola infundibulum
(Sabellidae). Lumbrinerids occur at all ocean depths.
Sensory and feeding structures
Like oenonids, most lumbrinerids lack anterior appendages, although a few species have one or
two small antennae. Most lack eyes. Nuchal organs are dorsolateral pits at the posterior margin
of the prostomium (Pleijel 2001).
Like other Eunicida, lumbrinerids have a ventral muscular proboscis with jaws. Lumbrinerid
maxillae have relatively short carriers that extend into the pharyngeal tissue and are structurally
similar to those of Eunicidae and Onuphidae. Recent phylogenetic analysis (Struck et al. 2006)
supports Colbath’s (1986) suggestion that lumbrinerid jaws, which are mineralized by calcite,
are distinct from those of eunicids and onuphids with aragonite mineralization. Functional
consequences of mineralization, which is absent in dorvilleid and oenonid jaws, have not been
explored, although presumably mineralized jaws are stiffer and more resistant to fracture (Koehl
1982). Whether these minerals increase resistance to abrasion as metals do in phyllodocid jaws
(e.g., Lichtenegger et al. 2002) has not been explored.
Motility
Most lumbrinerids burrow. In aquaria, specimens of Lumbrineris cf. latreilli built a main burrow
about 11 cm deep but fed primarily from side branches. Petch (1986) thus considered this
species discretely motile. Recent video observations reveal that L. cf. latreilli burrowing in sand
used the prostomium to move grains aside, retreated backward into previous, lined burrows, and
then revisited previously established paths; particles were incorporated into a mucous burrow
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
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Jumars, Dorgan & Lindsay
07 November 2014
lining as the worms burrowed. Rapid retreats were likely to pull pore water into the new tube
where it could be sampled by the nuchal organs, but this interpretation of body as piston used to
deliver sensory information needs to be confirmed (SM Lindsay, unpubl.).
Illustrations
Petch (1986; Fig. 5) includes a drawing of the branched burrow structure of Lumbrineris
cf. latreilli. Images of mandibles in Valderhaug (1985; Fig. 2) show growth lines that are
characteristic of different seasons and correlate with age. Jaws are also shown by Paxton (2009).
Feeding
Ockelmann & Muus (1978) studied population dynamics of the bivalve Mysella bidenta in
the Øresund. They observed Scoletoma fragilis to take (p. 35), “Foraminifera, small bivalves
and snails, tubicolous polychaetes, 0-group spatangoid [urchins] and Amphiura spp.” Arm
remains of these brittlestars made up the bulk of the gut contents. Adult S. fragilis generally
took bivalves < 3 mm long and crushed them with their jaws but left characteristic scratches on
the shells of survivors. According to Ockelmann & Muus (1978, p. 35) S. fragilis “searches for
prey both in the surface layer and deeper down in the sediment and apparently is one of the most
voracious polychaetes in the Øresund.”
Petch (1986) dissected Lumbrineris cf. latreilli from the intertidal of Westernport Bay,
Australia, for gut contents and watched behavior of live specimens in aquaria. Seventy-one
percent of individuals dissected had gut contents. Decaying fragments of seagrass were found
in 45% of specimens. One individual contained several whole nephtyid parapodia, but overall
the gut contents consisted mainly of sediment. Worms showed statistically significant preference
for sediments 16 - 31 µm diam., smaller than ambient modal grain size. Total numbers of worms
examined were not specified, but size preference data were given for 20 specimens. Stabili
et al. (2014) speculated that L. cf. latreilli burrowing into the mucus envelopes of Myxicola
infundibulum (Sabellidae) may feed on the envelopes, including their bacteria.
Based on extensive dissections for gut contents, Gaston (1987) classified Lumbrinerides
acuta, Lumbrineris albidentata and Scoletoma fragilis as carnivores—primarily on the basis of
empty guts, although 7 of 103 individuals of L. acuta contained forams, and all 15 juvenile S.
fragilis contained detritus. Fifty of 62 Lumbrineris impatiens contained detritus (the other dozen
having empty guts), and all 20 Lumbrineris latreilli and all 48 Ninoe nigripes contained detritus.
Carrasco & Oyarzún (1988) dissected Lumbrineris tetraura from grab samples at 7 m
water depth in the vicinity of Talcahuano fishing port in Chile. They found this species to
be carnivorous and highly selective for the sigalionid Sthenelais helenae, another burrowing
predator. L. tetraura was also frequently cannibalistic.
Levin & Mendoza (2007) found unidentified lumbrinerid species to have highly variable
trophic levels between methane seep sites. This variability likely has large taxonomic as well
as geographic components. A large majority of stable isotopic studies of lumbrinerids give
evidence of carnivory (Table A1). McLeod et al. (2010), on the other hand, found unidentified
species of Lumbrineridae in organic-rich New Zealand fjords (Doubtful-Bradshaw Sound fjord
complex) to have δ15N values more comparable to those of detritivorous polychaete species in
the same samples.
Levin et al. (1999) found unusually rapid incorporation of 13C from labeled diatom detritus
into lumbrinerids on the continental slope of North Carolina. Similarly, Sweetman & Witte
(2008) found rapid incorporation of 13C from labeled diatom detritus into lumbrinerids in
incubated cores from 688 m water depth in Korsfjorden, Norway. In contrast to deposit-feeding
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Paraonidae and Cirratulidae that showed gradual increase in Δδ13C, the value for Lumbrineridae
increased rapidly over 7 d, then decreased at 14 d, suggesting a rapid but brief response to an
influx of rich food.
Table A1. Studies finding δ15N% indicative of carnivory in Lumbrineridae
Citation
Location
Hobson et al. 2002
Northeast Water Polynya,
Baffin Bay
Tamelander et al. 2006 Barents Sea
Water depth (m) Taxon
247 - 680
Lumbrineris sp.
227 - 343
Scoletoma fragilis
Yoshino et al. 2006
Seto Inland Sea
Carlier et al. 2007
Bay of Banyuls-sur-Mer
5 - 35
Scoletoma fragilis, S.
impatiens
Dubois et al. 2007
Bay of Veys, Normandy
0
Lumbrineris tetraura
Choy et al. 2008
Nakdong River estuary, Korea
Nilsen et al. 2008
Sørfjord, northern Norway
Kon et al. 2010
mangrove swamp, Thailand
Sampaio et al. 2010
shelf near Lisbon
30 - 50
Hilbigneris gracilis
Grippo et al. 2011
inner shelf, Louisiana
5 - 20
Lumbrineris spp.
Deudero et al. 2011
Mallorca Island
5-8
Hilbigneris gracilis
Kędra et al. 2012
Kongsfjorden, Spitzbergen
15
Ouisse et al. 2012
Zostera beds near Roscoff
1.8 - 3.3
Deudero et al. 2014
Mallorca Island
Ha et al. 2014
Zostera beds, Dong-dae Bay,
South Korea
Rigolet et al. 2014
Bay of Concarneau
Sokołowski et al. 2014 Hornsund, Spitsbergen
Guild membership
10
0 - 10
unspecified
intertidal
5-8
intertidal
5 - 35
100
Lumbrineridae
Lumbrineris sp.
Scoletoma fragilis
Lumbrineris sp.
Lumbrineris mixochaeta
Lumbrineris sp.
Hilbigneris gracilis,
Lumbrineris latreilli
Lumbrineris sp.
Hilbigneris gracilis
Lumbrineris mixochaeta
Consistent with F&J, most lumbrinerids are carnivores on both sessile and motile prey, with a
few herbivorous and subsurface deposit-feeding exceptions (F&J). They are burrowers, and at
least one species seems to be discretely motile in a constructed burrow. Other species may be
more motile.
Research questions and opportunities
• Quantitative data on motility are lacking.
• It would be useful to check stable isotopic values in lumbrinerid populations that have
apparent gut contents of detritus to see if carnivory is more important than apparent gut
contents suggest (due to differences in digestibility and energy density).
• Stable isotope data could test the hypothesis that L. cf. latreilli feeds on the mucus envelope
of Myxicola infundibulum (Sabellidae, Stabili et al. 2014).
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A154
Lumbrineridae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
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Deudero S, Box A, Alós J, Arroyo NL, Marbà N. 2011. Functional changes due to invasive
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macroalga Caulerpa racemosa. Estuar. Coast. Shelf Sci. 93:106–16
Deudero S, Box A, Vázquez-Luis M, Arroyo NL. 2014. Benthic community responses to
macroalgae invasions in seagrass beds: Diversity, isotopic niche and food web structure at
community level. Estuar. Coast. Shelf Sci. 142:12–22
Dubois S, Marin-Léal JC, Ropert M, Lefebvre S. 2007. Effects of oyster farming on macrofaunal
assemblages associated with Lanice conchilega tubeworm populations: A trophic analysis
using natural stable isotopes. Aquaculture 271:336–49
Gaston GR. 1987. Benthic Polychaeta of the Middle Atlantic Bight: feeding and distribution.
Mar. Ecol. Prog. Ser. 36:251–62
Grippo MA, Fleeger JW, Dubois SF, Condrey R. 2011. Spatial variation in basal resources
supporting benthic food webs revealed for the inner continental shelf. Limnol. Oceanogr.
56:841–56
Ha S, Min WK, Kim DS, Shin KH. 2014. Trophic importance of meiofauna to polychaetes in a
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Hobson KA, Fisk A, Karnovsky N, Holst M., Gagnon JM, et al. 2002. A stable isotope (δ13C,
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the flow of energy and contaminants. Deep-Sea Res. Pt. II 49:5131–50
Kędra M, Kuliński K, Walkusz W, Legeżyńska J. 2012. The shallow benthic food web structure
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Koehl MAR. 1982. Mechanical design of spicule-reinforced connective tissues: Stiffness. J. Exp.
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Kon K, Kurokura H, Tongnunui P. 2010. Effects of the physical structure of mangrove vegetation
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Levin LA, Blair NE, Martin CM, DeMaster DJ, Plaia G, et al. 1999. Macrofaunal processing
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Levin LA, Mendoza GF. 2007. Community structure and nutrition of deep methane-seep
macrobenthos from the North Pacific (Aleutian) margin and the Gulf of Mexico (Florida
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
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07 November 2014
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A156
Magelonidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Magelonidae
Diversity and systematics
Magelonidae are spioniform polychaetes, easily identified by a spade-like prostomium, two long,
papillated palps, and a curious, creamy to pink translucency. They do not cluster in molecular
genetic analysis with Spionidae (Rousset et al. 2007); the morphological similarity appears
convergent. Instead, they are basal annelids and a sister clade to Oweniidae (Weigert et al.
2014). The number of species in Magelonidae has climbed steadily into the neighborhood of
70 (Mortimer & Mackie 2014). So far the family has resisted attempts to subdivide the single
genus Magelona into coherent, multiple, non-monotypic genera, with the exception of the single
species, Octomagelona bizkaiensis, which has 8 instead of 9 thoracic setigers (Aguirrezabalaga
et al. 2001). Most species are medium long (a few to 15 cm), and thin (< 1 mm diam).
Taxonomic issues troubled the feeding summary of F&J for Magelonidae. Jones (1977)
suggested that earlier European descriptions of feeding should have named M. mirabilis. Later
studies, however, revealed that in many European localities a previously undescribed species,
M. johnstoni, was also present (Fiege et al. 2000, Mortimer & Mackie 2014). Jones’ (1968)
description of feeding in Magelona was of a still unnamed species (Mortimer & Mackie 2014).
Habitat
Magelonids are most abundant in intertidal and shallow subtidal sediments ranging from beach
sands to muds. They are usually not dominant but are common at all shelf depths.
Sensory and feeding structures
Species of Magelona show unusual diversity in the shapes of their spade-like prostomia,
including the presence and prominence of lateral horns, smoothness or rugosity, and aspect
ratio (e.g., Mortimer et al. 2012). We suspect that these prostomial shapes and their deployment
below the sediment-water interface underlie the well known association of individual magelonid
species with narrow ranges of sediment types (Meisner & Darr 2009). No nuchal organs or eyes
have ever been reported in adults (Rouse 2001).
Although magelonids have been considered closely related to spionids based on their two
long palps, the palps of magelonids are papillated and lack the ciliated groove of spionids. The
long tentacles have discrete blood vessels (Jones 1968) and may be important in respiration as
well as feeding. In explaining the unusual insensitivity of M. cf. phyllisae to hypoxia in the
Gulf of Mexico “dead zone,” Gaston (1985) stated that, “Unlike many of the species in the fine
sediments of the study area, Magelona inhabited the reduced sediments below the sediment
surface.” In contrast to the palps of spionids that contain longitudinal, circular, and diagonal
muscles, magelonid palps have longitudinal muscles only (Filippova et al. 2005), consistent
with observations that they do not elongate or change shape during burrowing and feeding (KM
Dorgan, pers. obs.).
The eversible pharynx is unarmed but has radial pharyngeal muscles, and circumbuccal
muscles along the ventral area behind the mouth opening are likely important in pharyngeal
eversion (Filippova et al. 2005). The large size and balloon-like expansion of the pharynx
suggest that hydrostatic pressure likely contributes to eversion as well (KM Dorgan, pers.
obs). Although the flattened, spade-shaped prostomium extends anteriorly well beyond the
mouth, the pharynx is axial (Filippova et al. 2005). Filippova et al. (2005) suggested that the
diductor muscles that run circumferentially along the dorsal side of the mouth reflect a suctorial
functioning, although it seems plausible that they may function in pharyngeal retraction rather
than creating suction to capture prey.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Motility
Although tube building has not been seen in most species, Mortimer & Mackie (2009) and
Mortimer et al. (2012) reported evidence of a sediment tube on many specimens of Magelona cf.
falcifera, M. cincta, M. alleni, and M. symmetrica. Whereas some tubes observed may simply be
burrow linings agglutinated by mucous secretions, that of M. cincta was described as “a sheathlike, multilayered tube covered in sand grains” (Mortimer & Mackie 2009) and that of M. alleni
as a “red-purple papery tube” (Mortimer & Mackie 2014). Mortimer & Mackie (2014) described
characteristic sinuous, side-to-side movements of the thorax in M. johnstoni and its use of
pharyngeal eversion in burrowing. Burrowing may be more or less continuous in M. sacculata
(Fauchald 1983) and M. johnstoni (Mortimer & Mackie 2014).
Illustrations
Jones (1968) shows drawings of morphology of Magelona sp. from dorsal, ventral (Fig 1)
and lateral (Fig. 30) views, as well as the papillae on the palps (Fig. 32, 33). Drawings and
photographs by Mortimer et al. (2012, Fig. 13) well illustrate the range of prostomial shapes
among Magelona spp. Confocal images and drawings of the anterior musculature of M. cf.
mirabilis by Filippova et al. (2005) are both striking and informative.
Feeding
Jones (1968) and most other authors (e.g., Flint & Rabalais 1980) have characterized magelonids
as surface deposit feeders, but (as F&J summarized) with a tendency toward carnivory. F&J’s
characterization of magelonids as surface deposit feeders is questionable. Jones’ (1968) and
Mortimer & Mackie’s (2014) observations leave little doubt that some magelonids have the
capability to feed by deploying tentacles at the sediment-water interface when placed in sands
and offered organic-rich detritus only at the interface. That is not the only feeding mode of
magelonids, however. One of us (KM Dorgan, unpublished) has observed M. pitelkai burrowing
in sand below the sediment-water interface, moving backward and then deploying tentacles into
the void created by the most recent burrowing episode. The tentacles undulate in the void with
a traveling wave, much like snapping a rope from one end, contacting the burrow walls and
possibly driving fluid flow. Given the absence of any description of magelonid tentacles present
above the sediment-water interface from either diver observations or bottom cameras, we suggest
that feeding from burrow walls and fracture surfaces of mud is more likely than surface deposit
feeding in Magelona. In aquarium observations, M. johnstoni and M. mirabilis extended their
tentacles > 4 mm onto the surface only when stimulated to feed on new food at the sediment
surface (Mortimer & Mackie 2014). Minimal uptake of organic matter from 13C-labeled
phytoplankton by M. mirabilis (Kamp & Witte 2005) is also consistent with subsurface feeding.
Some magelonids definitely do ingest sediments. Dauer (1980) dissected 15 M. pettiboneae
from a sandy, intertidal beach in Florida. Two had guts completely packed with foraminiferans,
and 3 contained small bivalves; both the foraminiferans and bivalves stained with rose
Bengal. The remainder of the worms and much of the gut volume in the individuals that
contained bivalves were filled with clay, despite dominance of the ambient sediment by fine
sand. Magalhães & Barros (2011) dissected 160 M. papillicornis and 15 M. variomellata from
estuaries opening into Baía de Todos os Santos, northeastern Brazil. All contained detritus, and
the latter species also ingested some fine sand.
Stable isotopic studies, however, suggest that Jones’ (1968) observation of feeding on eggs
and nauplii may be indicative of greater carnivory than suggested by F&J. Levin et al. (2000)
assayed δ15N in M. sacculata from (methane) seep and non-seep sites off Northern California.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Its non-seep δ15N values were unremarkable at 8.6 and 10.6‰. The individual from a seep site,
however, was a real outlier at 21.5‰. That value, the highest for all species in Levin et al.’s
(2000 Table 8), is difficult to explain without substantial carnivory. Although not as extreme,
van Oevelen et al.’s (2009) values for M. papillicornis from the North Sea are higher than those
for other deposit feeders, again suggesting proclivity toward carnivory. Daigle (2011) also found
Magelona sp. to feed at higher trophic levels than the other polychaetes she sampled at 70 - 95
m water depths off Louisiana. Carnivory would be consistent with the relatively high weightspecific ammonium excretion rates measured by Gardner et al. (1993) in Magelona sp. collected
at about 40 m depth off Louisiana.
In the Bay of Biscay, on the other hand, Le Loc’h et al. (2008) found M. alleni with lower
15
δ N than any other deposit-feeding or carnivorous polychaete sampled. Grippo et al. (2011)
sampled benthos from depths ≤ 20 m off Louisiana. Magelona spp. δ15N values fell in the range
of other deposit feeders and omnivores but below carnivores. Given the taxonomic confusion,
in most cases we do not know whether some Magelona species are carnivorous or whether all
species are flexible in diet. When, where and on what various Magelona species tend to prey as
carnivores is not yet predictable, but stable isotopes suggest a tendency toward carnivory. The
other possibility is that elevated δ15N values may reflect subsurface deposit feeding rather than or
in addition to carnivory.
Guild membership
Whereas surface deposit feeding has been observed in constrained laboratory settings, we believe
that subsurface feeding is more common than indicated by F&J. Although carnivory seems more
likely than suggested, we tentatively characterize magelonids as subsurface deposit feeders that
utilize a pair of palps and may be very selective. Most are motile, although a few species make
tubes, indicating discrete motility. At least some species will opportunistically surface deposit
feed, and possibly suspension feed (suggested by the looping of the palps described by both
Jones (1968) and Mortimer & Mackie (2014) when doing so will yield high-value resources. We
conjecture that tube building may be associated with proclivity to surface deposit feed.
Research questions and opportunities
• Examination of dietary differences between different species and populations would be
informative.
• Behavioral observations of carnivory and subsurface deposit feeding are lacking.
• It is unknown whether magelonids secrete surfactants that are the digestive hallmarks of
other deposit-feeding polychaetes.
• Clay in the gut would appear to create problems for lipid transport to absorptive sites (Voparil
et al. 2008), arguing against carnivory in clay swallowers.
• Where (level in the sediments) and how magelonids selectively ingest clay in a sandy,
intertidal environment (Dauer 1980) remain to be determined.
References
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Daigle ST. 2011. What is the importance of oil and gas platforms in the community structure and
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Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A159
Magelonidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
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pouches. Mem. Mus. Victoria 71:177–201
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Rouse GW. 2001. Magelona Müller, 1858. See Rouse & Pleijel 2001, pp. 261–63
Rousset V, Pleijel F, Rouse GW, Erséus C, Siddall ME. 2007. A molecular phylogeny of annelids.
Cladistics 23:41–63
Weigert A, Helm IC, Meyer M, Nickel B, Arendt D, et al. 2014. Illuminating the base of the
annelid tree using transcriptomics. Mol. Biol. Evol. doi: 10.1093/molbev/msu080, 11 pp.
Maldanidae
Diversity and systematics
Maldanidae comprise about 250 species distributed among about 40 genera, 12 of them
monotypic. De Assis & Christoffersen (2010) suggested subfamilial relationships on the basis
of morphological cladistics. No molecular phylogeny of the family has been done, but both
molecular and morphological data place them close to Arenicolidae (e.g., Struck et al. 2007;
Zrzavý et al. 2009). Wilson (1983) suggested that sibling species are hidden within Axiothella
rubrocincta. Maldanids are easily identified by their long segments (hence the common name,
bamboo worm) and range in body sizes from meiofaunal (e.g., Micromaldane) to ~ 30 cm long.
Habitat
Maldanids live head downward in sediments at all ocean depths and are common in shallow
to shelf habitats, where they can number > 12,000 m-2 (Holte 2001). Although primarily
tube dwelling (classified as sessile, subsurface deposit feeders by F&J), their contributions to
bioturbation can be substantial as they not only feed on subsurface sediments and defecate on the
surface, but some species also use their fringed posteriors to “hoe” surface sediments down into
the burrow (Levin et al. 1997, Shull 2001).
Sensory and feeding structures
Maldanids have paired nuchal slits and can have simple eyespots on the prostomium, but no
anterior appendages. Slits have diverse orientations and shapes among species (De Assis &
Christoffersen 2011). Maldanids lack jaws, but otherwise exhibit considerable variability in
pharyngeal morphology, including a ventral pharynx with dorsolateral ciliary folds, a nonmuscular axial proboscis, as well as in-between stages (Tzetlin & Purschke 2005). Dorsolateral
ciliary folds are typically associated with small, likely highly selective adults or the juveniles of
larger species (Tzetlin & Purschke 2005), and this variation may reflect size-based differences in
feeding strategies.
Motility
Most maldanids are tubicolous, but considerable variability in tube shapes and robustness occurs
both among and within species, ranging from U shapes to angled or coiled burrows with one
surface opening to completely vertical burrows. Axiothella rubrocincta from Eagle Bay, San
Juan Island, Washington, builds vertical tubes (Wilson 1983). Kudenov (1978, 1982) carried out
a number of field and laboratory studies on Axiothella rubrocincta from Tomales Bay, California.
A. rubrocincta constructed U-shaped tubes that bottomed out about 30 cm deep in the sediment
with the two vertical members separated by about 10 - 15 cm. Spies (1969), however, apparently
either observed or assumed that A. rubrocincta from Tomales Bay lived in vertical tubes because
he accommodated individuals to vertical glass tubes so that they could be placed for observation
close to the side of a sand-filled aquarium. Clymenella zonalis builds a tube with similar J or U
shape (Mangum 1964).
Based on comparison of field samples of tubes versus ambient sediment, Spies (1969)
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observed modest selection against smaller particles for tube construction by A. rubrocincta
(median grain size for tubes of 358 versus 260 µm for the ambient sediment). Dufour et al.
(2008) observed some bias toward exclusion of fine and very fine silt by Maldane sarsi in tube
construction. These findings complemented earlier observations by Featherstone & Risk (1977)
of exclusion of fine particles and heavy minerals from the tubes of Clymenella torquata. Hughes
(1979), however, found little evidence of particle selection in tube construction by A. catenata,
Praxillella gracilis, and Nicomache lumbricalis, although the range of particle sizes was small.
Illustrations
Dufour et al.’s (2008; Fig. 1) CT scans of tubes of Maldane sarsi show feeding voids, and
Olivero & López Cabrera (2010) present photographs and interpretive drawings of similar
feeding voids in fossil Tasselia ordamensis. Hughes (1979; Fig. 1) shows drawings of angled
tube positions, including mounds and feeding cavities, of Axiothella catenata and Praxillella
gracilis, and Kudenov (1978) includes a drawing of the U-shaped tube of A. rubrocincta.
Kongsrud & Rapp (2011, Fig. 4) show photographs of tubes of Nicomache lobii from black
smokers and diffuse sedimentary vents. Kudenov (1977) includes sequential drawings of
pharyngeal eversion and feeding, as well as of pharyngeal morphology, in three species.
McDaniel & Banse (1979) include photographs of the mucus net structure of suspension-feeding
Praxillura maculata.
Feeding
Maldanids were characterized by F&J as subsurface deposit feeders, but numerous studies
subsequently have highlighted the importance of rapidly subducted surficial sediments in
maldanid diets. A. rubrocincta from Tomales Bay, California, fed on material that fell into its
head shaft, creating a feeding depression around it and a fecal mound at the other end of the U.
This mode of feeding resulted in ingestion of organic-rich surficial sediments (Kudenov 1978),
further enriched by selective deposition into the feeding depression (Yager et al. 1993). Ingested
food items included diatoms, other protists and small metazoans (Kudenov 1978). Hughes
(1979) studied burrow structures of Axiothella catenata, Praxillella gracilis and Nicomache
lumbricalis in the field and in laboratory aquaria. A. catenata and P. gracilis built inclined tubes,
horizontally displacing fecal mounds from the feeding depressions that resulted from subduction.
Both produced feeding voids at the bottoms of approximately straight tubes roughly 50 cm long.
A. catenata built at a shallower angle, placing the feeding void about 15 cm below the sedimentwater interface, whereas P. gracilis placed its feeding void roughly 30 cm deep. This subduction
of surficial sediment is similar to funnel feeding by arenicolids. N. lumbricalis tubes were coiled
with other tubes to form globular colonies, with feeding depths much closer to the surface.
Subduction of surface sediments occurs in some species with vertical burrows as well.
Clymenella torquata, for example, builds a vertical tube and subducts sediments close to its tube
(Rhoads & Stanley 1965). Subsurface feeding alone does not explain the rapid vertical transfer
of organic material by this species and other maldanids, however. Clymenella torquata was
observed to use posterior segments and the anal plaque to scrape surficial sediments into the
tube opening (Dobbs & Whitlatch, 1982). This “hoeing” behavior explains observed subsurface
peaks in tracers (Levin et al. 1997, Praxillella sp.; Shull 2001, Macroclymene zonalis) and
may enhance growth (Weinberg 1988). Campbell (2012) observed greater hoeing by intact
Clymenella torquata in organically enriched sediments than by injured worms (posterior
segments ablated). The latter showed reduced sediment transport overall.
Construction of a vertical tube has the obvious advantage for species that hoe surface
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materials of rapid, gravity-driven delivery of surficial sediments to the feeding region. A
vertical tube would appear disadvantageous for subsurface feeding due to the inherent structural
instability of excavating directly under a vertical tube, although the graded bedding produced by
C. torquata (Rhoads & Stanley 1965) suggests that structural instability may be less problematic
than intuition suggests, at least for this species. Sediment around the tube of M. sarsi, however,
does not appear to be graded by subsurface feeding; rather, the sediment around the tube is
compacted in discoidal rings that appear to represent sequential feeding areas that are filled
and abandoned as the worm grows and extends its burrow deeper into the sediment (Dufour
et al. 2008). Structures of these modern and analogous Pliocene fossil worm domiciles were
interpreted by Olivero & López Cabrera (2010) and do not appear consistent with vertical
downward transport of sediments near the tube that would be caused by consistent feeding at the
bottom of the tube. In cross section the tube and its surrounding structures resemble stacked,
inclined disks or tongues (extending radially and at a shallow upward angle away from the tube)
whose sizes increase with depth in the sediment and that in enemble resemble a pine cone. M.
sarsi and fossil Tasselia ordamensis, presumably by deposit feeding, apparently excavated
discoid or lobate feeding voids. Then they may have hoed them full of surface sediments for
subsequent ingestion in a form of caching and possibly gardening. In Olivero & López Cabrera’s
(2010) interpretation, once use of a cache location ended or a garden stopped producing well,
or the worm became too long for the existing tube, the remaining void was backfilled, the
tube was extended at the bottom, and a deeper discoidal void was excavated. This interesting
interpretation deserves to be investigated further in modern species. It implies much less
net, lifetime upward transport of sediments in this style of head-down deposit feeding than in
others—limited to only the volume of the current feeding voids. It should be emphasized that
not all maldanids that build vertical tubes are so limited in ingestion of subsurface sediments.
Maldanid species clearly vary in degree of dependence on freshly deposited material hoed
from the surface. Witte et al. (2003) documented rapid subduction by maldanids (not identified
below family level) in situ through tracer experiments at 1265 m water depth in the Sognefjord
despite the much lower density of maldanids than at Levin et al.’s (1997) bathyal site off North
Carolina, where the first experimental field evidence of rapid subduction by Praxillella sp.
was obtained. On the other hand, Gontikaki et al. (2011), in core samples and pulse-chase
experiments from 1080 m water depth in the Faroe-Shetland Channel, found no evidence of
uptake of surficial sediments by the resident maldanids (that were not identified below the family
level). The maldanid isotopic signatures that they found were also consistent with subsurface
deposit feeding. Yokoyama et al. (2009), by contrast, in samples from the intertidal to 10 m
depth in Ariake Sound found stable N and C levels in unidentified maldanid species to be similar
to those of ampharetids and sabellids, implying high dependence on surficial materials, whether
by subduction or hoeing.
Very interestingly, M. sarsi showed high δ15N values, even exceeding those of predatory
polychaetes at 15 m water depth in Kongsfjord, Svalbard (Kędra et al. 2012), at 100 m
water depth in Hornsund, Spitsbergen (Sokołowski et al. 2014), and at 343 m water depth in
the Barents Sea (Tamelander et al. 2006). At 60 m water depth in Gullmar Fjord, Sweden,
Magnusson et al. (2003) found M. sarsi to have δ15N values about the same as in Glycera alba
(Glyceridae). Even more suggestively, unlike other subsurface deposit feeders in the study, it
showed significant uptake of a hydrophobic pollutant applied at the surface of 29 d laboratory
incubations, indicative of hoeing. Maldanids (‘Maldanidae indeterminate’) dominated benthic
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detritivore biomass in samples from unspecified locations in Sørfjord, northern Norway and
also had δ15N contents in excess of those found in predatory polychaetes (Nilsen et al. 2008).
Macroclymene santanderensis in the Bay of Banyuls-sur-Mer were somewhat more enriched
thatn Nephtys sp. (Nephtyidae) but slightly less 15N enriched than Glycera alba (Glyceridae,
Carlier et al. 2007). M. santanderensis and Maldane glebifex from 5 - 35 m water depth
in the Bay of Concarneau showed enrichments comparable to those in Hilbigneris gracilis
(Lumbrineridae, Rigolet et al. 2014). Slightly more ambiguous are Iken et al.’s (2010) data from
the Chukchi Sea. Both Nicomache sp. and Praxillella sp. showed δ15N about 11‰ greater than
that of surficial sediments and close to those of predatory polychaetes in the same samples, but
there were no reported values for comparison from known surface deposit feeders.
Particle size selection. Several studies found little evidence of active particle size selection
in maldanids. Except for some winter samples (Kudenov 1982), there was little evidence of
particle size selection of ingesta by A. rubrocincta. Self & Jumars (1988) similarly found
no statistically significant size selection by A. rubrocincta from Eagle Bay, San Juan Island,
Washington, although this population is unlikely to be the same species studied by Kudenov (cf.
Wilson 1983). Kudenov (1978) pointed out, however, that concluding nonselectivity on the basis
of grain size is misleading for two reasons. First, maldanid species segregate spatially by grain
size (e.g., Hughes 1979) and so select for grain size on that basis. Also, the subduction that they
cause results in substantial organic enrichment compared to sediments at the feeding depth but
outside the feeding funnel. Hughes (1979) found little grain size selectivity among Axiothella
catenata, Praxillella gracilis, and Nicomache lumbricalis, although all the measured grains fell
between 90 and 150 µm in diameter, a range so small that selectivity would be hard to detect.
N. lumbricalis did ingest sediment grains significantly larger than those ingested by P. gracilis,
but primarily because it was found in coarser sediments. Rhoads & Stanley’s (1965) classic
documentation of graded bedding produced by Clymenella torquata implies that larger worms
can and do ingest larger particles than do smaller worms, on average producing net upward
displacement of finer particles and downward displacement of coarser ones, although these
observations do not necessitate a selection mechanism other than mouth (gape) size.
Pilgrim (1965) indicated that British C. torquata living in gravelly sediments ingest few
sediment particles, i.e., that the stomach of field-collected specimens is (p. 403), “filled with
a soft, whitish mass containing many diatoms.” She contrasted these British specimens with
smaller individuals of C. torquata collected at Beaufort, North Carolina, whose guts were
filled with sand similar in grain size to ambient sediments. Spies (1969) occasionally observed
strong selectivity against sediment ingestion (pp. 22 and 25): “Sometimes the stomachs and
intestines of dissected worms contained no large particles of substrate, but instead, smaller
particulate matter enters the mouth. This means that A. rubrocin[c]ta is not exclusively a
substrate ingestor and may be deriving some benefit from detritus.” He indicated that ingestion
of this fine particulate material was accomplished by ciliary currents without pharyngeal
retraction. Kudenov (1977) observed rejection of individual large particles and whole boluses in
Axiothella rubrocincta, Clymenella californica and Praxillella affinis pacifica through reversal
of pharyngeal cilia. This capability is likely to be general for maldanids, providing at least one
mechanism for selection.
Microbial dependence at vents and seeps. Some maldanids show strong capability to incorporate
chemosynthetically produced organic matter and show high tolerance of sulfides and hypoxia.
Axiothella rubrocincta and Praxillella affinis pacifica showed the greatest dietary dependence
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of any macrofaunal species on petroleum seepage in samples from the Santa Barbara Channel
(Spies & DesMarais 1983). In an arctic black-smoker vent field, small individuals of Nicomache
(Loxochona) lokii (≤ 2.5 cm long) were collected on chimney walls and had tubes heavily
encrusted with ferrous material, whereas large individuals (up to 12.5 cm long) formed dense, 5
cm thick mats in the upper stratum of sedimentary regions surrounding the chimney (Kongsrud
& Rapp 2011). Sulfur, carbon and nitrogen isotopic signatures of this species were consistent
with heavy dietary dependence on vent sulfide oxidizers (Kongsrud & Rapp 2011). Maldanids
were highly depleted in 13C at shallow abyssal methane seeps on the Aleutian margin (Levin &
Mendoza 2007), bathyal methane seeps off New Zealand (Thurber et al. 2010), and bathyal seeps
in the Gulf of Mexico (Demopoulos et al. 2010).
Outliers. Perhaps the most unusual feeding mode reported for maldanids is for Praxillura
maculata that spins a mucus web over radial supports extending from its tube opening (elevated
2-7 cm above the sediment-water interface). It captures suspended particles, likely primarily by
direct interception. The web is held perpendicular to both the seabed and the prevailing, weak
tidal currents and is periodically ingested and reformed (McDaniel & Banse 1979).
From a box core taken at 2496 m water depth in the South China Sea, Kaminski & Wetzel
(2004) described a vertical burrow whose geometry resembled that of a vertical maldanid tube,
but whose feeding void had been filled primarily by tubular benthic foraminiferans of a single
genus. Lack of an agglutinated sediment tube and rarity of this foram genus on the surface of
the collected core argue against a maldanid origin, but the prevalence of metazoans and protists
in early descriptions of maldanid gut contents (F&J) and more recent studies (Kudenov 1978)
do make one wonder whether a deep-sea maldanid has taken hoeing and caching to unexpected
extremes.
Guild membership
We list maldanids as discretely motile, tubicolous deposit feeders, usually infaunal in soft
sediments. F&J hinted that they were discretely motile through punctuated tube building, but
we also note that experimentally displaced individuals are generally able to burrow and resume
feeding relatively quickly (e.g., Du Clos et al. 2013). Both rapid subduction of surface sediments
by subsurface feeding and hoeing of surface sediments down into vertical tubes can result in
substantial ingestion of surficial material, indicating that not all maldanids should be considered
subsurface deposit feeders (F&J). Rather, various species in a range of environments appear
to use one or more of: subsurface deposit feeding, caching, and funnel feeding. Suspensionfeeding Praxillura maculata is an interesting exception in this generally deposit-feeding group.
No studies of feeding habits by interstitial maldanids (e.g., Micromaldane) have been done to our
knowledge, but we presume based on animal size that they feed on labile material.
Research questions and opportunities
• Inter- and intraspecific variability in rates and patterns of subduction vs. hoeing would be
interesting to explore. Sites of superdominance by Maldane sarsi (e.g., Holte 2001) would
be particularly interesting to explore with tracers of overturn.
• Feeding chambers of Maldane sarsi with potential for microbial gardening may reveal some
interesting microbial diversity.
• Any feeding information on Micromaldane would be the first and could provide interesting
comparisons with the interstitial arenicolid genus Branchiomaldane.
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Mycomyzostoma calcidicola, Myzostoma incertae sedis
Diversity and systematics
Placement of Mycomyzostoma calcidicola within a family became uncertain with the realization
that Endomyzostomidae as previously defined was polyphyletic (Summers & Rouse 2014). The
genus is monotypic. Adult cysts are 4.5 - 9 mm diam.
Habitat
M. calcidicola inhabits a hard gall comprising multiple plates on the stalk of its host pedunculate
crinoid (Grygier 2000). The description of Mycomyzostoma calcidicola by Eekhaut (1998)
aroused paleontological interest because of similarly located cysts in fossil crinoids (e.g., Hess
2010). Each infested crinoid carries only a single cyst (Eekhaut 1998).
Sensory and feeding structures
M. calcidicola has no lateral organs (where sensory cells ordinarily are concentrated in
myzostomes). A short proboscis with a muscle bulb inserts into the host axial duct (Eekhaut
1998), and an anogenital pore opens on the opposite side of the spherical body from the pharynx.
Much of the body volume consists of a simple digestive sack, lacking diverticula. The body has
the aspect of a bota bag.
Illustrations
Grygier (2000, Fig. 2.16) reproduces informative line drawings and a photograph from the
original description by Eekhaut (1998).
Feeding
M. calcidicola is parasitic on host internal fluids (Eekhaut 1998).
Guild membership
M. calcidicola is a sessile parasite.
Research questions and opportunities
• Impact on the host’s energy budget is unknown.
References
Eeckhaut I. 1998. Mycomyzostoma calcidicola gen. et sp. nov., the first extant parasitic
myzostome infesting crinoid stalks, with a nomenclatural appendix by MJ Grygier. Species
Divers. 3:89–103
Hess H. 2010. Myzostome deformation on arms of the Early Jurassic crinoid Balanocrinus
gracilis (Charlesworth). J. Paleo. 84:1031–4
Summers MM, Rouse GW. 2014. Phylogeny of Myzostomida (Annelida) and their relationships
with echinoderm hosts. BMC Evol. Biol. 14:170, 15 pp.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Myzostomatidae, Myzostoma
Diversity and systematics
Grygier (2000) included three genera in Myzostomatidae, Myzostoma with over 100 species,
Hypomyzostoma with 11 described species, and Notopharyngoides with 3 named species.
Extensive molecular genetic analysis by Summers & Rouse (2014) revealed that now monotypic
Contramyzostoma (previously 2 spp.), Mesomyzostoma (8 spp.) and Notopharyngoides (3 spp.)
also fell within Myzostomatidae. Future molecular genetic analysis is likely, however, to move
several species from Myzostoma to Eenymeenymyzostomatidae (Summers & Rouse 2014).
Morphotypes correspond roughly with genera. Overall adult body shape in Myzostoma
is typically that of a thin, spherical or spheroidal (a little longer than wide) cap or dome up
to a few millimeters in diameter—a secondary radial structure imposed on a fundamentally
bilateral symmetry. Myzostoma sphaera (previously Contramyzostoma) retains the approximate
shape of Myzostoma spp, yet lives curled within a soft cyst. Adults of other genera have
similar sizes. Hypomyzostoma takes the shape of the dorsal exoskeleton of a pillbug and lives
wrapped around an arm or pinnule of its host crinoid, like a bun around a sausage (Grygier
2000). Notopharyngoides is polyphyletic with a broad range of morphologies (Summers &
Rouse 2014). Contramyzosoma bialatum has a unique shape, with large ventral lobes extending
laterally > 4 times the body radius. Mesomyzostoma spp. are highly modified, typically
vermiform and 2 - 4 mm long.
Habitat
Most species are external commensals on crinoids living within proboscis reach of host food
grooves. Half a dozen Myzostoma spp. are ectocommensal on ophiuroids (Gryier 2000),
and may belong in a different family. Myzostoma and Hypomyzostoma spp. are free living.
Notopharyngoides platypus and Contramyzostoma spp. live in soft cysts on their crinoid hosts.
Notopharyngoides aruensis lives inside the mouth of its crinoid host. Mesomyzostoma spp. live
in the longitudinal canals or gonads of commatulid crinoids.
Sensory and feeding structures
Most of the following details are collected from Grygier (2000). Eyes and nuchal organs are
absent. Some but not all patches of external cilia are apparently sensory (Eekhaut & Jangoux
1993a). Sucker-like lateral organs, found near the lateral margins of all but Mesomyzostoma
spp., are mechano- and chemosensory (Eekhaut & Jangoux 1993b). The anterior of the body
is apparently reduced to a retractile, muscular proboscis through which the unciliated pharynx
extends (Eekhaut et al. 1995). Except in Mesomyzostoma, the proboscis retracts into a cavity or
sheath. The basal muscle bulb of the pharynx undergoes peristaltic contractions that carry food
from the mouth to the stomach (Eekhaut et al. 1995). The stomach opens into paired, branching
caeca and is followed by a thin and relatively short intestine (Grygier 2000). The pharynx is
axial, and the anus is terminal in Myzostoma. In Hypomyzostoma proboscis and anus are both
ventral. In Notopharyngoides, the anus is posterioventral; the proboscis is ventral in one species,
but dorsal in the other two. C. bialatum has a gut that turns a right angle; the mouth is dorsal,
and the anus, terminal. The pharyngeal muscle bulb is much reduced in Mesomyzostoma spp.,
and a retractile proboscis is lacking; mouth and anus are both terminal.
Motility
Cyst dwellers and the two species of internal parasites (Mesomyzstoma spp.) are effectively
sessile. Other members of the family are discretely motile.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Illustrations
Grygier (2000) presents many informative drawings of internal and external morphology. His
Fig. 2.1 shows photographs of external morphologies. Eekhaut & Lanterbecq (2005) provide
striking photographs of whole specimens as do Summers & Rouse (2014) and Summers et al.
(2014). Color drawings from the Challenger collections are also remarkable (von Graf 1884).
Feeding
All Myzostomatidae except Mesomyzstoma spp. are kleptoparasites ingesting particles
collected by their hosts. Stable isotope analysis has recently confirmed the lack of any
significant difference in 15N enrichment of Myzostoma fissum and its crinoid host, supporting
kleptoparasitism and similar diets in both (Caulier et al. 2014). Mesomyzstoma reichenspergi
lives in the longitudinal canals of its host; M. katoi feeds directly on host gonads (Grygier 2000).
The degree of selectivity among items from the ambulacral groove by the kleptoparasites is
not known, but the expense of intracellular digestion in terms of both regeneration of apical cell
parts (Eekhaut et al. 1995) and time spent digesting—plus the volumetric limits of intracellular
digestion—would argue for high selectivity, for example for microalgae containing chloroplasts
and their grana that could repay such costs. Crinoids are passive suspension feeders that
were thought to be relatively nonselective, but experiments have shown that they, too, prefer
microalgae to other kinds of particles (Kitizawa & Oji 2010).
Guild membership
Most species are sessile (cyst formers) or discretely motile and use an unarmed, protrusible
proboscis to suck in particles from ambulacral grooves of their hosts. Mesomyzstoma spp. are
internal parasites.
Research questions and opportunities
• Effects on host energy budgets are unknown.
• Kleptoparasitic Myzostomatidae present an opportunity to run experiments on selective
ingestion by presenting visually recognizable particles to the host and video recording food
passage upstream, at the location of the myzostome, and downstream to test for selective
ingestion. This design is reminiscent of classic experiments on food choice by birds from
items passing on a conveyor belt (e.g., Krebs et al. 1977).
References
Caulier G, Lepoint G, Van Nedervelde F, Eeckhaut I. 2014. The diet of the Harlequin crab
Lissocarcinus orbicularis, an obligate symbiont of sea cucumbers (holothuroids) belonging
to the genera Thelenota, Bohadschia and Holothuria. Symbiosis 62:91–9
Eeckhaut I, Dochy B, Jangoux M. 1995. Functional morphology of the introvert and digestive
system of Myzostoma cirriferum (Myzostomida). Acta Zool. 76:307–15
Eeckhaut I, Jangoux M. 1993a. Life cycle and mode of infestation of Myzostoma cirriferum
(Annelida): a symbiotic myzostomid of the comatulid crinoid Antedon bifida
(Echinodermata). Dis. Aquat. Organ. 15:207–17
Eeckhaut I, Jangoux M. 1993b. Integument and epidermal sensory structures of Myzostoma
cirriferum (Myzostomida). Zoomorphology 113:33–45
Eeckhaut I, Lanterbecq D. 2005. Myzostomida: a review of the phylogeny and ultrastructure.
Hydrobiologia 535/536:253–75
Grygier MJ. 2000. Class Myzostomida. See Beesley et al. 2000, pp. 297–329
Kitazawa K, Oji T. 2010. Particle selection by the sea lily Metacrinus rotundus Carpenter 1884
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
(Echinodermata, Crinoidea). J. Exp. Mar. Biol. Ecol. 395:80–4
Krebs JR, Erichsen JT, Webber MI, Charnov EL. 1977. Optimal prey selection in the great tit
(Parus major). Anim, Behav. 25:30–8
Summers MM, Al-Hakim I, Rouse GW. 2014. Turbo-taxonomy: 21 new species of Myzostomida
(Annelida). Zootaxa 3873:301–44
Summers MM, Rouse GW. 2014. Phylogeny of Myzostomida (Annelida) and their relationships
with echinoderm hosts. BMC Evol. Biol. 14:170, 15 pp.
von Graff L. 1884. Report on the Myzostomida collected during the voyage of HMS Challenger
during the years 1873-1876. Rept. Scient. Results Voyage Challenger, Zool. 10:1-216
Nephtyidae, Phyllodocida
Diversity and systematics
Each of the two major genera, Nephtys and Aglaophamus, contains about 50 known species. The
other three genera, Bipalponephtys, Inermonephtys and Micronephtys, contain a handful each.
The position of Nephtyidae within Phyllodocida is uncertain, but they may be closely related to
Pilargidae (Zrzavý et al. 2009; Struck et al. 2007). Adult lengths range from < 1 to > 40 cm.
Habitat
Nephtyids are burrowers in a range of soft sediments, from soft muds to beach sands and can be
found at any water depth. They often burrow just beneath the sediment-water interface.
Sensory and feeding structures
Nephtyids have a pair of short antennae and a pair of short palps. Eyes are sometimes present.
Nuchal organs are protrusions at the base of the prostomium (Pleijel 2001).
Nephtyids carry a large, axial, eversible pharynx tipped (when everted, except in
Inermonephtys) with papillae and armed with a lateral pair of opposed, unhinged teeth,
usually roughly conical in shape, with their tips pointing toward the body axis and slightly
backward. The conical teeth appear more useful for crushing than grasping and are located
along the pharyngeal wall rather than at the tip (Dinley et al. 2009). Two known exceptions
are Inermonephtys inermis and Nephtys glabra. The two teeth are more spindle shaped in the
former, and the latter carries an additional pair of plates bearing teeth (Ravara et al. 2010).
Nephtyidae would appear to be handicapped as deposit feeders by limited gut volume. The
four nephtyids measured by Penry & Jumars (1990) ranged from 9 to 16% of total body volume
occupied by the gut, whereas deposit-feeding polychaetes more typically have ~ 30% of their
volume as gut lumen (Jumars 1993).
Motility
Nephtyids are muscular burrowers and frequent swimmers. In muddy sediments in Bodega
Harbor, Nephtys caecoides is a shallow burrower, mostly within the top 5 cm of sediment, and
the burrow has two or more openings (Ronan 1977). Swimming behavior is similar to that
of Nereis, with sinusoidal waves passing forward and the parapodia used to apply a power
stroke (Clark & Clark 1960). Nephtys uses its pharynx to extend the burrow, like Nereis, but
forward movement into the burrow is always achieved by undulation, and Clark & Clark (1960)
suggested that Nephtys is unable to use the parapodia to “walk” forward, as we have observed
slowly moving nereidids to do (KM Dorgan, pers. obs.).
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Nephtyidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Illustrations
Mackie (2000; Fig 2E) and Dinley et al. (2009) illustrate the teeth. Pleijel (2001) illustrates
nuchal organs. Clark & Clark (1960) show numerous photographs and drawings of swimming
and burrowing Nephtys as well as their musculature. Ronan (1977; Fig. 4) shows an
x-radiograph of the shallow burrows of Nephtys caecoides.
Feeding
Most nephtyids appear to be predators most of the time (F&J). Incidental ingestion of sand
is also noted in some species (e.g., Gaston 1987). The strongest departure documented from
carnivory is for northeast US. Nephtys incisa that appear to deposit feed (Sanders 1956, 1960).
Tenore et al. (1977) experimentally documented the ability of N. incisa to assimilate organic
matter from seagrass detritus, with assimilation rates dependent on aging of the detritus and
accelerated by the presence of meiofauna that likely accelerated detrital breakdown and were
themselves subject to digestion by N. incisa. N. incisa would appear to have a hard time
subsisting on detritus, however, as its assimilation rate (weight of detritus per dry weight of
worm per time) is an order of magnitude lower than that measured for Capitella (Tenore et al.
1977). Another indication of N. incisa’s poor ability to extract organic matter from sediments is
its much slower accumulation of hydrophobic pollutants compared to more specialized deposit
feeders (Means & McElroy 1997).
Redmond & Scott (1990) in a series of laboratory experiments documented predation by N.
incisa from Long Island Sound on two amphipod species, Ampelisca abdita and Microdeutopus
gryllotalpa. The first of these experiments was not designed to examine effects of N. incisa,
which apparently caused more mortality than did the toxic sediments that constituted the
intended experimental treatment. They noted that all the N. incisa they dissected contained
sediments in addition to animal remains and argued to classify this species in the northeast U.S.
as an omnivore. N. incisa contrasts with the nereidid Alitta virens in a stable isotope analysis
with distance from a sewage outfall in the Firth of Forth. The latter showed a switch to direct
consumption of sewage-derived organic matter in the immediate vicinity of the outfall, whereas
N. incisa did not (Waldron et al. 2001). This divergence argues fairly strongly against deposit
feeding by N. incisa.
Noyes (1980) studied what is now known as Bipalponephtys neotena in shallow water in
Maine and southeastern Canada. Although his paper is often cited as further evidence of deposit
feeding in nephtyids, his observations on diet were quite limited. An unspecified number of
starved individuals failed to feed when offered fresh mussel tissue, dried liver powder, clumps
of diatoms or filamentous algae. No small prey capable of producing mechanical stimuli were
presented. Fecal pellets collected from an unspecified number of field-collected individuals
(p. 108), “contained a mixture of materials including several species of benthic diatoms, empty
copepod exoskeletons, unidentified organic material, and fine sand grains.” Juveniles were
reported to contain “a brown organic material.” These observations do not appear sufficient
to support the conclusion that (p. 113), “it is a nonselective omnivore and feeds by ingesting
sediment.” We suspect that “brown organic material” in predators may often be confused with
detritus but may more often be animal remains emulsified during digestion (Voparil et al. 2008).
Most other reports support carnivory on a range of prey items. Ockelmann & Muus (1978)
studied the population dynamics of a clam, Mysella bidentata, in shallow water in the Øresund.
They observed Nephtys spp. to ingest M. bidentata and other small mollusks, crushing them
between the teeth, as well as Foraminifera and small polychaetes.
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Nephtyidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Schubert & Reise (1986) studied Nephtys hombergii on tidal flats of Sylt by examining gut
contents of 218 individuals and conducting both laboratory prey choice experiments and field
enclosure experiments. All three approaches pointed to Scoloplos armiger and Heteromastus
filiformis as preferred prey, with nematodes also being important for smaller predator size
classes. In choice experiments, N. hombergii often captured only posterior portions of S.
armiger. These dietary preferences extend all the way to the westernmost Wadden Sea, where
long-term sampling reveals that H. filiformis and S. armiger have lower areal biomass in years
when N. hombergii is abundant (Beukema 1987). Olive et al. (1997) assumed that N. hombergii
in the Tyne estuary preyed on the dominant local infaunal species Spio martinensis and S.
armiger and found that reproductive failure of N. hombergii was consistent with low prey
abundance in winter 1993-1994.
N. hombergii farther south in the Lynher estuary in England, however, appeared to focus
on other prey. In a study of macrofaunal production, Warwick & Price (1975) dissected an
unspecified number of N. hombergii and found the majority of guts to be empty, but occasionally
found nematodes, ostracods and Nephtys chaetae. Sediments were never ingested. A simulation
model of this system (Warwick et al. 1979) indicated insufficient production of meiofauna
and macrofauna to support the observed areal biomass of N. hombergii, prompting the authors
to posit either inclusion of diatoms in the diet or a dependence on import of demersal or
planktonic migrants. They discounted the latter possibility for lack of evidence among the gut
contents. Even farther south in the Rance basin, Desroy et al. (1998) ran two-species enclosure
experiments in both the laboratory and the field and observed statistically significant emigration
and mortality of Hediste diversicolor recruits attributable to N. hombergii. Limited nitrogen
stable isotope data for N. hombergii also support carnivory (Table A2). We suspect that
Warwick et al.’s (1979) population of N. hombergii was not in steady state.
Table A2. Studies finding δ15N‰ indicative of carnivory in Nephtyidae
Author
Location
Water depth (m)
Taxon
Hobson et al. 1995
Northeast Water Polynya,
Baffin Bay
279
Nephtys sp.
Tucker et al. 1999
Massachusetts Bay
33
Nephtys sp.
Le Loc’h & Hily 2005,
Le Loc’h et al. 2008
Grande Vasière, Bay of
Biscay
80 - 130
Martinetto et al. 2006
Quashnet River, Massachusetts
unspecified
(shallow)
Tamelander et al. 2006
Barents Sea
Carlier et al. 2007
Bay of Banyuls-sur-Mer
Dannheim et al. 2007
Nephtys caeca
Aglaophamus circinata
213 - 227
Nephtys sp.
30 - 90
Nephtys sp.
German Bight
unspecified
Nephtys sp.
Levin & Mendoza 2007 Kodiak margin
4327 - 4480
Nephtyidae
Bodin et al. 2008
Seine & Bertheaume Bays,
Brittany
5 - 10
Nilsen et al. 2008
Sørfjord, northern Norway
unspecified
Schaal et al. 2008
Arcachon Bay
intertidal
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
Nephtys hombergii
Nephtys sp.
Nephtys hombergii
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
Author
07 November 2014
Location
Water depth (m)
Baeta et al. 2009a, b
Mondego estuary, Portugal
unspecified
(shallow)
Carlier et al. 2009
Salses-Leucate Lagoon,
Languedoc Roussillon
Guerin 2009
Poole Bay, south England
Sampaio et al. 2010
offshore of Lisbon
Fanelli et al. 2011
Catalan slope
651 - 1105
Grippo et al. 2011
Gulf of Mexico
5 - 15
Nepthtys spp.
Gillies 2012
vicinity of Windmill Islands,
Prydz Bay, Antarctica
0 - 50
Nephtyidae
Kędra et al. 2012
Kongsfjorden, Spitzbergen
15
Gillies et al. 2013
coast of Vestfold Hills,
Prydz Bay, Antarctica
Dannheim et al. 2014
German Bight
Fedosov et al. 2014
southern coast of Vietnam
Sokołowski et al. 2014
Hornsund, Spitsbergen
intertidal
Taxon
Nephtys cirrosa
Nephtys kersivalensis
unspecified (divNephtys spp.
er collected)
30 - 90
Nephtys sp.
Nephtys hystricis, N.
hombergii, N. incisa, N.
paradoxa, N. sp.
Aglaophamus malmgreni,
Nephtys ciliata
0 - 30
Nephtyidae
~ 30
Nephtys spp.
6 - 18
Nephtyidae
100
Aglaophamus malmgreni
Gaston (1987) dissected 50 continental-shelf specimens of Aglaophamus circinata, 27 of
Nephtys bucera, 4 of N. incisa, 5 of N. picta and 40 juvenile nephtyids not identified to species.
Most individuals were empty (44, 24, 4, 5, and 36, respectively). Of the 6 with identifiable
gut contents in A. circinata, 2 contained coarse sand, 2 contained forams, and 2 contained
polychaetes. Among the N. bucera, 1 contained coarse sand and peracarids, and 2 contained
polychaete chaetae. Among the juveniles, 4 contained “undigested food” that in 3 specimens
included polychaete chaetae.
McDermott (1987) studied N. bucera in the surf zone of an exposed, sandy beach in New
Jersey. Of 111 worms, 90 had identifiable gut contents. Their dominant prey were juvenile surf
clams, Donax variabilis, with the spionid Scolelepis squamata as the next most important dietary
item. Sand was rarely found in the guts.
Grippo et al. (2011) studied two proximate sites in the Gulf of Mexico. Aglaophamus verrilli
was clearly a top predator at the off-shoal site but lower in the δ15N-resolved food web at the
Ship Shoal site. Nephtyidae showed very high variance in δ15N on the Indian continental slope
(Hunter et al. 2012), suggesting strong inter-individual or interspecific variation in trophic level.
Guild membership
Most nephtyids are actively burrowing carnivores that use muscular and rapidly everting
pharynges with unhinged teeth to capture and crush prey. F&J listed them as motile. We suspect
that there is a range of behaviors among species from actively hunting to sit-and-wait predation
so that some species may be discretely motile.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Research questions and opportunities
• Simultaneous stable isotopic and gut-contents studies of populations that appear to deposit
feed would help to resolve whether they obtain significant nutrition from ingesting detritus.
• Interspecific differences in motility and their consequences for prey selection remain to be
quantified.
• Does tooth shape correlate with diet?
References
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Mondego estuary food web: Seasonal variation in producers and consumers. Mar. Environ.
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Baeta A, Valiela I, Rossi F, Pinto R, Richard P, et al. 2009b. Eutrophication and trophic structure
in response to the presence of the eelgrass Zostera noltii. Mar. Biol. 156:2107–20
Beukema JJ. 1987. Influence of the predatory polychaete Nephtys hombergii on the abundance of
other polychaetes. Mar. Ecol. Prog. Ser. 40:95–101
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Carlier A, Riera P, Amouroux J-M, Bodiou J-Y, Grémare A. 2007. Benthic trophic network in the
Bay of Banyuls-sur-Mer (northwest Mediterranean, France): An assessment based on stable
carbon and nitrogen isotopes analysis. Estuar. Coast. Shelf Sci. 72:1–15
Carlier A, Riera P, Amouroux JM, Bodiou JY, Desmalades M, Grémare A. 2009. Spatial
heterogeneity in the food web of a heavily modified Mediterranean coastal lagoon: stable
isotope evidence. Aquat. Biol. 5:167–79
Clark RB, Clark ME. 1960. The ligamentary system and the segmental musculature of Nephtys.
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Dannheim J, Brey T, Schröder A, Mintenbeck K, Knust R, et al. 2014. Trophic look at softbottom communities—Short-term effects of trawling cessation on benthos. J. Sea Res.
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Dannheim J, Struck U, Brey T. 2007. Does sample bulk freezing affect stable isotope ratios of
infaunal macrozoobenthos? J. Exp. Mar. Biol. Ecol. 351:37–41
Desroy N, Retière C, Thiébaut E. 1998. Infaunal predation regulates benthic recruitment: an
experimental study of the influence of the predator Nephtys hombergii (Savigny) on recruits
of Nereis diversicolor (OF Müller). J. Exp. Mar. Biol. Ecol. 228:257–72
Dinley J, Hawkins L, Paterson G, Ball AD., Sinclair I, et al. 2010. Micro-computed X-ray
tomography: a new non-destructive method of assessing sectional, fly-through and 3D
imaging of a soft-bodied marine worm. J. Microsc. 238:123–33
Fedosov AE, Tiunov AV, Kiyashko SI, Kantor UI. 2014. Trophic diversification in the evolution
of predatory marine gastropods of the family Terebridae as inferred from stable isotope data.
Mar. Ecol. Prog. Ser. 497:143–56
Gaston GR. 1987. Benthic Polychaeta of the Middle Atlantic Bight: feeding and distribution.
Mar. Ecol. Prog. Ser. 36:251–62
Gillies CL. 2012. Trophic ecology of the nearshore zone in east Antarctica: a stable isotope
approach. PhD thesis. Southern Cross Univ., Lismore, NSW, Australia
Gillies CL, Stark JS, Johnstone GJ, Smith S. 2013. Establishing a food web model for coastal
Antarctic benthic communities: a case study from the Vestfold Hills. Mar. Ecol. Prog. Ser.
478:27–41
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
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07 November 2014
Nereididae, Phyllodocida
Diversity and systematics
Nereidids are the most widely known polychaetes and are remarkably diverse, with > 500 species
described in > 40 genera. Most are medium to large worms, from a few centimeters to about a
meter long, but adults in some species are only a few millimeters long. Recently, the subfamily
Namanereidinae (nereidids lacking paragnaths as adults) has been revised (Glasby 1999), and
phylogeny of nereidids carrying paragnaths has been analyzed (Bakken & Wilson 2005). More
recently still, karyotyping has aided discrimination of some nereidids (Leitão et al. 2010), and
the full mitochondrial genome of Perinereis nuntia has been sequenced (Won et al. 2013).
Morphology-based cladistics within the family support only some prior subfamily designations
(Santos et al. 2005). Comprehensive molecular genetic analysis has not been carried out.
Habitat
Nereidids are most abundant and common in shallow-water sediments, but they are found on and
in nearly all kinds of substrata at all ocean depths. A few range into fresh waters, and some are
semi-terrestrial, occupying such habitats as rain pools in branching vegetation.
Sensory and feeding structures
Prostomial shape is highly variable. A pair of dorsal antennae is present in most species. A
median antenna is rarely present. Two ventral, biarticulated, usually large palps are present.
Eyes if present are in two pairs. Nuchal organs are dorsolateral pits at the posterior of the
prostomium. Chemoreception modulates feeding on the sediment surface, and nuchal organs
apparently coordinate this response (reviewed by Lindsay 2009). The peristomium is indistinct
and appears to be limited to lips (Pleijel 2001).
Nereidids carry a pair of lateral jaws within an eversible pharynx. The structures can be used
in burrowing (Dorgan et al. 2005) and defense behavior (Uyeno & Kier 2014) as well as feeding.
The jaws are usually roughly falcate, toothed (serrated) and complexly articulated. In some
groundwater species, subterminal teeth are replaced by a dish-shaped extension or joined with a
webbing that spans the space between teeth and may be used as a scoop in microphagous feeding
(Glasby et al. 2014). Nereidid pharynges also bear papillae and paragnaths (unarticulated teeth)
in varied arrangements that are variously hypothesized to be used in feeding and burrowing.
None of these hypotheses for paragnath function appears to be well tested (Bakken et al. 2009).
Recently Uyeno & Kier (2007) carried out a detailed analysis of muscle structure in the
eversible pharynx of Alitta virens. The pair of falcate jaws of A. virens is embedded in either
side of the muscular, dorsoventrally flattened-spheroidal pharyngeal bulb. They bear an opening
at the base, and the pharyngeal bulb musculature attaches to both the inner and outer surface
area of each tooth. The teeth are composed of glycine- and histidine-rich protein fibers and
are mineralized by an inorganic zinc-chloride compound (Birkedal et al. 2003). The bulb is
composed of small fiber bundles in varied orientations interdigitating with each other and
surrounded by a connective tissue sheath. Muscle fibers originate from the opening at the
base of the jaws or on the outer sides and insert in the connective tissue sheath, the surface of
the foregut, or in the basal bulb musculature. Connective tissue surrounding the musculature
forms a crossed-fiber arrangement with an angle of 22° from the longitudinal axis of the bulb,
reinforcing the pharyngeal bulb against radial expansion. This extracellular matrix surrounding
the pharyngeal bulb appears to act as a muscular hydrostat providing support for the muscles that
manipulate the jaws (Uyeno & Kier 2014).
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Motility
Nereidids are active polychaetes whose burrowing, crawling and swimming behaviors have
been relatively well studied. Gray (1939) described two gaits used by Hediste diversicolor
when crawling; a parapodial walking movement and undulation effected by alternate contraction
of longitudinal muscles. Ablation of chaetae resulted in slower crawling velocities and
more backward slipping both on sands and muds, but swimming worms showed no change
(Hesselberg & Vincent 2006). H. diversicolor swims with an anteriorly traveling, undulatory
wave in which parapodia generate thrust. Gray (1939) described the undulation as similar to
that of crawling worms but with higher amplitude and much lower efficiency, as the velocity of
undulatory waves greatly exceeds the forward velocity of the worm. Alitta virens extends its
burrow in mud by fracture, everting the pharynx to apply to burrow walls dorsoventral forces
that are amplified at the tip of the burrow (Dorgan et al. 2005). Worms change burrowing
behavior between sediments of different mechanical properties, using pharyngeal eversion to
apply greater stress in sediment analogs that have high fracture toughness, and using side-toside head movements to extend the burrow laterally and reduce the compressive elastic restoring
force in stiffer sediments (Dorgan et al. 2008). Forward movement in burrows can be achieved
with either the parapodial walking gait or undulation observed by Gray (1939) for crawling
worms, with undulation more commonly used at higher speeds (Dorgan, unpublished data).
Variability in the degree of motility in sediments occurs, including active burrowing and
burrow construction, but with a primarily discretely motile lifestyle. Hediste diversicolor is
necessarily sessile while suspension feeding, and periodic emergence from a burrow is apparent
from both observations and crawling traces extending from burrow openings. Territoriality
documented in some species reinforces the classification of nereidids as discretely motile
(Jumars 1978, Miron et al. 1991).
Illustrations
Bakken et al. (2009) show photographs of a diversity of paragnaths. Scaps (2002) shows
drawings of various feeding modes in H. diversicolor. Photographs of Alitta virens burrowing
in gelatin are shown by Dorgan et al. (2005, 2007). Uyeno & Kier (2014) show drawings of the
assorted muscle fibers in A. virens with their positions and orientations in the pharyngeal bulb,
including the foregut and the jaws.
Feeding
Changes in understanding of nereidid feeding have been evolutionary since F&J and generally
add further support for labeling nereidids as functionally omnivorous by showing dietary and
behavioral plasticity. Intraspecific aggression and cannibalism are frequent in nereidids (e.g.,
Costa et al. 2006, Tosuji & Sato 2006) and apparently can lead to even spacing at bathyal depths
as well as in shallow water (e.g., Jumars 1978, Reise 1979a). Territoriality can be interspecific as
well (Caron et al. 1996a, b) and need not result in even spacing (Caron et al. 2004).
Hediste diversicolor continues as the poster child for omnivory and multiple feeding
behaviors among nereidids. There is some regional genetic differentiation in this nominal
species (Virgilio et al. 2009). Among all nereidids, suspension feeding is best documented and
analyzed in H. diversicolor. It usually constructs a Y-shaped burrow with two openings at the
sediment-water interface. When suspension feeding it attaches a mucous bag to the burrow wall
and pumps water through the bag and the top two branches of the Y. Its pumping and filtering
capacities are well quantified (Riisgård & Larsen 2005). The extent to which H. diversicolor
depends on suspension feeding varies with time, location and worm size (e.g., Fidalgo e Costa
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et al. 2006). Switching to suspension feeding is triggered by high phytoplankton concentrations
(Riisgård & Kamermans 2001). Pumping activity, whether in feeding or respiration, peaks
just after dusk (Wenzhöfer & Glud 2004). H. diversicolor has at least three other feeding
modes. The most obvious is raptorial grasping of prey, carrion or macroalgae with its jaws;
ingestion occurs with or without tearing into smaller fragments. A second is laying of mucus
trap lines radiating from the burrow entrance that are then rolled up into the burrow opening
and ingested (Scaps 2002), and a third is deposit feeding, often in the presence of abundant
microphytobenthos (Esselink & Zwarts 1989, Lucas & Bertru 1997, Lucas et al. 2003). Deposit
feeding is an apparent route for uptake of arsenic compounds by H. diversicolor from polluted
sediments (Gaion et al. 2014). In a multi-estuary study by Fidalgo e Costa et al. (2006), mucus
was the the most frequent gut content, followed by sand, vegetable detritus, polychaetes, and
crustaceans. Reise’s (1979b) field experiments in the intertidal zone of Sylt suggest that at his
site nematodes may have provided ¼ of H. diversicolor’s daily intake of energy.
H. diversicolor and other nereidids have been suggested to “garden” algae and bacteria.
Nereis vexillosa and Platynereis bicanaliculata in Mitchell Bay, San Juan Island, Washington,
attach drift algal fragments to external surfaces of their tubes, affecting both redox conditions
and resource availability (Woodin 1977). Juveniles of both H. diversicolor and Alitta virens from
the Bay of Mont-Saint-Michel and the St. Lawrence estuary gather fragments of macrophytes
of many species and conditions of decay and store them in their irrigated burrows (Olivier et
al. 1995). Bacteriolytic activity has been documented in gut fluids of H. diversicolor (Lucas &
Bertru 1997). The presumption is that this collection of materials provides energetic and other
fitness benefits, but net benefit from gardening in a comprehensive energy budget has not yet
been documented. Engelsen & Pihl (2008) found that H. diversicolor prevented initial growth of
Ulva spp. propagules, reduced algal growth and even reduced full-grown algal mats, so effects on
grazed species can be substantial.
Tsuchiya & Kurihara (1979) found that decomposed macrophytes and microalgae were
consumed much faster by Neanthes japonica than were fresh materials and observed hyperbolic
saturation kinetics on most foods. One question raised about apparently herbivorous nereidids
living in seagrass beds is whether they ingest significant quantities of seagrass or specialize on
epiphytes and other fouling organisms. Gambi et al. (2000) studied epiphytes in an eelgrass bed
off the Island of Ischia and examined fecal pellets from field-collected Platynereis dumerilli as
well as worms offered various combinations of algae and seagrasses in the laboratory. They
also reviewed reports of herbivory in this species since F&J. P. dumerilli clearly prefers erect,
filamentous algae and macroalgae to seagrasses, likely because they are more easily torn with
jaws and more efficiently digested (Gambi et al. 2000). The species shows some sensitivity to
silver nanoparticles (García et al. 2014).
Although H. diversicolor can achieve net growth on an algal diet, it grows significantly faster
on higher-protein diets (Nesto et al. 2012). Nielsen et al. (1995) obtained specific growth rates
in H. diversicolor of 3% d-1 when suspension feeding on phytoplankton versus 7% d-1 when
raptorially feeding on shrimp. Fidalgo e Costa (2000) found high survival and high specific
growth rates (5 - 7% d-1) of H. diversicolor on a range of animal and plant foods with high
protein and moderate to high lipid contents. Nielsen et al. (1995) suggested that the specialized
suspension-feeding niche of H. diversicolor helped explain its sympatry with the otherwise
very similar Alitta virens. To date suspension feeding in other nereidid species has not been
documented, but Dorsey (1981) speculated on the basis of gut contents and mucus-secreting
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glands that Australonereis ehlersi may suspension feed. Whether feeding as a herbivore,
coprophage or deposit feeder, H. diversicolor shows high assimilation efficiency for the lipid
components of its diet (Bradshaw et al. 1989, 1990; Woulds et al. 2014).
At least part of the dietary flexibility of Alitta virens is grounded in digestive plasticity. Bock
& Mayer (1999) acclimated A. virens to diets of either mussel tissue alone, various mixtures of
mussel tissue and sediments or kelp tissue alone for three weeks. Presence of sediment in the
diet induced surfactant secretion and micelle formation, presumably aiding in the extraction
of hydrophobic organic compounds (Bock & Mayer 1999, Voparil et al. 2008). A diet rich in
mussel tissue gave A. virens a lipase/protease activity ratio more characteristic of a carnivore
than of a detritivore or deposit feeder (Bock & Mayer 1999) and induced it to form emulsions
rather than micelles containing lipid components of digesta (Voparil et al. 2008).
When fed sediments with hydrophobic contaminants, deposit-feeding Alitta succinea
exhibited rapid and efficient desorption of contaminants (~ 2/3 of bioavailable hydrophobic
contaminants within the first minute; Ahrens et al. 2001). Compared with the deposit feeder
Pectinaria gouldii (Pectinariidae), gut fluid surfactancy and both desorption and absorption
efficiencies were higher in A. succinea (Ahrens et al. 2001). Dietary breadth of the family
as a whole as well as of individual species also goes along with phenotypic and genotypic
osmotic adaptability that provides access to freshwater and terrestrial food resources such as in
Lycastopsis catarractarum living in South Pacific island treeholes and leaf axils where rainwater
collects (Glasby et al. 1990).
As judged from gut contents, selective deposit feeding on sand often is combined
with macrophagous carnivory, scavenging and herbivory (e.g., Dorsey 1981, Simplisetia
erythraeensis, avoiding ingestion of silt and clay but not sand). Even populations of the
same species may differ in this regard, however. Dauer (1980) observed omnivory (including
cannibalism, predation and herbivory), along with ingestion of sand grains (100 - 250 µm diam),
in Alitta succinea from Tampa Bay. In four mid-Atlantic U.S. locations, however, Pardo &
Dauer (2003) found A. succinea to favor particles near 20 µm in diameter, including numerous
diatoms, and to show no signs of macrophagous carnivory or carrion feeding. Two sites were on
intertidal mudflats, one was on an oyster reef, and the other was on a mussel bed. Magalhães &
Barros (2011) dissected 91 whole Laeonereis culveri from estuaries that open into the Baiá de
Todos os Santos, northeastern Brazil; all contained detritus and fine sand.
These results collectively suggest that incidental ingestion of sand (that may contain
abundant diatoms) is digestively compatible with macrophagy, i.e., that permeability and
chemical lability of the resulting (non-sand components of the) gut contents allow reasonably
efficient assimilation within a reasonably short gut residence time. Swallowing very fine grains
and much richer material such as animal flesh together may make it very difficult to optimize
the mix of digestive reagents, transport processes of digestive products to absorptive sites and
gut residence times. Neanthes japonica individuals that select large sediment grains maintain
a high feeding rate and a short gut residence time (Zhinan 1998). Perinereis aibuhitensis
shows extreme variation in feeding rates with food quality and quantity (Tsuchiya & Kurihara
1979, Zhang & Hu 2008), implying great digestive flexibility. Levin et al. (1999) found
Ceratocephale sp. on the continental slope of North Carolina quick to exploit experimentally
deposited, stable isotope-labeled, fresh diatom detritus. Alitta virens fed halibut wastes from
a recirculating aquaculture system grew well (Brown et al. 2011), making it a good candidate
for use in land-based, integrated aquaculture systems. Nereidids have become popular in
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multitrophic aquaculture because they feed on organic wastes caught in sand filters. Modest
dietary supplements can produce worms with lipid contents that make them attractive as food for
shrimp and fish broodstocks (e.g., Palmer et al. 2014, Perinereis helleri). Waldron et al. (2001)
also provided stable isotopic evidence that A. virens directly consumed sewage-derived organic
matter in close proximity to a sewage discharge in the Firth of Forth.
Deposit-feeding nereidids are generally regarded as feeding from the sediment surface, but
there is danger in generalizing only the behaviors that are easily seen. There is no anatomical
reason why nereidids cannot feed below the sediment-water interface, and experimental
results with subsurface burial of labeled organic detritus and with and without H. diversicolor
(Kristensen & Mikkelsen 2003) document that they do. It is likely that particles are stripped
from the burrow walls by paragnaths on the maxillary ring and are directed into the mouth when
the pharynx is retracted. The rod-like paragnaths described by Bakken et al. (2009, their Fig. 3)
would appear well adapted to this function.
Freshwater Namanereis tiriteae has been observed to feed on diatoms, small arthropods and
oligochaetes but also to ingest silt (Gray et al. 2009). We doubt that an animal this small (≤
2.1 mm long) can grow by deposit feeding. Stable isotopic data suggest a mixed diet including
primary producers and animals (Gray et al. 2009). We suspect that scoop-shaped jaws in many
species of groundwater nereidids (Glasby et al. 2014) enable them to sample thin layers of
sediment where high-value foods such as diatoms or other microbes are concentrated.
Stable isotopic data also support dietary diversity among nereidid species and flexibility
within nereidid species and individuals. Not unexpectedly Hediste diversicolor can show
substantial between-habitat differences in 15N-estimated trophic level (Rossi et al. 2014).
Carmichael et al. (2004) saw δ15N in Alitta succinea consistent with feeding close to the bottom
of the food web. Grippo et al. (2011) saw substantial seasonal and between-site variation
in apparent trophic level of Nereis micromma in shallow Louisiana waters based on its δ15N
signature. Neanthes spp. showed a mixture of angiosperm and edaphic algal food sources in a
study of the Graveline Bay Marsh, Mississippi, that used a combination of N, C and S isotopes
(Sullivan & Moncrief 1999). Changes in apparent food source along the Nanakita River estuary,
Japan, suggested that Neanthes japonica used different sources of C and N in the upper and
lower estuary and that its upper estuary values of δ13C and δ15N are best explained by feeding
on microbially reprocessed terrestrial C3 plant material (Kikuchi & Wada 1996). Simplisetia
aequisetis in the shallow Hopkins River estuary in Victoria, Australia, showed δ13C and δ15N
values consistent with surface deposit feeding (Lautenschlager 2011). Perinereis nuntia vallata
at a saltmarsh site and a sand bank in the Kariega River estuary on the southeast coast of South
Africa showed significant between-site differences in isotopic signature but individuals were
near the tops of the food webs sampled in both places (Richoux & Froneman 2007). Fatty acid
analyses confirmed a high diversity of food resources being utilized by this species (Richoux
& Froneman 2008). Nereimyra aphroditoides in shallow coastal lagoons of the Beaufort Sea
had 15N signatures intermediate between other carnivores and deposit feeders (Dunton et al.
2012). Abreu et al. (2006) compared a sewage-impacted site and a more pristine site in the
Patos Lagoon estuary, Brazil. Plant sources of detritus were more 15N-enriched at the latter site.
Laeonereis acuta had a ∆15N (‰) consistent with detritivory at both sites. Dietary flexibility
and 13C contents led Kanaya et al. (2008) to posit that Hediste atoka and H. diadroma might be
using a cellulase to access terrrestrial plant detritus. In the Porcupine Abyssal Plain at 4800 m
Nicon sp. showed the highest δ15N of any polychaete species, also exceeding values in all the
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fishes sampled (Iken et al. 2005). This result is difficult to explain, but one conjecture is that this
species is carnivorous on subsurface deposit feeders. A Nereis sp. collected from a vent field in
the Costa Rican margin was highly depleted in 13C, indicating feeding in a food web based on
aerobic methanotrophs (Levin et al. 2012), but its δ15N‰ suggests feeding about two trophic
levels above those aerobic methanotrophs.
Temperature, food availability (Deschênes et al. 2005) and photoperiod (Last 2003) can
influence feeding behavior of nereidids. At high temperatures and with abundant food, relative
frequencies of food capture and storage by Alitta virens increased (Deschênes et al. 2005). A.
virens appears to be strongly nocturnal (Last 2003), while H. diversicolor forages out from its
burrow during the day (Lambert et al. 1992) in contrast to its crepuscular pumping activity where
phytoplankton are abundant (Wenzhöfer & Glud 2004). These foraging differences have been
attributed to avoidance of predators with different foraging schedules, as well as cycles in prey
activity (Last 2003).
Guild membership
Nereidids are motile or (more often) discretely motile and are clearly omnivorous, although
digestive physiology suggests that specialization is more likely either among populations or
temporally than our litany of observed prey items suggests. Several species can switch between
surface deposit feeding and raptorial macrophagy. Simultaneous carnivory and deposit feeding
on mud seem to be digestively incompatible. Active suspension feeding is included in the mix
for Hediste diversicolor, and subsurface deposit feeding cannot be excluded a priori.
Research questions and opportunities
• The extent of sequential vs. simultaneous omnivory would be interesting to explore in a
natural environment.
• Functional morphology of diverse paragnaths is largely unknown, yet they are important
taxonomic characters.
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Nerillidae, incertae sedis
Diversity and systematics
With about 50 species in about 18 genera, Nerillidae are the most diverse of the strictly
meiofaunal families (Worsaae et al. 2005). Molecular and morphological data are somewhat
inconclusive but suggest affinity with Eunicida (Worsaae et al. 2005). Adult lengths range from
about 0.3 to 2 mm (Worsaae et al. 2005).
Habitat
Most species are interstitial in shallow water, but habitats range from fresh waters to deepsea hydrothermal vent fields (Worsaae & Rouse 2009). Anchiline caves house many species
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Jumars, Dorgan & Lindsay
07 November 2014
(Worsaae et al. 2009). Whereas many meiofaunal polychaetes are found only interstitially in
sandy sediments, nerillids occur in gravel containing enough mud to clog pore spaces, and some
species (e.g., Paranerilla limicola) are obligate mud dwellers (Worsae et al. 2005). Meganerilla
bactericola inhabits sulfur-oxidizing microbial mats in the Santa Barbara Basin (Summers et
al. 2013). Troglochaetus beranecki is widespread in amphi-Atlantic, hyporheic fresh waters
(Morselli et al. 1995).
Sensory and feeding structures
The prostomium carries paired, ciliated, ventral palps, nuchal organs and up to three antennae.
Nuchal organs are dorsolateral, ciliated pits at the posterior of the prostomium. One or two
pairs of eyes may be present. The peristomium is apparently limited to lips. Palps are absent in
Afronerilla and Paranerilla (Pleijel 2001). Nerillids have a bulbous, eversible, ventral pharynx.
Tooth-like structures have been described in some nerillids; they are submicrometer features of
the epithelium and are potentially capable of fine rasping (Purschke 1988). Some species are
described as having four jaws or stylets, but they are better described as having intracellular,
skeletal rods about 10 µm long and 1 µm in diameter, rather than more typical, cuticular jaws
(Purschke 1988, Tzetlin et al. 1992). The function of the rods may be to stiffen the tongue in
order to free rich foods like diatoms and bacterial films from sediment grains for ingestion as
well as to gain some muscular leverage (Tzetlin et al. 1992).
Motility
Nerillids move primarily by ciliary gliding under the power of a midventral ciliary band but
can also glide under a few grain layers of sediment by using dorsal and ventral ciliary currents
simultaneously. They can also use rapid muscular flexure in an escape response (Jouin &
Swedmark 1965, Worsae & Kristensen 2003). When Paranerilla cilioscutata emerges from
the sediments, its ciliary bands suffice for swimming propulsion, with the parapodia held in a
low-drag posture (Worsae & Kristensen 2003). Boaden (1961) described a large, slow-moving
nerillid, Meganerilla swedmarki, with no antennae but two large palps, and suggested a general
relationship among nerillid species of reduced antennae and enlarged palps associated with slow
locomotion.
Illustrations
Worsaae et al. (2009) provide informative drawings and scanning electron micrographs of
several nerillid species. Tzetlin & Saphonov (1992) show a drawing of the ventral mouth of
Trochonerilla mobilis surrounded by cilia. A similarly ciliated, ventral mouth is shown for
Longipalpa saltatrix by Worsaae et al. (2004).
Feeding
Diets of few Nerillidae are known, but their millimeter or submillimeter lengths would appear
to require ingestion of labile particles for digestion. Leptonerilla diatomeophaga is named
for its obvious diet in a habitat comprising a blanket of diatoms on lapilli (Núñez et al. 1997).
Meganerilla bactericola, found in the anoxic sulfide-oxidizing microbial mats of the Santa
Barbara Basin in California, has ectosymbiotic, nitrogen-fixing bacteria, but whether it obtains
nutrients from the symbiont or microbial mat is unknown (Summers et al. 2013). In interstitial
species the palps are generally short, and somewhat counterintuitively their ciliary motion carries
entrained particles away from the mouth (Worsae et al. 2004). In Longipalpa saltatrix that may
spend most of its time swimming in shallow anchialine caves, however, the palps are over half
the length of the worm, and ciliary motion induces mouthward currents—suggesting that it may
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
suspension feed or sweep up the most recently settled particles (Worsae et al. 2004).
Guild membership
Nerillids are motile ciliary gliders that, due to their small size, we presume feed on labile organic
material including diatoms and bacterial films.
Research questions and opportunities
• Few feeding data exist. The diversity of habitats occupied by nerillids suggest greater
diversity in feeding habits than found in meiofaunal annelids restricted to coarse sands.
References
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polychaete. Environ. Microbiol. Rept. 5:492–8
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Oenonidae, Eunicida
Diversity and systematics
Oenonidae (with which Arabellidae is a junior synonym, Orensanz 1990) are carnivorous or
parasitic Eunicida that have similar external morphology to lumbrinerids and comprise about
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Jumars, Dorgan & Lindsay
07 November 2014
100 species in about 18 genera. Oenone, Halla and Tainokia were removed from Lysaretidae
recently and placed into the Oenonidae (Colbath 1989). Much of the generic diversity stems
from monotypic, parasitic species. Fossil jaws of Synclinophora dating from the Silurian (420–
440 mya) closely resemble oenonid jaws; Oenonidae is the only extant family that appears to
be represented among Silurian scolecodonts (Eriksson et al. 2004). Oenonidae, however, based
on molecular genetic evidence does not appear to be the most basal recent family in Eunicida
(Struck et al. 2006). Free-living species often approach a length of 1 m. Parasitic forms
can be longer than their hosts (Labrorostratus zaragoensis in the trichobranchid Terebellides
californica; Hernández-Alcántara & Solís-Weiss 1998).
Habitat
Free-living oenonids can be found in mud or sand at any ocean depth. Many oenonids are
parasitic, and multiple parasites can occupy only a portion of the host’s body (e.g., Steiner &
Amaral 2009). Most parasitic Oenonidae have polychaete hosts and show a high degree of host
specificity (Martin & Britayev 1998).
Sensory and feeding structures
Most oenonids lack prostomial appendages, but a few have either a median antenna or a pair
of small antennae or all three, inserted so that they can be withdrawn into the space between
the prostomium and peristomium; in some species a medial dorsal notch in the peristomium
accommodates antennae. Nuchal organs, as dorsolateral, eversible pits or small knobs, also lie
between the prostomium and peristomium (Pleijel 2001). Up to two pairs of eyes may be present.
Like other Eunicida, oenonids have a ventral, muscular proboscis with elaborate jaws. In
free-living species the maxillae are characterized by long, thin, paired carriers that extend into
the pharyngeal tissue plus a more ventral, unpaired, medial ‘carrier,’ similar to that of Eunicidae
and Onuphidae (Paxton 2009). Maxillae are typically reduced in parasitic species. Mandibles
(carried beneath the maxillae) are usually relatively small. The free-living Drilonereis mexicana,
however, lacks mandibles entirely, whereas the parasitic Biborin ecbola entirely lacks maxillae
(Hilbig 1995). Unlike the jaws of onuphids, eunicids, and lumbrinerids that are mineralized with
aragonite or calcite, jaws of Arabella iricolor and Oenone fulgida are apparently composed of
non-crystaline material, probably scleroprotein (Colbath 1986).
Motility
Free-living species are motile, burrowing in mud or sand, and can crawl along the sediment
surface. Parasitic taxa are presumably discretely motile or sessile.
Illustrations
Hernandez-Alcantara & Solis-Weiss (1998; Fig 1) draw the parasitic Labrorostatus zaragozensis
filling most of the body cavity of its polychaete host, Terebellides californica. Paxton (2009;
Fig. 2c), Colbath (1989; Fig. 2), and Steiner & Amaral (2009; Fig. 4) illustrate jaws.
Feeding
Observations of feeding and gut contents are still rare except for Halla okudai and parthenopeia.
Both strongly preferred bivalve prey and showed strong preferences among bivalve species and
sizes (Saito & Imabayashi 1997, Osman et al. 2010). H. okudai grew fastest on its preferred prey
(Saito et al. 1999), but its degree of preference was affected by prior dietary experience (Saito
et al. 2003). Both species appeared to use chemosensing to hunt, raising the prostomium above
the sediment-water interface to sense bivalve-associated chemicals in the bottom boundary layer.
They rapidly secreted a toxin-containing gel (Kawai et al. 1999) around the edges of the shell
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and then consumed the disabled bivalve in its entirety.
The few available 15N measurements indicate a very high trophic level (unambiguous
carnivory) for oenonids. In Catalan slope sediments three unidentified individuals of the family
had the highest mean δ15N of any polychaetes tested (Fanelli et al. 2011). A single specimen
of Halla parthenopeia from the Bay of Banyuls-sur-Mer had δ15N content similar to that of
glycerids and lumbrinerids and higher than that of nephtyids (Carlier et al. 2007). Arabella
iricolor from seagrass beds around Mallorca Island was more highly enriched in 15N than were
sympatric lumbrinerids (Deudero et al. 2014). Biomass-specific N uptake by oenonids on the
Indian continental margin was three times the median value for polychaetes, again supporting
carnivory (Hunter et al. 2010, Fig. 6).
Guild membership
Oenonids are carnivores or parasites using a pair of jaws. Free-living species are motile
burrowers. Those that eat slowly moving or sessile prey like bivalves require motility to
encounter prey.
Research questions and opportunities
• Feeding behavior has been studied in only a couple of species of free-living oenonids, and
very little is known about parasitic taxa.
• Are all or most free-living species specialists on bivalves?
• Functional mechanics of the long maxillary carriers are unknown.
References
Carlier A, Riera P, Amouroux J-M, Bodiou J-Y, Grémare A. 2007. Benthic trophic network in the
Bay of Banyuls-sur-Mer (northwest Mediterranean, France): An assessment based on stable
carbon and nitrogen isotopes analysis. Estuar. Coast. Shelf Sci. 72:1–15
Colbath GK. 1986. Jaw mineralogy in eunicean polychaetes (Annelida). Micropaleontology
32:186–9
Colbath GK. 1989. Revision of the family Lysaretidae, and recognition of the family Oenonidae
Kinberg, 1865 (Eunicida: Polychaeta). Proc. Biol. Soc. Wash. 102:116–23
Eriksson ME, Bergman CF, Jeppsson L. 2004. Silurian scolecodonts. Rev. Palaeobot. Palynol.
131:269–300
Fanelli E, Papiol V, Cartes JE, Rumolo P, Brunet C, Sprovieri M. 2011. Food web structure of the
epibenthic and infaunal invertebrates on the Catalan slope (NW Mediterranean): Evidence
from δ13C and δ15N analysis. Deep-Sea Res. Pt. I 58:98–109
Hernandez-Alcantara P, Solis-Weiss V. 1998. Parasitism among polychaetes: a rare case
illustrated by a new species: Labrorostratus zaragozensis, n. sp.(Oenonidae) found in the
Gulf of California, Mexico. J. Parasitol. 84:978–82
Hilbig B. 1995. Family Oenonidae Kinberg, 1865. In Taxonomic atlas of the benthic fauna
of the Santa Maria Basin and the western Santa Barbara Channel, Vol. 5, Polychaeta:
Phyllodocida (Syllidae and Scale-Bearing Families), Amphinomida, and Eunicida. ed. JA
Blake, B Hilbig, PH Scott, pp. 315–39. Santa Barbara Museum of Natural History: CA
Hunter WR, Levin LA, Kitazato H, Witte U. 2012. Macrobenthic assemblage structure and
organismal stoichiometry control faunal processing of particulate organic carbon and
nitrogen in oxygen minimum zone sediments. Biogeosciences 9:993–1006
Kawai K, Kunitake H, Saito H, Imabayashi H. 1999. Paralytic and digestive activities of jellylike substances secreted by a lysaretid polychaete, Halla okudai. Benthos Res. 54:1–7
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Martin D, Britayev TA. 1998. Symbiotic polychaetes: Review of known species. Oceanogr. Mar.
Biol. Ann. Rev. 36:217–340
Orensanz JM. 1990. The eunicemorph polychaete annelids from Antarctic and Subantarctic
seas: With addenda to the Eunicemorpha of Argentina, Chile, New Zealand, Australia, and
the southern Indian Ocean. In Biology of the Antarctic Seas, ed. LS Kornicker 21:1–183.
Washington, D.C.: American Geophysical Union
Osman IH, Gabr HR, El-Etreby SG. 2010. Rearing trials of Halla parthenopeia under laboratory
conditions (Polychaeta: Oenonidae). J. Exp. Mar. Biol. Ecol. 383:1–7
Paxton H. 2009. Phylogeny of Eunicida (Annelida) based on morphology of jaws. Zoosymposia
2:241–64
Pleijel F. 2001. Family Oenonidae Kinberg, 1865. See Rouse & Pleijel 2001, pp. 166–8
Saito H, Imabayashi H. 1994. Food preference of the polychaete Halla okudai. J. Fac. Appl.
Biol. Sci. Hiroshima Univ. 33:151–7
Saito H, Imabayashi H, Kawai K. 1999. Growth of the bivalve-feeder Halla okudai (Polychaete:
Lysaretidae) under wild and rearing conditions, in relation to species and abundance of prey
organisms. Fisheries Sci. 65:230–4
Saito H, Imabayashi H, Suzuki C, Kawai K. 2003. Effect of experience on prey species selection
by the bivalve feeder Halla okudai (Polychaeta: Lysaretidae). Mar. Freshw. Behav. Phy.
36:67–76
Steiner TM, Amaral ACZ. 2009. Arabella aracaensis, a new species with growth rings on its
mandibles, and some remarks on the endoparasitic Labrorostratus prolificus (Polychaeta:
Oenonidae) from southeast Brazil. J. Nat. Hist. 43:2537–51
Struck T, Purschke G, Halanych K. 2006. Phylogeny of Eunicida (Annelida) and exploring data
congruence using a partition addition bootstrap alteration (PABA) approach. Syst. Biol.
55:1–20
Onuphidae, Eunicida
Diversity and systematics
Onuphidae comprise about 320 species in 22 genera, with Diopatra as the most speciose genus
and 5 genera monospecific. Molecular data (Struck et al. 2006) support earlier suggestions based
on jaw morphology and aragonite mineralization of a close relationship between Onuphidae
and Eunicidae (Colbath 1986). More extensive recent data support monophyly of both families
(Zanol et al. 2010, 2014). The family was last revised by Paxton (1986). Onuphids range from a
few millimeters to about 3 m long (Paxton 2000).
Habitat
Onuphids are found worldwide at all depths and on varied substrata. Most are tubicolous, often
in soft sediments, but some are motile, and quill worms (Hyalinoecia spp.) carry their tubes with
them in clearly discrete motility.
Sensory and feeding structures
The prostomium is roughly hemispherical. Eyes if present are a single pair of dorsolateral spots.
Onuphids have well developed dorsolateral nuchal grooves at the posterior of the prostomium
that range from straight to nearly circular and two frontal and five occipital antennae with
extensive sensory structures (Paxton 1986). The prostomium is a complete ring.
Like other Eunicida, they have a ventral muscular proboscis with strongly articulated jaws.
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Just anterior to the mouth are labial palps, and just posterior is a lower lip that together may help
manipulate food items. Their mandibles are two elongated shafts connected via a ligament and
terminating anteriorly as cutting plates over which the maxillae slide. The single pair of carriers
is short, and the first pair of maxillae are generally falcate and smooth (Paxton 1986).
Motility
Most onuphids build tubes comprising a secreted inner layer and an external agglutinated layer
of sediments and other inclusions, but the motile quill worms carry a transparent tube with a
tougher secretion that lacks attached sediments and is difficult to cut with scissors (Paxton 1986).
Quill-worm tubes typically have 1-3 one-way valves at each end that make the tube difficult to
enter from the outside, may be circular or elliptical in cross section and can be strengthened by
lateral ribs (Orensanz 1990, Budaeva 2012). A smooth ventral surface of the tube limits friction,
accommodating the nomadic lifestyle of these presumably scavenging (F&J) and predatory
(Gaston 1987) forms. Striking numbers of Hyalinoecia tubicola can gather at a carrion fall at
shelf or slope depths surprisingly quickly (PA Jumars, personal observations). A few onuphids,
notably members of the genus Australonuphis, lack tubes entirely and are more motile.
Illustrations
Nishi and Kato (2009) show striking in situ photographs of Longibrachium arariensis, which
appears to be a sit-and-wait predator/scavenger. Paxton (1986; Fig. 5) shows SEM images of
nuchal grooves of Hyalinoecia tubicola, as well as drawings of nuchal organs of other onuphids.
Budaeva (2012) shows drawings and photographs of the morphology of the quill-worm
Leptoecia midatlantica. Remarkable photographs of the quill worm Hyalinoecia tubicola are
shown at <http://www.naturamediterraneo.com>.
Feeding
Evidence has solidified that some populations of tube-dwelling onuphids are primarily
herbivorous. Bailey-Brock (1984) assessed abundance of 1.5 - 3 cm long Diopatra leuckarti on
a Hawaiian intertidal reef flat where they reached abundances of 2.2 × 104 m-2. The invertedJ-shaped tubes were so dense that they trapped sediments, creating mounds 3 - 5 m wide and
up to 500 m long, parallel to shore. Bailey-Brock (1984) observed the worms to feed at low
tide on the algae attached to neighboring tubes and on the sand between them. No observations
were made at high tide. Kinbergonuphis simoni fed ground alfalfa in laboratory experiments
showed similar growth rates and maturation times to animals in the field (Hsieh & Simon 1991).
Kim (1992) performed elegant field measurements of natural kelp abundance and manipulated
kelp abundance at several sites 12 - 14 m deep in Monterey Bay, convincingly demonstrating
that Diopatra ornata grew faster and larger when supplied with more kelp. There was no local
numerical response to local food abundance, likely because larvae dispersed, and settlement
apparently did not respond to the kelp manipulations. In separate field experiments, Gulbransen
& McGlathery (2013) documented substantial 15N transfer from the non-native rhodophyte
Gracillaria vermiculophylla to Diopatra cuprea on an intertidal marsh and mudflat in Virginia.
Dağli et al. (2005) studied gut and fecal pellet contents of Diopatra aciculata in the intertidal of
Izmir Bay near Degas, Turkey. Contents were primarily seagrass leaves and associated algae. In
the laboratory, it routinely ate the same diet but preferred polychaetes and amphipods and reacted
most rapidly to rotten animals. When none of these foods was present, it detritus fed, likely
explaining its preference for organic-rich, polluted areas of the bay (Dağli et al. 2005).
Members of the genus Longibrachium are named for the length of their anterior few pairs
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of parapodia. Nishi & Kato (2009) reported that 16 cm long L. arariensis in 10 - 15 m of water
on the Pacific side of central Honshu could be caught on hook and line baited with a small
euphausiid. They subsequently made live aquarium observations on retrieved specimens to
complement diver-taken photographs in situ. L. ararensis builds its tube flush with the sand
surface and deploys its elongated parapodia around the tube opening in a radial array. The
parapodia are waved slowly up and down in apparent chemosensing for animal prey and carrion.
A few onuphids, notably members of the genus Australonuphis, lack tubes. Australonuphis
spp. are chemotactic scavengers. They aggregate on carrion in the swash zone, hundreds having
been seen on a washed-up whale (Paxton 1979). Individuals apparently rely on chemical cues
pumped into the sediment by waves and emerge upon a suitable cue from carrion, a behavior
that is exploited in their capture for fish bait (Paxton 2000). Suggestive of some omnivory,
bait collectors relate that it is more difficult to obtain a response to carrion when the beach is
heavily laden with macroalgal wrack (Paxton 2000). In the Concepción methane seep area δ15N
values for the quill worms Hyalinoecia sp. (that are discretely motile and carry a tube) indicated
carnivory or carrion feeding (Sellanes et al. 2008).
There have been observations of some detritivory in both tube-dwelling and motile onuphids.
Gaston (1987) dissected 6 Hyalinoecia artifex (1 with forams and 5 with peracarids), 14 Nothria
conchylega (all with detritus and 3 with forams), 6 Onuphis atlanticum (all with detritus), and
54 Onuphis pallidula (49 with detritus and 5 empty). Gaston (1987) considered H. artifex to
be a predator and the other onuphids (including the motile N. conchylega) to be surface deposit
feeders. One of 3 sampled onuphids showed rapid uptake of labeled, fresh phytodetritus in
incubated cores from 688 m water depth in Korsfjorden, Norway (Sweetman & Witte 2008).
Graeve et al. (1997) studied fatty acid composition in Onuphis conchylega collected from 50
m depth off Spitzbergen. Only 4% of its lipids were storage lipids, and its fatty acid composition
did not reflect carnivory or feeding on diatoms and was closest to the fatty acid profile of
suspension-feeding brittle stars Ophiopholis aculeata and Ophiacantha bidentata. These results
imply that the onuphids in these late summer samples were in poor nutritional condition and
perhaps deposit feeding. In contrast, Drazen et al. (2008) analyzed three individual Paradiopatra
sp. from the base of the Monterey Abyssal Fan at 4100 m water depth. They found significant
concentrations of storage lipids as well as ratios of 18:1ω9/18:1ω7 consistent with detritivory
but with a higher dependence on predation than the shallow-dwelling Onuphis conchylega. They
suggested that this sit-and-wait omnivore, unlike polychaete species that have a steadier supply
of food, relied upon storage lipids to bridge periods of food shortage. In onuphids that occupy
tubes anchored in sediments, stable isotopic data are generally consistent with omnivory (Drazen
et al. 2008, Paradiopatra sp.; McLeod et al. 2010, Onuphidae; Boyle et al. 2012, Onuphidae).
Guild membership
F&J’s classification of Onuphidae as omnivorous generalists using articulated jaws has been
largely upheld. There does appear to be some preference for herbivory among tubicolous species
and carnivory or scavenging among motile species. These differences may reflect encounter as
sedentary animals likely encounter more macroalgal and macrophyte material than carrion, and
carrion is more effectively encountered by mobile animals. Motilities range from discretely
motile tube builders to more mobile scavengers lacking tubes.
Research questions and opportunities
• Onuphids present abundant opportunities to test assimilation and growth rates under varying
opportunities for both simultaneous and sequential omnivory.
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07 November 2014
• We suspect that carrion would be preferred by both tubicolous and motile species if offered
in choice experiments.
• Longibrachium spp. appear to be good candidates for studies of chemosensing.
References
Bailey-Brock JH. 1984. Ecology of the tube-building polychaete Diopatra leuckarti Kinberg,
1865 (Onuphidae) in Hawaii: community structure, and sediment stabilizing properties. Zool.
J. Linn. Soc. 80:191–9
Boyle MD, Ebert DA, Cailliet GM. 2012. Stable-isotope analysis of a deep-sea benthic-fish
assemblage: evidence of an enriched benthic food web. J. Fish Biol. 80:1485–507
Budaeva N. 2012. Leptoecia midatlantica, a new species of the deep-sea quill-worms
(Polychaeta: Onuphidae: Hyalinoeciinae) from the Mid-Atlantic Ridge. Zootaxa 3176:45–60
Colbath GK. 1986. Jaw mineralogy in eunicean polychaetes (Annelida). Micropaleontology
32:186–9
Dăgli E, Ergen Z, Cinar ME. 2005. One-year observation on the population structure of Diopatra
neapolitana Delle Chiaje (Polychaeta: Onuphidae) in Izmir Bay (Aegean Sea, eastern
Mediterranean). Mar. Ecol. 26:265–72
Drazen JC, Phleger CF, Guest MA, Nichols PD. 2008. Lipid, sterols and fatty acids of abyssal
polychaetes, crustaceans, and a cnidarian from the northeast Pacific Ocean: food web
implications. Mar. Ecol. Prog. Ser. 372:157–67
Gaston GR. 1987. Benthic Polychaeta of the Middle Atlantic Bight: feeding and distribution.
Mar. Ecol. Prog. Ser. 36:251–62
Graeve M, Kattner G, Piepenburg D. 1997. Lipids in Arctic benthos: does the fatty acid and
alcohol composition reflect feeding and trophic interactions? Polar Biol. 18:53–61
Gulbransen D, McGlathery K. 2013. Nitrogen transfers mediated by a perennial, non-native
macroalga: a 15N tracer study. Mar. Ecol. Prog. Ser. 482:299–304
Hsieh H-L, Simon JL. 1991. Life history and population dynamics of Kinbergonuphis simoni
(Polychaeta: Onuphidae). Mar. Biol. 110:117–25
Kim SL. 1992. The role of drift kelp in the population ecology of a Diopatra ornata Moore
(Polychaeta: Onuphidae) ecotone. J. Exp. Mar. Biol. Ecol. 156:253–72
McLeod RJ, Wing SR, Skilton JE. 2010. High incidence of invertebrate-chemoautotroph
symbioses in benthic communities of the New Zealand fjords. Limnol. Oceangr. 55:2097–
106
Nishi E, Kato T. 2009. Longibrachium arariensis, a new species of Onuphidae (Annelida:
Polychaeta) from the shallow water of Izu Peninsula, central Japan, with notes on its feeding
behavior. Zootaxa 2081:46–56
Orensanz JM. 1990. The eunicemorph polychaete annelids from Antarctic and Subantarctic
seas: With addenda to the Eunicemorpha of Argentina, Chile, New Zealand, Australia, and
the southern Indian Ocean. In Biology of the Antarctic Seas, ed. LS Kornicker 21:1–183.
Washington, D.C.: American Geophysical Union
Paxton H, 1979, Taxonomy and aspects of the life history of Australian beachworms (Polychaeta:
Onuphidae), Austral. J. Mar. Freshw. Res. 30:265–94
Paxton H. 1986. Generic revision and relationships of the family Onuphidae (Annelida:
Polychaeta). Rec. Austral. Mus. 38:1-74
Paxton H. 2000. Family Onuphidae. See Beesley et al. 2000, pp. 99–104
Sellanes J, Quiroga E, Neira C. 2008. Megafauna community structure and trophic relationships
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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at the recently discovered Concepción methane seep area, Chile, ~36°S. ICES J. Mar. Sci.
65:1102–11
Struck T, Purschke G, Halanych K. 2006. Phylogeny of Eunicida (Annelida) and exploring data
congruence using a partition addition bootstrap alteration (PABA) approach. Syst. Biol.
55:1–20
Sweetman AK, Witte U. 2008. Macrofaunal response to phytodetritus in a bathyal Norwegian
fjord. Deep-Sea Res. Pt. I 55:1503–14
Zanol J, Halanych KM, Fauchald K. 2014. Reconciling taxonomy and phylogeny in the
bristleworm family Eunicidae (polychaete, Annelida). Zool. Scr. 43:79–100
Zanol J, Halanych KM, Struck TH, Fauchald K. 2010. Phylogeny of the bristle worm family
Eunicidae (Eunicida, Annelida) and the phylogenetic utility of noncongruent 16S, COI and
18S in combined analyses. Molec. Phylogen. Evol. 55:660–76
Opheliidae
Diversity and systematics
Opheliidae comprise about 135 species, excluding 34 Travisia spp. Each of 7 genera contain ≤
4 species; the remainder are roughly evenly distributed among the principal 6 genera. Recent
molecular work found Travisia and Kesun to be a sister group to Scalibregmatidae (Persson &
Pleijel 2005, Paul et al. 2010). We discuss Travisia under Scalibregmatidae, although in a few
cases past data are presented for Opheliidae with no genus specified, leaving some ambiguity.
Remaining opheliids fall into two clades with distinctive morphologies and behaviors and the
unfortunate names Ophelininae (including Ophelina and Armandia) and Opheliinae (including
Ophelia and Thoracophelia). Polyopthalmus is morphologically similar to Armandia and falls
within a clade of Armandia in a molecular-based phylogeny (Law et al. 2014). Molecular data
suggest that opheliids fall close to Capitellidae within Annelida (Struck et al. 2011, Paul et al.
2010). Even more recent molecular studies suggest a sister relationship with cirratulids and
siboglinids (Weigert 2014). Opheliids range from < 5 mm to > 7 cm long (Rouse 2001).
Habitat
With some exceptions, different genera of Opheliidae seem to inhabit different environments.
Thoracophelia (= Euzonus) species are found fairly high in the intertidal of sandy beaches in
distinct zones of high abundance (McConnaughey & Fox 1949). Unusually high hemoglobin
content (Dangott & Terwilliger 1986, Law et al. 2013) appears to be an adaptation to variable
oxygen conditions in this environment. Ophelia spp. are also found in sandy beaches but lower
in the intertidal. Ophelina spp. live in soft muds, whereas Armandia and Polyopthalmus are
found in heterogeneous sediments. Habitat appears to be only loosely related to burrowing mode
(Law et al. 2014). Opheliids are found in soft sediments at all ocean depths.
Sensory and feeding structures
The tip of the prostomium of some Ophelininae has a small palpode; otherwise anterior
appendages are absent. Armandia brevis has prostomial and segmental ocelli that are described
in detail by Hermans & Cloney (1966) and Hermans (1969). Eyes are absent in Opheliinae.
Nuchal organs occur in pits at the posterior of the prostomium and are eversible. Several species
of opheliids have two pairs (Purschke 1997).
The non-muscular, eversible pharynx is axial and ciliated, but its shape varies considerably
among species. The Opheliinae (Ophelia and Thoracophelia) have a more bubble-like proboscis,
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Jumars, Dorgan & Lindsay
07 November 2014
whereas that of Armandia, Ophelina, and Polyopthalmus tends to be more dorsoventrally
asymmetrical and lobate, with the mouth tentacles of A. maculata differing from the more
tongue-like proboscis of other Ophelininae (Tzetlin & Zhadan 2009).
Opheliid gut morphology also varies, even within a subfamily. Armandia agilis and A.
maculata have simple, tubular guts, whereas Ophelina acuminata has three distinguishable gut
compartments (Penry & Jumars 1990). O. acuminata in addition has a dorsoventral partition that
splits the midgut into left and right halves (Penry 1988). Such partitions are used in engineered
flows to increase mixing at low pipe Reynolds numbers (Sturman et al. 2006). Ophelia bicornis
has a ‘rear-assist’ system, a cilated and papillated anal tube that speeds the exit of spent sand
digesta (Harris 1991). A pair of caeca near the foregut-midgut junction may be common to all
opheliids; their function is unknown (Penry 1988).
Motility
Opheliids are active burrowers, and the group including Armandia and Ophelina are strong
swimmers as well. Law et al. (2014) compared muscle structure and burrowing behavior
between representative species of the two clades. Armandia brevis has thick longitudinal
muscles that act with oblique muscles to bend the body into undulations used for burrowing and
swimming, making it well suited to burrowing through the unconsolidated “fluff” layer of muds
(Dorgan et al. 2013). Armandia uses the same undulatory gait for burrowing and swimming
(Dorgan et al. 2013). Most Armandia spp. found in the water column are reproductive, and the
posterior end is curved upward with mucus-covered chaetae extending outward like a fan (Clark
& Hermans 1976). Thoracophelia mucronata, which burrows in beach sands by peristalsis,
has an abdomen similar in morphology to A. brevis, but with circular muscles in the thorax that
are important in peristaltic movements (Law et al. 2014). T. mucronata has a highly modified
anterior septum used to inflate the head region during burrowing (Law et al. 2014). In contrast,
A. brevis has an open body cavity with two very thin anterior septa not used in burrowing
(presumably for pharynx eversion), and Ophelia bicornis has two septa that increase the internal
pressure of the head region for burrowing but are less muscular than that of T. mucronata,
apparently intermediate between Armandia and Thoracophelia (Harris 1994, Law et al. 2014).
Traces left by burrowing Thoracophelia and Ophelia resemble the ichnofossils Macaronichnus,
with evidence of high rates of sediment reworking (Clifton & Thompson 1978, Dafoe et al.
2008a, Seike 2008, Quiroz et al. 2010).
Illustrations
Clark & Hermans (1976) show a photograph of the posterior of Armandia modified for
swimming as well as drawings and a photograph of swimming Ophelina. Patterns of burrowing
and swimming are shown for Armandia by Dorgan et al. (2013). Law et al. (2014) show
photographs of Armandia brevis and Thoracophelia mucronata, including live animals, muscle
structure, and a sequence of images of head expansion by T. mucronata while burrowing. Tzetlin
& Zhadan (2009) show SEM images of pharynx morphology in several opheliids. Purschke
(1997) shows an SEM of the everted nuchal organ of Ophelia rathkei.
Feeding
Thoracophelia mucronata deposit feeds on sandy beaches, with a gut throughput time an order
of magnitude higher than that of other deposit feeders of similar weight (Kemp 1988). Kemp
(1985, 1986) calculated that bacterial carbon in the sand would provide < 10% of the daily
carbon requirement for T. mucronata, with worms capable of assimilating carbon from refractory
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carbohydrates in isotopically-labeled Ulva, even without bacterial degradation. More recently,
stable isotope analysis showed T. furciferus at a higher trophic position than suspension-feeders
on a sandy beach in Uruguay, but not as high as the glycerid, Hemipodus olivieri, which mixing
models suggest feeds on suspension feeders (Bergamino et al. 2011). Despite a mean gut
residence time of 4 min (Kemp 1986), T. mucronata shows statistically significant selection for
felsic over mafic mineral grains (Dafoe et al. 2008b). This selection accounts for characteristic
trace fossils (Macaronichnus) long known from the fossil record, but the bases for selection
(specific gravity, shape, texture, organic content or some other feature) have not been determined.
Ophelia spp. also deposit feed on sandy beaches. An interesting case is that of Ophelia
verrilli, which is intertidal in the Gulf of Maine and subtidal south of Cape Cod. Like many
other deposit feeders, it begins to ingest sediments (sand in this case) only when it exceeds about
1 cm in length, which it does only in its second year after settlement (Riser 1987). Carmichael et
al. (2004) assayed animals from several estuaries surrounding Pleasant Bay, Cape Cod. Ophelia
spp., Nephtys spp. and Nereis spp. tied for the highest 15N enrichment. Ophelia neglecta from the
Bay of Banyuls-sur-Mer had an intermediate δ15N signature (Carlier et al. 2007).
Although Armandia and Ophelina are morphologically similar, with slender, rigid bodies,
and both move by undulation, many Armandia species are smaller (a few centimeters long) and
are found in heterogeneous sediments, whereas larger Ophelina live in soft muds (cf. Law et al.
2014). Both Armandia loboi, from 5 - 12 m water depth in sandy gravel on the southwestern
Argentinian coast (Elias & Bremec 2003) and A. brevis from intertidal southern California
(Dorgan, personal observation) have sand grains in their gut contents. By diluting natural sand
with various amounts of sand from which organic material was removed, Tamaki (1985) created
known gradients in food quantity and observed Armandia sp. individuals to arrange themselves
at local areal densities proportional to local food quantity in the same way regardless of the
absolute abundance of individuals in the experiment, implying lack of intraspecific, competitive
interference. Surprisingly, however, in an extensive study of intertidal animals from Ariake
Bay, southern Japan, Yokoyama et al. (2005) found an Armandia sp. to have the highest δ15N of
any other species except one indisputably carnivorous goniadid and one fish species that were
barely higher. In a stable isotope study of the brackish Gamo Lagoon adjacent to Sendai Bay on
the east coast of Japan, Kanaya et al. (2007) observed Armandia lanceolata to have a δ15N that
would place it a trophic level above all the other macrobenthos. Guérin (1971) found that larvae
of Polyophthalmus pictus, which nests within a clade of Armandia and has similar morphology
and body size (Law et al. 2014), died when provided with only diatoms as food but grew to
maturity in two months when provided with zooplankton remains. Deposit-feeding A. brevis
accumulated more chlorinated hydrocarbons from sediments than did a non-deposit-feeding
amphipod, as would be expected from the deposit-feeding syndrome (Meador et al. 1997).
In spite of their generally muddier habitats, some Ophelina spp. exhibit similarly high 15N
enrichment to Armandia. Ophelina sp. from approximately 4400 m water depth on the Kodiak
margin showed approximately as much 15N enrichment as goniadids and nephtyids from the same
site (Levin & Mendoza 2007). Ophelina acuminata from the Chukchi Sea was as enriched as
lumbrinerids from the same location (Iken et al. 2010). Ophelina cylindricaudata from the high
arctic Canada Basin did not show similarly extreme enrichment, however, and had δ15N similar
to that of spionids and cirratulids (Iken et al. 2005). Ophelina neglecta from the shallow Bay of
Banyuls-sur-Mer showed enrichment suggestive of a mixture of surface and subsurface deposit
feeding, only about 1‰ above Lanice conchilega (Terebellidae).
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Opheliids as a whole have intriguingly high δ15N values, suggesting either much higher
selectivity than is apparent from behavioral observations, digestion that is especially efficient
on refractory compounds, or considerable microbial degradation of organic material being
consumed. Sweetman & Witte (2008) analyzed natural δ13C and δ15N values of various
invertebrates at 4800 m water depth at the base of the Monterey Deep-Sea Fan. Opheliidae had
the highest δ15N values, prompting Sweetman & Witte (2008) to conjecture that these opheliids
were predators on protists. Unfortunately, they did not specify which genera of opheliids were
found, and it is quite likely that they sampled Travisia, no longer part of Opheliidae, as Drazen et
al. (2008) sampled the same region and observed that a Travisia sp. had the highest δ15N.
Würzberg et al. (2011) analyzed fatty acid composition in polychaetes from 600 - 5337 m
water depths in the Southern Ocean. Of the families sampled, Opheliidae showed considerable
intrafamilial variability, likely in part because of inclusion of Travisia (now also including
previous Kesun spp.), no longer included in Opheliidae. However, both “Opheliidae” and
Scalibregmatidae sampled had high concentrations of markers associated with foraminiferans
(protists) and with calanoid copepods, presumably sedimented as remains onto the seabed.
Guild membership
Opheliids are motile, burrowing subsurface deposit feeders feeding with an unarmed pharynx,
but high stable nitrogen enrichment raises questions about their source of nutrients for growth.
Research questions and opportunities
• Diverse gut morphologies and pharyngeal structures raise questions about variability in
feeding strategies.
• It would be interesting to test the hypothesis that the gut partition in Ophelina acuminata
enhances mixing of digesta in comparison with simpler opheliid guts.
• High δ15N values among opheliids are intriguing and merit further study.
• The mechanism of selection for felsic and against mafic sediment grains by T. mucronata is
unknown.
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Orbiniidae
Diversity and systematics
Over 150 orbiniid species are known in about 20 genera, although recent molecular data suggest
that several nominal species may be hiding complexes under a single name (e.g., Scoloplos
armiger) and that the number of species may currently be greatly underestimated (Bleidorn et
al. 2009). Their phylogenetic position within Annelida is uncertain, but there is recent evidence
that they are sister to cirratulids and siboglinids (Weigert et al. 2014). Recent molecular data
have placed the often interstitial genus Questa within Orbiniidae (e.g., Bleidorn 2005), and its
morphological similarity to juvenile Scoloplos spp. (Beerman et al. 2011) argues for a division of
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orbiniids into two morphotypes based on size. Also diminutive (< 1 and often ≤ 0.5 cm long) are
Proscoloplos and Pettibonella spp. Most other species are 3 - 30 cm long.
Habitat
Orbiniids are burrowers and interstitial forms common in muddy and sandy shallow-water and
shelf habitats and have recently been found at hydrothermal vents and cold seeps as well (e.g.,
Van Dover & Fry 1994, Thurber et al. 2010). It is less widely known that they are common if not
abundant at bathyal depths (e.g., Jumars 1975, Blake 1996, Hilbig 2001) and can occur abyssally
as well (e.g., Kröncke et al. 2003, Laguionie-Marchais et al. 2013). Questa spp. are generally
found in sandy sediments (Giere & Erseus 1998). Proscoloplos can reach very high densities in
algal turfs (Kelaher & Rouse 2003).
Sensory and feeding structures
Orbiniids lack anterior appendages and feed with eversible pharynges. They often have a pair
of anterior eyes, and nuchal organs are present as dorsolateral slits near the posterior of the
prostomium. The ventral muscular pharynx of juveniles (Purschke 1988) is replaced by a
non-muscular, ciliated, generally sac-like, but sometimes digitate, axial proboscis in the larger
species (≥ 3 cm long as adults, e.g., Parkinson 1978, Beerman et al. 2011, Tzetlin & Purschke
2005, Tzetlin & Zhadan 2009). Tzetlin & Zhadan (2009) described the pharynx as having
numerous folds and patterns to increase surface area. Smaller taxa (e.g., Questa spp.) retain the
muscular pharynx of juveniles as adults (Beerman et al. 2011). Pharyngeal morphology and
feeding behaviors of questids more closely resemble those of other meiofaunal annelids (e.g.,
Nerillidae, Protodrilidae, Dinophilidae; Giere & Riser 1981) and the juveniles of several other
families (e.g., cirratulids, flabelligerids; Beerman et al. 2011) than larger orbiniids. The pharynx
of Q. paucibranchiata has an eversible, tongue-like organ and a pair of dorsolateral ciliary folds
(Beerman et al. 2011).
Motility
In the larger species, parapodial orientation is lateral in thoracic segments, but the notopodia are
usually dorsal in abdominal segments, bracketing more medial branchiae. The vertical notopodia
may protect branchiae from abrasion and create space for water flow over the gills between the
body and the burrow wall. A position angled upward and toward the posterior may increase
friction and resist backward movement, and potentially counter upward forces on the body from
digging into stiff muds or granular material under the weight of overlying sediments, although
they may lack the rigidity for a substantial mechanical role.
Larger worms do not use the pharynx in burrowing in either sandy or muddy sediments
(Haploscoloplos elongatus, Parkinson 1978; Leitoscoloplos pugettensis, Orbinia johnsoni, and
Naineris dendritica, Francoeur & Dorgan 2014), although the pharynx does seem to be used
by juveniles to burrow (Anderson 1961). Larger species burrowing in mud (Leitoscoloplos
spp.) exhibit a periodic twisting behavior that seems to be unique among peristaltic burrowers
(Francoeur & Dorgan 2014). Twisting behavior was also observed in orbiniids burrowing in
beach sands (N. dendritica, O. johnsoni), but with much less regularity. Francoeur & Dorgan
(2014) suggested that twisting facilitates burrow extension in muds by fracture, as rotating
the ovoid cross-section to orient the longer axis to expand the crack-shaped burrow allows the
worm to exert greater tensile stress orthogonal to the crack. All species observed burrow by
retrograde peristalsis, in which the wave of contraction travels opposite the direction of motion,
and segments are separated by septa (Parkinson 1978; Francoeur and Dorgan 2014). Short-term
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colonization experiments documented motility in Proscoloplos bondi (Kelaher & Rouse 2003).
Although most species are motile burrowers, an undescribed species with hypertrophied
anterior gills lives in bathyal, hypoxic, stably stratified brine pools with seep mussels. It is seen
to hold and wave the thorax above the sediment-water and mussel-water interface, presumably to
enhance respiratory exchange (Hourdez et al. 2001). Descriptions of its motility are lacking, but
we presume it maintains the ability to burrow and is discretely motile. The waving posture raises
curiosity about when and what it eats.
Illustrations
Tzetlin & Zhadan (2009; Fig. 1) show SEM images of everted and inverted pharynges. Giere
& Riser (1981) and Giere & Erséus (1988) show images of the mouth opening and muscular
pharynx of Questa. Francoeur & Dorgan (2014) show sequential photographs of orbiniids
burrowing in clear sediment analogs and provide a supplementary movie of burrowing worms.
Parkinson (1978) provides drawings of burrowing Haploscoloplos elongatus.
Feeding
Giere and Riser (1981) described Questa trifurcata as protruding and retracting a tongue-like
buccal pad while moving among sand grains, and they found fragments of plant material,
diatoms, and sand grains in the guts, a description that seems to fit other questids as well (Giere
& Erséus 1998).
Data have supported F&J’s classification of larger orbiniids as subsurface deposit feeders.
There still do not appear to be any direct tests of particle selectivity in larger orbiniids, but Rice
et al. (1986) concluded that selection for small particles must have occurred in their experiments
with Scoloplos spp. from Maine (mostly S. robusta) in order to explain the high organic content
of fecal mounds. They reported that some coarser sediments were evident in the fecal mounds
of larger worms. Rice et al. (1986) measured assimilation efficiencies and feeding rates and
calculated that worms could potentially meet their nitrogen but not their carbon requirements
from bacterial biomass. Scoloplos spp. are conveyer-belt species that feed near the redox
potential discontinuity (Rice et al. 1986).
Based on an inventory of organic material in the sediments, Bianchi (1988) suggested that
subsurface deposit-feeding Leitoscoloplos fragilis at a sandy intertidal site in Delaware depended
on diatoms for food. Parkinson (1978) found diatoms as well as foraminiferans and sand in guts
of Haploscoloplos elongatus from an intertidal sand flat, although he did not determine whether
diatoms and Foraminifera were enriched relative to bulk sediment. Herman et al.‘s (2000)
labeling experiments in the intertidal of the Westerschelde estuary did not show rapid utilization
of living diatoms by Scoloplos armiger. Its δ13C did support a microphytobenthic source of
carbon, but uptake of 13C from labeled diatoms was only moderate, suggesting low selectivity,
and its high natural δ15N was consistent with high δ15N of other subsurface deposit feeders,
suggesting feeding on microbially reworked organic matter of microphytobenthic origin. Evrard
et al. (2010) assayed stable isotopes in S. armiger from shallow-water (~ 2 m water depth) sands
in Hausstrand off Sylt in the Wadden Sea and obtained similar results, i.e., apparent dependence
on microphytobenthic organic matter but a high δ15N. Consistent with nutritional dependence on
diatoms, experimental burial of Ulva detritus locally decreased the abundance of S. armiger in
three intertidal flats of the Oosterschelde estuary (Rossi 2006).
Dunton & Schell (1987) sampled orbiniids from 3 - 6 m water depth in Stefansson Sound in
the Beaufort Sea and found their δ13C content consistent with feeding on kelp detritus. Stable
isotope data in general show high δ15N for subsurface deposit-feeding orbiniids. Lautenschlager
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(2011) studied invertebrates of the intermittently open, shallow (mean depth of 2 m) Hopkins
River estuary in Victoria, Australia. Scoloplos sp. there had the highest δ15N value of any species
assayed, and far higher than other deposit and suspension feeders. In the Roscoff Aber Bay,
however, S. armiger had δ15N values comparable to those of deposit-feeding Arenicola marina
and Notomastus latericeus (Ouisse et al. 2011). Similarly, S. armiger collected from silty sand
at 13 m water depth in the North Sea, where the water is too turbid to allow net production by
microphytobenthos, had 15N and 13C contents similar to those of other deposit feeders at the
site (van Oevelen et al. 2009). The whole community, however was enriched in 15N and 13C
relative to local suspended and deposited detritus, leading van Oevelen et al. (2009) to invoke
substantial particle selectivity. Kędra et al. (2012) reported δ15N and δ13C values in a total of
three individuals sampled in two seasons from a 15 m deep station in Kongsfjorden, Svalbard.
They were identified as “Scoloplos armiger/Leitoscoloplos mammosus.” The two individuals
sampled in winter had signatures typical of deposit feeders, but the single individual sampled
in summer showed δ15N values more characteristic of carnivores. Schaal et al. (2008) in the
intertidal zone of Arcachon Bay found δ15N values for Phylo foetida intermediate between those
of predatory nephtyids and glycerids and substantially higher than that of Cirratulus cirratus
(Cirratulidae). Rigolet et al. (2014) in shallow-water samples from Concarneau Bay found
Orbinia cuvierii to reach δ15N values well above those of other deposit feeders at the site and
consistently above those of Hilbigneris gracilis (Lumbrineridae). Signa et al. (2013) examined
15
N enrichment at three sites in three shallow coastal ponds along a guano enrichment gradient
on the northeast coast of Sicily. Orbiniids (not identified farther) were found at each site and
showed large between-site differences in apparent enrichment over values measured in ambient
sediments. Reasons underlying this high variability between taxa and sites—and occasionally
very high values of δ15N in orbiniids—remain obscure, but such variability is not unusual among
subsurface deposit feeders.
At both hydrothermal vents and cold seeps, orbiniids show strong dependence on
chemoautrophic production (Van Dover & Fry 1994, Thurber et al. 2010). The ‘seepworm’
Methanoaricia dendrobranchiata occurs “in writhing masses of literally thousands of specimens”
(Blake 2000). It is not a deep burrower, and regionalization with vertically oriented notopodia
in the abdomen is notably absent. As the name implies, it carries elaborate gills. Based on its
highly depleted 13C, this species appears to gain all its nutrition from chemosynthetic microbes,
but through unknown means it is substantially enriched in 15N (MacAvoy et al. 2002, 2008).
Bergquist et al. (2007) examined stable isotopic signatures of animals from the Juan de Fuca
Ridge and found Scoloplos sp. also to be at the extreme of δ13C depletion, prompting them to
suggest “the possibility of a unique bacterial food source.”
Guild membership
Based on little evidence F&J considered all orbiniids to be nonselective, subsurface deposit
feeders. Larger orbiniids seem to fit F&J’s classification of subsurface deposit feeders, although
some evidence for selectivity now exists, whereas Questa and other small and juvenile orbiniids
are limited by size from bulk deposit feeding and ingest organic-rich materials, including
diatoms. Both large and small forms are motile.
Research questions and opportunities
• Experiments to test explicitly for particle selection by large forms are yet to be performed.
• The clear size and pharyngeal morphology dichotomy between small and large orbiniids
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make this group well suited to size-dependent comparisons of feeding behaviors, foods and
selection mechanisms.
• Alternative hypotheses for occasionally high values of δ15N should be tested.
References
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Beermann A, Giere O, Purschke G. 2011. Ultrastructure of the ventral pharynx in the
interstitial annelid Questa paucibranchiata (Orbiniidae) and its phylogenetic significance.
Zoomorphology 130:167–80
Bergquist DC, Eckner JT, Urcuyo IA, Cordes EE, Hourdez S, et al. 2007. Using stable isotopes
and quantitative community characteristics to determine a local hydrothermal vent food web.
Mar. Ecol. Prog. Ser. 330:49–65
Bianchi TS. 1988. Feeding ecology of subsurface deposit-feeder Leitoscoloplos fragilis Verrill.
I. Mechanisms affecting particle availability on intertidal sandflat. J. Exp. Mar. Biol.
Ecol.115:79–97
Blake JA. 1996. Family Orbiniidae Hartman, 1942. In Taxonomic Atlas of the Benthic Fauna of
the Santa Maria Basin and Western Santa Barbara Channel, Vol. 6, The Annelida. Part 3:
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Barbara: Santa Barbara Museum of Natural History
Blake JA. 2000. A new genus and species of polychaete worm (Family Orbiniidae) from
methane seeps in the Gulf of Mexico, with a review of the systematics and phylogenetic
interrelationships of the genera of Orbiniidae. Cah. Biol. Mar. 41:435–49
Bleidorn C. 2005. Phylogenetic relationships and evolution of Orbiniidae (Annelida, Polychaeta)
based on molecular data. Zool. J. Linn. Soc. 144:59–73
Bleidorn C, Hill N, Erséus C, Tiedemann R. 2009. On the role of character loss in orbiniid
phylogeny (Annelida): Molecules vs. morphology. Mol. Phylogen. Evol. 52:57–69
Dunton KH, Schell DM. 1987. Dependence of consumers on macroalgal (Laminaria
solidungula) carbon in an arctic kelp community: δ13C evidence. Mar. Biol. 93:615–25
Evrard V, Soetaert K, Heip C, Huettel M, Xenopoulos MA, Middelburg JJ. 2010. Carbon and
nitrogen flows through the benthic food web of a photic subtidal sandy sediment. Mar. Ecol.
Prog. Ser. 416:1–16
Francoeur AA, Dorgan KM. 2014. Burrowing behavior in mud and sand of morphologically
divergent polychaete species (Annelida: Orbiniidae). Biol. Bull. 226:131–45
Giere O, Erséus C. 1998. A systematic account of the Questidae (Annelida, Polychaeta), with
description of new taxa. Zool. Scr. 27:345–60
Giere OW, Riser NW. 1981. Questidae—Polychaetes with oligochaetoid morphology and
Development1. Zool. Scr. 10:95–103
Herman PM, Middelburg JJ, Widdows J, Lucas CH, Heip CH. 2000. Stable isotopes as
trophic tracers: combining field sampling and manipulative labelling of food resources for
macrobenthos. Mar. Ecol. Prog. Ser. 204:79–92
Hilbig B. 2001. Deep-sea polychaetes in the Weddell Sea and Drake Passage: first quantitative
results. Polar Biol. 24:538–44
Hourdez S, Frederick LA, Schernecke A, Fisher CR. 2001. Functional respiratory anatomy of
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Jumars PA. 1975. Environmental grain and polychaete species diversity in a bathyal benthic
community. Mar. Biol. 30:253–66
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mobile, benthic predators in the Gulf of Mexico. Mar. Ecol. Prog. Ser. 225:65–78
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incorporated by heterotrophs in Gulf of Mexico hydrocarbon seeps: an examination of
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phylogenetic importance in Polychaeta (Annelida). Zoomorphology 108:119–35
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van Dover CL, Fry B. 1994. Microorganisms as food resources at deep-sea hydrothermal vents.
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input and processing in two contrasting North Sea sediments: insights from stable isotope
and biomass data. Mar. Ecol. Prog. Ser. 380:19–32
Weigert A, Helm IC, Meyer M, Nickel B, Arendt D, et al. 2014. Illuminating the base of the
annelid tree using transcriptomics. Mol. Biol. Evol. doi: 10.1093/molbev/msu080, 11 pp.
Oweniidae
Diversity and systematics
Oweniidae comprise about 55 species in 4 genera (Capa et al. 2012). They have recently
been shown to fall basally within annelids, closely related to Magelonidae (Struck et al. 2014,
Weigert et al. 2014). The well-studied, cosmopolitan species Owenia fusiformis likely comprises
multiple species (Blake 2000, Ford & Hutchings 2005), so localities are given here along with
citations. Adults range from < 1 to > 10 cm long, but the tubes of large species can be several
times longer (Rouse 2001).
Habitat
Oweniidae are geographically and hypsographically widespread (with Galathowenia and
Myriochele found down to abyssal depths). They live in sandy to muddy sediments, with the
tentaculate Owenia generally found in sandier sediments and species lacking anterior appendages
more common in muddy sediments, but with numerous exceptions. Oweniids can be the most
common taxa under mussels in mussel beds (McLeod et al. 2014).
Sensory and feeding structures
Shapes and extents of pro- and peristomia vary greatly among Oweniidae. Oweniids also
exhibit considerable diversity in feeding appendages, including a tentacular crown (Owenia),
a pair of grooved palps (Myriowenia) or lips alone (Galathowenia & Myriochele). They lack
nuchal organs but may have lateral eyespots on either the prostomium or peristomium (Rouse
2001). All have a bulb organ (ventral proboscis) that protrudes slightly from the mouth and is
used in tube building but is not fully eversible (Purschke & Tzetlin 1996). Oweniids also have
dorsolateral ciliary folds (Myriochele oculata, Purschke & Tzetlin 1996).
Motility
Although tube dwelling, Owenia and Myriowenia were classified by F&J as discretely motile,
and several studies have since elaborated on the movements of Owenia fusiformis with their
tubes. Gluing grains at only the posterior end maintains tube flexibility needed to bend over
to the sediment surface in deposit feeding, but the resulting imbrication (apparent in Fig. 2 of
Noffke et al. 2009) serves other functions as well. Arrow-head like, it resists pulling of the tube
out from the sediments by predators seizing its exposed anterior end. When sediment transport
buries the tube too deeply to reach the sediment surface by bending over, the animal throws
bends in the remaining exposed tube and levers against the grain friction to pull the tube farther
out (Nowell et al. 1989). To change horizontal position, the animal orients and undulates the
posterior portion of its tube horizontally. The imbrication acts as a ratchet to move the tube
horizontally, posterior end first. When the tube is pulled too deeply to bend over, the animal
again levers the anterior out, bending the anterior to be more vertical without making the
posterior end move. This cycle is repeated to move farther. It is not unusual for an individual
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to move tens of centimeters horizontally in the laboratory overnight (PA Jumars, unpublished
observations). Neuropodia are modified to form distinctive tori of densely packed hooks (Rouse
2001) that likely not only help the animals stay in their tubes, but transfer muscle forces to tubes
when moving them through sand.
A number of authors since F&J have documented particle selection in oweniid tube
construction. Nowell et al. (1989) noted selection for elongate grains in O. fusiformis tubes.
Bamber (1984) documented shape-specific exclusion of (roughly spherical) fly ash in fieldcollected tubes of O. fusiformis from the UK. He also ran laboratory experiments on Myriochele
oculata and found strong selection against fly ash. Self & Jumars (1988) showed very strong
selection for angular particles over spherical glass beads in laboratory experiments with O.
fusiformis from False Bay, Washington. Noffke et al. (2009) conducted extensive comparisons
of particle size in tubes of O. fusiformis from the North Sea versus ambient sediments, finding
strong selection for larger particles in tube building. They noted that the tube may be up to
three grain layers thick and echoed Fager’s (1964) observation that a flat side of the grain is
used in attachment. Preference for elongate particles appears widespread if not universal among
oweniids (photographs in Parapar 2006, Capa et al. 2012).
Illustrations
Eckman et al. (1981; plate 1A) shows a photograph of the tube of O. fusiformis surrounded by a
characteristic feeding pit. Gambi (1989; Fig. 2) shows a drawing of O. fusiformis in its tube with
upward-opening imbrications facilitating downward movement of the tube in the sediment and
preventing upward movement. Sequential illustrations show deposit- and suspension-feeding
behaviors (Gambi 1989; Fig. 6). Capa et al. (2012) show photographs, drawings, and SEM
images of the morphology and tube structure of representatives of 4 genera. Parapar (2006)
shows images of anterior morphology and tube structure of Myriochele spp.
Feeding
F&J classified the three morphotypes: tentacular crown (Owenia), a pair of grooved palps
(Myriowenia) or lips alone (Galathowenia & Myriochele), as suspension/surface deposit feeders,
surface deposit feeders, and subsurface deposit feeders, respectively. Lengths of palps are quite
variable among Myriowenia spp. The first two of those guild assignments have largely been
supported, but several observations now indicate that even oweniids without anterior appendages
feed at the sediment surface rather than below.
In still or slowly flowing water, O. fusiformis created characteristic circular pits around the
tube by bending the flexible tube over so the tentacles reached the sediment surface for deposit
feeding (Eckman et al. 1981). Nowell et al. (1989) observed that most of the time the animal
flexed the tube back and forth, nodding at about 0.3 Hz and rarely touching the sediment,
suspension feeding rather than deposit feeding. In strong currents, the tube bent over with the
current so the tentacles contacted the sediment surface when suspension feeding (Nowell et al.
1989), taking advantage of resuspension up the lee side of its bent-over tentacular crown.
The only experimental data on particle selection for ingestion in oweniids appear to be for
O. fusiformis in deposit-feeding mode. Self & Jumars (1988) conducted laboratory ingestion
experiments with glass and plastic beads. With the particle spectra presented (an important
caveat), O. fusiformis showed no significant selection for particle size but significant selection
for particles of lower specific gravity. We do not yet understand the mechanism underlying
an ability to select for low specific gravity without also selecting smaller particles but can
independently verify Dales’ (1957) description of surface deposit feeding.
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Speculation by F&J that oweniids lacking anterior appendages feed in a buried position
has been discredited by observations. Parapar (2006) published scanning electron micrographs
of diatom frustules still in the mouth of Myriochele olgae. Fiege et al. (2000) photographed
feeding circles made by surface deposit-feeding M. fragilis at about 4200 m depth in the eastern
Mediterranean. They inferred from its patchy distribution that it may be taking advantage of
horizontal fluxes of detritus to or along the base of the continental slope. Similar feeding circles
have been attributed to Myriochele at 3450 - 3950 m water depth in the Venezuela Basin (Young
et al. 1985). Thomsen (1999) measured the difference in concentration of suspended material
upstream and downstream of a bed of Myriochele sp. under 1340 m of water in the Celtic Sea
and calculated that horizontal supply of suspended material equaled vertical sedimentation,
doubling the rate of food supply over gravitational deposition alone. Likely the tube field
induced sedimentation of particles subsequently taken by surface deposit feeding. TH Pearson
cited in Wlodarska-Kowalczuk & Pearson (2004) has observed Galathowenia oculata to feed
similarly to Myriochele spp. by bending over to sweep the sediment surface. There appear
to have been no direct observations of suspension feeding in Myriochele or Galathowenia.
Dales (1957) thought it unlikely that Myriochele was a suspension feeder given the minimal
development of the tentacular crown in species of this genus. Based on simple mechanics of
particle encounter (Rubenstein & Koehl 1977; Shimeta & Jumars 1991), we also doubt that
species of Myriochele or Galathowenia could subsist by suspension feeding alone.
Most stable isotopic data are consistent with feeding on suspended or recently deposited
detritus by oweniids, with two notable exceptions (most data being for O. fusiformis). In two
separate studies in Ariake Sound, Japan, Yokoyama et al. (2005; 2009) found O. fusiformis to fall
among suspension feeders, surface deposit feeders and omnivores in δ15N content. Similarly,
Grippo et al. (2011) found O. fusiformis from the Gulf of Mexico to have the lowest δ15N of any
polychaete. Nilsen et al. (2008) reported δ15N values for Galathowenia oculata from Sørfjord,
northern Norway, consistent with feeding on phytodetritus. Amaro (2005), however, sampled
O. fusiformis from a depositional area under the Frisian Front off Netherlands at 30 - 40 m water
depth, and found δ15N levels comparable to those in predatory polychaetes at the site. Bodin
et al. (2008) also found O. fusiformis in Seine Bay in the Iroise Sea to have δ15N substantially
higher than other deposit and suspension feeders and comparable to nephtyids, glycerids and
other carnivores. Reasons for the high values are unclear.
Guild membership
Oweniids are primarily surface deposit feeders, although those with a tentacular crown (Owenia
spp.) also suspension feed. It is possible that Myriowenia spp. may suspension feed with palps,
but such feeding has not been documented. Significant suspension feeding by Myriochele or
Galathowenia spp. is unlikely. Although mostly tubicolous, oweniids can extend and move their
tubes, so we consider them discretely motile.
Research questions and opportunities
• Frequency and distance of movement in nature are unknown.
• Silberstein (1987) suggested that oweniids were difficult for goniadids to prey upon because
of their imbricated and tapered structure. Experimental tests have not been done.
References
Amaro TPF. 2005. The benthic shift of the Frisian Front (southern North Sea) ecosystem—
possible mechanisms. PhD thesis. Wageningen Univ., Wageningen, Netherlands
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doi: 10.1146/annurev-marine-010814-020007
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Jumars, Dorgan & Lindsay
07 November 2014
Bamber RN. 1984. The utilization of fly ash by two tube-building polychaetes. J. Exp. Mar. Biol.
Ecol. 81:107–13
Blake JA. 2000. Family Oweniidae Rioja, 1917. In Taxonomic Atlas of the Benthic Fauna of the
Santa Maria Basin and the Western Santa Barbara Channel. Vol. 7. The Annelida. Part 4:
Polychaeta: Flabelligeridae to Sternaspidae, ed. JA Blake, B Hilbig, PV Scott, pp. 97-127.
Santa Barbara, CA: Santa Barbara Museum of Natural History
Bodin N, Le Loc’h F, Caisey X, Le Guellec AM, Abarnou A, et al. 2008. Congener-specific
accumulation and trophic transfer of polychlorinated biphenyls in spider crab food webs
revealed by stable isotope analysis. Environ. Pollut. 151:252–61
Capa M, Parapar J, Hutchings P. 2012. Phylogeny of Oweniidae (Polychaeta) based on
morphological data and taxonomic revision of Australian fauna. Zool. J. Linn. Soc. 166:236–
78
Dales RP. 1957. The feeding mechanism and structure of the gut of Owenia fusiformis Delle
Chiaje. J. Mar. Biol. Ass. UK 36:81–9
Eckman JE, Nowell A, Jumars PA. 1981. Sediment destabilization by animal tubes. J. Mar. Res.
39:361–74
Fager EW. 1964. Marine sediments: effects of a tube-building polychaete. Science 143:356–91
Fiege D, Kröncke I, Barnich R. 2000. High abundance of Myriochele fragilis Nilsen & Holthe,
1985 (Polychaeta: Oweniidae) in the deep sea of the Eastern Mediterranean. Hydrobiologia
426:97–103
Ford E, Hutchings PA. 2005. An analysis of morphological characters of Owenia useful to
distinguish species: description of three new species of Owenia (Oweniidae: Polychaeta)
from Australian waters. Mar. Ecol. 26: 181–96
Gambi MC 1989 Osservazioni su mofologia funzionale e comportamento trofico di Owenia
fusiformis Delle Chiaje (Polychaeta, Oweniidae) in rapporto ai fattori ambientali. Oebalia
15:145–55
Grippo MA, Fleeger JW, Dubois SF, Condrey R. 2011. Spatial variation in basal resources
supporting benthic food webs revealed for the inner continental shelf. Limnol. Oceangr.
56:841–56
McLeod IM, Parsons DM, Morrison MA, Van Dijken SG, Taylor RB. 2014. Mussel reefs on soft
sediments: a severely reduced but important habitat for macroinvertebrates and fishes in New
Zealand. NZ J. Mar. Freshw. Res. 48:48–59
Nilsen M, Pedersen T, Nilssen EM, Fredriksen S. 2008. Trophic studies in a high-latitude fjord
ecosystem — a comparison of stable isotope analyses (δ13C and δ15N) and trophic-level
estimates from a mass-balance model. Can. J. Fish. Aquat. Sci. 65:2791–806
Noffke A, Hertweck G, Kröncke I, Wehrmann A. 2009. Particle size selection and tube structure
of the polychaete Owenia fusiformis. Estuar. Coast. Shelf Sci. 81:160–8
Nowell ARM, Jumars PA, Self RFL, Southard JB. 1989. The effects of sediment transport and
deposition on infauna: Results obtained in a specially designed flume. In Ecology of Marine
Deposit Feeders, ed. GR Lopez, GL Taghon, JS Levinton, pp. 247–68. New York: SpringerVerlag
Parapar J. 2006. The genera Myriochele and Myrioglobula (Polychaeta, Oweniidae) in Icelandic
waters with the revision of type material of Myriochele heeri Malmgren, 1867, and the
description of a new species. J. Nat. Hist. 40:523–47
Purschke G, Tzetlin AB. 1996. Dorsolateral ciliary folds in the polychaete foregut: structure,
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Jumars, Dorgan & Lindsay
07 November 2014
prevalence and phylogenetic significance. Acta Zool. 77:33–49
Rouse GW. 2001. Oweniidae Rioja, 1907. See Rouse & Pleijel 2001, pp. 185–8
Rubenstein DI, Koehl MAR. 1977. The mechanisms of filter feeding: some theoretical
considerations. Am. Nat. 111:981–94
Self R, Jumars PA. 1988. Cross-phyletic patterns of particle selection by deposit feeders. J. Mar.
Res. 46:119–43
Shimeta JS, Jumars PA. 1991. Mechanisms of particle encounter by suspension feeders.
Oceanogr. Mar. Biol. Ann. Rev. 29:191–257
Silberstein M. 1987. Feeding ecology of the polychaete worm, Glycinde polygnatha Hartman
1950, an infaunal predator, with notes on life history. MS thesis. San José State Univ., San
José, California
Thomsen L. 1999. Processes in the benthic boundary layer at continental margins and their
implication for the benthic carbon cycle. J. Sea Res. 41:73–86
Weigert A, Helm IC, Meyer M, Nickel B, Arendt D, et al. 2014. Illuminating the base of the
annelid tree using transcriptomics. Mol. Biol. Evol. doi: 10.1093/molbev/msu080, 11 pp.
Wlodarska-Kowalczuk M, Pearson TH. 2004. Soft-bottom macrobenthic faunal associations and
factors affecting species distributions in an Arctic glacial fjord (Kongsfjord, Spitsbergen).
Polar Biol. 27:155–67
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subtidal bottoms in inner Ariake Sound, southern Japan, determined by stable isotopes.
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Yokoyama H, Tamaki A, Koyama K, Ishihi Y, Shimoda K, Harada K. 2005. Isotopic evidence for
phytoplankton as a major food source for macrobenthos on an intertidal sandflat in Ariake
Sound, Japan. Mar. Ecol. Prog. Ser. 304:101–16
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lebensspuren: a comparison of sedimentary provinces in the Venezuela Basin, Caribbean
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Paralacydoniidae, Phyllodocida
Diversity and systematics
Paralacydoniidae are known from Paralacydonia paradoxa and P. weberi. Molecular data
(Böggemann 2009) suggest a close relationship with Lacydoniidae, although numerous previous
studies suggest closer relationships with other Phyllodocida (cf. Pleijel 2001). They are mediumsized worms, about 10 cm long.
Habitat
Paralacydoniids are infaunal in muddy sediments over a broad depth range (Pleijel 2001) but are
most commonly reported from shelf depths.
Sensory and feeding structures
Paralacydonia spp. have a pair of small antennae and a pair of small palps and may have anterior
eyespots. Pleijel (2001) includes an SEM image of possible nuchal organs in P. paradoxa, two
on each side near the posterior of the prostomium, appearing as small knobs in depressions.
Typical of Phyllodocida, they have an unarmed, muscular, axial proboscis with terminal papillae
(Rizzo & Oliveira 2011).
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Jumars, Dorgan & Lindsay
07 November 2014
Motility
Paralacydoniidae have a pointed, glycerid-like anterior, consistent with burrowing through muds
by fracture (Che & Dorgan 2010).
Illustrations
Rizzo & Oliveira (2011) and Pleijel (2001) show images of morphology, including an everted
pharynx with papillae (Rizzo & Oliveira 2011; Fig. 2B).
Feeding
Because of their affinities with Nephtyidae and Glyceridae (Pleijel & Dahlgren 1998; Rousset et
al. 2007), they are presumed to be carnivorous, but data to support that conclusion do not appear
to exist.
Guild membership
Morphology suggests motility, and we guess that they are predators using an unarmed pharynx.
Research questions and opportunities
• Any feeding or motility information will be the first.
References
Böggemann M. 2009. Polychaetes (Annelida) of the abyssal SE Atlantic. Org. Divers. Evol.
9:251–428
Che J, Dorgan KM. 2010. It’s tough to be small: dependence of burrowing kinematics on body
size. J. Exp. Biol. 213:1241–50
Pleijel F. 2001. Paralacydonia Fauvel, 1913. See Rouse & Pleijel 2001, pp. 130–1
Pleijel F, Dahlgren T. 1998. Position and delineation of Chrysopetalidae and Hesionidae
(Annelida, Polychaeta, Phyllodocida). Cladistics 14:129–50
Rizzo AE, Oliveira JRL. 2011. Paralacydonia (Polychaeta: Paralacydoniidae) off Rio de Janeiro,
Brazil. Mar. Biodivers. Rec. 4:e84, 8 pp.
Rousset V, Pleijel F, Rouse GW, Erséus C, Siddall ME. 2007. A molecular phylogeny of annelids.
Cladistics 23:41–63
Paraonidae
Diversity and systematics
Paraonidae comprise over 140 species in 7 genera, about half of them in Aricidea, with only one
genus monotypic. Morphology suggests close relationship with orbiniids (Rouse & Fauchald
1997), but molecular data have not supported this suggestion. Their position within Annelida
remains uncertain (Zrzavý et al. 2009) but possibly close to Sternaspidae (Bleidorn 2005).
Adults range in length from about 2 mm to 4 cm (Glasby 2000).
Habitat
Paraonids (along with cirratulids) are common community dominants in the deep sea,
particularly at bathyal depths, but are also found in shallow-water sediments and down to
hadal depths. Levinsenia gracilis at slope depths off North Carolina was more abundant under
biogenic depressions than under level sediments or mounds (Schaff & Levin 1994). Blake
(1994) observed some vertical segregation of paraonid species in this same region.
In a meta-analysis of ten fish farms at five different Spanish locations, Martinez-Garcia et al.
(2013) found that paraonids were particularly sensitive to organic enrichment. Diaz-Castaneda
& Valenzuela-Solano (2009), on the other hand, found that paraonids were among the most
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abundant and diverse taxa under a tuna farm in Baja California. Mangion et al. (2014) under
tuna cages off Malta saw a more complex, time-varying response in paraonid abundance that
may resolve the apparent discrepancies.
Sensory and feeding structures
The prostomium is fused with the peristomium and usually rounded (Rouse 2001). The
peristomium is a small region surrounding the mouth. On the prostomium, paraonids have a
characteristic single median antenna and sometimes an eversible, anterior, sensory palpode.
Nuchal organs are slit-like, and eyes are often present. Considerable variability in pharyngeal
morphology occurs in the family; Paraonella nordica has a non-muscular axial proboscis with a
ciliated foregut but no dorsolateral ciliary folds, whereas Aricidea nolani has ventral dorsolateral
ciliary folds that lead directly into the esophagus (Purschke & Tzetlin 1996). Purschke & Tzetlin
(1996) suggested that paraonids exhibit an ontogenetic shift from dorsolateral ciliary folds to an
axial proboscis similar to that of orbiniids, and Tzetlin & Purschke (2005) generalized paraonids
to have ciliated, axial, non-muscular probosces similar to those of orbiniids and some opheliids.
Paraonids have simple, tubular guts, but their gut volumes are relatively high compared to body
volume, consistent with deposit feeding (Penry & Jumars 1990).
Motility
Paraonidae are burrowers. Risk & Tunnicliffe (1978) studied the association of Paraonis
fulgens with particular grain sizes and confirmed previously reported feeding traces consisting
of horizontally outward spiraling paths originating from vertical exploration shafts. This mining
pattern is suited to exploitation of food concentrations associated with bedding planes. Risk &
Tunnicliffe (1978) suggested that diatoms were the likely food being mined but did not present
direct evidence. The mining pattern would be just as effective for mining slowly settling,
organic-rich detritus from a turbidite layering.
Illustrations
Risk & Tunnicliffe (1978) show photos and drawings of spiral traces made by P. fulgens, and
Roder (1971) shows a drawing of the spiral traces extending into deeper, branching burrows.
A good idea of typical morphologies in Paraonidae is given by the stippled line drawings and
scanning electron micrographs in Aguirrezabalaga & Gil (2009).
Feeding
Among paraonids, F&J found feeding information only on P. fulgens, which has also received
the most study subsequently. Within this one species, conflicting accounts of selectivity were
reported by F&J, including nonselective deposit feeding and specialization on diatoms. Recent
data have supported this variability in selectivity and have also suggested considerable variability
in feeding depth within sediments.
Gaston et al. (1992) examined gut contents of 27 P. fulgens and 12 P. pygoenigmatica from a
variety of shallow-water sites in the Gulf of Mexico. P. fulgens was found in sands with higher
silt and clay content (4% vs. 2-3% for P. pygoenigmaticus), and their guts contained < 5 to 50%
diatoms by volume, with the remainder being detritus (undefined but presumably including
sediments). P. pygoenigmaticus gut contents never exceeded 5% diatoms by volume, with
the remainder again being detritus. Gaston et al. (1992) suggested that these differences were
explained by habitat differences rather than selectivity. In gut contents from the Middle Atlantic
Bight, Gaston (1987) reported finding detritus in all of the paraonids he dissected: 13 Aricidea
catherinae, 10 A. cerrutti, 5 A. simplex, 5 A. wassi, 5 Cirrophorus lyriformis, 5 Levinsenia
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gracilis, and 5 Paradoneis lyra. Guts of Levinsenia hawaiiensis, described from subtidal
sediments in Hawaii, were “sometimes filled with sediment” (Giere et al. 2008).
Early in situ tracer experiments with 13C-labeled diatoms and with Chlorella on the
continental slope off North Carolina showed rapid uptake by Aricidea quadrilobata (Blair et al.
1996, 2001). Similarly rapid uptake was seen in paraonids at a North Carolina mudflat (Thomas
& Blair 2002). At 1080 m water depth in the Faroe-Shetland Channel, Gontikaki et al. (2011)
found extremely high variance in δ15N among Paraonidae and a mean higher than for Glyceridae.
Scalibregmatidae and Capitellidae were even more enriched in 15N, however, so the mean value
for Paraonidae may be more indicative of deep deposit feeding than of carnivory. In 3 and 6 d
incubations after pulse-chase application of labeled phytodetritus, paraonids showed moderate
uptake as a percentage of carbon biomass in the 3 d incubation and none in the 6 d. The most
parsimonious explanation of these background δ15N levels and incubation results is that the
paraonids had a wide range of feeding depths within the sediments. These results are quite
similar to Sweetman & Witte’s (2008a) for background δ15N values for paraonids and their in
situ pulse-chase experiments with labeled diatom detritus at the base of the Monterey Deep-Sea
Fan at 4100 m water depth. Sweetman & Witte (2008a) saw no label in 4 of 6 paraonids in their
incubations, one ingested a small amount, and one was heavily labeled and by itself responsible
for a large fraction of total label uptake. Sweetman & Witte (2008b) in samples and laboratory
pulse-chase experiments with samples from Korsfjorden, Norway, did not report ambient δ15N
values for paraonids but did see significant uptake of labeled diatom detritus by them.
Levin & Mendoza (2007) in two paraonids from a methane seep on the Unimak continental
margin observed δ15N about 4‰ higher than that for ampharetids but comparable to that for
spionids and well below that of glycerids. They calculated that 13% of paraonid tissue was
derived from methane. A northern Gulf of Mexico methane seep paraonid had a δ13C signature
also suggesting a mixture of phytoplankton- and methane-derived carbon, with its δ15N
indicating feeding near the base of the food web (Demoupoulos et al. 2010).
Guild membership
Paraonids are motile deposit feeders that appear to feed on both surface and subsurface
sediments even though they are rarely observed on the surface. We believe that, absent a recent
pulse of phytodetritus, subsurface feeding is the more common mode.
Research questions and opportunities
• Experimental tests of site selectivity could be informative, controlling for organic content and
grain size-frequency distributions.
• It is unknown how characterisitic of paraonids the spiral traces of P. fulgens may be.
• There are few behavioral observations on species other than P. fulgens.
References
Aguirrezabalaga F, Gil J. 2009. Paraonidae (Polychaeta) from the Capbreton Canyon (Bay of
Biscay, NE Atlantic) with the description of eight new species. Sci. Mar. 73:631–66
Blair NE, Levin LA, DeMaster DJ, Plaia G. 1996. The short-term fate of fresh algal carbon in
continental slope sediments. Limnol. Oceangr. 41:1208–19
Blair NE, Levin LA, DeMaster DI, Plaia G, Martin C, et al. 2001. The biogeochemistry of
carbon in continental slope sediments: the North Carolina margin. In Organism-Sediment
Interactions, ed. JY Aller, SA Woodin, RC Aller, 243–62. Columbia: Univ. South Carolina
Press
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Blake JA. 1994. Vertical distribution of benthic infauna in continental slope sediments off Cape
Lookout, North Carolina. Deep-Sea Res. Pt. II. 41:919–27
Bleidorn C. 2005. Phylogenetic relationships and evolution of Orbiniidae (Annelida, Polychaeta)
based on molecular data. Zool. J. Linn. Soc. 144:59–73
Demopoulos AWJ, Gualtieri D, Kovacs K. 2010. Food-web structure of seep sediment
macrobenthos from the Gulf of Mexico. Deep-Sea Res. Pt. II. 57:1972–81
Díaz-Castañeda V, Valenzuela-Solano S. 2009. Polychaete fauna in the vicinity of bluefin tuna
sea-cages in Ensenada, Baja California, Mexico. Zoosymposia 2:505–26
Gaston GR. 1987. Benthic Polychaeta of the Middle Atlantic Bight: feeding and distribution.
Mar. Ecol. Prog. Ser. 36:251–62
Gaston GR, McLelland JA, Heard RW. 1992. Feeding biology, distribution, and ecology of two
species of benthic polychaetes: Paraonis fulgens and Paraonis pygoenigmatica (Polychaeta:
Paraonidae). Gulf Res. Rep. 8:395–9
Glasby CJ. 2000. Family Paraonidae. See Beesley et al. 2000, pp. 82–4
Gontikaki E, Mayor DJ, Narayanaswamy BE, Witte U. 2011. Feeding strategies of deep-sea
sub-arctic macrofauna of the Faroe-Shetland Channel: Combining natural stable isotopes and
enrichment techniques. Deep-Sea Res. Pt. I 58:160–72
Giere O, Ebbe, B, Erséus C. 2008. Questa (Annelida, Polychaeta, Orbiniidae) from Pacific
regions—new species and reassessment of the genus Periquesta. Org. Divers. Evol. 7:304–19
Levin LA, Mendoza GF. 2007. Community structure and nutrition of deep methane-seep
macrobenthos from the North Pacific (Aleutian) margin and the Gulf of Mexico (Florida
escarpment). Mar. Ecol. 28:131–51
Mangion M, Borg JA, Thompson R, Schembri P.J. 2014. Influence of tuna penning activities on
soft bottom macrobenthic assemblages. Mar. Poll. Bull. 79:164–74
Martinez-Garcia E, Sanchez-Jerez P, Aguado-Giménez F, Ávila P, Guerrero A, et al. 2013. A
meta-analysis approach to the effects of fish farming on soft bottom Polychaeta assemblages
in temperate regions. Mar. Poll. Bull. 69:165–71
Penry DL, Jumars PA. 1990. Gut architecture, digestive constraints and feeding ecology of
deposit-feeding and carnivorous polychaetes. Oecologia 82:1–11
Purschke G, Tzetlin AB. 1996. Dorsolateral ciliary folds in the polychaete foregut: structure,
prevalence and phylogenetic significance. Acta Zool. 77:33–49
Risk MJ, Tunnicliffe VJ. 1978. Intertidal spiral burrows: Paraonis fulgens and Spiophanes
wigleyi in the Minas Basin, Bay of Fundy. J. Sed. Res. 48:1287–92
Rouse GW. 2001. Paraonidae Cerruti 1909a. In Rouse & Pleijel 2001, pp. 61–4
Rouse GW, Fauchald K. 1997. Cladistics and polychaetes. Zool. Scr. 26:139–204
Röder H. 1971. Gangsystem von Paraonis fulgens Levinsen 1883 (Polychaeta) in ökologischer,
ethologischer und actuopaläontologischer Sicht. Senck. Mar. 3:3–51
Schaff TR, Levin LA. 1994. Spatial heterogeneity of benthos associated with biogenic structures
on the North Carolina continental slope. Deep-Sea Res. Pt. II. 41:901–18
Sweetman AK, Witte U. 2008a. Response of an abyssal macrofaunal community to a
phytodetrital pulse. Mar. Ecol. Prog. Ser. 355:73–84
Sweetman AK, Witte U. 2008b. Macrofaunal response to phytodetritus in a bathyal Norwegian
fjord. Deep-Sea Res. Pt. I 55:1503–14
Thomas CJ, Blair NE. 2002. Transport and digestive alteration of uniformly 13C-labeled diatoms
in mudflat sediments. J. Mar. Res. 60:517–35
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Tzetlin A, Purschke G. 2005. Pharynx and intestine. Hydrobiologia 535:199–225
Zrzavý J, Říha P, Piálek L, Janouškovec J. 2009. Phylogeny of Annelida (Lophotrochozoa): totalevidence analysis of morphology and six genes. BMC Evol Biol. 9:189, 14 pp.
Parergodrilidae
Diversity and systematics
Parergodrilidae are known from two monotypic, interstitial genera, Parergodrilus and
Stygocapitella. Neither grows much longer than 1 mm. Molecular methods have revealed that
these diminutive species are related to orbiniids (Bleidorn et al. 2003, Hall et al. 2004, Jördens
et al. 2004, Bleidorn 2005) and that there may be several cryptic species hidden within one name
(Schmidt & Westheide 2000).
Habitat
Parergodrilus heideri is found in damp terrestrial soils (Rota 1997). Stygocapitella subterranea
is interstitial in the high intertidal and even further landward (Schmidt 1970).
Sensory and feeding structures
There are no appendages on the hemispherical prostomium. Stygocapitella carries a pair of
dorsal nuchal organs at the posterior of the prostomium, but Parergodrilus lacks them entirely.
The peristomium is a complete ring (Rouse 2001). P. heideri feeds with a ventral pharynx and
employs a large, distally expanded, adhesive tongue in ingesting particles (Purschke 1987,
Rota 1997). Compared with other meiofaunal polychaetes (e.g., Protodrilidae, Saccocirridae),
the pharyngeal muscle is much smaller in Stygocapitella and appears to be partially replaced
with a large gland; in Parergodrilus, the muscle is absent, and the gland is larger than that of
Stygocapitella (Tzetlin & Purschke 2005, Purschke 1987). In contrast to many other small
polychaetes, both species lack cilia in the buccal cavity (Purschke 1999). Cilia are also absent
from the body surface, which is covered with thick cuticle. This absence or reduction of cilia is
likely an adaptation to a semi-terrestrial or terrestrial lifestyle, respectively (Purschke 1999).
Motility
There are no published data on motility.
Illustrations
Purschke (1999) shows SEM images of external morphology and chaetae of both species.
Feeding
Diets of neither genus are known, but the size of the adults argues that they must ingest labile
organic material.
Guild membership
We presume that they are motile interstitially and feed on labile materials.
Research opportunities
• Any data on feeding or motility would be the first.
• Apparent convergence with Clitellata makes a comparison of terrestrial lifestyles interesting.
References
Bleidorn C. 2005. Phylogenetic relationships and evolution of Orbiniidae (Annelida, Polychaeta)
based on molecular data. Zool. J. Linn. Soc. 144:59–73
Bleidorn C, Vogt L, Bartolomaeus T. 2003. New insights into polychaete phylogeny (Annelida)
inferred from 18S rDNA sequences. Mol. Phylogen. Evol. 29:279–88
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Hall KA, Hutchings PA, Colgan DJ. 2004. Further phylogenetic studies of the Polychaeta using
18S rDNA sequence data. J. Mar. Biol. Ass. UK 84:949–60
Jördens J, Struck T, Purschke G. 2004. Phylogenetic inference regarding Parergodrilidae and
Hrabeiella periglandulata (“Polychaeta,” Annelida) based on 18S rDNA, 28S rDNA and
COI sequences. J. Zool. Syst. Evol. Res. 42:270–80
Purschke G. 1987. Anatomy and ultrastructure of ventral pharyngeal organs and their
phylogenetic importance in Polychaeta (Annelida). III. The pharynx of the Parergodrilidae.
Zool. Jahrb., Abt. Anat. Ontog. Tiere 115:331–62
Purschke G. 1999. Terrestrial polychaetes—models for the evolution of the Clitellata (Annelida)?
Hydrobiologia 406:87–99
Rota E. 1997. First Italian record of the terrestrial polychaete Parergodrilus heideri reisinger,
with anatomical and ecological notes. Ital. J. Zool. 64:91–6
Rouse GW. 2001. Parergodrilidae Reisinger, 1925 and Hrabeiella Pizl and Calupsky, 1984. See
Rouse & Pleijel 2001, pp. 290–2
Schmidt H, Westheide W. 2000. Are the meiofaunal polychaetes Hesionides arenaria
and Stygocapitella subterranea true cosmopolitan species?—results of RAPD-PCR
investigations. Zool Scr. 29:17–27
Schmidt P. 1970. Zonation of the interstitial polychaete Stygocapitella subterranea
(Stygocapitellidae) in European sandy beaches. Mar. Biol. 7:319–23
Tzetlin A, Purschke G. 2005. Pharynx and intestine. Hydrobiologia 535:199–225
Pectinariidae, Terebelliformia
Diversity and systematics
Pectinariidae comprise about 60 species in five genera (Hutchings & Peart 2002) and are one
of the 5 families that constitute Terebelliformia. Colgan et al. (2001) based on molecular
genetic data suggested that Pectinariidae fall in a clade with Ampharetidae and out of a clade
that includes Alvinellidae, Terebellidae and Trichobranchidae. Their study did not include the
terebellid genus Pista, however, which Rousset et al. (2004) found to be very closely related to
Pectinaria.
Pectinariids are medium-sized worms, typically 1 - 10 cm long as adults (Hutchings & Peart
2002). They have characteristic golden paleae extending anteriorly from a flattened operculum.
Their rigid, conical tubes constructed of sand grains give them their common name, “ice cream
cone worms,” and are oriented with the wider, anterior end down in the sediment.
Habitat
Pectinariids inhabit sediments and require a range of sand sizes because worms use ever-larger
grains for tube construction as they grow (Busch & Loveland 1975). Although they are most
abundant at shelf depths, pectinariids are common members of bathyal communities and have
been reported from at least as deep as 3400 m (Levin et al. 2000).
Sensory and feeding structures
A pro- and peristomium are not identifiable in adults. The golden paleae characteristic of
pectinariids are modified notochaetae from the first segment (fused to the head) and extend
anteriorly to form a rake-like structure used to loosen grains. Immediately ventral to the paleae
is a cephalic veil (tentacular membrane) that is taxonomically important in unifying the group
and in distinguishing species (Hutchings & Peart 2002) but whose function has not, to our
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knowledge, been studied—nor has pharyngeal eversibility. Nuchal organs are present on the
membrane lateral to the mouth; eyes occur in juveniles of some species (Rouse 2001). Grooved,
ciliated, buccal tentacles or palps are attached to the ventral surface of the cephalic veil rather
than to an “upper lip” as in other terebelliforms, and the tentacles do not seem to be retractable
into the buccal cavity (Zhadan & Tzetlin 2002). Like other Terebelliformia, pectinariids have a
muscular ventral pharynx with a ciliated buccal cavity (Zhadan & Tzetlin 2002).
Motility
F&J reviewed evidence of particle selection for tube building and of alternative burrow structure
based on ambient sediment properties. In sands having a low angle of repose, pectinariids had
one surface opening, but in muddier sediments they had two. Because of this difference in the
mechanics of slumping between sands and muds, F&J hypothesized that pectinariids in coarsergrained, nutrient-poor sediment exhibit greater motility than those in fine-grained sediments.
Dobbs & Scholly (1986) found that in fine-grained sediments, Lagis koreni established U- or
V-shaped burrows that it maintained through irrigation and with its tentacles, i.e., engaged in
funnel feeding with the feeding site and defecation mound laterally displaced.
In Cistenides gouldii, Busch & Loveland (1975) documented preference for large grains in
tube construction and for larger grains as tube length and worm size increased. The species was
absent from well sorted, fine or coarse sediments with median grain sizes < 40 or > 500 µm.
Busch & Loveland (1975) also pointed out exponential increase in tube weight with tube length
as a potential drawback of conical tube construction. Bamber (1984) observed modest selection
against roughly spherical fly ash particles in tube construction by L. koreni. This species has
some capacity to move through the water column as a young juvenile by secreting a high-drag,
mucus streamer (Olivier et al. 1996) in a manner reminiscent of post-larval migration in tellinid
bivalves (Cummings et al. 1993). Nonlinear increase in tube weight with tube length likely
limits this mechanism to very small, post-larval pectinariids.
Illustrations
Busch & Loveland (1975) show photographs of tubes. Hutchings and Peart (2002) include
stippled line drawings of external morphology in several species. Rouse & Pleijel (2001) include
a detailed painting of Pectinaria and its tube.
Feeding
Pectinariids are head-down deposit feeders that use paleae for scraping and tentacles for feeding
(F&J). More than half of collected sediments pass over the dorsum as pseudofeces (F&J), and
both pseudofeces and feces are ejected through the open tip of the cone onto the sediment-water
interface. Selectivity for grains larger than the median grain size is well established (F&J, Ronan
1977, Whitlatch & Weinberg 1982, Dobbs & Scholly 1986). Dobbs & Scholly (1986) suggested
that selection for larger particles enabled worms to preferentially ingest fecal pellets from the
co-occurring bivalve Abra alba, which were abundant in gut contents. Dobbs & Scholly (1986)
measured defecation and pseudodefecation rates (dry weight per time) of L. koreni maintained
in laboratory aquaria and found that worms in fine-grained sediment exhibited higher ratios of
pseudodefecation:defecation than those in coarser sediments, although individuals exhibited
considerable variability over short periods. Rates on both sediments continued to increase for
at least the first 89 h, and changes were more dramatic on finer sediments. Through the first 119
h pseudofecal production in the fine sediments was significantly greater. It is not clear whether
food quality was changing or digestion was adapting or both. Feeding rates varied with both
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Jumars, Dorgan & Lindsay
07 November 2014
animal and ambient grain sizes as well as bacterial density but were generally higher on coarser
sediments (Whitlatch & Weinberg 1982).
Dobbs & Scholly (1986) observed that in fine-grained sediments Lagis koreni would
sometimes engage in surface deposit feeding by extending its tentacles onto the sediment
surface, and that its inhalant respiratory currents sometimes drew fine sediments through the
cone tip and down into the feeding cavern. They described particle retrieval as “sloppy” because
fecal pellets, plant detritus, and organic aggregates were observed to fall from the tentacles
into the feeding cavity and were not always retrieved. L. koreni also showed diel periodicity in
activity level, greater in the dark (Nicolaidou 1988). Fries et al. (1999) observed that fecal and
pseudofecal mounds of C. gouldii could trigger ripple formation and migration, processes with
potential feedback to its food supply.
Ahrens et al. (2001) confirmed surfactant activity in the digestive fluids of C. gouldii,
a unifying characteristic of deposit-feeder digestion, and found that it was highly effective
in causing rapid desorption of sediment-bound, hydrophobic contaminants. Efficiency of
desorption and subsequent absorption was lower than that of the nereidid Alitta succinea,
however, attributed to lower gut-fluid surfactancy of C. gouldii (Ahrens et al. 2001).
C. gouldii in separate studies from various estuaries on Cape Cod apparently fed low
in the food web (low δ15N) and had δ13C indicative of feeding on detritus derived from
microphytobenthos or macroalgae (Carmichael et al. 2004, Martinetto et al. 2006). C.
hyperborea from 15 m depth in Kongsfjorden, Svalbard, also showed the lowest δ15N of
polychaetes sampled, consistent with feeding on fresh detritus (Kędra et al. 2012). In a
Posidonia bed 5 - 8 m water depth off Mallorca Island, Lagis koreni also showed the lowest δ15N
value of any polychaete (Deudero et al. 2011). Follow-up work (Deudero et al. 2014) continued
to show 15N levels in L. koreni more compatible with herbivory and surface deposit feeding
than with subsurface deposit feeding. Interestingly, Maldane sarsi (Maldanidae), another headdown deposit feeder, in Kongsfjorden, Svalbard, at 15 m water depth had the highest δ15N of
polychaetes sampled, ~1.5 trophic levels higher than C. hyperborea, indicating substantial
differences in feeding (Kędra et al. 2012). Their low δ15N values suggest that these pectinariids
are likely feeding on near-surface sediments, supporting Dobbs & Scholly’s (1986) observations
of surface and funnel feeding. The trophic position of C. hyperborea in the Chukchi Sea is more
difficult to resolve from the δ15N values given by Iken et al. (2010) because the range among
species is limited, but it appears higher than that of Chaetozone setosa (Cirratulidae), near that of
Notomastus latericeus (Capitellidae) and below that of Nephtys ciliata (Nephtyidae) consistent
with subsurface deposit feeding. Pectinaria hyperborea from sediments at 30 - 60 m water depth
in the northern Bering Sea had δ15N about 6 ‰ higher than that of surrounding sediments, but
lipid analysis suggested that this enrichment was due to selection by the worms for bacterially
reworked organic matter rather than to carnivory (North et al. 2014).
Guild membership
All are head-down deposit feeders, although there seems to be considerable variability in the
depth of feeding. There are clear cases of funnel feeding and of subsurface deposit feeding.
Motility can be punctuated by bouts of funnel feeding (discrete motility) or can be more
continuous. Effective depth of feeding (funnel or subsurface) and motility vary both with species
and with sediment composition and transport.
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07 November 2014
Research questions and opportunities
• Mechanics of the paleae and cephalic veil and the mechanisms of selection for large particles
remain to be analyzed. The model of Jumars et al. (1982) suggests that strong adhesives
could produce a bias toward larger particles.
• Are low or variable δ15N values related to selection for large particles?
• The relationships of speed and frequency of movement to food quality and sediment
mechanics have not been quantified.
• Effects of tube weight and size on burrowing costs and mechanics remain to be analyzed.
References
Ahrens MJ, Hertz J, Lamoureux EM, Lopez GR, McElroy AE, Brownawell BJ. 2001. The role of
digestive surfactants in determining bioavailability of sediment-bound hydrophobic organic
contaminants to 2 deposit-feeding polychaetes. Mar. Ecol. Prog. Ser. 212:145–57
Bamber RN. 1984. The utilization of fly ash by two tube-building polychaetes. J. Exp. Mar. Biol.
Ecol. 81:107–13
Busch DA, Loveland RE. 1975. Tube-worm-sediment relationships in populations of Pectinaria
gouldii (Polychaeta: Pectinariidae) from Barnegat Bay, New Jersey, USA. Mar. Biol.
33:255–64
Carmichael RH, Rutecki D, Annett B, Gaines E, Valiela I. 2004. Position of horseshoe crabs in
estuarine food webs: N and C stable isotopic study of foraging ranges and diet composition.
J. Exp. Mar. Biol. Ecol. 299:231–53
Colgan DJ, Hutchings PA, Brown S. 2001. Phylogenetic relationships within the
Terebellomorpha. J. Mar. Biol. Ass. UK 81:765–73
Cummings VJ, Pridmore RD, Thrush SF, Hewitt JE. 1993. Emergence and floating behaviours of
post-settlement juveniles of Macomona liliana (Bivalvia: Tellinacea). Mar. Freshw. Behav.
Phy. 24:25–32
Deudero S, Box A, Alós J, Arroyo NL, Marbà N. 2011. Functional changes due to invasive
species: Food web shifts at shallow Posidonia oceanica seagrass beds colonized by the alien
macroalga Caulerpa racemosa. Estuar. Coast. Shelf Sci. 93:106–16
Deudero S, Box A, Vázquez-Luis M, Arroyo NL. 2014. Benthic community responses to
macroalgae invasions in seagrass beds: Diversity, isotopic niche and food web structure at
community level. Estuar. Coast. Shelf Sci. 142:12–22
Dobbs FC, Scholly TA. 1986. Sediment processing and selective feeding by Pectinaria koreni
(Polychaeta: Pectinariidae). Mar. Ecol. Prog. Ser. 29:165–76
Fries JS, Butman CA, Wheatcroft RA. 1999. Ripple formation induced by biogenic mounds.
Mar. Geol. 159:287–301
Hutchings P, Peart R. 2002. A review of the genera of Pectinariidae (Polychaeta) together with a
description of the Australian fauna. Rec. Aust. Mus. 54:99–127
Iken K, Bluhm B, Dunton K. 2010. Benthic food-web structure under differing water mass
properties in the southern Chukchi Sea. Deep-Sea Res. Pt. II 57:71–85
Jumars PA, Self RFL, Nowell ARM. 1982. Mechanics of particle selection by tentaculate deposit
feeders. J. Exp. Mar. Biol. Ecol. 64:47-70
Kędra M, Kuliński K, Walkusz W, Legeżyńska J. 2012. The shallow benthic food web structure
in the high Arctic does not follow seasonal changes in the surrounding environment. Estuar.
Coast. Shelf Sci. 114:183–91
Levin LA, Gage JD, Martin C, Lamont PA. 2000. Macrobenthic community structure within and
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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beneath the oxygen minimum zone, NW Arabian Sea. Deep-Sea Res. Pt. II. 47:189–226
Martinetto P, Teichberg M, Valiela I. 2006. Coupling of estuarine benthic and pelagic food webs
to land-derived nitrogen sources in Waquoit Bay, Massachusetts, USA. Mar. Ecol. Prog. Ser.
307:37–48
North CA, Lovvorn JR, Kolts JM, Brooks ML, Cooper LW, et al. 2014. Deposit-feeder diets
in the Bering Sea: potential effects of climatic loss of sea ice-related microalgal blooms.
24:1525–42
Nicolaidou A. 1988. Notes on the behaviour of Pectinaria koreni. J. Mar. Biol. Ass. UK 68:55–9
Olivier F, Desroy N, Retière C. 1996. Habitat selection and adult-recruit interactions in
Pectinaria koreni (Malmgren) (Annelida: Polychaeta) post-larval populations: Results of
flume experiments. J. Sea Res. 36:217–26
Ronan TE Jr. 1977. Formation and paleontologic recognition of structures caused by marine
annelids. Paleobiology 3:389–403
Rouse GW. 2001. Pectinariidae de Quatrefages, 1866. See Rouse & Pleijel 2001, pp. 243–5
Rousset V, Rouse GW, Siddall ME, Tillier A, Pleijel F. 2004. The phylogenetic position of
Siboglinidae (Annelida) inferred from 18S rRNA, 28S rRNA and morphological data.
Cladistics 20:518–33
Whitlatch RB, Weinberg JR. 1982. Factors influencing particle selection and feeding rate in the
polychaete Cistenides (Pectinaria) gouldii. Mar. Biol. 71:33–40
Zhadan AE, Tzetlin AB. 2002. Comparative morphology of the feeding apparatus in the
Terebellida (Annelida: Polychaeta). Cah. Biol. Mar. 43:149–64
Phascolosomatidae, Sipuncula
Diversity and systematics
After the revision by Kawauchi et al. (2012), Phascolosomatidae comprises two genera,
Phascolosoma with about 20 species, and Apionosma with about 4. There is evidence of high
levels of genetic differentiation, however, between widely separated populations currently under
one species name (Kawauchi & Giribet 2010). Phascolosomatids are small to medium-sized
sipunculans, with trunk lengths 2 - 12 cm (Kawauchi et al. 2012). Rice et al. (2012) noted
that Phascolosoma turnerae is long lived, individual specimens having survived > 20 yr in the
laboratory. Recent sequencing of the complete mitochondrial genome of P. esculenta supports
inclusion of Sipuncula within Annelida (Shen et al. 2009).
Habitat
Most Phascolosomatidae live in burrows, crevices or sandy pockets in shallow, warm waters.
Their principal biotope is dead coral reef (Murina 1984). Three species are reported from
bathyal depths, A. capitatum, P. saprophagicum, and P. turnerae. A. capitatum is known
from bathyal and abyssal depths in the northeast Atlantic (Gibbs 1986). P. turnerae is found
in burrows in submerged wood, oriented orthogonal to the grain, at bathyal depths in the
Florida Straits and northern Gulf of Mexico (Rice 1985). It was recently found together with
wood remains at bathyal depths in the northwestern Mediterranean and may be even more
cosmopolitan (Saiz et al. 2014). It is also found burrowed in sediments at the base of tubeworm
colonies and mussel beds on methane and oil seeps east of the Lesser Antilles and in the northern
Gulf of Mexico (Olu et al. 1996, MacAvoy et al. 2005). More recently, P. aff. turnerae has been
collected from carbonate crusts at bathyal cold seeps in the Levantine Basin of the Mediterranean
Sea (Rubin-Blum et al. 2014). P. saprophagicum is known from burrows in whale bones at
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Jumars, Dorgan & Lindsay
07 November 2014
bathyal depths in the southwest Pacific (Gibbs 1987). At the opposite extreme, P. arcuatum
occurs in the upper intertidal of mangrove swamps from India to Queensland (Green & Dunn
1976). Green (1975) described it as semi-terrestrial.
Sensory and feeding structures
The introvert carries recurved hooks in regularly spaced rings (for scraping) except in A.
trichocephalus, where they are absent (Kawauchi et al. 2012). Short tentacles are confined to
a crescent around a conical or hemispherical, dorsal nuchal organ (Cutler 1994). Eyespots are
generally present as variably developed ocular tubes (Hermans & Eakin 1969, Cutler 1994).
The introvert in Phascolosoma spp. is often about the same length as the trunk, whereas in
Apionosoma it is roughly 3 times as long (Cutler 1994). As in other sipunculans, the mouth and
anus are closely juxtaposed, enabling the double helical twisting of a long gut within the trunk
and setting up an ideal topology for osmotic counterflows.
Motility
Cutler (1994) suggested that species in this group are relatively sessile, but we know of no
studies of post-settlement motility.
Illustrations
Edmonds (2000, Fig. 5.15) and Cutler (1994) provide line drawings of external morphology.
Many informative photographs are available through Google Images under the search term
{Phascolosoma}. On 8 April 2014, images of four species of Phascolosoma were available at
<http://tolweb.org/images/Sipuncula/2487>, but none in life position.
Feeding
Rice (1976, pp. 126–7) observed P. perlucens placed with their burrows intact in an aquarium to
deposit feed on the coral surface but also to scrape with their external introvert hooks. According
to Murina (1984) and Cutler (1994), the majority of species in this group use the introvert to
scrape algae, small invertebrates and detritus from surrounding surfaces.
Rice (1985, p. 59) described the gut contents of P. turnerae taken from burrows in decaying
wood as: “a whitish gray fine particulate matter believed to be a fine sediment.” A few fragments
of calcareous material, foraminiferans, and a few wood fibers were found among the particulate
matter and could have originated from within the sediment surrounding the submerged wood or
from the surface of the wood itself. Rice et al. (2012) concluded that “members of P. turnerae
seem to consume bacteria removed from the fibers in which they live.” Gibbs (1987) described
P. saprophagicum from whale bones trawled from 880 m water depth. He noted oil droplets
among the gut contents.
Roesijadi et al. (1978) included P. agassizii in a study of uptake of hydrocarbons from
contaminated sediments. Like the other deposit feeder in the experiments (a tellinid bivalve),
and consistent with uptake patterns now known from many deposit feeders (Mayer et al. 2001),
it showed rapid uptake. P. perlucens in Costa Rica showed similarly high uptake (Spongberg
2006). Chen & Lu (2007) tested activities of cellulase, amylase and lipase in deposit-feeding P.
esculenta. Their activities decreased in that same order. High cellulase activity hints at potential
capability to digest refractory components of detritus and possibly long gut retention times.
Stable isotopic evidence from cold seeps indicates considerable variety in diet for P.
turnerae, with 15N usually but not always enriched relative to other surface deposit feeders
(MacAvoy et al. 2005, 2008; Cordes et al. 2010; Becker et al. 2013). This result seems likely
if P. turnerae scrapes local microbial films and other fouling organisms from the tube fields in
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Jumars, Dorgan & Lindsay
07 November 2014
which it resides, conferring a degree of omnivory.
Stable isotopic evidence for Phascolosoma spp. from non-seep habitats also generally
indicates feeding on some combination of detritus and higher trophic-level food sources. P.
granulatum from an intertidal vermetid gastropod reef in Sicily had δ15N about one trophic level
higher than a sabellid at the site and close to those of nereidid and eunicid species (Columbo
et al. 2013). These results are consistent with scraping of detritus and fouling organisms from
the surrounding vermetid tubes. We would predict a similar result for stable isotopic analyses
of individuals resident in submerged wood and eating a mixture of scraped bacteria and other
fouling organisms. Rubin-Blum et al. (2014) documented a distinctive microbial assemblage
on and in P. aff. turnerae different from that of surrounding biofilms. Worm-associated bacteria
included epibiotic, filamentous forms.
In stable-isotope studies of food webs in southeast Asian mangrove swamps, both P.
arcuatum and P. nigrescens had 13C signatures consistent with feeding on material derived from
mixtures of mangrove leaves and microalgae (Rodelli et al. 1984, Herbon 2011, Tu et al. 2012;
Kon et al. 2010). 15N content for both species was higher than expected for a single trophic level
above the detrital resource (Herbon 2011, Tu et al. 2012, Kon et al. 2010). Given the lack of
suitable capture appendages, we doubt Herbon’s (2011) suggestion of feeding by P. arcuatum
on other polychaetes but find the results consistent with a degree of omnivory. Kon et al. (2010)
classified P. nigrescens as a subsurface deposit feeder, but Kon et al. (2011) classified it as a
surface deposit feeder; the basis of neither determination was given.
Guild membership
We infer that most species are discretely motile, but large individuals burrowed into calcium
carbonate or wood may become effectively sessile. All species appear capable of surface deposit
feeding and (except for A. trichocephalus) scraping, the latter conferring a degree of omnivory.
Extent of engagement in subsurface deposit feeding is unknown.
Research questions and opportunities
• No observational or experimental data appear to exist on effects of hook-wielding
phascolosomatids on surrounding fouling, infaunal and bacterial communities.
• Gut fluid and particle residence times are unknown. They may be particularly long in species
living in the high intertidal.
• Stable isotopic measurements and lipid profiles on P. turnerae burrowed in wood and P.
saprophagicum from whale bones would be informative.
• Feeding experiments are in order on deposit-feeding species to test whether high δ15N values
can result from digestion of refractory organic material and whether Phascolosoma spp.
engage in subsurface deposit feeding.
• Does variation in associated microbiota with P. turnerae across this phascolosomatid’s varied
habitats and substrata underlie its broad habitat range, or have multiple species been included
under one name (Rubin-Blum et al. 2014)?
• There appear to be no feeding data on Apionosoma spp.
References
Becker EL, Cordes EE, Macko SA, Lee RW, Fisher CR. 2013. Using stable isotope compositions
of animal tissues to infer trophic interactions in Gulf of Mexico lower slope seep
communities. PLoS ONE 8:e74459, 16 pp.
Chen XX, Lu CY. 2007. Effects of four metal ions on digestive enzyme activities of
Phascolosoma esculenta. J. Oceanogr. Taiwan Strait 26:528–35
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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doi: 10.1146/annurev-marine-010814-020007
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Jumars, Dorgan & Lindsay
07 November 2014
Colombo F, Costa V, Dubois SF, Gianguzza P, Mazzola A, Vizzini S. 2013. Trophic structure of
vermetid reef community: High trophic diversity at small spatial scales. J. Sea Res. 77:93–9
Cordes EE, Becker EL, Fisher CR. 2010. Temporal shift in nutrient input to cold-seep food webs
revealed by stable-isotope signatures of associated communities. Limnol. Oceangr. 55:2537–48
Cutler EB. 1994. The Sipuncula: Their Systematics, Biology and Evolution. Ithaca, NY: Cornell
Univ. Press
Edmonds SJ. 2000. Phylum Echiura. See Beesley et al. 2000, pp. 353–74
Gibbs PE. 1986. The taxonomy of some little-known Sipuncula from the north-east Atlantic
region including new records. J. Mar. Biol. Ass. UK 66:335–41
Gibbs PE. 1987. A new species of Phascolosoma (Sipuncula) associated with a decaying whale’s
skull trawled at 880 m depth in the south-west Pacific. NZ J. Zool. 14:135–7
Green WA. 1975. Phascolosoma lurco: A semi-terrestrial sipunculan. In Proceedings of the
International Symposium on the Biology of the Sipuncula and Echiura, Vol. I, ed. ME Rice,
M Todorović, pp. 267–80. Beograd, Yugoslavia: Naučno Delo
Green JP, Dunn DF. 1976. Chloride and osmotic balance in the euryhaline sipunculid
Phascolosoma arcuatum from a Malaysian mangrove swamp. Biol. Bull. 150:211–21
Herbon CM. 2011. Spatial and temporal variability in benthic food webs of the mangrove fringed
Segara Anakan Lagoon in Java, Indonesia. PhD thesis. Univ. Bremen: Germany
Hermans CO, Eakin RM. 1969. Fine structure of the cerebral ocelli of a sipunculid,
Phascolosoma agassizii. Z. Zellforsch. Mik. Ana. 100:325–39
Kawauchi GY, Giribet,G. 2010. Are there true cosmopolitan sipunculan worms? A genetic
variation study within Phascolosoma perlucens (Sipuncula, Phascolosomatidae). Mar. Biol.
157:1417–31
Kawauchi GY, Sharma PP, Giribet G. 2012. Sipunculan phylogeny based on six genes, with a
new classification and the descriptions of two new families. Zool. Scr. 41:186–210
Kon K, Kurokura H, Tongnunui P. 2010. Effects of the physical structure of mangrove vegetation
on a benthic faunal community. J. Exp. Mar. Biol. Ecol. 383:171–80
Kon K, Kurokura H, Tongnunui P. 2011. Influence of a microhabitat on the structuring of the
benthic macrofaunal community in a mangrove forest. Hydrobiologia 671:205–16
MacAvoy SE, Fisher CR, Carney RS, Macko SA. 2005. Nutritional associations among fauna at
hydrocarbon seep communities in the Gulf of Mexico. Mar. Ecol. Prog. Ser. 292:51–60
MacAvoy SE, Morgan E, Carney RS, Macko SA. 2008. Chemoautotrophic production
incorporated by heterotrophs in Gulf of Mexico hydrocarbon seeps: an examination of
mobile benthic predators and seep residents. J. Shellfish Res. 27:153–61
Mayer LM, Weston DP, Bock MJ. 2001. Benzo[a]pyrene and zinc solubilization by digestive
fluids of benthic invertebrates—a cross-phyletic study. Environ. Toxicol. Chem. 20:1890–900
Murina G-V. 1984. Ecology of Sipuncula. Mar. Ecol. Prog. Ser. 17:1–7
Olu K, Sibuet M, Harmegnies F, Foucher J-P, Fiala-Medioni A. 1996. Spatial distribution of
diverse cold seep communities living on various diapiric structures of the southern Barbados
prism. Prog. Oceanogr. 38:347–76
Rice ME. 1976. Sipunculans associated with coral communities. Micronesica 12:119–32
Rice ME. 1985. Description of a wood-dwelling sipunculan, Phascolosoma turnerae, new
species. Proc. Biol. Soc. Wash. 98:54–60
Rice ME, Reichardt HF, Piraino J, Young CM. 2012. Reproduction, development, growth, and
the length of larval life of Phascolosoma turnerae, a wood-dwelling deep-sea sipunculan.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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07 November 2014
Invertebr. Biol. 131:204–15
Rodelli MR, Gearing JN, Gearing PJ, Marshall N, Sasekumar A. 1984. Stable isotope ratio as a
tracer of mangrove carbon in Malaysian ecosystems. Oecologia 61:326–33
Roesijadi G, Anderson JW, Blaylock JW. 1978. Uptake of hydrocarbons from marine sediments
contaminated with Prudhoe Bay crude oil: Influence of feeding type of test species and
availability of polycyclic aromatic hydrocarbons. J. Fish. Res. Board Can. 35:608–14
Rubin-Blum M, Shemesh E, Goodman-Tchernov B, Coleman DF, Ben-Avraham Z, et al.
2014. Cold seep biogenic carbonate crust in the Levantine Basin is inhabited by burrowing
Phascolosoma aff. turnerae, a sipunculan worm hosting a distinctive microbiota. Deep-Sea
Res. Pt. I 90:17–26
Saiz JI, Cartes JE, Mamouridis V, Mecho A, Pancucci-Papadopoulou MA. 2014. New records
of Phascolosoma turnerae (Sipuncula: Phascolosomatidae) from the Balearic Basin,
Mediterranean Sea. Mar. Biodivers. Rec. 7:e16, 5 pp.
Shen X, Ma X, Ren J, Zhao F. 2009. A close phylogenetic relationship between Sipuncula and
Annelida evidenced from the complete mitochondrial genome sequence of Phascolosoma
esculenta. BMC Genomics 10:136, 11 pp.
Spongberg AL. 2006. PCB concentrations in intertidal sipunculan (Phylum Sipuncula) marine
worms from the Pacific coast of Costa Rica. Rev. Biol. Trop. 54(Suppl. 1):27–33
Tu NPC, Ha NN, Matsuo H, Tuyen BC, Tanabe S, Takeuchi I. 2012. Biomagnification profiles of
trace elements through the food web of an integrated shrimp mangrove farm in Ba Ria Vung
Tau, South Vietnam. Am. J. Environ. Sci. 8:117–29
Pholoidae, Aphroditiformia
Diversity and systematics
Pholoidae currently comprise 23 species distributed among 5 genera, 3 of them monotypic.
Pholoe contains 15 of the species. Pettibone’s (1992) revision treated all 5 genera. Pholoids are
at risk of falling within Sigalionidae based on future molecular genetic findings (Norlinder et al.
2012). Even if they were synonymized, however, we would separate them out as a morphotype.
Pholoidae are stiff, small, flattened hemispheroidal worms, usually 0.2 - 3 cm long and carry
elytra bearing distinctive, concentric circles.
Habitat
Pholoids occupy a wide diversity of habitats but are most common on soft substrata at shelf
and bathyal depths, where they can be community dominants (e.g., Grassle & Maciolek 1992,
Heip & Craeymeersch 1995). Some extend into the abyss (Böggemann 2009). Abundances
can approach 2 000 m-2 (Cañete et al. 1999). Most species are epifaunal, but some will burrow
near the sediment-water interface, and still others live in crevices in hard substrata or interstices
in mixed sediments. Metaxypsama uebelackerae is strictly interstitial (Pleijel 2001). Pholoe
minuta occurs free living but also as a commensal in the burrow of Echiurus echiurus (Rachor &
Bartel 1981).
Sensory and feeding structures
The prostomium is small and rounded, its posterior margin overlapped by the first segment. The
peristomium is limited to lips (Pleijel 2001). Small lateral antennae may be present. The medial
dorsal antenna may be anterior or occipital. An antenna-like ventral tubercle is often present
ventral to the medial dorsal antenna. Nuchal organs are not known (Pleijel 2001). Two pairs of
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Jumars, Dorgan & Lindsay
07 November 2014
eyes are often present. Despite not being fused, four hooked teeth that flare basally for muscle
attachment operate as one pair of jaws opening and closing dorsoventrally. They are associated
with glands producing secretions whose functions have not been explored (Wolf 1986), and they
are carried within a muscular, axial, eversible pharynx tipped, when everted, with papillae.
Motility
Pleijel’s (1983) aquarium observations indicate that Pholoe minuta is an actively hunting
predator that will burrow in search of sedentary prey. Other information on motility is lacking.
Illustrations
Pleijel (2001) provides an informative collection of photographs of various species. Padovanni
& Amaral (2013) present an informative combination of light and scanning electron micrographs
of Pholoe microantennata. Pettibone’s (1992) line drawings give a good idea of morphological
diversity in the family.
Feeding
The most studied species is Pholoe minuta. Pleijel (1983) analyzed gut contents and fecal
pellets from individuals dredged and sledged from 20 - 35 m water depth in the Koster area and
near the mouth of ldefjorden, Sweden. A total of 93 worms were analyzed for gut contents,
and 149 were subjected to fecal analyses. Identifiable prey were found in only about 1/3 of the
specimens. Sedentary polychaetes were prominent prey in both locations, especially Prionospio
sp., sometimes including portions of the tube. Foraminiferans were the dominant prey in fecal
samples from specimens collected in Idefjorden. These studies documented one instance of
cannibalism. Pleijel (1983) also conducted aquarium observations documenting three successful
attacks on Prionospio malmgreni that resulted in ingestion of only part of each worm. Pholoe
minuta is a hunting predator on sedentary polychaetes, foraminiferans and assorted meiofauna
(Pleijel 1983). Heffernan (1988) analyzed fluid from the putative venom gland of Pholoe minuta
and found it to contain the amino acid tryptophan, but function of the secretions has not been
established.
The majority of stable isotope values are completely consistent with carnivory. δ15N
values for P. minuta taken from a 13 m deep station in the southern North Sea are close to
those of Anaitides mucosa (Phyllodocidae) and Glycera spp. (Glyceridae, van Oevelen et
al. 2009). Values for Pholoe sp. collected at 39 m water depth in the Chukchi Sea similarly
indicate carnivory (Iken et al. 2010). So do Kędra et al.’s (2012) values for Pholoe assimilis
from 15 m water depth in Kongsfjorden, Svalbard, but they shift toward less enrichment in the
summer, suggesting that its prey species then feed more directly on fresh phytodetritus. Fatty
acid composition in P. assimilis from the same area is consistent with carnivory on prey that
utilize both diatoms and bacteria (Legeżyńska et al. 2014). Sweetman et al. (2013) studied
hydrothermal vent sites at 500 - 600 m water depths in the Arctic. Most δ15N values they
observed in P. assimilis were consistent with carnivory, but one was far less enriched, suggesting
a more direct link to vent microbes.
Guild membership
We regard pholoids as epifaunal and shallowly burrowing carnivores using a pair of jaws within
an eversible pharynx to ingest prey and pieces of prey. Pholoids at hydrothermal vents might be
able to feed on filamentous bacteria. Pholoe minuta apparently is a motile hunter; some other
species may sit and wait.
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Jumars, Dorgan & Lindsay
07 November 2014
Research questions and opportunities
• Motility remains to be quantified.
• Composition and functions of the secretions of the glands associated with the jaws remain to
be identified.
References
Böggemann M. 2009. Polychaetes (Annelida) of the abyssal SE Atlantic. Org. Divers. Evol.
9:251–428
Cañete JI, Leighton GL, Aguilera FF. 1999. Polychaetes from Aysén Fjord, Chile: distribution,
abundance and biogeographical comparison with the shallow soft-bottom polychaete fauna
from Antarctica and the Magellan Province. Sci. Mar. 63(Suppl. 1):243–52
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from quantitative bottom samples. Am. Nat. 139:313–41
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properties in the southern Chukchi Sea. Deep-Sea Res. Pt. II 57:71–85
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Arctic benthic community: how much can fatty acids tell? Mar. Biol. 161:821–36
Kędra M, Kuliński K, Walkusz W, Legeżyńska J. 2012. The shallow benthic food web structure
in the high Arctic does not follow seasonal changes in the surrounding environment. Estuar.
Coast. Shelf Sci. 114:183–91
Norlinder E, Nygren A, Wiklund H, Pleijel F. 2012. Phylogeny of scale-worms (Aphroditiformia,
Annelida), assessed from 18SrRNA, 28SrRNA, 16SrRNA, mitochondrial cytochrome c
oxidase subunit I (COI), and morphology. Mol. Phylogen. Evol. 65:490–500
Padovanni N, Amaral ACZ. 2013. New species of the scale worm genus Pholoe (Polychaeta:
Pholoidae) from southeast Brazil. Zootaxa 3710:485–97
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Phyllodocidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Phyllodocidae, Phyllodocida
Diversity and systematics
Phyllodocidae comprise about 400 species, with Phyllodoce as the most speciose genus. Eumida
sanguinea was recently shown to contain 10 cryptic species within just part of its described
range, implying a much larger number of species in the family (Nygren & Pleijel 2011). Adults
range from a few millimeters to about 1 m long (Pleijel 2001). Within Phyllodocida, the family
is closely related to glycerids (Struck et al. 2011). Molecular data suggest that the holopelagic
families Alciopidae, Typhloscolecidae, and Lopadorhynchidae are derived Phyllodocidae and
may be synonymized with Phyllodocidae (Struck & Halanych 2010). We treat each nominal
family separately here because they differ in habitat and morphology: The historically
recognized families largely correspond to morphotypes that are the targets of our functional
grouping. Molecular genetic analyses are also revising understanding of phylogeny within
benthic Phyllodocidae (Eklöf et al. 2007).
Habitat
Benthic Phyllodocidae are found epifaunally or infaunally across all substrata and depths. A few
species of Eteone in the northwest Pacific have invaded fresh water (Wilson 2000).
Sensory and feeding structures
Phyllodocidae have a pair of antennae and a pair of palps as well as anteriorly-oriented cirri.
A medial antenna or nuchal papilla may be present (Pleijel 2001). Nuchal organs are diverse
in both structure and location, including pits, posterior prostomial lobes, or distinct eversible
structures, and can occur as far back as the first segment (Pleijel 2001). Phyllodocids often
have a single pair of eyes with lenses. The pharynx is muscular and axial. They lack jaws but
have terminal papillae around the mouth opening and sometimes have papillae elsewhere on
the pharynx (Fauchald & Rouse 1997). Two species, Phyllodoce rosea and Phyllouschakovius
armigerum have numerous sharp, backward-pointing teeth on the outside of the everted pharynx
(O’Connor 1987, Blake 1988). Phyllodoce pettiboneae has fewer, larger teeth, and species of
Mysta and Zverlinum have smaller hardenings lining the pharynx (Blake 1988).
Motility
Phyllodocids are active burrowers and crawlers. Their crawling resembles that of nereidids,
including both parapodial walking and body undulations, but kinematics of benthic forms have
not, to our knowledge, been studied.
Illustrations
Nygren & Pleijel (2011) show photographs illustrating color variability within the Eumida
sanguinea species complex. Jenkins et al (2002) illustrate morphology of the blood-sucking
Galapagomystides aristata, including a schematic of proboscis eversion. Pleijel (2001, Plate 7ad) provides photographs in anterior views of characteristic phyllodocid morphologies.
Feeding
Phyllodoce mucosa apparently has some dietary flexibility. In a study of spatial dispersion in the
Wadden Sea intertidal zone, Reise (1979a) observed it to be primarily a carrion feeder attracted
to dead bivalves and decaying shore crabs, noting that this activity ceased in bright sunlight. In
an experimental field study of predation on meiofauna, Reise (1979b) observed that it preyed
particularly on juvenile hydrobiids in field enclosure experiments, but neither P. mucosa nor
Eteone longa had statistically significant effects on abundance of permanent meiofauna. Some
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Phyllodocidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
of the variation in diet in P. mucosa is seasonal. Lee et al. (2004) found P. mucosa to be cold
tolerant and higher in abundance on tidal flats in winter, when freeze events supply carrion, and
predators of P. mucosa are scarcer. P. mucosa was attracted to carrion from as far as 15 m away
on an ebbing tide. It quickly reached satiety and moved away from the carrion. As many as 447
worms were recorded to reach a single crushed mussel within 20 min at dusk. The species feeds
mainly at nocturnal low tides. It would not prey on motile, living, juvenile polychaetes, bivalves
or crustaceans but took the same prey immediately after they were killed by freshwater shock or
lost motility (Lee et al. 2004).
In a follow-up study to observations made by Behrends & Michaelis (1977), Michaelis
& Vennemann (2005) described interactions between Eteone longa and Scolelepis squamata
(Spionidae) at low tide in the Wadden Sea in Germany. E. longa tunneled a few grain layers
deep in the sediment, mounding the surface. As E. longa neared the opening of the tubedwelling S. squamata, the latter attempted escape over the sediment surface. E. longa emerged
from the same opening and searched for the slime trail of S. squamata, forming radial search
marks until it found the trail. S. squamata meanwhile wriggled to lay a sinusoidal trail across
the sediment surface that slowed the search by E. longa. Flight and pursuit sometimes extended
below the sediment surface. The majority of contact-producing encounters resulted in ingestion
of posterior segments of the spionid, which continued to flee, but then produced a characteristic
‘feather-stitch’ trail. In aquarium experiments, S. squamata instead swam to escape.
Dauer (1980) dissected 40 specimens of Eteone heteropoda from intertidal sands in Florida;
27 were empty. Three contained remains of Alitta succinea. Four contained 10 - 15 grains
of sand each. Three were about 1/3 full of unpelletized silt-clay. The remaining 3 individuals
combined a few sand grains with numerous, diatom-containing fecal pellets assumed to have
been made by another species. Gaston (1987) dissected 21 Phyllodoce mucosa and 10 Eteone sp.
A from the Middle Atlantic Bight of the U.S.A. All guts were empty. He classified both species
as carnivores.
A large majority of stable isotope measurements support carnivory in Phyllodocidae (Table
A3). Based on stable N and C signatures and mixture modeling, Bergquist et al. (2007) inferred
that Protomystides verenae fed on a maldanid and a snail in its hydrothermal vent community.
At least one result provides some evidence against predation, however. E. longa from Gamo
Lagoon in Japan had δ15N barely elevated over that of a sympatric spionid (Kanaya et al. 2007).
In long-term tracer experiments on the North Carolina continental slope, Mystides sp. was
heavily labeled 14 mo after application of 13C-labeled phytodetritus (Levin et al. 1999), likely
through an intermediate trophic level. Gontikaki et al. (2011) combined measurement of natural
levels of stable isotopes with short 13C-labeled phytodetrital incubations in refrigerated cores
from the Faroe-Shetland Channel at 1080 m water depth. Eteone sp. and Phyllodoce sp. showed
minor uptake of the label after 6 d incubation, perhaps through another trophic level—but lower
by an order of magnitude than in some surface deposit feeders.
Pharyngeal armature in Phyllodoce rosea and Phyllouschakovius armigerum is reminiscent
of that in Goniadidae associated with feeding on tube-building animals. Further circumstantial
evidence is the collection of P. rosea from maldanid-like tubes (O’Connor 1987).
Galapagomystides aristata, endemic to hydrothermal vents of the eastern Pacific, appears to
have an unusual lifestyle among phyllodocids. Anatomy suggests that it sucks blood (Jenkins
et al. 2002). It lacks an anus, has midgut diverticula characteristic of leeches and other bloodfeeding animals, and has been collected with its gut lumen filled with blood. Its stable C and N
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Phyllodocidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
composition is consistent with feeding on Paralvinella grasslei or Riftia pachyptila (Jenkins et
al. 2002). Protomystides sp. may blood feed on the tubeworm Escarpia laminata at seeps on the
northern Gulf of Mexico continental slope (Becker et al. 2010).
Table A3. Studies finding δ15N% indicative of carnivory in Phyllodocidae.
Citation
Location
Carmichael et al. 2004
Nauset Beach, Massachusetts
Marinetto et al. 2006
Bergquist et al. 2007
Water depth (m) Taxon
intertidal
Eteone longa
Quashnet River,
Massachusetts,
shallow
(unspecified)
Eteone lactea
Endeavor segment, Juan de
Fuca Ridge
~ 2200
(unspecified)
Protomystides verenae
Levin & Mendoza 2007 Unimak margin, Alaska
3267
Becker et al. 2010
seeps, N. Gulf of Mexico
530 - 2800
Iken et al. 2010
Chukchi Sea
39 - 54
Schaal et al. 2010
Brest harbor
shallow
(unspecified)
Gontikaki et al. 2011
Faroe-Shetland Channel
Calizza et al. 2013
Posidonia bed, Tyrrhenian Sea
Løkken 2013
Isfjorden, Svalbard
Sokołowski et al. 2014
Hornsund, Spitsbergen
100
Zapata-Hernández et
al. 2014
off peninsula Taito, Chile
460 - 700
1080
6
410 - 422
Phyllodocidae A & B
Protomystides sp.
Phyllodoce groenlandica
Eulalia viridis
Eteone sp.
Phyllodocidae sp.
Phyllodocidae
Phyllodoce groenlandica
Phyllodocidae
Guild membership
F&J characterized Phyllodocidae as carnivores, scavengers or subsurface deposit feeders. It is
not clear why surface deposit feeding was excluded. We now doubt whether any phyllodocids
can grow by feeding on sediments and agree with other summaries (Wilson 2000, Pleijel 2001)
that the overwhelming evidence is for carnivory and carrion feeding. Some earlier workers
reporting deposit feeding (summarized in F&J) may have mistaken emulsified animal tissues
(Voparil et al. 2008) for detritus. Sanders et al. (1962) dissected 6 Eteone heteropoda. Two
were empty, whereas 3 contained sand and diatoms, and 1 contained sand and detritus. It
may not be possible with the suction pump of E. heteropoda to take diatoms without taking
sand. Ingestion of a mixture of sand and diatoms may not require radically different digestive
approaches from carnivory. The three mud-containing individuals reported by Dauer (1980)
are more puzzling, but until evidence of growth on a diet of sediments is obtained, we regard
phyllodocids as carnivores or scavengers. Motility is implied by scent following that appears to
be a dominant mode of prey location by phyllodocids, but we cannot exclude the possibility of
sit-and-wait predation in some species or populations, in part dependent on local prey mobility
and abundance.
Research questions and opportunities
• Putatively deposit-feeding phyllodocids (e.g., E. heteropoda) should be examined for
digestive capacity relative to total body volume (Penry & Jumars 1990) and for the presence
of surfactants in their digestive fluids.
• Evidence of growth on a diet of sediments is lacking.
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Phyllodocidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
• Other than attraction distances and times (to carrion), little quantitative information is
available on motility.
References
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thesis. Pennsylvania State Univ.: State College, PA
Behrends G, Michaelis H. 1977. Zur Deutung der Lebensspuren des Polychaeten Scolelepis
squamata. Senckenberg. Marit. 9:47–57.
Bergquist DC, Eckner JT, Urcuyo IA, Cordes EE, Hourdez S, et al. 2007. Using stable isotopes
and quantitative community characteristics to determine a local hydrothermal vent food web.
Mar. Ecol. Prog. Ser. 330:49–65
Blake JA. 1988. New species and records of Phyllodocidae (Polychaeta) from Georges Bank and
other areas of the western North Atlantic. Sarsia 73:24–57
Calizza E, Costantini ML, Carlino P, Bentivoglio F, Orlandi L, Rossi L. 2013. Posidonia
oceanica habitat loss and changes in litter-associated biodiversity organization: A stable
isotope-based preliminary study. Estuar. Coast. Shelf Sci. 135:137–45
Carmichael RH, Rutecki D, Annett B, Gaines E, Valiela I. 2004. Position of horseshoe crabs in
estuarine food webs: N and C stable isotopic study of foraging ranges and diet composition.
J. Exp. Mar. Biol. Ecol. 299:231–53
Dauer DM. 1980. Population dynamics of the polychaetous annelids of an intertidal habitat in
upper old Tampa Bay, Florida. Int. Rev. Ges. Hydrobio. 65:461–87
Eklöf J, Pleijel F, Sundberg P. 2007. Phylogeny of benthic Phyllodocidae (Polychaeta) based on
morphological and molecular data. Mol. Phylogen. Evol. 45:261–71
Fauchald K, Rouse G. 1997. Polychaete systematics: past and present. Zool. Scr. 26:71–138
Gaston GR. 1987. Benthic Polychaeta of the Middle Atlantic Bight: feeding and distribution.
Mar. Ecol. Prog. Ser. 36:251–62
Gontikaki E, Mayor DJ, Narayanaswamy BE, Witte U. 2011. Feeding strategies of deep-sea subarctic macrofauna of the Faroe-Shetland Channel: Combining natural stable isotopes and
enrichment techniques. Deep-Sea Res. Pt. I 58:160–72
Iken K, Bluhm B, Dunton K. 2010. Benthic food-web structure under differing water mass
properties in the southern Chukchi Sea. Deep-Sea Res. Pt. II 57:71–85
Jenkins CD, Ward ME, Turnipseed M, Osterberg J, Dover CL. 2002. The digestive system of
the hydrothermal vent polychaete Galapagomystides aristata (Phyllodocidae): evidence for
hematophagy? Invertebr. Biol. 121:243–54
Kanaya G, Takagi S, Nobata E, Kikuchi E. 2007. Spatial dietary shift of macrozoobenthos in a
brackish lagoon revealed by carbon and nitrogen stable isotope ratios. Mar. Ecol. Prog. Ser.
345:117–27
Lee CG, Huettel M, Hong JS, Reise K. 2004. Carrion-feeding on the sediment surface at
nocturnal low tides by the polychaete Phyllodoce mucosa. Mar. Biol. 145: 575–83
Levin LA, Blair NE, Martin CM, DeMaster DJ, Plaia G, Thomas CJ. 1999. Macrofaunal
processing of phytodetritus at two sites on the Carolina margin: in situ experiments using
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C-labeled diatoms. Mar. Ecol. Prog. Ser. 182:37–54
Levin LA, Mendoza GF. 2007. Community structure and nutrition of deep methane-seep
macrobenthos from the North Pacific (Aleutian) margin and the Gulf of Mexico (Florida
escarpment). Mar. Ecol. 28:131–51
Martinetto P, Teichberg M, Valiela I. 2006. Coupling of estuarine benthic and pelagic food webs
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Phyllodocidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
to land-derived nitrogen sources in Waquoit Bay, Massachusetts, USA. Mar. Ecol. Prog. Ser.
307:37-48
Michaelis H, Vennemann L. 2005. The “piece-by-piece predation” of Eteone longa on Scolelepis
squamata (Polychaetes )—traces on the sediment documenting chase, defence and
mutilation. Mar. Biol. 147:719–24
Nygren A, Pleijel F. 2011. From one to ten in a single stroke – resolving the European Eumida
sanguinea (Phyllodocidae, Annelida) species complex. Mol. Phylogen. Evol. 58:132–41
Penry DL, Jumars PA. 1990. Gut architecture, digestive constraints and feeding ecology of
deposit-feeding and carnivorous polychaetes. Oecologia 82:1–11
Pleijel F. 2001. Phyllodocidae Örsted 1843a. See Rouse & Pleijel 2001, pp. 132–5
Reise K. 1979a. Spatial configurations generated by motile benthic polychaetes. Helgoländ.
Wiss. Meer. 32:55–72
Reise K. 1979b. Moderate predation on meiofauna by the macrobenthos of the Wadden Sea.
Helgoländ. Wiss. Meer. 32:453–65
Sanders HL, Goudsmit EM, Mills EL, Hampson GE. 1962. A study of the intertidal fauna of
Barnstable Harbor, Massachusetts. Limnol Oceanogr. 7:63–79
Schaal G, Riera P, Leroux C, Grall J. 2010. A seasonal stable isotope survey of the food web
associated to a peri-urban rocky shore. Mar. Biol. 157:283–94
Sokołowski A, Szczepańska A, Richard P, Kędra M, Wołowicz M, et al. 2014. Trophic structure
of the macrobenthic community of Hornsund, Spitsbergen, based on the determination of
stable carbon and nitrogen isotopic signatures. Polar Biol. 37:1247–60
Struck TH, Halanych KM. 2010. Origins of holopelagic Typhloscolecidae and Lopadorhynchidae
within Phyllodocidae (Phyllodocida, Annelida). Zool. Scr. 39:269–75
Struck TH, Paul C, Hill N, Hartmann S, Hösel C, et al. 2011. Phylogenomic analyses unravel
annelid evolution. Nature 470:95–8
Voparil IM, Mayer LM, Jumars PA. 2008. Emulsions versus micelles in the digestion of lipids by
benthic invertebrates. Limnol. Oceangr. 53:387–94
Wilson RS. 2000. Family Phyllodocidae. See Beesley et al. 2000, pp. 145–8
Zapata-Hernández G, Sellanes J, Thurber AR, Levin LA. 2014. Trophic structure of the bathyal
benthos at an area with evidence of methane seep activity off southern Chile (~45°S). J. Mar.
Biol. Ass. UK 94:659–69
Pilargidae, Nereidiformia, Phyllodocida
Diversity and systematics
Pilargidae comprise about 100 species in 11 genera, only one monotypic. They may be closely
related to Hesionidae (Dahlgren et al. 2000) or Nephtyidae (Struck & Halanych 2010), although
support for neither relationship has yet been very strong. Two morphotypes are recognized, one
cylindrical (e.g., Synelmis), the other more oval or rectangular in cross section (e.g., Sigambra),
though the distinction is not always clear. In each morphotype, length:width ratios vary widely.
They are small to medium-sized worms, from a few millimeters to a few centimeters long.
Habitat
Pilargids are rarely abundant but are most common at shelf and slope depths in mixed sediments.
They can be found in sediments at any water depth.
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Pilargidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Sensory and feeding structures
The prostomium is often wider than long and ranges from an approximately rectangular prism
to hemispheroidal. The peristomium is limited to lips (Pleijel 2001). Eyes when present are
paired—up to 5 pairs. Nuchal organs, in species where known, form ciliated slits at the posterior
of the prostomium (Pleijel 2001), but none are visible in some taxa (e.g., Glasby & Marks 2013).
Pilargids have zero, two or three dorsal antennae and two ventral palps that may be distinct or
completely fused. Some genera have axial, muscular pharynges tipped by papillae that bear
sensory cells, similar to the pharynges of some hesionids and syllids (Tzetlin & Purschke 2005),
but papillae may be lacking (Glasby & Marks 2013). Well articulated jaws are absent, but teeth
are variably developed in several species of Hermundura, and may be capable of opposable
grasping (Glasby & Hocknull 2010). Sigambra grubii has a muscular stomach extending
through the first five chaetigers, with lateral gut caeca in the following segments (Salazar-Vallejo
1990, Fig. 1).
Motility
Many Pilargidae are motile burrowers. Sigambra bassi extends burrows by fracture using a
large, eversible pharynx that extends anteriorly a distance roughly equal to the body width.
When fully everted, the pharynx shows a ring of distal papillae surrounding a large mouth
opening (KM Dorgan & EAK Murphy, unpublished data). Ancistrosyllis commensalis inhabits
burrows of Notomastus lobatus, A. groenlandica is commensal with the burrowing holothuroid
Molpadia, and a species reported as Pilargis berkeleyae (but that may instead by P. pacifica
cf. Salazar-Vallejo & Harris 2006) is commensal in tubes of Chaetopterus cautus (Martin &
Britayev 1998). They likely have more limited motility, than more independent species.
Illustrations
Pleijel (2001) provides informative stippled line drawings and electron micrographs showing
principal features of the family. Glasby & Marks (2013) provide informative line drawings and
micrographs of several species of Synelmis. Salazar-Vallejo & Harris (2006) provide stippled
line drawings of several species of Pilargis.
Feeding
F&J remarked on the lack of data on pilargid feeding. We know of no published evidence of diet
or feeding behavior. The only study of gut contents we could find was for Sigambra grubei. Of
10 individuals, 9 were empty or incomplete. Gut contents in the 10th were listed as “unidentified
material” (Magalhães & Barros 2011). We found stable isotope data only for Synelmis sp. at a
hydrocarbon seep on the Florida escarpment: Synelmis sp. was calculated to obtain 37% of its
carbon from methane sources, but the diversity of microbial δ15N signatures at the site made
trophic level of Synelmis sp. uncertain from its 15N content (Levin & Mendoza 1997).
Guild membership
F&J classed pilargids tentatively as burrowing carnivores using an armed or unarmed pharynx.
We have no reason to change this suggestion, but it rests on feeding habits of related families and
inference from morphology rather than direct evidence beyond a few empty guts.
Research questions and opportunities
• Data on feeding are largely lacking, whether from gut contents, behavioral observations,
stable isotopes, or tracers.
• Motility has not been quantified.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A233
Pilargidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
References
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the phylogeny of Nereidiform polychaetes (Annelida). J. Zool. Syst. Evol. Res. 38:249–53
Glasby CJ, Hocknull SA. 2010. New records and a new species of’Hermundura’Müller, 1858,
the senior synonym of“Loandalia”Monro, 1936 (Annelida: Phyllodocida: Pilargidae) from
northern Australia and New Guinea. The Beagle: Records of the Museums and Art Galleries
of the Northern Territory 26:57–67
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Phyllodocida: Pilargidae) in Australia. Zootaxa 3646:561–74
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Nat. Hist. 24:507–17
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Polychaeta, Pilargidae). J. Nat. Hist. 40:119–59
Salazar-Vallejo SI, Nishi E, Anguspanich S. 2001. Rediscovery of Talehsapia annandalei
(Polychaeta: Pilargidae) in Songkhla Lagoon, Thailand. Pac. Sci. 55:267–73
Struck TH, Halanych KM. 2010. Origins of holopelagic Typhloscolecidae and Lopadorhynchidae
within Phyllodocidae (Phyllodocida, Annelida). Zool. Scr. 39:269–75
Tzetlin A, Purschke G. 2005. Pharynx and intestine. Hydrobiologia 535:199–225
Poecilochaetidae, Spioniformia
Diversity and systematics
Poecilochaetidae comprise about 30 accepted species in the genus Poecilochaetus. In a
phylogenetic analysis based on morphological characters, Eibye-Jacobson (2005) found 24
Poecilochaetus spp. to be monophyletic and Trochochaetidae to be a sister clade. The latter
close relationship was also found by Capa et al. (2012), who in addition identified some affinity
with Sabellariidae. Poecilochaetids are notoriously fragile, so lengths are not well known, but
range from roughly 1 to several centimeters.
Habitat
Poecilochaetids build Y- , V- or U-shaped burrows in soft sediments from shallow water to hadal
depths (Allen 1904, Mackie 1990). Burrows generally extend 5 - 10 cm into the sediments (e.g.,
Reise 2002, Fig. 7F). Poecilochaetids are usually rare, but can reach high local abundances, i.e.,
are extremely patchy.
Sensory and feeding structures
A small, hemispherical prostomium rests on a more expansive peristomium. The prostomium
in shallow-water species usually carries two pairs of eyes, the anterior ones generally larger. A
pair of long, ciliated, grooved palps inserts at the postectal margins of the prostomium and can
extend at least half the body length (Allen 1904). The most anterior appendage projects forward
from the upper lip (peristomium) and is usually (incorrectly) termed a medial antenna (Rouse
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2001). The pharynx is ventral, muscular, short, ciliated, and eversible (Allen 1904). Several
pairs of anteriorly directed postchetal lobes and capillary chaetae surround the prostomium,
forming a basket or cage. Nuchal organs are present in one of three forms: an inconspicuous
mound; an elongate, medial structure; or, three elongate lobes (1 medial and 2 lateral)—and are
supplemented with inter-ramal sense organs on most setigers (Eibye-Jacobsen 2011). Nuchal
lobes when present attach dorsally at the posterior of the prostomium.
Motility
Allen (1904) described formation of a burrow between two plates of glass separated by 1/16
in (1.6 mm). In that confine (Allen 1904, p. 83), “The burrowing was accomplished with the
head end of the worm, more particularly with the forwardly directed parapodial cirri of the
first segment and the long bristles belonging to it. During the process the anterior part of the
body was constantly waved to and fro in a transverse direction. The burrowing movement was
persisted in until the complete U-shaped tube had been formed.” Once the burrow was built, a
constant posteriorward current was produced by a fanning motion of posterior chaetal bundles
(Allen 1904). Poecilochaetid burrows are occupied long enough to be inhabited by pinnotherid
commensals (Taylor 1966, cited in Wilson 2000).
Illustrations
Allen (1904) provides a strikingly detailed color drawing of Poecilochaetus serpens (Plate 7,
Fig. 1) and also illustrates the U-shaped burrow (Plate 9, Fig. 12). Eibye-Jacobsen (2011, Fig.
1) provides remarkable scanning electron micrographs of sensory appendages and palps. Line
drawings provided by Wilson (2000) are very informative.
Feeding
The only direct evidence of diet appears to be Allen’s (1904) observation through the body wall
of abundant diatom frustules in the gut of Poecilochaetus serpens and Magalhães & Barros’
(2011) recording of “detritus” as gut contents in 16 incomplete specimens of Poecilochaetus
johnsoni from estuaries of northeast Brazil. Dannheim et al. (2014, supplemental materials)
collected grab samples at about 30 m water depth in the German Bight. They found very similar
δ15N and δ13C in P. serpens and Lanice conchilega. L. conchilega (Terebellidae) is known to
suspension and surface-deposit feed. The δ15N signature of Goniada maculata was ~ 3‰ higher.
Results from a stable isotope study in Arachon Bay were more confusing (Dubois et al.
2014). There was little dynamic range in δ15N across the full range of polychaetes sampled,
which included P. serpens near the middle of the range. Multiple organic sources, each with
different δ15N, complicated interpretations of trophic levels (Dubois et al. 2014).
Guild membership
Although data are limited, discrete motility is well supported. We know of no observations of
feeding behavior. Allen (1904) described P. serpens as coiling palps on the sediment surface in
a laboratory ant farm but did not report feeding observations. Based on morphological similarity
with Spionidae, and some compatible stable isotope data, it seems likely that Poecilochaetus spp.
surface-deposit and suspension feed, but direct observations and experiments are still lacking.
Research questions and opportunities
• Observations and experiments are needed to exclude one or more of subsurface deposit
feeding, surface deposit feeding and suspension feeding in Poecilochaetus spp.
• Flume experiments are in order to determine whether Poecilochaetus spp. show the kind of
palp coiling seen in some spionids and chaetopterids.
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Jumars, Dorgan & Lindsay
07 November 2014
References
Allen EJ. 1904. The anatomy of Poecilochaetus, Claparède. Q. J. Microsc. Sci. 48:79–151 +
Plates 7–12
Capa AM, Hutchings P, Peart R. 2012. Systematic revision of Sabellariidae (Polychaeta) and
their relationships with other polychaetes using morphological and DNA sequence data.
Zool. J. Linn. Soc. 164:245–84
Dannheim J, Brey T, Schröder A, Mintenbeck K, Knust R, et al. 2014. Trophic look at softbottom communities—Short-term effects of trawling cessation on benthos. J. Sea Res.
85:18–28
Dubois S, Blanchet H, Garcia A, Massé M, Galois R, et al. 2014. Trophic resource use by
macrozoobenthic primary consumers within a semi-enclosed coastal ecosystem: stable
isotope and fatty acid assessment. J. Sea Res. 88:87–99
Eibye-Jacobsen D. 2005. A preliminary phylogenetic analysis of Poecilochaetidae (Annelida:
Polychaeta) at the species level. Mar. Ecol. 26:171–80
Mackie ASY. 1990. The Poecilochaetidae and Trochochaetidae (Annelida: Polychaeta) of Hong
Kong. In Proceedings of the Second International Marine Biological Workshop: The Marine
Flora and Fauna of Hong Kong and Southern China, ed. B. Morton, pp. 337–62. Hong
Kong: Hong Kong Univ. Press
Magalhães WF, Barros F. 2011. Structural and functional approaches to describe polychaete
assemblages: ecological implications for estuarine ecosystems. Mar. Freshw. Res. 62:918–26
Rouse GW. 2001. Poecilochaetus Claparède, 1875. See Rouse & Pleijel 2001, pp. 266–8
Taylor JL. 1966. A Pacific polychaete in southeastern United States. Quart. J. Florida Acad. Sci.
29:21–6
Wilson RS. 2000. Family Poecilochaetidae. See Beesley et al. 2000, pp. 196–7
Poeobidae, Cirratuliformia
Diversity and systematics
Poeobidae is represented by Poeobius meseres alone and may be demoted to generic status
within Flabelligeridae (Burnette et al. 2005). P. meseres likely originated progenetically from
benthic Flabelligeridae (Struck 2006). Worms range up to 27 mm long (Uttal & Buck 1996).
Habitat
P. meseres is holopelagic and is broadly distributed in midwater depths below the oxygen
minimum. In Monterey Canyon, abundance peaked at 1800 m, and they extended down to 2300
m (Robison et al. 2010). The species is likely to experience vertical range expansion with the
shoaling of oxygen minima (Gilly et al. 2013)
Sensory and feeding structures
Anatomical structure, including an invertible anterior, consisting of the pro- and peristomium
and first chaetiger, is similar to Flabelligeridae, with the exception that Poeobidae have a flexible
tongue that functions similarly to the ciliated lips of Flabelligeridae (Filippova et al. 2003). P.
meseres has a pair of long, grooved, ciliated palps. Nuchal organs are ciliated ridges that extend
along the dorsum around the base of each palp (Robbins 1965).
Motility
Unlike many holopelagic polychaetes with elongated chaetae for swimming, P. meseres lacks
chaetae entirely. Their gelatinous bodies also suggest that they are not strong swimmers. Uttal
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Jumars, Dorgan & Lindsay
07 November 2014
& Buck (1996) observed ROV videos of worms “hanging neutrally buoyant in the water column”
with mucus nets deployed for feeding.
Illustrations
In situ photographs of P. meseres are shown by Uttal & Buck (1996; Fig. 1) and Burnette et al.
(2005). Robbins (1965) shows drawings of internal structures as well as of the head with the
tongue-like “elastic pad” extended.
Feeding
Uttal and Buck (1996) studied feeding behavior and gut contents of P. meseres. It uses a mucus
net to passively collect particles via gravitational deposition as well as palps to grasp larger
particles. Stomach contents (of 62 worms) were dominated by zooplankton fecal pellets but
also included phytoplankton and microzooplankton. Phytoplankton were found in proportions
representative of water-column productivity, consistent with passive suspension feeding.
Similarly, Robbins (1965) described gut contents to include diatoms, radiolarians, planktonic
foraminiferans, and algae.
Guild membership
Poeobidae are passive suspension feeders that primarily use mucus nets to encounter particles
settling by gravitational deposition. They are motile but appear to be weak swimmers that
position themselves primarily by adjusting buoyancy.
Research questions and opportunities
• The importance of chemosensing in particle encounter by the palps is unknown.
• There do not appear to be stable isotope or lipid marker assessments of dietary source and
effective trophic level.
References
Burnette AB, Struck TH, Halanych KM. 2005. Holopelagic Poeobius meseres (“Poeobiidae,”
Annelida) is derived from benthic flabelligerid worms. Biol. Bull. 208:213–20
Filippova AV, Tzetlin AB, Purschke G. 2003. Morphology and ultrastructure of the anterior
end of Diplocirrus longisetosus Marenzeller, 1890 (Flabelligeridae, Polychaeta, Annelida).
Hydrobiologia 496:215–23
Gilly WF, Beman JM, Litvin SY, Robison BH. 2013. Oceanographic and biological effects of
shoaling of the oxygen minimum zone. Annu. Rev. Marine Sci. 5:393–420
Robbins DE. 1965. The biology and morphology of the pelagic annelid Poeobius meseres Heath.
J. Zool. 146:197–212
Robison BH, Sherlock RE, Reisenbichler KR. 2010. The bathypelagic community of Monterey
Canyon. Deep-Sea Res. Pt. II 57:1551–6
Struck TH. 2006. Progenetic species in polychaetes (Annelida) and problems assessing their
phylogenetic affiliation. Integr. Comp. Biol. 46:558–68
Uttal L, Buck KR. 1996. Dietary study of the midwater polychaete Poeobius meseres in
Monterey Bay, California. Mar. Biol. 125:333–43
Polygordiidae
Diversity and systematics
Polygordiidae are known from about 17 species in a single genus of former archiannelids.
Molecular data suggest a close relationship with Saccocirrus (Struck et al. 2002), and also
seem to support much earlier suggestions of a close relationship with opheliids based on similar
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Jumars, Dorgan & Lindsay
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undulatory behavior and musculature (Clark & Hermans 1976, Law et al. 2014). They are
generally very thin worms < 3 cm long.
Habitat
Most polygordiids are interstitial, generally in coarse sands. Two Polygordius cf. antarctica
were recently recovered from an experimentally deployed piece of whale bone emplaced for a
year at 21 m water depth off Deception Island, Antarctica (Taboada et al. 2013).
Sensory and feeding structures
Polygordiids bear two anterior terminal appendages that have variously been termed palps,
antennae and palpoids. Innervation and structure argue for a sensory function (Rouse 2001),
and we know of no evidence that they are used to manipulate food toward the ventral mouth.
Polygordiids bear ovoid nuchal organs at the rear of the prostomium (Rouse 2001). They bear
ciliated, dorsolateral, pharyngeal folds that are eversible and have few gland cells and only weak
musculature (Purschke & Tzetlin 1996), distinguishing them from other former archiannelids,
most of which have a ventral muscular pharynx. Purschke & Tzetlin (1996) described their
pharynges as similar to that of Saccocirrus papillocercus, in the group of Saccocirridae that lack
a muscular pharyngeal bulb and are presumed carnivorous. (See the Saccocirridae section.)
Rota & Carchini (1999) described P. antarcticus as having an “upper buccal lip slightly
protrusible, so as to show the anterior middorsal ridge of pharynx” that from their images (Fig.
3f, g) appears to be potentially useful in scraping.
Motility
Polygordiids travel through interstitial spaces in sands using undulatory movements, achieved
by alternating contraction of large bands of longitudinal muscle (Rota & Carchini 1999, Fig. 5)
with bending achieved by simultaneous oblique muscle contraction, similar to movements by
Armandia brevis (Dorgan et al. 2013). Our observations of weak peristaltic movements (KM
Dorgan, pers. obs.) are supported by recent finding of minute circular muscles in the body wall
of P. appendiculatus (Lehmacher et al. 2013). Out of sediments, their resemblance to namesake
Gordian knots becomes apparent.
Illustrations
Ramey et al. (2006; Fig. 2) and Rota & Carchini (1999, Fig 3f,g) show ventral mouth position
and morphology. Cross-sections of muscle structure of P. antarcticus are shown by Rota
& Carchini (1999; Fig. 5). Purschke & Tzetlin (1996; Fig 2A) show a scanning electron
micrograph of the everted pharynx of Polygordius sp.
Feeding
F&J classified polygordiids as surface deposit feeders (SMX) without indicating a source for this
information. Explicit feeding or gut-content studies are scarce, yet accounts of feeding mode are
quite varied. Rota and Carchini (1999) found organic debris, diatom skeletons, and sand grains
in the gut of P. antarcticus from the Ross Sea. Cowles (1903) raised recently settled larval P. cf.
appendiculatus (likely P. jouinae) from the east coast of the US on sand enriched with diatoms
and found diatom remains in the guts. Gaston et al. (1998, p. 843) classified Polygordius spp.
as carnivores without indicating a source for this information. Ramey (2008), Ramey & Bodnar
(2008) and Ramey et al. (2009) classified P. jouinae as a deposit feeder but also did not cite a
source for this information. In both laboratory experiments (Ramey & Bodnar 2008) and field
samples (Ramey et al. 2009), however, this species spent more time and consequently showed
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Jumars, Dorgan & Lindsay
07 November 2014
higher animal densities in organically enriched sands, consistent with feeding on organic-rich,
flocculent material placed or found (respectively) there.
Guild membership
Polygordius is motile, and based on small size likely specializes on labile material such as
diatoms. Feeding on other protists and small animals is possible.
Research questions and opportunities
• Gut-content and stable-isotope analyses would be useful.
• Motility and its dependence on food abundance are unquantified.
References
Clark RB, Hermans CO. 1976. Kinetics of smimming in some smooth-bodied polychaetes. J.
Zool. 178:147–59
Cowles RP. 1903. Notes on the rearing of the larvae of Polygordius appendiculatus and on the
occurrence of the adult on the Atlantic coast of America. Biol. Bull. 4:125–8
Dorgan KM, Law CJ, Rouse GW. 2013. Meandering worms: mechanics of undulatory burrowing
in muds. Proc. Roy. Soc. B 280:20122948, 9 pp.
Gaston GR, Rakocinski CF, Brown SS, Cleveland CM. 1998. Trophic function in estuaries:
response of macrobenthos to natural and contaminant gradients. Mar. Freshw. Res. 49:833–
46
Law CJ, Dorgan KM, Rouse GW. 2014. Relating divergence in polychaete musculature to different
burrowing behaviors: A study using Opheliidae (Annelida). J. Morphol. 275:548–71
Lehmacher C, Fiege D, Purschke G. 2013. Immunohistochemical and ultrastructural analysis of
the muscular and nervous systems in the interstitial polychaete Polygordius appendiculatus
(Annelida). Zoomorphology 133:21–41
Purschke G, Tzetlin AB. 1996. Dorsolateral ciliary folds in the polychaete foregut: structure,
prevalence and phylogenetic significance. Acta Zool. 77:33–49
Ramey PA. 2008. Processes affecting macrofaunal community structure in sandy sediments on
the New Jersey inner continental shelf with a focus on the dominant polychaete, Polygordius
jouinae. PhD thesis, Rutgers Univ.: New Brunswick, NJ
Ramey PA, Bodnar E. 2008. Selection by a deposit-feeding polychaete, Polygordius jouinae, for
sands with relatively high organic content. Limnol. Oceangr. 53:1512–20
Ramey PA, Fiege D, Leander BS. 2006. A new species of Polygordius (Polychaeta:
Polygordiidae): from the inner continental shelf and in bays and harbours of the northeastern United States. J. Mar. Biol. Ass. UK 86:1025–34
Ramey PA, Grassle JP, Grassle JF, Petrecca RF. 2009. Small-scale, patchy distributions of
infauna in hydrodynamically mobile continental shelf sands: Do ripple crests and troughs
support different communities? Cont. Shelf Res. 29:2222–33
Rota E, Carchini G. 1999. A new Polygordius (Annelida: Polychaeta) from Terra Nova Bay, Ross
Sea, Antarctica. Polar Biol. 21:201–13
Rouse GW. 2001. Polygordiidae Czerniavsky. See Rouse & Pleijel 2001, pp. 279–81
Struck TH, Westheide W, Purschke G. 2002. Progenesis in Eunicida (“Polychaeta,” Annelida)—
separate evolutionary events? Evidence from molecular data. Mol. Phylogen. Evol. 25:190–9
Taboada S, Wiklund H, Glover AG, Dahlgren TG, Cristobo J, Avila C. 2013. Two new Antarctic
Ophryotrocha (Annelida: Dorvilleidae) described from shallow-water whale bones. Polar
Biol. 36:1031–45
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Polynoidae
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doi: 10.1146/annurev-marine-010814-020007
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Jumars, Dorgan & Lindsay
07 November 2014
Polynoidae, Aphroditiformia
Diversity and systematics
The size of Family Polynoidae can be overwhelming and makes generalization difficult. These
scaleworms currently comprise > 750 species in > 160 genera, nearly half monotypic. Molecular
genetic work is revealing cryptic species (Neal et al. 2014). Only 13 genera contain ≥ 10
species; Harmothoe is the most speciose, with 150. It has recently been revised (Barnich &
Fiege 2009, Salazar-Silva 2010). Polynoidae among Aphroditiformia are most closely related to
Acoetidae (Wiklund et al. 2005, Norlinder et al. 2012). A typical shape is a flattened, elongate
hemispheroid, but some species are long and slender. Eulagisca gigantea can be 19 cm long and
10 cm wide (Hutchings 2000), but most species are 1 - 3 cm long.
Habitat
Polynoids can be found in any oxic, benthic marine environment. Epifaunal polynoids are
among the most conspicuous polychaetes viewed from ROVs or submersibles. Some species,
e.g., Bylgides sarsi, frequently swim off the bottom. In shallow water, B. sarsi rests in the
sediments during the day and swims at night (Sarvala 1971). The 5 known species of Drieschia
and the 2 known species of Podarmus are transparent, holopelagic, rare, and poorly known
ecologically. Over half of the polychaetes known to be commensal are polynoids, most
frequently with echinoderms or with tube and burrow makers from several phyla (Martin &
Britayev 1998). Roughly 20% of polynoid species are commensal (Martin & Britayev 1998).
Among the more unusual commensal habitats, Gorekia crassicirris finds refuge within the oral
cavities of at least two species of Antarctic spatangoid urchins (Schiaparelli et al. 2011).
Sensory and feeding structures
Sensory structures are abundant and crowded to face forward on and around a small,
hemispheroidal or bilobed prostomium. Most polynoids have paired lateral antennae and a
medial antenna. Just above the mouth, many species in addition carry a papilliform or antennalike frontal tubercle. Two ventral palps are fused to the first segment. Two pairs of eyes are
often present. Nuchal organs are present but poorly documented in most species descriptions.
In some genera they form a nuchal fold over the rear of the prostomium (Hutchings 2000). The
peristomium is limited to a small lip region (Pleijel 2001). The axial, muscular pharynx is
eversible and carries one pair of beak-like jaws, usually with two large teeth on each jaw of the
pair. In the confusing jargon often applied to the family, the structure is called “four jaws” or
“two pairs of jaws.” The single pair of jaws (in our terminology) is strongly articulated and is
associated with what may be venom glands (Wolf 1976). The everted pharynx is tipped with a
circlet of papillae. Polynoids have lateral gut diverticula in most segments.
Motility
F&J noted that polynoids included actively moving predators and sit-and-wait predators.
Schiaparelli et al. (2010) made interesting observations on the commensal relation between
Eunoe opalina and its shelf and bathyal holothuroid host. Eunoe opalina is discretely motile in
the reference frame of its bathyal, epifaunal host holothuroid, living in a pit of its own making
on the ventral side of the host near its mouth (Schiaparelli et al. 2010) but is thereby motile with
respect to the seafloor. Schiaparelli et al. (2010) term it a “hitchhiker.” It is not known to what
extent the holopelagic forms are cruising predators versus sit-and-wait predators.
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Jumars, Dorgan & Lindsay
07 November 2014
Illustrations
Hutchings (2000) and Pleijel (2001) provide informative stippled line drawings and photographs
of Polynoidae. Schiaparelli et al. (2010, 2011) provide notable photographs of Eunoe opalina
on and off its host holothuroid and Gorekia crassicirris in and out of its spatangoid host’s
gut. Glover et al. (2005) provide informative and artful photographs and scanning electron
micrographs of Bathykurila guaymasensis.
Feeding
Plyuscheva et al. (2010) analyzed gut contents of 145 Lepidonotus squamatus and 143
Harmothoe imbricata from three shallow-water habitats in the White Sea, two sponge beds and
an aquacultured mussel bed. Both species showed broad diets that frequently included diatoms,
hydroids, sponges and invertebrate prey, with considerably more differences in diet accounted
for by site than by scaleworm species. Few between-species differences in diets were consistent
across sites except that H. imbricata took fewer bryozoans and caprellid amphipods.
An additional example of kleptoparasitism to those reviewed in F&J has emerged in Acholoe
squamosa as a commensal of burrowing starfish. It has been observed with its head inside the
mouth of its host, presumably feeding on stomach contents (Freeman et al. 1998). Gorekia
crassicirris inhabits the lumen of the digestive tract of burrowing urchins at shelf and bathyal
depths around Antarctica. Only three specimens have been dissected, and none had gut contents,
so the feeding consequences of the commensalism remain to be determined (Schiaparelli et al.
2011). Sato et al. (2001) regarded small animals and organic particles entrained in the filtering
current of a thalassinid host to be the food of commensal Hesperonoe hwanghaiensis, but they
did not specify the nature of the evidence.
Gastrolepidia clavigera lives commensally with at least 13 species of holothuroids (Martin
& Britayev 1998). It lives externally near the mouth or anus and retreats into the digestive tract
when startled (Britayev & Lyskin 2002). It was initially considered unusual among commensal
polynoids for taking host tissue, i.e., being at least partly parasitic (Britayev & Lyskin 2002).
Of 65 dissected specimens from three host species, 87% had gut contents. Sponge remains
were the most frequent item found, followed by crustacean remains, including a parasite of the
holothuroid hosts. Polychaetes, forams, algae, and one bivalve were also found. Limited sand
and detritus were thought to come from ingested prey species. Stable isotope analysis confirms a
trophic level in G. clavigera well above those of its hosts (Caulier et al. 2014).
With application of careful gut contents analysis and the benefit of stable isotope analysis,
documented parasitism by polynoids has become more frequent, and is often combined with
predation on non-host species. “Hitchhiking” Eunoe opalina on epifaunal holothuroids
encountered and ingested a wide diversity of foods, including host tissues, diverse invertebrates,
foraminiferans and both benthic and planktonic diatoms (Schiaparelli et al. 2011). Ophiuroid
arm nipping was universal among the 7 specimens dissected.
Branchipolynoe spp. are commensals on gills of vent and seep mussels. Desbruyères et
al. (1985) reported both mussel pseudofeces and gill filaments among the gut contents of B.
symmitilidae from the Galapagos vents. Van Dover (2002) measured a 3.5‰ enrichment in δ15N
in B. seepensis relative to host tissues from Mid-Atlantic Ridge vent fields, Colaço et al. (2002)
measured a 3‰ enrichment, and De Busserolles et al. (2009) measured a 3.9‰ enrichment,
providing strong evidence that the diet includes host tissues or occasional parasites of the
host. Britayev et al. (2003) dissected 24 specimens of B. aff. seepensis from the Mid- Atlantic
Ridge and found no evidence of feeding on host tissues. They concluded that the species was
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Jumars, Dorgan & Lindsay
07 November 2014
a kleptoparasite. We regard the stable isotope data as good integrators over the growth of the
polynoids and suspect that kleptoparasitism is frequent and helpful in fueling maintenance
metabolism, but parasitism may be key to growth and reproduction of the polynoids.
Takahashi et al. (2012) measured stable isotopic contents of individual amino acids in three
Branchipolynoe pettiboneae individuals and its host mussel in vents and seeps. δ15N contents of
an adult B. pettiboneae taken from a mussel were consistent with parasitism on the mussel, but
δ15N of a free-living adult and of a commensal juvenile were not.
Free-living polynoids are among the most dominant invertebrate predators at hydrothermal
vents and at cold seeps. Unidentified polynoids at Gorda Ridge showed δ15N 6.8 - 7.7‰ higher
than local bacterial mat material (Van Dover & Fry 1994). At Juan de Fuca Ridge, no bacterial
mat results were reported, but 4 polynoids had the highest δ15N values of any invertebrate (Van
Dover & Fry 1994). Later studies at the Juan de Fuca Ridge detailed results for 9 species of
polynoids. Each species showed a narrow diet as evidenced by low variance of δ15N and δ13C
values, with several polynoid species sharing in partial predation of vent tubeworm dominants
(Bergquist et al. 2007). Two-species prey models did a good job of explaining the isotopic
variability seen in several cold-seep polynoids in the Gulf of Mexico (Cordes et al. 2010).
Free-living polynoids, however, are not exclusively carnivorous. Bathykurila guaymasensis
is a specialist grazer on Beggiatoa mats around vents at Guaymas Basin and on whale bones
in the southern California continental borderland; molecular genetic analysis suggests that two
species may be included under this name (Glover et al. 2005). Lepidonotopodium piscesae
and Branchinotogluma sp. from the Juan de Fuca Ridge had δ15N values that exceeded
those in Paralvinella pandorae by < 1‰ and an enriched δ13C indicative of direct feeding
on vent microbes (Levesque et al. 2006). Levesque et al. (2006, p. 730) reported visual
observations of both polynoid species eating particulate organics as well as preying on vent
macrofauna. Gaudron et al. (2012) in short-term colonization experiments in a newly opened
vent field documented substantial change in δ15N signatures of Lepidonotopodium riftense
and Branchinotogluma sandersi over time, likely indicating a switch in feeding from bacterial
detritus to animal prey. Reid et al. (2012) reported δ15N signatures of two individual polynoids
(not identified further) from vent fields of the Mid-Atlantic Ridge compatible with feeding
on surface sediments or other bacterial sources. To explain his stable isotope results, Soto
(2009) posited a diet mixture of bacteria and bacterivores in Branchinotogluma grasslei from
hydrothermal vent fields in Guaymas Basin. Vereshchaka et al. (2000) reported a δ15N‰ from
Polynoidae (not identified further) collected from the Broken Spur region of the Mid-Atlantic
Ridge; it suggests a middle to high trophic level.
A single individual of Harmothoe sp. from a cold seep in the Gulf of Mexico was not
enriched in 15N (MacAvoy et al. 2002) but also not unusually depleted in 13C so that it may have
immigrated to the site. A subsequent study found variable enrichment of 15N in Harmothoe
sp. among seep sites and suggested that Harmothoe sp. fed primarily on another scaleworm,
Branchinotogluma sp. that in turn fed on a mixture of the vestimentiferan Lamellibrachia
luymesi and assorted other prey (MacAvoy et al. 2008). Levin & Mendoza (2007) sampled
methane seep and nearby non-seep, deep-sea sites on the Florida escarpment and the Aleutian
margin. They reported stable isotope values for 4 polynoids collected on seeps and 2 collected
away from them (not identified below family level). The non-seep worms had clearly predatory
δ15N signatures, as did one of the seep worms. Three seep worms, however, had δ15N and δ13C
contents much more suggestive of substantial direct feeding on microbial mats or microbial
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detritus. In a bathyal region with evidence of methane seepage off southern Chile, a polynoid
was estimated to have a trophic level of 4.3 (where a level of 1 equals that of the source of
organic carbon), higher than any other polychaete assayed (Zapata-Hernández et al. 2014).
Kiyashko et al. (2014) sampled Harmothoe derjugini and H. impar impar at water depths
> 2000 m in the Sea of Japan. 15N enrichment of size-sorted H. derjugini failed to support the
hypothesis of cannibalism. Stable N and C values and fatty-acid signatures in both species were
consistent with feeding on epipelagic crustaceans, the diet potentially dominated by Metridia
pacifica from mid waters. Harmothoe antilopes from 5 - 35 m water depths in the Bay of
Concarneau also had 15N enrichment consistent with carnivory (Rigolet et al. 2014).
Scattered stable isotope results are also available from non-seep, non-vent environments for
polynoids not identified to the species level. Nilsen et al. (2008) used an Ecopath mass-balance
model to estimate a trophic level of 2.3 for Polynoidae collected in Sørfjord, northern Norway.
Grall et al. (2006) reported δ15N consistent with carnivory for 3 (pooled) polynoids collected
from the Bay of Brest. Iken et al. (2010) calculated a trophic level of 3.0 - 3.2 for 15 polynoids
collected from shelf depths in the southern Chukchi Sea. Løkken (2013) calculated a trophic
level of 3 for polynoids (9 individuals total) over the full range of water depths sampled (0 - 420
m) in Isfjorden, Svalbard. On the Chukchi shelf, McTigue (2013) reported δ15N values for single
individuals of Eunoe sp. and Byglides sp. that are consistent with carnivory. In a Laminaria
forest at 2.5 m water depth near Roscoff, Leclerc et al. (2013) saw clearly carnivorous δ15N
signatures in Harmothoe sp.
Guild membership
More recent findings largely support results in F&J. Most free-living species are carnivores.
For most species, however, it is unknown whether they are active hunters (motile) or sit-andwait predators (discretely motile). Added observations on carnivory (e.g., Abrams et al. 1990),
however, cast further doubt upon early reports of deposit feeding in Bylgides sarsi (F&J), as
does basic gut morphology. Some polynoid species at vents and seeps include microbial mat
material and microbial detritus in their diets, and at least one species is a mat specialist. Many
polynoids include algal fragments in their diets, but the nutritional significance of this inclusion
remains obscure. Some commensals take advantage of diet selection by their hosts, feeding
kleptoparasitically or coprophagically. “Hitchiking” commensals are “parasitic” on host motility,
enhancing prey encounter rates without incurring motility costs, but may also consume host
tissues. Most polynoids are epibenthic or reside in tubes and burrows of their hosts, but some do
burrow. Drieschia and Podarmus spp. are holoplanktonic.
Research questions and opportunities
• Strong evidence of deposit feeding (i.e., presence of surfactant micelles in digesta or net
growth on a know diet of sediments) is lacking.
• In species that ingest macroalgae, evidence of digestion and assimilation is still lacking.
• It would be interesting to know how carnivorous commensals living on moving hosts
filter out mechanical “noise” from their hosts to detect and capture other prey. Are these
commensalisms more likely to involve what was originally an actively moving scaleworm
rather than a sit-and-wait predator species, since the problem of filtering out self noise has
already been solved?
• No evidence yet exists for the functions of secretions produced by putative venom glands.
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Jumars, Dorgan & Lindsay
07 November 2014
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Glover AG, Goetze E, Dahlgren TG, Smith CR. 2005. Morphology, reproductive biology
and genetic structure of the whale-fall and hydrothermal vent specialist, Bathykurila
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Jumars, Dorgan & Lindsay
07 November 2014
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Pontodoridae, Phyllodocida
Diversity and systematics
Pontodoridae comprise a single species, Pontodora pelagica. The species reaches a maximum
length of about 0.5 cm, with 17 - 18 segments.
Habitat
P. pelagica is holopelagic and found in the upper mixed layer (Fernández-Álamo 2006) and mid
waters (Batistić et al. 2012).
Sensory and feeding structures
The rounded prostomium bears a single pair of dorsolateral antennae and a single pair of
unarticulated, ventrolateral palps, all four at the anterior of the prostomium and extended
laterally. A single pair of eyes is present. Nuchal organs are lateral and globular. The
peristomium is indistinct and may be limited to lips. The pharynx is muscular and axial. When
everted it carries sparse, pointed papillae externally and is tipped with a ring of papillae (Pleijel
2001).
Motility
Extent of motility is unknown. The species may be an active hunter or a sit-and-wait predator.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Jumars, Dorgan & Lindsay
07 November 2014
Illustrations
Pleijel (2001) provides a line drawing of body morphology, including long chaetae.
Feeding
Diets are unknown. Antennae, palps, and long neuropodial lobes suggest hydromechanical
detection capabilities. The muscular pharynx and small size suggest feeding on phytoplankton,
other protists or small zooplankton.
Guild membership
The species is motile or discretely motile and presumably macrophagous, but diet is unknown.
Research opportunities
• Any data on motility or feeding would be the first.
References
Batistić M, Jasprica N, Carić M, Čalić M, Kovačević V, et al. 2012. Biological evidence of a
winter convection event in the South Adriatic: A phytoplankton maximum in the aphotic
zone. Cont.Shelf Res. 44:57–71
Fernández-Álamo MA. 2006. Composition, abundance and distribution of holoplanktonic
polychaetes from the expedition “El Golfo 6311-12” of Scripps Institution of Oceanography.
Sci. Mar. 70:209–15
Pleijel F. 2001. ‘Minor’ holopelagic Phyllodocida. See Rouse & Pleijel 2001, pp. 121–3
Protodrilidae
Diversity and systematics
On the basis of both molecular genetics and morphological cladistics, Protodrilidae have recently
undergone major revision (Martínez et al. 2014). Six clades were distinguished and used to
describe and redefine corresponding genera. The count of named species is about 35, but is
expected to double quickly in view of the molecular results (Martínez et al. 2014). Adult lengths
are roughly 0.3 - 3 cm. Morphological resemblance to Saccocirrus appears to be convergent (Di
Domenico et al. 2014).
Habitat
The majority of protodrilids have been extracted from medium sands to gravels from the
intertidal to water depths of about 100 m. Within Protodrilus, species with particularly long
palps bearing bands of motile cilia and bacillary glands are characteristic of coarse sands (Di
Domenico et al. 2013, Martínez et al. 2013). In a survey of sandy beaches, Protodrilus spp. were
found with Saccocirrus in the swash zones of reflective beaches where wave flow is highest and
grain sizes are large (Di Domenico et al. 2009). At least some species of Protodrilus are able
to thrive in hypoxic conditions (Zaika & Sergeeva 2012). One Protodrilus species yet to be
described is apparently holopelagic in a lighted anchiline cave (Martínez et al. 2009, Wilkens et
al. 2009).
Sensory and feeding structures
Protodrilids bear a pair of ciliated, ungrooved palps (or tentacles) inserted ventrally on the
triangular or rounded prostomium, a pair of dorsolateral nuchal organs and sometimes a pair of
eyes (each a single cell). The palps or tentacles in Protodrilus have a central canal that is part of
the hydrostatic system of the worm (Purschke 1993). Species that live in medium to fine sands
have shorter palps than those from coarse sands and gravels with larger interstices (Martínez et
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Jumars, Dorgan & Lindsay
07 November 2014
al. 2013). Nuchal organs vary in shape among species. The peristomium is a complete ring.
Protodrilus spp. have a ventral, ciliated, muscular pharynx with a grating plate presumably used
in scraping bacteria and diatoms from sand grains. Astomus spp. lack a buccal opening and
functional gut altogether, but do not bear obvious symbionts (Jouin 1992, Rouse 2001).
Motility
Protodrilids glide over surfaces with cilia, and some species show undulatory swimming
(Martínez et al. 2013). Undulatory swimming is a short-lived escape behavior seen primarily in
large-bodied species of Lindrilus, Protodrilus and Megadrilus (Martínez et al. 2013). Especially
in Megadrilus, it may lead to fragmentation. Protodrilus has a duo-gland adhesive system on
the posterior margin of the pygidium for attaching to surfaces (Martin 1978a) as well as mucussecreting bacillary glands that facilitate ciliary gliding (Martin 1978b). More persistent or
frequent swimming would seem necessary in the holopelagic species to provide an adequate
particle encounter rate for feeding.
Illustrations
Martínez et al. (2013) combine stippled line drawings and micrographs very effectively to
illustrate one species from each of three of the six genera. Bailey-Brock et al. (2010) include
drawings of morphology of two Astomus spp. and of Protodrilus albicans. Di Domenico et
al. (2013) include light and SEM micrographs of Protodrilus spp. morphology, including the
muscular pharynx and ciliated region around the mouth. Jouin (1979) shows photographs and
drawings of the morphology of the gutless Astomus taenoides.
Feeding
Most protodrilids probably feed by removing organic-rich coatings from mineral grains
(Westheide 1990). Some Protodrilus spp. have been suggested to suspension feed on particulate
fluxes carried by pressure-driven interstitial flow (Di Domenico et al. 2013). The only specific
data on feeding that we found were for P. flavocapitatus from the Crimean coast that were
maintained for two months on a diet comprising Isochrysis galbana, Tetraselmis suecica,
Phaeodactylum tricornutum and Rhodomonas salina (Kopiy 2013), supporting the generally
accepted but poorly documented idea that Protodrilus feeds on microphytobenthos and bacteria
(von Nordheim 1983). The holopelagic species of protodrilid found in an anchiline cave
(Martínez et al. 2009, Wilkens et al. 2009) presumably encounters suspended phytoplankton
and other rich particles in its unique environment by direct interception through its swimming.
Astomus spp. appear to rely on epidermal microvilli for uptake of dissolved organic matter and
on epidermal vesicles and lysosomes for uptake of particles (Jouin 1979).
Guild membership
Protodrilids are motile and presumably feed on labile material. Astomus spp. appear to be
unique among annelids in existing solely on uptake of dissolved organic matter and particles
without internal bacterial mutualists. Two species of marine oligochaetes are also gutless
and osmotrophic, but take up inorganic compounds that are used by microbial symbionts in
chemoautotrophy (Felbeck et al. 1983). The holopelagic protodrilid may be unique among
polychaetes in being an active suspension feeder (using swimming to generate flow over its
encounter structures) that does not use a mucus bag.
Research questions and opportunities
• Tracer experiments to test uptake capacity of Astomus for specific organic compounds and
organic particles would be informative.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Jumars, Dorgan & Lindsay
07 November 2014
• Data on feeding behaviors and identities of ingested material in the field are lacking.
• Understanding of suspension feeding in the holopelagic species awaits both its morphological
and taxonomic description and analysis in a hydrosol filtration context.
References
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from the Hawaiian Islands and comparison with specimens from French Polynesia. Pac. Sci.
64:463–72
Di Domenico M, Lana PC, Garrafoni ARS. 2009. Distribution patterns of interstitial polychaetes
in sandy beaches of southern Brazil. Mar. Ecol. 30:47–62
Di Domenico M, Martínez A, Lana P, Worsaae K. 2013. Protodrilus (Protodrilidae, Annelida)
from the southern and southeastern Brazilian coasts. Helgol. Mar. Res. 67:733–48
Di Domenico M, Martínez A, Lana P, Worsaae K. 2014. Molecular and morphological
phylogeny of Saccocirridae (Annelida) reveals two cosmopolitan clades with specific habitat
preferences. Mol. Phylogen. Evol. 75:202–18
Felbeck H, Liebezeit G, Dawson R, Giere O. 1983. CO2 fixation in tissues of marine oligochaetes
(Phallodrilus leukodermatus and P. planus) containing symbiotic, chemoautotrophic
bacteria. Mar. Biol. 75:187–91
Jouin C. 1979. Description of a free-living polychaete without gut: Astomus taenioides n. gen., n.
sp. (Protodrilidae, Archiannelida). Can. J. Zool. 57:2448–56
Jouin C. 1992. The ultrastructure of a gutless annelid, Parenterodrilus gen. nov. taenioides (=
Astomus taenioides) (Polychaeta, Protodrilidae). Can. J. Zool. 70:1833–48
Kopiy V. 2013. Some aspects of the biology and the present state of the population of Protodrilus
flavocapitatus (Polychaeta: Protodrilidae) in the coastal zone of Crimea (the Black Sea). J.
Black Sea/Mediterr. Environ. 19:162–8
Martin GG. 1978a. The duo-gland adhesive system of the archiannelids Protodrilus and
Saccocirrus and the turbellarian Monocelis. Zoomorphologie 91:63–75
Martin GG. 1978b. A new function of rhabdites: mucus production for ciliary gliding.
Zoomorphologie 91:235–48
Martínez A, Di Domenico M, Jörger K, Norenburg J, Worsaae K. 2013. Description of three
new species of Protodrilus (Annelida, Protodrilidae) from Central America. Mar. Biol. Res.
9:676–91
Martínez A, Di Domenico M, Rouse GW, Worsaae K. 2014. Phylogeny and systematics of
Protodrilidae (Annelida) inferred with total evidence analyses. Cladistics doi:10.1111/
cla.12089 in press
Martínez, AM, Palmero AM, del Carmen Brito M, Núñez J, Worsaae K. 2009. Anchialine fauna
of the Corona lava tube (Lanzarote, Canary Islands): diversity, endemism and distribution.
Mar. Biodivers. 39:169–82
Purschke G. 1993. Structure of the prostomial appendages and the central nervous system in the
Protodrilida (Polychaeta). Zoomorphology 113:1–20
Rouse GW. 2001. Protodrilida Pettibone, 1982. See Rouse & Pleijel 2001, pp. 281–4
von Nordheim H. 1983. Systematics and ecology of Protodrilus helgolandicus sp. n., an
interstitial polychaete (Protodrilidae) from subtidal sands off Helgoland, German Bight.
Zool. Scr. 12:171–7
Wilkens H, Iliffe TM, Oromí P, Martínez A, Tysall TN, et al. 2009. The Corona lava tube,
Lanzarote: geology, habitat diversity and biogeography. Mar. Biodivers. 39:155–67
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Jumars, Dorgan & Lindsay
07 November 2014
Zaika V, Sergeeva N. 2012. Deep-water benthic polychaetes (Vigtorniella zaikai and Protodrilus
sp.) in the Black Sea as indicators of the hydrogen sulfide zone boundary. Vestnik Zoologii
46:e-19–e-27
Protodriloididae
Diversity and systematics
The interstitial family Protodriloididae comprises two species of Protodriloides. Morphologybased grouping of Protodriloididae with Protodrilidae and Saccocirridae into Protodrilida has not
been upheld by molecular methods (Di Domenico et al. 2014). The two Protodriloides species
are 1 - 2 cm long and very thin (Di Domenico et al. 2014).
Habitat
Protodriloides spp. are interstitial in sandy beaches.
Sensory and feeding structures
The single pair of palps or tentacles in Protodriloides differ from Protodrilus: They lack a
central canal (Purschke & Jouin 1988), insert terminally on the prostomium, and are only
sparsely ciliated (Di Domenico et al. 2014). Nuchal organs are dorsal rather than dorsolateral
(Di Domenico et al. 2014). The pharynx of Protodriloides chaetifer has a ventral muscular bulb
and investing muscles that move the mouthparts forward but no tongue-like organ for scraping.
Motility
Whereas Protodrilus spp. and other meiofaunal annelids that move by ciliary gliding lack
inextensible cuticle fibers, Protodriloides move by elongating and contracting the body, and have
cuticular fibers (Jouin 1966). Purschke & Jouin (1988) described locomotion as “muscular and
ciliary.”
Illustrations
Rouse (2001) includes a drawing of Protodriloides chaetifer.
Feeding
Purschke & Jouin (1988) suggested that lack of a scraping, tongue-like organ may indicate
carnivory on small, interstitial animals rather than scraping of bacteria and diatoms. There are no
published data, however, on diets.
Guild membership
We presume that the species are motile and that they must feed on labile material due to their
small gut volumes.
Research opportunities
• Any feeding data or quantitative information on motility would be the first.
References
Di Domenico M, Martínez A, Lana P, Worsaae K. 2014. Molecular and morphological
phylogeny of Saccocirridae (Annelida) reveals two cosmopolitan clades with specific habitat
preferences. Mol. Phylogen. Evol. 75:202–18
Jouin C. 1966. Morphologie et anatomie comparée de Protodrilus chaetifer Remane et
Protodrilus symbioticus Giard, création du nouveau genre Protodriloides (Archiannélides).
Cah. Biol. Mar. 7:139–55
Purschke G, Jouin C. 1988. Anatomy and ultrastructure of the ventral pharyngeal organs of
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Protodriloididae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Saccocirrus (Saccocirridae) and Protodriloides (Protodriloidae fam. n.) with remarks on the
phylogenetic relationships within the Protodrilida (Annelida: Polychaeta). J. Zool. 215:405–32
Rouse GW. 2001. Protodrilida Pettibone, 1982. See Rouse & Pleijel 2001, pp. 281–4
Protomyzostomatidae, Myzostoma
Diversity and systematics
The recent family revision by Summers & Rouse (2014) left the family-level description
unchanged (Grygier 2000). The sole genus, Protomyzostomum comprises 6 species (Summers et
al. 2014). They are oval discs (longer than wide) up to 3.2 cm long (Grygier 2000).
Habitat
Protomyzostomum spp. are known from high-latitude and Japanese waters in gonads or bursae of
brittlestar and basketstar hosts.
Sensory and feeding structures
Eyes and nuchal organs are absent. Lateral organs are small in most species and are dorsally
located. Anus and mouth are terminal. A proboscis is absent, and the pharyngeal muscle bulb
is reduced relative to free-living myzostomes, but a degree of protrusion and retraction of the
pharynx is feasible (Grygier 2000). Four to 25 pairs of diverticula ramify irregularly off a long
stomach (Grygier 2000).
Motility
Parapodia are reduced, implying limited motility within the host.
Illustrations
Grygier (2000) draws dorsal and saggital section views of P. polynephris. Summers et al. (2014)
show color photographs of live specimens of two species of Protomyzostomum.
Feeding
All species feed on host tissues.
Guild membership
Protomyzostomatids are relatively sessile endoparasites of their hosts.
Research opportunities
• Energetic and fitness costs to the host are not quantified but are probably high, as castration
has been reported (Fedotov 1912, 1914; Summers & Rouse 2014).
References
Fedotov D. 1912. Protomyzostomum polynephris, eine neue Myzostomidenart. Zool. Anz.
39:649–53
Fedotov D. 1914. Die anatomie von Protomyzostomum polynephris Fedotov. Z. Wiss. Zool.
109:631–96
Grygier MJ. 2000. Class Myzostomida. See Beesley et al. 2000, pp. 297–329
Summers MM, Al-Hakim I, Rouse GW. 2014. Turbo-taxonomy: 21 new species of Myzostomida
(Annelida). Zootaxa 3873:301-44
Summers MM, Rouse GW. 2014. Phylogeny of Myzostomida (Annelida) and their relationships
with echinoderm hosts. BMC Evol. Biol. 14:170, 15 pp.
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Psammodrilidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Psammodrilidae
Diversity and systematics
Psammodrilidae are known from 5 species in a single genus. Two species, Psammodrilus
aedificator and P. fauveli, have been suggested to be progenetic, showing close resemblance to
juvenile P. balanoglossoides (Swedmark 1964, Struck 2006). Based on morphology typical of
interstitial organisms (e.g., well-developed cilia, no cuticle, reduced or absent coelom) Worsaae
& Kristensen (2005) suggested the opposite, that larger psammodrilids may have evolved from
the smaller P. fauveli. Position within Annelida is uncertain. Adults are < 1 to 8 mm long.
Habitat
Psammodrilids are considered interstitial in coarse sediments, although only Psammodrilus
fauveli is < 1 mm long (Worsaae & Kristensen 2005).
Sensory and feeding structures
The prostomium is elongate, rounded and completely ciliated. Psammodrilidae lack anterior
appendages but have elongate thoracic cirri. An anterior tuft of cilia is termed the apical sensory
organ (Worsaae & Sterrer 2006). Some species have ciliated pits, but disagreement exists about
whether they constitute nuchal organs (Rouse 2001). Two pairs of eyes may be present (Rouse
2001). The peristomium is a complete ring containing the mouth.
The unusual pharyngeal apparatus in P. balanoglossoides, which Swedmark (1964) describes
as functioning like a pump to enable the animal to remove diatoms and other microflora from
sand grains, is lacking in the smaller P. fauveli. Kristensen & Norrevang (1982) described the
pharynx of P. aedificator as eversible whereas that of P. balanoglossoides is non-eversible, and
the mouth of the former is O-shaped whereas that of the latter is Y-shaped. Psammodrilids
have a unique collar region in which the epidermal cells have microvilli and lack cilia and
cuticle, which Worsaae & Kristensen (2005) suggest may be an absorptive surface for uptake of
dissolved molecules from seawater.
Motility
There appears to be considerable variability in motility within the family. Swedmark (1964)
described Psammodrilus fauveli as motile, using ciliary movement, and P. balanoglossoides
as semi-sessile, building thin, transparent mucus tubes that adhere to sand grains. The latter
was observed to swim using cirri as propellers (Kristensen & Norrevang 1982). P. aedificator
is less motile than P. balanoglossoides. It builds pyramidal “houses” out of sand grains and
extends the anterior out of an apical opening to graze on surrounding grain surfaces (Kristensen
& Norrevang 1982). Unique among annelids, with the possible exception of Lobatocerebridae
(Rieger 1980), whose affinities with Annelida are uncertain (Rouse & Fauchald 1995), the
body is covered with cilia (Worsaae & Sterrer 2006). Worsaae & Sterrer (2006) described P.
moebjergi and P. swedmarki as moving by ciliary action on lateral, ventral, and dorsal surfaces.
They can move forward or backward and attach to substrate with the thoracic cirri and pygidium,
suggesting potential for inchworm-like locomotion. Changes in body width and length indicate
muscular as well as ciliary locomotion (Worsaae & Sterrer 2006).
Illustrations
Kristensen & Norrevang (1982; Fig. 1) include an excellent stippled line drawing of
Psammodrilus aedificator extending its anterior out of its sand-grain house to feed. They
also include scaled drawings of 2 other species. Worsaae & Sterrer (2006) include drawings,
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Jumars, Dorgan & Lindsay
07 November 2014
photographs, and scanning electron micrographs of two species of Psammodrilus. The latter
show cilia covering most of the animals, including the thoracic cirri, and their Fig. 8A clearly
shows the open mouth.
Feeding
P. aedificator from West Greenland was described as feeding on “detritus and diatoms, which are
“vacuum cleaned” from the surroundings as far as the mouth reaches (Kristensen & Norrevang
1982). Large particles were often observed in the pharynx, but they never passed beyond the
collar region. Sometimes detritus balls were regurgitated. Thus, the pharynx apparatus seems
to work as a sorting mechanism in addition to its function as a suction pump (Kristensen &
Norrevang 1982).
Guild membership
Small size indicates feeding on labile material, and motility is variable (motile to discretely
motile) within the family.
Research questions and opportunities
• Diverse motility and unusual ciliation make psammodrilids good targets for studies of
locomotion and interactions between diet and motility.
• Tests of uptake kinetics for organic solutes would be informative.
References
Kristensen RM, Nørrevang A. 1982. Description of Psammodrilus aedificator sp. n. (Polychaeta)
with notes on the Arctic interstitial fauna of Disco Island, W. Greenland. Zool. Scr. 11:265–
79
Rieger RM. 1980. A new group of interstitial worms, Lobatocerebridae nov. fam.(Annelida) and
its significance for metazoan phylogeny. Zoomorphologie 95:41–84
Rouse GW. 2001. Psammodrilidae Swedmark, 1952. See Rouse & Pleijel 2001, pp. 293–5
Rouse GW, Fauchald K. 1995. The articulation of annelids. Zool. Scr. 24:269–301
Struck TH. 2006. Progenetic species in polychaetes (Annelida) and problems assessing their
phylogenetic affiliation. Integr. Comp. Biol. 46:558–68
Swedmark B. 1964. Interstitial fauna of marine sand. Biol. Rev. 39:1–42
Worsaae K, Kristensen RM. 2005. Evolution of interstitial polychaetes. Hydrobiologia
535/536:317–38
Worsaae K, Sterrer W. 2006. Description of two new interstitial species of Psammodrilidae
(Annelida) from Bermuda. Mar. Biol. Res. 2:431–45
Pseudocirratulidae
Diversity and systematics
Pseudocirratulus kingstonensis, the only species in the family, is known from two specimens
reaching 14.5 cm in length and 2.5 mm in diameter.
Habitat
They were collected in the intertidal zone of Jamaica and St. Thomas.
Sensory and feeding structures
Eyes and nuchal organs have not been described. No appendages or gills remain on the
specimens (Petersen 1994), although gills were indicated in the original description (Augener
1918). The peristomium appears to have two complete rings (Augener 1918). The gut is simple
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07 November 2014
and tubular (Petersen 1994). Overall appearance of the worms is close to that of earthworms, but
no clitellum is present.
Motility
Lacking feeding appendages, the species is probably motile.
Illustrations
No illustrations are published.
Feeding
We guess that P. kingstonensis may be found to be a subsurface deposit feeder.
Feeding guild
We conjecture that P. kingstonensis is a motile, subsurface deposit feeder.
Research questions and opportunities
• Any data on motility or feeding would be the first.
References
Augener H. 1922. Über litorale polychäten von Westindien. Sitzungsberichte der Gesellschaft
der Naturforschende Freunde zur Berlin Jahrgang 1922:38-53
Petersen ME. 1994. Pseudocirratulus kingstonensis Augener, 1922: not a cirratulid but an
annelid of uncertain affinities (Polychaeta?: Pseudocirratulida new order, Pseudocirratulidae
new family). Mémoir. Mus. Natl Hist. 162: 634 [Abstract only]
Pulvinomyzostomatidae, Myzostoma
Diversity and systematics
Recent family revision of myzostomes left this family definition unchanged (Summers & Rouse
2014). Pulvinomyzostomum, the sole genus, grew to three named species, however (Summers
et al. 2014). Each species has a different body plan, but all are ≤ 6 mm long. In P. pulvinar the
female body is roughly in the shape of an upward facing suction cup, but with a small gap in
its rim at the posterior of the animal; males are < 0.1 times as long as females and ovoid disk
shaped. P. inaki has a more classic ovoid disk shape in the females, slightly longer than wide,
whereas the much smaller males are slightly wider than long (Summers et al. 2014). P. messingi
has converged on the “sausage bun” shape of Hypomyzostoma spp. (Summers et al. 2014).
Habitat
In P. pulvinar and inaki large females are found in the mouth and esophagus of their featherstar hosts, often with the anus protruding, whereas much smaller males roam more widely
(Grygier 2000, Summers et al. 2014). P. messingi adopts the same posture as Hypomyzostoma
spp., wrapped around an arm of its stalked crinoid host with its body axis parallel to the arm
(Summers et al. 2014). Differentiation of sexes in size and shape is not known.
Sensory and feeding structures
Nuchal organs and eyes are absent. In P. pulvinar, lateral organs, thought to be both mechanoand chemosensory, are located around the rim of the “suction cup” (dorsolaterally). Mouth and
anus open dorsally. In P. inaki, lateral organs are ventrolateral, and mouth and anus are terminal.
In P. messingi, lateral organs are also ventrolateral, but mouth and anus are ventral. Probosces in
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Jumars, Dorgan & Lindsay
07 November 2014
all three species are retractile. In P. pulvinar the pharynx opens into a long stomach with three
pairs of branching diverticula. Internal morphology of the other two species is not yet described.
Motility
All three species are discretely motile, and the dwarf males may be somewhat more motile or at
least not so restricted to the mouth region of the host.
Illustrations
Grygier (2000, Fig. 2.19) provides clearly labeled, stippled line drawings of P. pulvinar in
both dorsal view and saggital section. Summers et al. (2014) show color photographs of live
specimens of both of the other two species.
Feeding
Despite gross differences in body plans, all three species are kleptoparasites on food streams of
their hosts. Neither of the oral kleptoparasites fully blocks the mouth of its host.
Guild membership
All three species are discretely motile kleptoparasites using a muscular proboscis to divert host
food streams.
Research questions and opportunities
• Energy costs to the host from kleptoparasitism are unknown.
• P. messingi affords an opportunity to run experiments on selective ingestion by presenting
visually recognizable particles to the host and video recording food passage upstream, at the
location of the myzostome, and downstream to test for selective ingestion. This design is
reminiscent of classic experiments on food choice by birds from items passing on a conveyor
belt (e.g., Krebs et al. 1977). Myzostome selectivity would be more difficult to address for
the other two species.
References
Grygier MJ. 2000. Class Myzostomida. See Beesley et al. 2000, pp. 297–329
Krebs JR, Erichsen JT, Webber MI, Charnov EL. 1977. Optimal prey selection in the Great Tit
(Parus major). Anim. Behav. 25:30–8
Summers MM, Al-Hakim I, Rouse GW. 2014. Turbo-taxonomy: 21 new species of Myzostomida
(Annelida). Zootaxa 3873:301-44
Summers MM, Rouse GW. 2014. Phylogeny of Myzostomida (Annelida) and their relationships
with echinoderm hosts. BMC Evol. Biol. 14:170, 15 pp.
Sabellariidae, Sabellida
Diversity and systematics
Sabellariidae comprise about a dozen genera with a total of about 130 species. Most are 1 - 6 cm
long. Capa et al. (2012) and Hutchings et al. (2012) used morphology and molecular genetics
to revise the family. Sabellariids on that basis are clearly monophyletic, but their relationship to
other Sabellida (Fabriciidae, Sabellidae, Serpulidae and Siboglinidae) remains murky, with the
possibility that they may be more closely related to Spionidae (Capa et al. 2012).
Habitat
Sabellariids are known as sand-mason worms and usually build their tubes either attached to hard
substrata or to other sabellariid tubes, in some cases forming massive reefs, but some species
are solitary. The majority of species inhabit high-energy, shallow-water environments where
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Sabellariidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
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Jumars, Dorgan & Lindsay
07 November 2014
sand transport is frequent. Selection for tube materials can be strong, for example for particular
foraminiferan species when foraminiferan tests are scarce in ambient sediments (Reuter et al.
2009). Despite the use of sand for tube building, several species are bathyal, and a few are
abyssal (Kirkegaard 1996).
Field observations and experiments suggest great sensitivity to fluid and sediment dynamics.
Where this gregarious species inhabits energetic regimes, Phragmatopoma californica tube
openings flare to produce a honeycomb. Where flows are weaker and more unidirectional P.
californica produces hoods that face into the current, with adjacent tube hoods facing in the same
direction (Thomas 1994). A clear effect of such flow blockage is induced local deposition.
Laboratory results on habitat use have been difficult to interpret. Davies et al. (2009) built a
device that used vortical flow and an airlift system to suspend sand in an attempt to dynamically
maintain a steady concentration of suspended material. They found that Sabellaria spinulosa
showed positive tube growth when exposed to suspended sediments and net tube loss when
not. Worms showed moderate bias in tube building toward particles below the modal size of
sediments placed in the tank, but the results are difficult to interpret because no attempt was
made to correct for potential size selection by the air-lift resuspension system or to scale flows
and suspended loads produced in the apparatus to those in the field. Similar fossil tubes date
back to at least the Middle Jurassic (Lazăr & Grădinaru 2014).
Sensory and feeding structures
All sabellariids carry a pair of ciliated, grooved, peristomial palps with nuchal organs just above
their bases. A median cirrus (sometimes called a medial organ) and eyes may be present on the
diminutive prostomium, but antennae are absent. The peristomium is limited to lips around the
mouth. One to three rows of paleae of the first chaetiger in whorls form an operculum that can
cover the tube opening. Most species have ventral, paired, ciliated, grooved, tentacular, oral
filaments originating from inner portions of the opercular lobes anterior to the mouth. Filaments
may be simple or branching. Posterior to the ventral mouth is a (tube-) building organ capable
of gluing sand grains into the tube (Rouse 2001). Palp length varies inversely with elaboration
of oral filaments, which are particularly reduced in some deep-sea species of Phalacrostemma
(Hartman 1944; Lechapt & Kirtley 1998).
Motility
Adults appear unable to move and build a new tube if displaced, so we regard sabellariids as
sessile.
Illustrations
Capa et al. (2012) and Hutchings et al. (2012) provide informative line drawings, photographs
and scanning electron micrographs of feeding structures. Nishi & Nuñez’ (1999, Fig. 5) in situ
photograph of a bristling Lygdamis wirtzi is not to be missed.
Feeding
Nishi & Nuñez (1999) published a photograph of Lygdamis wirtzi in situ, revealing an impressive
paired array of branching, flow-impeding spines surrounding the projecting opercular peduncles,
with ~ 100 pairs of tentacular filaments embedded within this array. In suspension-feeding
mode, the ventral surface of the animal faces upstream in both P. californica and Sabellaria
alveolata (Nishi & Nuñez 1999, Dubois et al. 2005), and presumably in other species.
Dubois and coworkers in the most extensive sabellariid feeding studies to date placed
sections cut from a Sabellaria alveolata reef into a laminar flow apparatus. On a mixture of
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
phytoplankton, they found zero retention of particles < 2 µm in diameter, roughly 50% retention
of particles 3 µm in diameter and roughly 90% retention of particles 5 µm in diameter (Dubois
et al. 2003). Dubois et al. (2006) described ingestion and rejection paths for particles in S.
alveolata post capture. Their interpretations of capture paths and mechanisms have been more
controversial (Riisgård & Nielsen 2006, Dubois et al. 2006). In particular, gut contents establish
that grains with higher settling velocities are encountered and ingested in the field (Riisgård &
Nielsen 2006) than were used in the laboratory. Riisgård & Nielsen’s (2006) detailed analysis
led them to conclude that S. alveolata is a passive suspension feeder that can supplement its
seston diet by surface deposit feeding. This inference is consistent with flow-impeding tube
structures and spines.
There remains a gap in observations of particle encounter and feeding rates under natural
flow velocities and suspended loads. Given the very slow particle transport velocities
documented near tentacular filaments by Dubois et al. (2005) compared to the flow velocities
expected in the field, coupled with the very low clearance rates observed (Dubois et al. 2009),
it seems very likely that inertial and gravitational mechanisms play a large role in particle
encounter in energetic field environments. The spine arrays illustrated by Nishi & Nuñez (1999)
would provide excellent means to slow wave and current flows local to an individual worm,
allowing deposition onto the embedded feeding tentacles.
Guerin (2009) sampled Sabellaria spinulosa from shallow subtidal, natural and artificial reefs
in Poole Bay, southern England. Its δ15N consistently fell 1 - 2‰ higher than that of sympatric
Bispira volutacornis (Sabellidae), a primary consumer in this system. S. spinulosa from 15 - 35
m water depth in the Bay of Concarneau fell close to Euspira pulchella in 15N enrichment but >
1‰ above that of an unidentified sabellid (Rigolet et al. 2014). In the rocky intertidal zones of
the Kariega and Great Fish estuary coastal regions of eastern South Africa, δ15N values suggested
that Gunnarea gaimardi fed primarily on nearshore suspended material but that it supplemented
that diet with some zooplankton, placing it above Perna perna (mussels) but below Tetraclita
serrata (barnacles) in the food web (Richoux et al. 2014a). Lipid profiles indicated that G.
gaimardi had a diet rich in diatoms (Richoux et al. 2014b). Dubois & Colombo (2014) analyzed
a similar trio of species from the intertidal of the Bay of Douarnenez in Brittany. Sabellaria
alveolata again on average fell intermediate between the sympatric mussel (Mytilus edulis) and
barnacle (Chthamalus montagui) in trophic level, though the barnacle did not separate as clearly
from the sabellariid, especially in summer, and the diets of all three species could be explained as
species-specific and time-varying differing mixtures of Ulva, suspended particulate material and
sedimentary organic matter (Dubois & Colombo 2014). These data are consistent with earlier
results of Lefebvre et al. (2009) who found S. alveolata from the English Channel off Normandy
to be more enriched in 15N than any of four suspension-feeding molluscs. S. alveolata and
Lanice conchilega (Terebellidae) both showed greater dietary dependence on microphytobenthos
and macroalgae than did any of the molluscs.
Guild membership
Sabellariids are passive, sessile suspension feeders typically inhabiting high-energy, sedimenttransporting regimes. They probably rely on gravitational deposition enhanced by slowing of
the ambient flow by form drag and skin friction with their projecting structures, together with
direct interception and inertial impaction. We concur with Riisgård & Nielsen’s (2006) analysis
that the diet is likely supplemented by surface deposit feeding. The inverse relationship between
length of the palps and elaboration of oral filaments suggests that deeper-water species with
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
longer palps and fewer filaments may rely more extensively on deposit feeding.
Research questions and opportunities
• Quantification of clearance rates under realistic flow regimes and suspended loads remains to
be accomplished, as does any quantitative estimate of the contribution from surface deposit
feeding.
• Tube and spine structures strongly suggest that members of this family feed by creating flow
impedance that induces gravitational deposition onto the oral filaments or within reach of the
palps. This hypothesis remains to be tested.
References
Capa M, Hutchings PA, Peart R. 2012. Systematic revision of Sabellariidae Johnston, 1865
(Polychaeta) and relationships with other polychaetes. Zool. J. Linn. Soc. Lond. 164: 245–84
Davies AJ, Last KS, Attard K, Hendrick VJ. 2009. Maintaining turbidity and current flow in
laboratory aquarium studies, a case study using Sabellaria spinulosa. J. Exp. Mar. Biol. Ecol.
370:35–40
Dubois S, Barillé L, Cognie B. 2009. Feeding response of the polychaete Sabellaria alveolata
(Sabellariidae) to changes in seston concentration J. Exp. Mar. Biol. Ecol. 376:94–101
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Sabellidae, Sabellida
Diversity and systematics
Sabellidae comprises about 465 species in about 40 genera, 6 of them monotypic. It no longer
contains Fabriciinae, which have been raised to familial level and have been found to be more
closely related to Serpulidae than to Sabellidae (Kupriyanova & Rouse 2008). Relationships
within the family (former Subfamily Sabellinae) are still unresolved (Capa et al. 2011) and
complicated by cryptic species and invasives (Capa et al. 2013). Typical body lengths are 1 - 10
cm, although the largest species can reach nearly 0.5 m (Rouse 2001).
Habitat
Sabellidae are most common in shallow water attached to hard substrata and infaunal in
sediments, but there are bathyal and abyssal representatives on hard and soft substrata, and even
hadal representatives (Paterson et al. 2009). Sabellidae are tube builders. Most build tubes from
sediment grains. Glomerula piloseta secretes a calcareous tube (Perkins 1991, Vinn et al. 2008).
Sensory and feeding structures
The prostomium comprises the tentacular crown of sabellids, made up of a laterally paired set of
up to several hundred radioles, each with a band of tissue that continues ventrally to the mouth
and includes a pair of pit-like nuchal organs just above the mouth. Eyes in some species are
compound like those of arthropods, and can occur on the tips of the radioles. The peristomium is
a complete, often collared, ring and can bear a pair of eyespots (Rouse 2001).
Motility
Sabellids are regarded as sessile (F&J).
Illustrations
Rouse (2001) provides informative stippled line drawings and photographs displaying basic
morphology. Capa et al. (2013) provide some striking photographs of Branchiomma species.
Feeding
Understanding of suspension-feeding mechanisms in sabellids has advanced substantially. They
generally feed in currents much faster than their own cilia can produce, as measurements by
Merz (1984) in both the laboratory and field documented for Eudistylia vancouveri. The cilia
work to alter particle trajectories and enhance encounter rates when particles approach at very
close range (Riisgård et al. 2002). A dominant mechanism of particle encounter in all the species
analyzed so far is unsteady fluid and particle motion induced by the driving lateral cilia on the
pinnules effecting encounter with the mucus-carrying ciliary tract on the downstream side of the
pinnule (e.g., Mayer 2000). As one might expect, the interaction of ambient flow with this ciliary
mechanism maximizes successful capture rates at intermediate ambient flow speeds and with
particular postures and orientations of the branchial crown (Nash & Keegan 2003). Histological
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sections of Bispira volutacornis collected at 10 m water depth on the west coast of Ireland
documented that the major food items were resuspended benthic diatoms, and experiments with
carmine particles established a mean gut residence time for undigested particles of this size to be
7.7 h at 14˚C (Nash & Keegan 2003).
The most detailed and thoroughly analyzed information on suspension-feeding rates and
mechanics exists for Sabella pavonina collected by SCUBA from 30 m water depth in the
Gullmarsfjord (Riisgård & Iverson 1990) and for Euchone papillosa recovered from cores
at 75 m depth in the oligotrophic Gulf of Lions (Riisgård et al. 2002). S. pavonina could be
maintained for months on monocultures of Phaeodactylum tricornutum or Dunaliella marina. S.
pavonina filtered continuously even at very low seston concentrations, and filtering represented <
1% of its total energetic expenditure. Slowing filtration rate with decreasing temperature may be
accounted for entirely by the change in fluid viscosity (Riisgård & Ivarsson 1990). This species’
peak retention efficiency was for particles about 3 µm diam., but remained high for particles as
large as 8 µm (Jørgensen et al. 1984). Maximal filtering rate measured on Dunalliella marina or
Rhodomonas sp., was 114.5 liters h-1 g-1 dry wt., the highest rate so far reported for any sabellid
or serpulid (Jordana et al. 2001). Filtration rates decreased above a cell concentration of about 4
× 103 cells ml-1, likely because the gut could be kept filled at a lower filtering rate. The measured
filtration rates are apparently limited by ingestion rate and digestion time, however, as there is
no evidence that ciliary activity decreases at high food concentrations (Riisgård et al. 2002).
Numerical simulation of the apparently dominant capture mechanism qualitatively reproduced
observed particle paths (Mayer 1994) but substantially underestimated observed encounter
rates (Mayer 2000); the model only partially captures the relevant particle and fluid dynamics.
Euchone papillosa feeding on 6 µm diam. Rhodomonas sp. also appeared to use primarily the
same downstream capture mechanism and showed a remarkably similar filtration rate of 115
liters h-1 g-1 dry wt. For Potamilla occelata, Schizobranchia insignis, Eudistylia vancouveri and
two serpulid species, area of ciliary bands (A, mm2) scales with worm dry wt. (W, mg) as ln A =
3.59 + 0.648 ln W (r 2 = 0.99, Henderson & Strathmann 2000).
Shumway et al. (1988) measured respiration and filtration rates in Myxicola infundibulum
from the shallow subtidal Damariscotta River estuary in Maine. They estimated a filtration rate
of 2.78 liters h-1 g-1 dry wt. Riisgård et al. (2002) suggested that they may have underestimated
potential filtration rate because of the high cell concentrations used (2 - 3.5) × 104 cells ml-1).
Shumway et al. (1988) measured similar clearance rates on three different species of microalgae.
When they fed a mixture of three (but not the same three) microalgae, they observed a wider
range of species-specific clearance rates, suggesting selective feeding despite only a small range
in cell diameters.
Other species of sabellids have gained interest in aquaculture contexts, one as a pest. Native
to the intertidal of South Africa, Terebrasabella heterouncinata settles on the growing edges
of intertidal gastropod shells, inducing the gastropod to produce the worm’s tube and thereby
leaving a flaw in the shell. The worm suspension feeds on particles carried by currents past the
shell. T. heterouncinata can reach epidemic levels in abalone farms, reducing abalone growth
rates and market values (Chalmers 2002). The worm grew faster on abalone when the abalone
received commercial feed rather than kelp, suggesting that food quality for this suspension feeder
was enhanced in the feed (Chalmers 2002). Experiments with microencapsulation show that T.
heterouncinata ingests particles up to about 30 µm in diameter (Shields et al. 1998).
Branchiomma luctuosum and Sabella spallanzanii have garnered interest in multitrophic
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aquaculture as potential “biofilters” for suspended particles, including bacteria. In paired
experiments with natural suspensions, Sabella spallanzanii removed a greater quantity of
protein-containing particles whereas Branchiomma luctuosum removed more lipid- and
carbohydrate-containing particles (Cavallo et al. 2007). The basis for this statistically significant
difference in selection is unknown. Both species, collected from the Gulf of Taranto, showed
high clearance rates in laboratory experiments with pure cultures of Vibrio alginolyticus,
with retention efficiencies in S. spallanzanii and B. luctuosum, respectively, of 70 and 98%.
Clearance rates were estimated at 12.4 and 43.2 liters h-1 g-1 dry wt, respectively, at relatively
low cell concentrations (Licciano et al. 2005). The ability of S. spallanzanii to concentrate
multiple species of bacteria in the field was confirmed in field collections (Stabili et al. 2006).
Similar abilities have been shown in invasive (to the Mediterranean) Branchiomma bairdi
(Stabili et al. 2014). An independent estimate of maximal clearance rate in S. spallanzanii
invasive to Australia was 2.7 liters h-1 g-1 dry wt. (Clapin 1996 cited in Lemmens et al. 1996),
but experimental details have not been published. Estimates may in this and other species be
influenced by circadian rhythms: S. spallanzanii shows light-entrained fan activity, higher in the
dark (Aguzzi et al. 2006). Growth rates of S. spallanzanii in co-culture with mussels in a nonfed, eutrophic setting have been promising (Giangrande et al. 2014).
Carlier et al. (2007) in the Bay of Banyuls-sur-Mer found δ13C and δ15N in Megalomma
vesiculosum equal to their values in Lanice conchilega (Terebellidae). Trophic level is difficult
to estimate because neither planktonic nor benthic microalgal signatures were measured. M.
vesiculosum from a seagrass meadow near Roscoff showed δ15N‰ indicative of feeding even
lower in the food web (Ouisse et al. 2012). McMahon et al. (2006) analyzed stable isotopic
content of invertebrates from an intertidal site in Svalbard and did tracer uptake experiments
with 13C-labeled ice algae. Euchone analis’ isotopic signature was consistent with feeding
on phytoplankton rather than ice algae, and it took up relatively little of the labeled ice algae.
McTigue (2013) studied sites of exploratory oil drilling on the Chukchi shelf and compared
them with nearby reference sites. Euchone analis (n = 3) from the drilled sites showed δ15N
2.5‰ above that of net phytoplankton. Leclerc et al. (2013) studied seasonal change in trophic
relations in a Laminaria forest 2.5 m below sea level near Roscoff. The δ13C in Branchiomma
bombyx showed significant change in diet between November and March. Although not
statistically significant, δ15N also showed a shift toward lower enrichment in March, consistent
with greater dependence then on phytoplankton. Values of δ15N in both seasons were consistent
with feeding at a low trophic level, although those in Amphiglena mediterranea (sampled
only in November) were even lower. Euspira pulchella from 15 - 35 m water depth in the
Bay of Concarneau fell close to Sabellaria spinulosa (Sabellariidae) in δ15N, near the higher
end of values seen in suspension-feeding polychaetes there and > 1‰ higher than seen in an
unidentified sabellid. Of all the polychaetes sampled by Sokołowski et al. (2014) at 100 m water
depth in Hornsund, Spitsbergen, Chone paucibranchiata showed the least 15N enrichment.
Stable isotopic measurements for sabellids identified only to the family level generally are
consistent with feeding one trophic level above the local microalgae or the local suspended
organic materials, but with notable exceptions. Sabellids from the southeastern Australian shelf
showed low δ15N (Davenport & Bax 2002). Sabellids from 18 - 30 m water depth off King
George Island, Antarctica, showed δ13C indicative of feeding on phytoplankton (Corbisier et al.
2004). In shallow Ariake Sound (< 30 m) in southern Japan, sabellids had δ13C and δ15N values
very close to those of a brachiopod (Yokoyama et al. 2009). Sabellids at 1080 m water depth
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in the Faroe-Shetlands Channel had a δ15N between those of unspecified Ampharetidae and
Terebellidae (Gontikaki et al. 2011). Sabellidae similarly showed low δ15N in the southeastern
Chukchi Sea (Feder et al. 2011) and in a Posidonia bed at 5 - 8 m water depth off Mallorca
Island (Deudero et al. 2011). Dunton et al. (2012) sampled estuaries and lagoons draining
into the Beaufort Sea and compared invertebrates caught there with those on the Beaufort Sea
shelf. The lagoon and estuarine sabellids fell near Spionidae in their stable isotope contents and
were consistent with feeding on suspended organic matter. The shelf sabellids, however, were
enriched in 15N by 4.7‰ over shelf suspended organic matter; no phytoplankton were sampled,
and the only other polychaete available for comparison was Maldane sarsi, which often shows
unusually high enrichment in 15N (See Maldanidae, herein). McTigue (2013) at the drilled
sites on the Chukchi shelf reported 1 unidentified sabellid with δ15N slightly less enriched than
his net phytoplankton sample; 2 sabellids collected at control sites, however, had δ15N 3.6‰
above that of local net phytoplankton. Without taxonomic resolution, site and species effects
are confounded. Løkken (2013) found sabellids in shallow water (1 - 25 m) of Isfjorden,
Svalbard to have the lowest δ15N of any polychaete collected. Fedosev et al. (2014) studied
a shallow-water (6 - 18 m) sand community off southern Vietnam; sabellids had the lowest
δ15N and δ13C enrichments of any polychaete sampled (close in δ15N to Spionidae), but neither
microphytobenthos nor phytoplankton values were measured.
Sweetman et al. (2010) undertook laboratory incubations of cores from a mangrove swamp
in Pearl Harbor, Hawaii, introducing 13C-labeled Chlorella sp. Sabellidae showed high uptake of
the labeled cells. Somewhat surprisingly, unspecified sabellids were second only to unspecified
capitellids in concentrating poly- and perfluorinated compounds in shallow water of the Mai Po
Marshes Nature Reserve in Hong Kong (Loi et al. 2011). Nephtyids, however, were the only
other polychaetes assayed. Through uptake and concentration mechanisms that are not well
known, some sabellids show extraordinary capability to concentrate vanadium in their branchial
crowns—to an extent that deters predators (Fattorini & Regoli 2012).
Guild membership
All the data appear consistent with the classification of sabellids as sessile, mixed (ciliary)
suspension feeders largely dependent upon bottom currents to bring particles within range
of their downstream collecting systems. Food sources may include bacteria, phytoplankton,
resuspenced microphytobenthos, or nonliving organic particles, providing substantial range in
stable isotopic signatures.
Research questions and opportunities
• Stable isotopic measurements on sabellids identified to the species level could provide
additional insight into diet and partitioning among sympatric species.
• Diet analysis in species and locations showing unexpectedly high 15N enrichment would be
informative; size fractionation and cell-sorter separation of seston for stable isotopic analysis
could be revealing.
• It could be useful to displace solitary, infaunal species in experimental tests of the hypothesis
that they are unable to construct new tubes (are sessile rather than discretely motile).
• Do most species of sabellids show diel periodicity in feeding and to what water depths?
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Stabili L, Licciano M, Lezzi M, Giangrande A. 2014. Microbiological accumulation by the
Mediterranean invasive alien species Branchiomma bairdi (Annelida, Sabellidae): Potential
tool for bioremediation. Mar. Poll. Bull. 86:325–31
Sweetman AK, Middelburg JJ, Berle AM, Bernardino AF, Schander C, et al. 2010. Impacts
of exotic mangrove forests and mangrove deforestation on carbon remineralization and
ecosystem functioning in marine sediments. Biogeosciences 7:2129–45
Vinn O, ten Hove HA, Mutvei H. 2008. On the tube ultrastructure and origin of calcification in
sabellids (Annelida, Polychaeta). Palaeontology 51:295–301
Yokoyama H, Sakami T, Ishihi Y. 2009. Food sources of benthic animals on intertidal and
subtidal bottoms in inner Ariake Sound, southern Japan, determined by stable isotopes.
Estuar. Coast. Shelf Sci. 82:243–53
Saccocirridae
Diversity and systematics
Saccocirridae were formerly considered archiannelids. The 22 species of Saccocirrus had long
been grouped with Protodrilus (Hermans 1969) based on similar ventral pharyngeal organs
with a muscular buccal bulb and no jaws (Purschke & Jouin 1988). Molecular data have not
supported a close relationship with Protodrilus, however, and the position of Saccocirridae
within Annelida remains uncertain (Di Domenico et al. 2014c).
Numerous authors have noted two distinct groups of Saccocirrus based on morphological
differences: members of the group represented by S. papillocercus have paired gonads and
lack a muscular pharyngeal organ and ventral cilia, whereas that represented by S. krusadensis
have an unpaired gonad and have a muscular pharyngeal organ and ventral cilia (Brown 1981,
Bailey-Brock et al. 2003, Di Domenico et al. 2014c). This dichotomy is strongly supported by
molecular data, and the S. krusadensis clade has been placed in the new genus Pharyngocirrus
(Di Domenico et al. 2014c). Saccocirrids are 0.3 to ~ 2 cm long (Di Domenico et al. 2014c).
Habitat
Saccocirrids are interstitial in coarse sands. Di Domenico et al. (2014b, c) distinguished the
habitat of Pharyngocirrus spp. as being intertidal in sheltered intertidal or subtidal sediments
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having a redox gradient, whereas Saccocirrus spp. are found intertidally in exposed, oxygenated
beaches. S. pussicus is restricted largely to reflective beaches (Di Domenico et al. 2014a, b).
Both genera are found worldwide.
Sensory and feeding structures
Saccocirridae have two long, innervated palps and two small, prostomial eyes. Nuchal organs
are oval and elongated on the dorsum (Di Domenico et al. 2014b, c). Di Domenico et al. (2014a)
found palps to be more important in feeding in the Saccocirrus papillocercus morphotype,
specifically in S. pussicus found in exposed beaches.
S. papillocercus has an I-shaped mouth opening with both anterior and posterior slits
resulting in 4 lips (Purschke & Tzetlin 1996), in contrast to the slit-like mouth of Pharyngocirrus
(= Saccocirrus) eroticus (Gray 1969). The pharyngeal region of S. papillocercus resembles that
of Polygordius spp. in having dorsolateral ciliary folds (Purschke & Tzetlin 1996).
Motility
Gray (1969) described small individuals of S. eroticus as using smooth ciliary movement, with
transition to inch-worm-like movement in larger worms. Larger worms attach the tail lappets to
the substratum using a duo-gland adhesive system and extend the anterior using a combination
of ciliary beating and contraction of a thin layer of circular muscles. The anterior can be rapidly
contracted via longitudinal muscles, or the head can attach to the substratum, which Gray (1969)
suggested may be by mouth suction. Worms missing tails used chaetae to grip the substratum
during forward movement.
Di Domenico et al. (2014a) described a muscular swimming behavior produced by
undulatory movements of the trunk musculature in S. pussicus. It was observed in a few
specimens provided with a thin layer of sediment and still water.
Illustrations
Di Domenico et al. (2014b) provide informative micrographs of P. gabriellae and S. pussicus. Di
Domenico et al. (2014c) include illustrations of morphology of representatives of the two genera.
Gray (1969) shows drawings and photographs of external morphology and internal anatomy,
including musculature. Bailey-Brock et al. (2003) provide scanning electron micrographs of the
mouth and nuchal organs in species of both genera.
Feeding
Brown (1981) suggested that the species with ventral cilia, e.g., Pharyngocirrus krusadensis,
are herbivorous, based on Gray’s (1969) description of feeding with ventral cilia by P. eroticus:
“Use of the strong cilia of the ventral surface of the head sets up a strong water current. Bacteria,
diatoms, and algae are drawn into this current from the shell gravel (around which the animal
crawls), and into the mouth. The cuticular and highly muscular pharynx with its diverticula
appears to have a mechanical crushing and sorting function. However, large diatom particles
can be seen in the gut, almost filling the gut cavity, and so the exact role of the pharynx in the
digestive process remains uncertain. The oesophageal region is glandular, and absorption occurs
in the intestine. Food is moved through the gut by the cilia of the ventral groove since the gut
does not have a well developed muscle layer.”
Brown (1981) described P. krusadensis as “browsing over the sediment, sweeping reddish
algal and bacterial coating from the particles of rock with its small patches of peristomial cilia.”
Guts of P. tridentiger contained other algal cells and diatoms (Brown 1981). In addition to
fragmented material, including bacteria, algal cells and diatoms, the guts of P. alanhongi also
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contained a copepod and foraminiferans (Bailey-Brock et al. 2003), indicating that species with a
pharynx and ventral cilia are not strictly herbivorous.
Brown (1981) suggested that species lacking ventral cilia, which also lack an eversible
muscular pharynx (Bailey-Brock et al. 2003) and remain in the genus Saccocirrus (Di Domenico
et al. 2014), are carnivorous. Within this group, Rao & Ganapati (1967) described Saccocirrus
minor as being “quite active and carnivorous, feeding on the smaller microfauna of the sand”
but did not explicitly mention gut contents or provide further details. The gut of S. oahuensis
contained foraminiferans, one of which, drawn by Bailey-Brock et al. (2003), appears to be over
half the diameter of the worm itself, indicating that the mouth gape must be substantial.
Di Dominico et al. (2014a) maintained laboratory cultures of S. pussicus on Skeletonema sp.
from lab cultures or on net plankton collected at the beaches from which worms were collected.
They described a constant waving motion of the palps with captured particles transferred to
the mouth by helicoidal coiling of the palps and inferred that this form of suspension feeding
happened both at the sediment-water interface and interstitially. They also observed direct
ingestion of particles by the mouth in a detritus-feeding mode.
Guild membership
Both morphotypes are small and rely on labile material. Both appear capable of surface feeding
with the palps or directly with the mouth and of suspension feeding with coiled palps on rich
particles that they encounter from suspension. It appears that Pharyngocirrus spp. are more
herbivorous and Saccocirrus spp. are more carnivorous, but there is likely some overlap in diet.
All are motile crawlers and ciliary gliders.
Research opportunities
• Molecular support of the dichotomy between the two morphotypes makes these two groups
ideal for comparison of differences in feeding behavior based on pharyngeal morphology and
habitat.
• Rearing experiments on alternative foods could be used to test the hypothesis that
Saccocirrus spp. are more carnivorous than Pharyngocirrus spp. in potential diets.
• Lipid analysis of field-collected material could provide tests of that hypothesis in realized
diets.
• No suspension-feeding experiments have been carried out in well quantified flows and
suspended loads in the context of hydrosol filtration theory. Microfluidic cells (Marcos &
Stocker 2006) would seem ideal for such experiments with animals of this size toward goals
of describing hydrosol encounter mechanisms and quantifying clearance rates.
References
Bailey-Brock JH, Dreyer J, Brock RE. 2003. Three new species of Saccocirrus (Polychaeta:
Saccocirridae) from Hawai’i. Pac. Sci. 57:463–78
Bailey-Brock JH, Jouin-Toulmond C, Brock RE. 2010. Protodrilidae (Annelida: Polychaeta)
from the Hawaiian Islands and comparison with specimens from French Polynesia. Pac. Sci.
64:463–72
Brown R. 1981. Saccocirridae (Annelida: Archiannelida) from the central coast of New South
Wales. Aust. J. Mar. Freshwater Res. 32:439–56
Di Domenico M, Martínez A, Almeida TCM, Martins MO, Worsaae K, et al. 2014a.
Response of the meiofaunal annelid Saccocirrus pussicus (Saccocirridae) to sandy beach
morphodynamics. Hydrobiologia 734:1–16
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Di Domenico M, Martínez A, Amaral ACZ, da Cunha Lana P, Worsaae K. 2014b. Saccocirridae
(Annelida) from the southern and southeastern Brazilian coasts. Mar. Biodivers. 44: 313–25
Di Domenico, Martínez A, Lana P, Worsaae K. 2014c. Molecular and morphological phylogeny
of Saccocirridae (Annelida) reveals two cosmopolitan clades with specific habitat
preferences. Mol. Phylogen. Evol. 75:202-18
Gray JSA. 1969. New species of Saccocirrus (Archiannelida) from the west coast of North
America. Pac. Sci. 23:238–51
Hermans CO. 1969. The systematic position of the Archiannelida. Syst. Biol. 18:85–102
Marcos, Stocker R. 2006. Microorganisms in vortices: a microfluidic setup. Limnol. Oceanogr.
Meth. 4:392–8
Purschke G, Jouin C. 1988. Anatomy and ultrastructure of the ventral pharyngeal organs of
Saccocirrus (Saccocirridae) and Protodriloides (Protodriloidae fam. n.) with remarks on the
phylogenetic relationships within the Protodrilida (Annelida: Polychaeta). J. Zool. 215:405–32
Purschke G, Tzetlin AB. 1996. Dorsolateral ciliary folds in the polychaete foregut: structure,
prevalence and phylogenetic significance. Acta Zool. 77:33–49
Rao GC, Ganapati PN. 1968. The interstitial fauna inhabiting the beach sands of Waltair coast.
Proc. Natn. Inst. Sci. India B 34:82–125
Scalibregmatidae
Diversity and systematics
Scalibregmatidae comprise about 100 species in 17 genera, 7 of them monotypic. Travisia is
by far the most diverse, with 34 species. Morphological similarity between Travisia and other
scalibregmatids was recognized long ago (Ashworth 1901), but molecular genetic analysis
only recently found Travisia to be a sister clade to Scalibregmatidae and clearly distinct from
Opheliidae (Persson & Pleijel 2005, Paul et al. 2010, Martínez et al. 2013, Law et al. 2014),
resulting in its transfer from Opheliidae to Scalibregmatidae. Scalibregma inflatum is one of
the most conspicuously cosmopolitan polychaete species, but there are many reasons to suspect
that it is a cryptic species complex (Mackie 1991), and it apparently has not yet been subjected
to detailed molecular genetic scrutiny. Most scalibregmatids are 1 - 6 cm long as adults, though
deep-burrowing Travisia spp. often approach the top of this range and diameters nearly half their
lengths (Griggs et al. 1969). Burrower shapes can be maggot like or more elongate. Members of
the Axiokebuita-Speleobregma clade are typically < 1 cm long.
Habitat
Burrowing scalibregmatids are found in soft sediments, mostly mud with high water and clay
content, at all ocean depths (Kudenov & Blake 1978). They can locally dominate some shelf and
slope muds, S. inflatum reaching abundances of > 27000 m-2 at some bathyal stations off North
Carolina (Blake & Hilbig 1994). Scalibregmatidae are among the deeper-burrowing infauna
off of the North Carolina coast (Aller et al. 2002, Levin et al. 1997). At least two species of
the Axiokebuita-Speleobregma clade live in coarse gravel or crevices where inertial flows carry
seston (Martínez et al. 2013) but others are found in the deep sea under much more quiescent
conditions; at least one species occurs at hydrothermal vents (Parapar et al. 2011).
Sensory and feeding structures
The prostomium may be bluntly conical, T-shaped with lateral horns or Y-shaped with two
anterolaterally projecting lobes (Rouse 2001). The prostomium may bear a pair of eyes and
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carries a pair of dorsolateral, eversible nuchal organs at its posterior margin in burrowing forms.
In the Axiokebuita-Speleobregma clade, the nuchal organs are ciliated grooves that nearly meet
medially (Martínez et al. 2014). Innervation for a pair of palps is present, but palps are absent
in most species. Four species in an Axiokebuita-Speleobregma clade that live interstially in
coarse grains or in crevices have evolved ventral, grooved, ciliated palps (Martínez et al. 2014).
Scalibregmella antennata with apparent antennae or palps may not belong in Scalibregmatidae
(Martínez et al. 2014). The scalibregmatid peristomium is a complete ring dorsally but may not
be ventrally (Rouse 2001). Scalibregmatidae, including Travisia, have an axial, non-muscular
proboscis with well-developed, cilated lobes (Tzetlin & Zhadan 2009). The proboscis is similar
to that of Orbiniidae (Tzetlin & Zhadan 2009).
Motility
Burrow galleries of S. inflatum have been known for some time (McIntosh 1868). It is not
unusual to find scalibregmatid burrows as deep as 50 cm in the sediments (Ashworth 1901,
Hertweck & Reineck 1966, Hutchings 2000). Scalibregma inflatum collected at shelf depths in
Puget Sound burrow through crack propagation and use a characteristic side-to-side motion of
the horns to propagate a leading crack incrementally without exerting much force (Dorgan et al.
2006). In laboratory aquaria each individual normally maintains a single opening to the surface
with multiple radiating burrows branching and curving laterally away at a range of sediment
depths from the central, vertical shaft. In containers maintained for months, individuals were
never seen on the sediment surface (PA Jumars, personal observations, with the caveat that no
nocturnal observations were made). Like related arenicolids and opheliids, scalibregmatids
have a mostly open body cavity with septa separating only a few anterior segments. The body
as a consequence looks balloon like ex situ. The cross-section in situ, however, is compressed
dorsoventrally by elastic rebound of the sediments, emphasizing bilateral rather than cylindrical
symmetry (Dorgan et al. 2006).
In Axiokebuita cavernicola Martínez et al. (2013) described, “Short muscular undulatory
swimming periods observed after disturbance, duration no longer than a few seconds. Juveniles
more active but not showing undulatory movements. Instead, they swim presumably by
metachronal beating of the cilia on the transverse ciliary bands on the trunk.” They observed
that, “Speleobregma lanzaroteum swims in the water column of the cave by gentle undulations
of the body accompanied by slow movements of the parapodia. In vials or Petri dishes, animals
swim in the same way or lie immobile, attached by pygidial lobes.”
Illustrations
The diversity of anterior anatomy in the family is well caricatured in Fig. 1 of Martínez et al.
(2014). Martínez et al. (2013) provide highly informative photographs and scanning electron
micrographs of members of the Axiokebuita-Speleobregma clade. Di Domenico et al. (2014) do
the same for Scalibregma and Pseudoscalibregma spp.
Feeding
Dauer (1980) dissected 20 individuals of Travisia hobsonae from the intertidal of upper old
Tampa Bay, Florida, where ambient median grain size was 175 µm. Five individuals had empty
guts. The others were filled with sand of median grain size 230 µm with no grains < 100 µm and
none > 475 µm. The species clearly selected for grains larger than the median size. Capitellids
at the same site had ingested smaller particles.
Scalibregma inflatum at bathyal depths off North Carolina has received the most attention
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since F&J. Live phytoplankton cells have been recovered at 14 cm depth in the sediments,
suggesting rapid subduction (Cahoon et al. 1994). Blair et al. (1996) documented rapid in situ
uptake of 13C-labeled Chlorella sp. by S. inflatum and rapid subduction of labeled material.
Blake (2000) implied finding caches in S. inflatum burrows. A follow-up labeling experiment
with diatoms in the same region where the Chlorella was emplaced did not find rapid uptake,
leading the authors to posit that S. inflatum took advantage of greater subduction by maldanids in
this patch of bottom to avoid going to the surface for fresh organic material (Levin et al. 1997).
Number and depth of other burrowers were positively correlated with maldanid abundance
(Levin et al. 1997).
Gontikaki et al. (2011) found very high δ15N in Scalibregmatidae from the Faroe-Shetland
Channel, similar to those of Capitellidae, and they suggested that both groups were subsurface
deposit feeders. Similarly, Pseudoscalibregma parvus from arctic vent and nearby sites had
fairly high δ15N (Sweetman et al. 2013). The one Scalibregmatidae individual sampled by Iken
et al. (2001) from the Porcupine Abyssal Plain (NE Atlantic) had a δ15N that was relatively low
among polychaetes sampled, and they described the gut contents as 50% fresh phytodetritus
and 50% sediment, consistent with surface deposit feeding or caching. Iken et al. (2010) found
δ15N for Scalibregma inflatum from the Chukchi Sea intermediate among polychaetes sampled
and consistent with subsurface deposit feeding. Yoshino et al. (2006) found similar results for
unidentified Scalibregmatidae from shallow water off of Japan. Two scalibregmatid individuals
analyzed by McLeod et al. (2010) from 400 m depth in fjords in New Zealand had δ15N values
similar to those of capitellids and cirratulids sampled, although differences in δ15N between
terrestrial organic material and that from other primary producers prevented a clear determination
of trophic level.
Travisia spp. include subsurface burrowers. In a study of vertical distributions of North
Carolina slope polychaetes, Blake (1994) noted that 70% of Kesun (= Travisia) gravieri
individuals were captured in the 2-5 cm layer below the interface. Some Travisia spp. are
especially deep burrowers that may specialize on mining organic-rich material buried in
turbidites (e.g., Fig. 8 of Griggs et al. 1969) and may die quickly if exposed to normoxic
seawater (Manwell 1960), making them particularly difficult to study.
Drazen et al. (2008a) analyzed natural δ13C and δ15N values for animals in the abyssal
Monterey Deep-Sea Fan. Travisia sp. had the highest values for both δ13C and δ15N, even higher
than those of rattail fishes whose gut contents included carrion, other fishes, and invertebrates
(Drazen et al. 2008a). Lipid analyses provided hints of an unusual feeding ecology but did not
quite pinpoint the diet of Travisia sp. or the processes responsible for their isotopic enrichment.
Drazen et al. (2008b) found Travisia sp. to have very low levels and an unusual composition of
polyunsaturated fats but also high levels of phytosterols.
Similar results were found in the same region by Sweetman & Witte (2008) for unspecified
Opheliidae, and it seems likely that they sampled Travisia, although some opheliids have
been shown to have high 15N values as well. Sweetman & Witte (2008) suggested that the
“Opheliidae” sampled may have been predators on protists. Similarly, Dunton et al. (2012)
analyzed a specimen of Travisia forbesii from a coastal lagoon of the Beaufort Sea and found its
δ15N to be about the same as that of Nephtys sp. (Nephtyidae). Travisia kerguelensis from the
deep Southern Ocean displayed fatty acid compositions typical of carnivores, with high values
of fatty acids associated with calanoid copepods and foraminiferans (Würzberg et al. 2011).
The fatty acid associated with calanoid copepods was also found in considerable proportions
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in non-Travisia Scalibregmatidae, which also had high concentrations of fatty acids associated
with diatom detritus, indicating selection for recently deposited, rich organic material (Würzberg
et al. 2011). We suspect, however, that prokaryotic microbial transformations (e.g., Kikuchi &
Wada 1996, Goedkoop et al. 2006) may partially account for the high values often observed for
subsurface deposit feeders in general (Witte et al. 2003, Sweetman & Witte 2008, Gontikaki et
al. 2011) and Monterey Deep-Sea Fan Travisia in particular. Based on the highly invaginated,
complex gut structure of Travisia foetida and its distinctive, rotten-garlic odor, Penry & Jumars
(1990) suggested that microbial fermentation may be important in digestion.
Martínez et al. (2013) suggested that gravel- and crevice-dwelling members of the
Axiokebuita-Speleobregma clade suspension feed, stating (p. 623) that, “Speleobregma swims
in the water column of the cave and feeds on suspended organic matter (Iliffe et al. 2000).” We
find no mention by Iliffe et al. (2000) of feeding or swimming in Speleobregma. We suspect that
Iliffe et al.’s (2000) observations of continuous swimming in Speleonectes were confused with
Speleobregma. The mechanics of suspension feeding by swimming to produce relative velocity
of food particles with stubby collecting devices seem less than optimal. Feeding on surfaces
in quiescent microenvironments seems more likely given the similar morphology of deep-sea
Axiokebuita spp. (Parapar et al. 2011).
Guild membership
New evidence largely corroborates F&J’s conclusion from previous evidence that burrowing
scalibregmatids are subsurface deposit feeders. Size selection and fatty acid signatures
argue against retaining the idea that scalibregmatids are nonselective. S. inflatum can clearly
include surface deposit feeding and probably caching in its repertoire. Travisia may be partly
carnivorous on foraminiferans and efficient at extracting calanoid remains from ingested
sediments. Suspension feeding in some members of the Axiokebuita-Speleobregma clade has
been suggested; their small body sizes likely make selection of labile ingesta necessary either
from suspension or from surrounding surfaces with their stubby, ventral palps. Most species are
motile. Suspension feeders attaching their pygidia to the substratum could be discretely motile.
Research opportunities
• No feeding observations or experiments appear to have been published on or with members
of the Axiokebuita-Speleobregma clade.
• In situ motility data are lacking for any scalibregmatid.
• Extent of carnivory and microbial enrichment of 15N in Travisia spp. both warrant further
investigation.
References
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Ashworth JH. 1901. The anatomy of Scaligregma inflatum Rathke. Quart. J. Microsc. Soc.
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Blair NE, Levin LA, DeMaster DJ, Plaia G. 1996. The short-term fate of fresh algal carbon in
continental slope sediments. Limnol. Oceanogr. 41:1208–19
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Blake JA. 1994. Vertical distribution of benthic infauna in continental slope sediments off Cape
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Hatteras, North Carolina. Deep-Sea Res. Pt. II 41:875–99
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Serpulidae, Sabellida
Diversity and systematics
Living Serpulidae comprise about 670 species in about 70 genera, of which about 250 species
and 20 genera fall in Spirorbinae. Only 16 genera of serpulids contain 10 or more species, and
22 are monotypic. Serpulids range from ~ 2 mm to > 10 cm long (Rouse 2000).
Serpulid alpha taxonomy leaves much to be desired (Ten Hove & Kupriyanova 2009).
Higher-level taxonomy is also changing rapidly (Kupriyanova et al. 2006), and recent molecular
evidence places them as a sister clade to Fabriciidae but further removed from Sabellidae
(Kupriyanova & Rouse 2008).
Habitat
All serpulids secrete calcareous tubes. At least 5 species in 2 genera have invaded fresh waters
(Glasby & Timm 2008; e.g., Kupriyanova et al. 2009, Li et al. 2012). Serpulids feed with a
radiolar crown homologous with that of sabellids. Although most abundant in shallow water,
serpulids occur at all depths, generally attached to hard substrata. They are common, often in
dense aggregations, near hydrothermal vents (Ten Hove & Zibrowius 1986, Levin et al. 2012).
Members of the genus Ditrupa, however, settle into and grow their tubes in shelf sediments to
water depths of 200 m or more. They may concentrate at shelf edges where stratified waters
support internal waves (Hartley 2014). At least two other species of serpulids show some
apparent shell adaptation to soft sediments in the form of straightening during growth to project
above the sediment surface (Rzhavsky 1994): Bushiella kofiadii often settles on tubes of Nothria
conchylega (Onuphidae) and untwists its normal whorls when it does so. Antarctic Helicosiphon
biscoeensis lives under rapid deposition and apparently uncoils the tube to keep up with
sedimentation and maintain access to seston above the sediment-water interface. Turret-shaped
tubes as in Paradexiospira vitrea may be a way to accommodate rapid sedimentation while
maintaining mechanical strength (Rzhavsky 1994). Species that attach to flapping substrata
such as kelp or seagrass fronds avoid thick shells and often have longitudinal ridges, even
though these ridges may be reduced or absent when the same species settles on rocks. Rhzavsky
(1994) aptly suggested that reducing thickness reduces the dynamic, inertial forces that could
detach the shell, while ridges can retain mechanical strength. Ridges can also decrease vortexexcited oscillation (Every et al. 1982). Tube secretion appears to be energetically expensive, in
Ficopomatus enigmaticus exceeding the costs of somatic growth and reproduction (Dixon 1980).
Sensory and feeding structures
The prostomium comprises the tentacular crown of serpulids. It is a laterally paired structure,
with each half made up of 3 to > 20 radioles and a dorsal lip that continues ventrally to the
mouth. An unpaired nuchal organ is the dorsal part of a pouch formed as a dorsal pit just above
the mouth (Orrhage 1980). A chitinized or calcified operculum derived from the second radiole
is present in most species. The peristomium is complete and usually forms a collar over the lip
of the tube (Rouse 2001). A buccal organ of any kind is lacking, but the esophagus and much of
the gut is ciliated (Rouse 2001). Eyes in Serpulidae are diverse in both structure and location.
Paired ocellar clusters are common at the posterior of the prostomium as are compound eyes on
the radioles. Other variants include an unpaired red ocellus at the base of the opercular ampulla,
a girdle of red ocelli around the thorax behind the collar, and stalked eyes at the base of the
pinnules (Smith 1985, Purschke et al. 2006, ten Hove & Kupriyanova 2009).
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Motility
Excluding individuals that attach to floating objects, hulls, turtles, other moving shells and
whales, serpulids are sessile or have very limited mobility. Sediment-dwelling, solitary forms
retain some mobility needed to deal with issues of sedimentation and ripple migration. Ditrupa
arietina is susceptible to erosion that results in horizontal posture for the tube (e.g., Fig. 1b in
Guizien et al. 2010). Both upright and horizontal postures are seen in the field (Jordana et al.
2000). Aquarium observations revealed only limited burrowing capability in the closely related
D. gracillima (ten Hove & Smith 1990). In fine sediments, smooth-tubed specimens used the
radioles first to excavate and then to anchor, pulling the shell along and back into the sediments.
Repeated burrowing bouts led to a concave-upward posture for the tube, with only its two ends
showing at the surface. In similar trials with sand, worms failed to attempt burrowing at all (ten
Hove & Smith 1990).
Illustrations
Color photographs and scanning electron micrographs provided by ten Hove & Kupriyanova
(2009) give a good visual impression of diversity within Serpulidae. Rouse (2001) provides
labeled drawings useful in identifying anterior anatomical structures.
Feeding
Like sabellids, serpulids generally feed in currents much faster than their own cilia can produce,
as dye visualization in the laboratory and field documented for Spirobranchus giganteus
(Strathmann et al. 1984). Also as in sabellids, the cilia work to alter particle trajectories and
enhance encounter rates when particles approach at very close range (Riisgård et al. 2002). A
dominant mechanism of particle encounter in all the species analyzed so far is unsteady fluid and
particle motion induced by the driving lateral cilia on the pinnules, effecting encounter with the
mucus-carrying ciliary tract on the downstream side of the pinnule (e.g., Mayer 2000).
The largest number of studies since F&J have been done on Ditrupa arietina, which in many
ways is an unusual serpulid. It is free living (not attached to hard substrata) in shelf sands from
Iceland to Senegal and in the Mediterranean (ten Hove & Smith 1990). It is most abundant in
sands without fines, where recently settled juveniles may depend on large sand grains to anchor
their initially mucoid tubes (Grémare et al. 1998). Both ends of the tube are open, and the
arcuate shells, round in cross section, reaching lengths of about 3 cm, are often confused with
those of the scaphopod Dentalium (ten Hove & Smith 1990). Wilson (1976) noted that solitary
corals frequently settle on the anterior of the tube, with twice the frequency of settlement on the
concave side compared with the convex and other two faces. The pattern of fouling indicates a
posture with the narrower, posterior half to three-fourths of the worm tube buried. The concave
side is likely to face downstream (the most stable configuration in a flow) and be favored for
settlement because of its reduced shear stress compared to the other faces and because of the
presence of a leeward eddy that circulates resuspended materials up the downstream side of
the tube. Additional evidence that the concave side is more often downstream comes from
the distribution of drill holes made by predators; they would be expected to approach from
downstream (Morton & Harper 2009). The longitudinal distribution of drill holes in modern and
fossil specimens is concentrated toward the anterior end (Morton & Harper 2009, Martinell et
al. 2012). Gambi’s (1986), Gambi & Jerace’s (1997), and Morton & Salvador’s (2009) studies
of epibionts also support a vertical orientation of the tube, as do Gambi’s (1986) observations on
apparent tube extensions attributed to the need to keep pace with sedimentation.
Hong (1984) is often cited to indicate that D. gracillima surface deposit feeds. His only
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statement to this effect is, “However, it seems that the D. arietina [gracillima cf. ten Hove &
Smith 1990] in Korean waters is probably surface deposit feeders because they are found in
the clayey silty bottom and then a ciliary current through the branchial filaments of the worm
helps to capture the deposited material in bedload.” The aquarium observations of D. gracillima
burrowing with its radioles leave little doubt that it could pick up deposits if the tube opening
is close to the sediment-water interface. Clay and silt do not in general transport as bedload,
however, and bedload by definition is no longer deposited. Hong’s (1984) conjecture is
presented without evidence of behavior or gut contents and deserves to be tested before deposit
feeding is considered one of D. gracillima’s feeding modes.
Each month for 13 mo Jordana et al. (2001a) collected feces excreted by 10 freshly fieldcollected D. arietina and identified the contents. Particle sizes ranged from 0.4 to 47 µm diam.
(bacteria to foraminiferans). They observed large particles grasped between opposed pinnules on
the same filament and passed to adjacent pinnule pairs sequentially toward the mouth. A large
fraction of the identified particles comprised pelagic and benthic diatoms. With 14C-radiolabeled
diets of Skeletonema costatum, Isochrysis galbana, Pseudoalteromonas holoplanktis and
Synechococcus sp., these authors measured D. arietina assimilation efficiencies of 85, 71, 72,
and 64%, respectively. Stable isotopic data also point to suspension feeding. D. arietana from
relict, shelf-edge sands in the Bay of Biscay had δ15N consistent with feeding on near-bottom
suspended material and lower enrichments than any other invertebrates at that sand site. They
fell in the same range as values for suspension-feeding bivalves in the Grand Vasière nearby and
below those of deposit feeders collected there (Le Loc’h et al. 2008).
Using flow cytometry to identify picoplankton to broad taxonomic groups, Jordana et al.
(2001b) conducted monthly grazing experiments with field-collected bottom water and 3 batches
of 40 D. arietina for 13 mo. Picoeukaryotes constituted 95% of the grazed picoplanktonic
carbon. Grazing rates correlated positively with prochlorophyte and picoeukaryote
concentrations but were not strongly correlated with cyanobacterial concentrations, even though
the latter constituted a majority of the picoplankton carbon from August through October,
suggesting selection against cyanobacterial ingestion. Clearance rates ranged from 0.05 - 2.56
liters h-1 g-1 dry wt. Riisgård et al. (2002) measured higher specific clearance rates of 15.7 liters
h-1 mg-1 dry wt. Feeding rates were set by frequency and duration of radiole deployment rather
than by the rate at which cilia moved fluid (Duchêne et al. 2000); filtering during deployment
appeared continuous (Riisgård et al. 2002). Continuous filtering during radiole deployment
appears general: For Serpula columbiana and Simplaria potswaldi and three sabellid species,
area of ciliary bands (A, mm2) scales with worm dry weight (W, mg) as ln A = 3.59 + 0.648 ln W
(r 2 = 0.99, Henderson & Strathmann 2000). If filtering were discontinuous such a good fit would
not be expected.
In laboratory measurements of deployment duration made on batches of 12 - 15 D. arietana
collected from each of two field sites and acclimated to the laboratory for 24 h, percent of time
that radioles were deployed in filtered seawater varied seasonally with phase of the reproductive
cycle and physiological state, decreasing after spawning (Jordana et al. 2000). Inter-individual
variability in time spent feeding varied widely, however. Worms responded to added food by
increasing duration rather than number of their feeding bouts (Jordana et al. 2000). Dill &
Fraser (1997) in some elegant laboratory behavioral experiments provided a repeatable fright
stimulus and showed that Serpula vermicularis compared its current feeding conditions with
those recently past and would spend less time hiding if current food availability was high. These
observations are consistent with optimal foraging predictions for lost-opportunity costs under
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rapidly varying resource conditions of suspended food quantity and quality in shallow-water
bottom boundary layers.
In Jordana et al.’s (2001b) study, on an annual basis picoplankton accounted for only 15%
of chlorophyll a ingested by the worm. It is appropriate to ask whether serpulids can grow
on bacteria in this size class as sole food source. Gosselin & Qian (2000) found that juvenile
Hydroides elegans exhibited positive growth at bacterial concentrations of ~ 2 × 106 bacteria
ml-1, although not as rapid as on a diet of Isochrysis galbana at saturating concentrations of 105
to 106 ml-1. Hydroides dianthus has been raised to maturity on diets of the single phytoplankton
species Isochrysis galbana, Phaeodactylum cornutum and Nannochloris sp., though the worm
matured most slowly on the latter and matured most quickly on a diet of all three (Leone 1970).
Serpulids can occur in dense aggregations capable of reducing suspended loads and
appreciably decreasing turbidity. Davies et al. (1989) measured the clearance rate of
Ficopomatus enigmaticus as 8.79 liters h-1 g-1 dry wt. (Bruschetti et al. 2008). Bruschetti
et al. (2008) observed that dense reefs of this invasive worm in shallow water could reduce
turbidity sufficiently to enhance production by microphytobenthos. The other clearance rate
estimate made since F&J is for Pomatoceros triqueter on Dunaliella. At 5.0 liters h-1 g-1 dry
wt. (Klöckner 1978) it came close to Dales’ (1957) estimate made with graphite particles. All
published estimates for serpulids were tabulated by Jordana et al. (2001b).
In terms of isotopic evidence of trophic level, Pomatoceros lamarcki in the Bay of Veys,
northern France, fell slightly below Lanice conchilega (a suspension-feeding terebellid), and
slightly above Crassostrea gigas in δ15N, with a δ13C signature suggestive of a mixture of
particulate organic matter and microphytobenthos (Dubois et al. 2007). Serpula vermicularis
from shallow water in the Bay of Banyuls-sur-Mer fell about 0.6 ‰ above L. conchilega in
δ15N (Carlier et al. 2007). In shallow-water fjord communities of New Zealand, Wing & Jack
(2012) also found isotopic signatures of a serpulid to fall near those of other suspension feeders:
Neovermillia sphaeropomatus fell close to the bivalve Aulacomya maoriana in both δ15N and
δ13C, with δ13C suggesting a macroalgal food source. In δ15N signature N. sphaeropomatus fell
even closer to the tunicate Cnemidocarpa bicornuta and the brachiopod Terebratella sanguinea.
Lojen et al. (2005) found that serpulids (including Salmacina sp. and Josephella marenzelleri)
raised near a fish farm obtained roughly 30% of their total body nitrogen from organic matter
released by the farm and thus showed potential to sequester its organic wastes.
Neovermillia sp. from the vicinity of hydrothermal vents on the Costa Rica margin was
extremely depleted in both 13C and 15N. This signature likely indicates feeding directly on
aerobic methanotrophs (Levin et al. 2012).
Guild membership
All the evidence of which we are aware indicates that serpulids are sessile suspension feeders
using a mixed (cilia plus ambient flow, intermediate between active and passive) mode. Diets
include microalgae, bacteria and small detrital particles.
Research questions and opportunities
• It would be interesting to know if serpulids share diel feeding periodicity with sabellids.
• Experiments to test extents and mechanisms of differences in diet selection between serpulid
species could be informative.
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Riisgård HU, Grémare A, Amouroux JM, Charles F, Vétion G, et al. 2002. Comparative study
of water-processing in two ciliary filter-feeding polychaetes (Ditrupa arietina and Euchone
papillosa) from two different habitats. Mar. Ecol. Prog. Ser. 229:113–26
Rouse GW. 2000. Family Serpulidae. See Beesley et al. 2000, pp. 184–9
Rouse GW. 2001. Serpulidae Rafinesque, 1815. See Rouse & Pleijel 2001, pp. 198–201
Rzhavsky AV. 1994. On the morphoecology of spirorbid tubes (Polychaeta: Spirorbidae).
Ophelia 39:177–82
Smith RS. 1985. Photoreceptors of serpulid polychaetes. PhD thesis, James Cook Univ.,
Townsville, Queensland
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Strathmann RR, Cameron RA, Strathmann MF. 1984. Spirobranchus giganteus (Pallas) breaks a
rule for suspension-feeders. J. Exp. Mar. Biol. Ecol. 79:245–9
ten Hove HA, Smith RS. 1990. Rec. Aust. Mus. 42:101–18
ten Hove HA, Kupriyanova EK. 2009. Taxonomy of Serpulidae (Annelida, Polychaeta): the state
of affairs. Zootaxa 2036:1–126
ten Hove HA, Zibrowius H. 1986. Laminatubus alvini gen. et sp. n. and Protis hydrothermica sp.
n. (Polychaeta, Serpulidae) from the bathyal hydrothermal vent communities in the eastern
Pacific. Zool. Scr. 15:21–31
Wilson JB. 1976. Attachment of the coral Caryophyllia smithii S. & B. to tubes of the polychaete
Ditrupa arietina (Müller) and other substrates. J. Mar. Biol. Ass. UK 56:291–303
Wing S, Jack L. 2012. Resource specialisation among suspension-feeding invertebrates on rock
walls in Fjordland, New Zealand, is driven by water column structure and feeding mode.
Mar. Ecol. Prog. Ser. 452:109–18
Siboglinidae, Sabellida
Diversity and systematics
Siboglinidae comprise about 180 species in 33 genera. The largest genus, Siboglinum, contains
63 species, whereas 14 genera are monotypic. Four morphotypes largely correspond with
taxonomic groupings that preceded their aggregation into a single family of polychaetes (Pleijel
et al. 2009). Fortunately, the four major groupings originally made on morphological grounds
have held up in molecular genetic analysis (Echinger et al. 2013), and their informal names
therefore are still in use. We must re-emphasize that our descriptions of morphology and feeding
apply only to adults. The most robust morphotype is that of vestimentiferans, some of which
can reach 1.5 m in length (Rouse 2001); they include the genera Alaysia, Arcovestia, Escarpia,
Lamellibrachia, Oasisia, Paraescarpia, Ridgeia, Riftia, Seepiophila, and Tevnia. Most closely
related to the vestimentiferans are the moniliferans (Halanych et al. 2001, Eichinger et al.
2013). They comprise seven species in the genus Sclerolinum (Eichinger et al. 2013). They and
the frenulates are long, skinny worms, usually < 1 mm diam., but with a length/diam. ratio ≥
100. Frenulates include Birsteinia, Bobmarleya, Choanopherus, Crassibrachia, Cyclobrachia,
Diplobrachia, Galathealinum, Heptabrachia, Lamellisabella, Nereilinum, Oligobrachia,
Polarsternium, Polybrachia, Siboglinoides, Siboglinum, Siphonobrachia, Spirobrachia,
Unibrachium, Volvobrachia, and Zenkevitschiana. The fourth morphotype, all members of the
genus Osedax, is less vermiform and is dendritic at both ends, like a bonsai tree including its
roots. Combined trunk and crown length ranges from 1.2 mm to 5.9 cm (Amon et al. 2014).
Siboglinids may date back to the Ediacaran Period (Moczydłowska et al. 2014).
Habitat
Osedax chemically etches its way into whale, cow, fish and presumably any large bones (Jones
et al. 2008, Rouse et al. 2011, Amon 2013) with prolific acid secretions (Tresguerres et al. 2013).
The bones constitute its burrow lining or “tube.” All other siboglinids secrete chitinous tubes.
Vestimentiferans are found at hydrothermal vents and hydrocarbon seeps. Hydrothermalvent vestimentiferans have a tube open at only the anterior end, which is located in a turbulent
vent plume that entrains boluses of oxygen-rich bottom water, providing both oxygen and sulfide
ions in close spatial and temporal juxtaposition (Ott et al. 1998). Vestimentiferan species from
mud seeps, however, have modified, dendritic, tube posteriors that are permeable and serve to
collect sulfide produced in the sediments (Haas et al. 2009), and Lamellibrachia satsuma has an
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Jumars, Dorgan & Lindsay
07 November 2014
open tube bottom in mud (Miura et al. 2002). This genus also has been found on a shipwreck
(Gambi et al. 2011). At least one cold-seep species, Escarpia spicata, is apparently also able to
utilize sulfide produced by whale falls (Feldman et al. 1998).
Monoliferan tubes lack rings or segments but can be opened or closed by the worm at
the posterior end. Four of the known species occur on wood or other similar materials (e.g.,
cardboard or leather). The other three occur in muds (Sahling et al. 2005). Tubes of frenulates
bear rings or segments or both and are open at both ends. Their habitat is primarily mud.
Sensory and feeding structures
Siboglinidae lack a mouth opening and functional gut. The prostomium is small and rounded
conical, absent, or completely surrounded by palps. No nuchal organs or eyes are reported. The
peristomium is a complete ring usually terminated by a clear groove (Rouse 2001). The four
morphotypes differ substantially in palp structure. In vestimentiferans, the anterior is a plume
comprising hundreds of palps fused into parallel laminae. Moniliferans bear two unfused palps
of intermediate length (palp length ~ 10 × palp diam.). Frenulates bear 1-300 palps that may be
free or partially fused. They are very long and thin (palp length ~ 50 times × diam.; Smirnov
2008). Most Osedax species bear four anterior palps with abundant pinnules, serving as gills
(Tresguerres et al. 2013), but some species have palps without pinnules, and one lacks palps
entirely (Vrijenhoek et al. 2009).
All siboglinids feed in cooperation with internal, bacterial mutualists. In all of the
tube-building siboglinids, bacteria are held in a specialized organ named a trophosome. In
vestimentiferans the trophosome occupies the posterior 2/3 of the robust body, In monoliferans
and frenulates it occupies the posterior 1/3 to 1/2.
Motility
Siboglinids are sessile. Tube leaving has not been described.
Illustrations
Rouse’s (2001) line drawings are useful for aligning siboglinids with more standard terminology
of polychaete morphology. Through line drawings and photographs, Southward et al. (2005)
provide a good introduction to the morphology of the tube-building siboglinids. Vrijenhoek et al.
(2009) provide color photographs of diverse Osedax spp.
Feeding
Tube-building siboglinids all feed on organic matter synthesized by their internal bacterial
mutualists. Mutualists are fed with energy-rich, reduced, inorganic compounds. Hydrothermal
vent vestimentiferans take up sulfide through the plume. Because in other siboglinids the
reduced inorganic compounds originate at the bottom of the tube, some uptake may occur on
parts of the body other than the palps. All vestimentiferans and most moniliferan species are
assumed to be thiotrophic, but highly negative δ13C values led Pimenov et al. (1999) to suggest
methane oxidation by Sclerolinum contortum from Haskon Mosby Mud Volcano (Pimenov
et al. 1999). Alternative explanations for the low δ13C values have been given, however, and
evidence for methanotrophy by moniliferans remains questionable (Dando et al. 2008; Thurber et
al. 2010). Unequivocal evidence of methanotrophic symbionts has been found in one frenulate,
Siboglinum poseidoni (Schmaljohann et al. 1990), and more than one strain of bacteria may
occur in the trophosome (Zimmermann et al. 2014).
Osedax spp. house heterotrophic symbionts secreting enzymes that hydrolyze collagen, the
dissolved products sustaining both host and symbionts (Goffredi et al. 2007). The mutualistic
bacteria are concentrated in the posterior, root-like portion of the body (Goffredi et al. 2005).
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Jumars, Dorgan & Lindsay
07 November 2014
Carbon isotopic data and fatty acid signatures support fatty acid transfer from the symbiont
bacteria to the host rather than direct fatty acid uptake by the host (Goffredi et al. 2005).
Because there is little doubt as to the source of organic nutrients for siboglinids, we do not
catalog additional information on stable isotope concentrations in these worms here. They are
mentioned under entries for other families when feeding on bacteria or feeding on siboglinids is
a possibility into which values for siboglinids can give insight.
Guild membership
Tube-building siboglinids are sessile osmotrophs utilizing mutualistic bacteria to produce organic
materials using reduced compounds provided by the host. As host-mutualist units, they have net
uptake of sulfide or methane as energy sources. Osedax spp. as host-mutualist units have net
uptake of hydrolysis products of collagen.
Research questions and opportunities
• Distributions of reductant uptake sites over the bodies of tube builders that have each tube
end open, openable or permeable remain poorly known.
• The possibility of additional species being methanotrophic remains open.
References
Amon DJ. 2013. Bone-eating worms and wood-eating bivalves: characterising the ecology of
deep-sea organic falls from multiple ocean basins. PhD thesis. Univ. Southampton, England
Amon DJ, Wiklund H, Dahlgren TG, Copley JT, Smith CR, et al. 2014. Molecular taxonomy of
Osedax (Annelida: Siboglinidae) in the Southern Ocean. Zool. Scr. 43:405–17
Dando PR, Southward AJ, Southward EC, Lamont P, Harvey R. 2008. Interactions between
sediment chemistry and frenulate pogonophores (Annelida) in the north-east Atlantic. DeepSea Res. Pt. I 55:966–96
Eichinger I, Hourdez S, Bright M. 2013. Morphology, microanatomy and sequence data of
Sclerolinum contortum (Siboglindae, Annelida) of the Gulf of Mexico. Org. Divers. Evol.
13:311–29
Feldman RA, Shank,TM, Black MB, Baco AR, Smith CR, et al. 1998. Vestimentiferan on a
whale fall. Biol. Bull. 194:116–9
Gambi MC, Schulze A, Amato E. 2011. Record of Lamellibrachia sp.(Annelida: Siboglinidae:
Vestimentifera) from a deep shipwreck in the western Mediterranean Sea (Italy). Mar.
Biodivers. Rec 4:e24, 6 pp.
Goffredi SK, Johnson SB, Vrijenhoek RC. 2007. Genetic diversity and potential function of
microbial symbionts associated with newly discovered species of Osedax polychaete worms.
Appl. Environ. Microbiol. 73:2314–23
Goffredi SK, Orphan VJ, Rouse GW, Jahnke L, Embaye T, et al. 2005. Evolutionary innovation:
a bone-eating marine symbiosis. Environ. Microbiol. 7:1369–78
Haas A, Little CTS, Sahling H, Bohrmann G, Himmler T, Peckmann J. 2009. Mineralization
of vestimentiferan tubes at methane seeps on the Congo deep-sea fan. Deep-Sea Res. Pt. I
56:283–93
Halanych KM, Feldman RA, Vrijenhoek RC. 2001. Molecular evidence that Sclerolinum
brattstromi is closely related to vestimentiferans, not to frenulate pogonophorans
(Siboglinidae, Annelida). Biol. Bull. 201:65–75
Jones WJ, Johnson SB, Rouse GW, Vrijenhoek RC. 2008. Marine worms (genus Osedax)
colonize cow bones. Proc. R. Soc. Lond. B 275:387–91
Miura T, Nedachi M, Hashimoto J. 2002. Sulphur sources for chemoautotrophic nutrition of shallow
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Jumars, Dorgan & Lindsay
07 November 2014
water vestimentiferan tubeworms in Kagoshima Bay. J. Mar. Biol. Ass. UK, 82:537–40.
Ott JA, Bright M, Schiemer F. 1998. The ecology of a novel symbiosis between a marine
peritrich ciliate and chemoautotrophic bacteria. Mar. Ecol. 19:229–43
Pimenov N, Savvichev A, Rusanov I, Lein A, Egorov A, et al. 1999. Microbial processes of
carbon cycle as the base of food chain of Håkon Mosby Mud Volcano benthic community.
Geo-Mar. Lett. 19:89–96
Pleijel F, Dahlgren TG, Rouse GW. 2009. Progress in systematics: from Siboglinidae to
Pogonophora and Vestimentifera and back to Siboglinidae. C. R. Biol. 332:140–8
Rouse G. 2001. A cladistic analysis of Siboglinidae Caullery, 1914 (Polychaeta, Annelida):
formerly the phyla Pogonophora and Vestimentifera. Zool. J. Linn. Soc. 132:55–80
Rouse GW, Goffredi SK, Johnson SB, Vrijenhoek RC. 2011. Not whale-fall specialists, Osedax
worms also consume fishbones. Biol. Lett. 7:736–9
Sahling H, Wallmann K, Dählmann A, Schmaljohann R, Petersen S. 2005. The physicochemical
habitat of Sclerolinum sp., at Hook Ridge hydrothermal vent, Bransfield Strait, Antarctica.
Limnol. Oceanogr. 50:598–606
Schmaljohann R, Faber E, Whiticar MJ, Dando PR. 1990. Co-existence of methane- and sulphurbased endosymbioses between bacteria and invertebrates at a site in the Skagerrak. Mar.
Ecol. Prog. Ser. 61:119–24
Moczydłowska M, Westall F, Foucher F. 2014. Microstructure and biogeochemistry of the
organically preserved Ediacaran metazoan Sabellidites. J. Paleontol. 88:224–39
Smirnov RV. 2008. Morphological characters and classification of the subclass Monilifera
(Pogonophora) and the problem of evolution of the bridle in pogonophorans. Russ. J. Mar.
Biol. 34:359–68
Southward EC, Schulze A, Gardiner SL. 2005. Pogonophora (Annelida): form and function.
Hydrobiologia 535/536:227–51
Thurber AR, Kröger K, Neira C, Wiklund H, Levin LA. 2010. Stable isotope signatures and
methane use by New Zealand cold seep benthos. Mar. Geol. 272:260–9
Tresguerres M, Katz S, Rouse GW. 2013. How to get into bones: proton pump and carbonic
anhydrase in Osedax boneworms. Proc. R. Soc. Lond. B 280:20130625, 9 pp.
Vrijenhoek RC, Johnson SB, Rouse GW. 2009. A remarkable diversity of bone-eating worms
(Osedax; Siboglinidae; Annelida). BMC Biol. 7:74, 13 pp.
Zimmermann J, Lott C, Weber M, Ramette A, Bright M, et al. 2014. Dual symbiosis with cooccurring sulfur-oxidizing symbionts in vestimentiferan tubeworms from a Mediterranean
hydrothermal vent. Environ. Microbiol. doi:10.1111/1462-2920.12427 in press
Sigalionidae, Aphroditiformia
Diversity and systematics
Sigalionidae comprise about 210 species in 30 genera, 10 of them monotypic. The only
genera with > 10 species are, in decreasing order of species richness, Sthenelais, Pisione,
Sigalion, Sthenolepis, Pelogenia, and Leanira. Pholoidae is the most closely related family
among the scaleworms, although a recent molecular phylogenetic analysis places Pholoidae
within Sigalionidae, albeit without sufficiently strong support to synonymize the two families
(Norlinder et al. 2012). The families formerly known as Pholoididae and Pisionidae proved more
definitively to be clades within Sigalionidae (Norlinder et al. 2012). Pettibone (1997) revised
part of the family, but generic revision is urgently needed (Hutchings 2000).
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
Most sigalionids are elongate burrowers of two major morphotypes: robust, medium-tolarge worms (with adults 2 - 20 cm long) elliptical or rectangular in cross-section, and small (≤
2 cm long) scale-less, more cylindrical worms (the genera Anoplopisione, Pisione, Pisionella,
and Pisionidens). Because the latter morphotype corresponds with members of the former
family Pisionidae, we refer to it as the pisionid morphotype. Two non-burrowing outliers
are Sthenelanella spp. that have spinning glands like those of Acoetidae and also use them
to construct fibrous tubes and Pholoides spp. that do not burrow and have a more classically
scaleworm shape—relatively short and flattened hemispheroidal. Sthenelanella spp. are typically
2 - 3 cm long (Pettibone 1969). Pholoides spp. can be as short as 3 mm, and rarely exceed 1.2
cm long.
Habitat
Most sigalionids burrow in soft sediments. The large, burrowing morphotype can be found at
any water depth. The pisionid morphotype is more characteristic of environments with abundant
interstitial animals (coarse sands and gravels in shallow water and shelf depths) and also extends
into fresh water (San Martin et al. 1998). Rarely are the animals small enough, however, to
be truly interstitial (Pleijel 2001) except in gravels (San Martin et al. 1998). Sthenelanella is
known from soft and mixed bottoms primarily at shelf depths. Pholoides spp. can be found on
nearly any bottom type from shallow water to bathyal depths. Some species are chasmolithic
in carbonates and often associated with chimneys in cold seeps (e.g., Sumida et al. 2004) but
Pholoides spp. are also found on non-seep sediments in both suboxic and normoxic regions (e.g.,
Tarazona et al. 1988, Miranda & Brasil 2014).
Sensory and feeding structures
Sigalionids outside the pisionid morphotype have rounded to rectangular prostomia bearing
a pair of long, slender palps and a pair of small, anterolateral antennae. A median antenna
is also usually present. The prostomium may carry one or (more usually) two pairs of eyes.
Nuchal organs are present usually as ovoid, dorsolateral pads just posterior to the prostomium.
The peristomium is limited to lips (Pleijel 2001a). The pharynx is muscular, axial, and when
everted is tipped by papillae. The pharynx is equipped with four hooked teeth with internal
canals connected to putative venom glands, similar to jaws of polynoids (Wolf 1986). As in
polynoids, they operate as a single pair of beak-like jaws, opening and closing dorsoventrally.
The gland secretions have yet to be characterized chemically or functionally. The pharynx in
Anaplopisione, however, is unarmed.
The pisionid morphotype is more diverse in gross prostomial morphology. The prostomium
is long and conical in Pisionidens but difficult to identify in Pisione, being greatly reduced and
surrounded by the buccal segment. A pair of eyespots is usually present in the region of the
second or third segment. Nuchal organs appear to be absent. Head appendages are limited to the
ventral palps and the dorsal and ventral cirri of the buccal segment, all of which point forward;
the exceptions are Pisionella, which also bears a median antenna, and Pisionidens, with paired
frontal antennae. Notoacicula of the buccal segment in Pisione project forward and medially
through the integument, superficially resembling opposed stylets. They are considerably forward
of and above the mouth opening, however, and no function has yet been ascribed to them. They
might be useful for stripping organic material adherent to sediment grains.
Motility
The large morphotype is well suited to burrowing in mud by crack propagation (Dorgan et al.
2006). For most species it is unknown whether they actively hunt or sit and wait. Pernet (2005),
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
however, described sit-and-wait behavior in Sthenelais berkeleyi, which burrows into sand and
uses antero-dorsally oriented chaetae to form a cylindrical opening that maintains a respiratory
connection to the sediment-water interface, a “chaetal snorkel.” Sthenelanella spp. are assumed
to be discretely motile tube dwellers. The smaller, more cylindrical morphotype moves
interstitially in gravel and burrows in sands. It is not known whether Pholoides sits and waits or
is a hunting predator.
Illustrations
Hutchings (2000) provides informative line drawings of the anterior anatomy of sigalionids.
Pleijel (2001b) provides informative drawings and scanning electron micrographs of pisionid
anterior appendages. San Martín et al. (1998, Fig. 2) show a stippled lined drawing of a partially
everted pharynx in Pisione garciavaldecasasi that clearly shows the spatial relationship of the
pharyngeal apparatus and the projecting notoacicula. Yamanishi (1998) provides line drawings
of 10 species of Pisione.
Feeding
Pernet (2005) offered polynoids as prey to buried Sthenelais berkeley. When the prey
approached S. berkeley extended its palps from the sediment to gauge its prey before striking,
very much in the manner described by Daly (1973) for Harmothoe imbricata. Pernet (2005)
unfortunately was able to study only a single individual.
From samples at 13 m water depth in the North Sea van Oevelen et al. (2009) reported δ15N
in Sthenelais boa and Sigalion spp. consistent with carnivory and similar to enrichment levels in
Nephtys hombergii. Guerin (2009) reported δ15N in unidentified Sigalionidae from 10 m depth
in Poole Bay, southern England, also consistent with carnivory. Sthenelais boa from the Bay of
Brest showed δ15N consistent with carnivory and exceeded among polychaetes only by Glycera
tridactyla (Schaal et al. 2010). Labioleanira yhleni from the Catalan slope also showed a δ15N
consistent with carnivory (Fanelli et al. 2011). Rigolet et al. 2014 reported Sthenelais boa to be
near the top of the food web in the Bay of Concarneau, Bay of Biscay, at 15 - 35 m water depth.
In Posidonia beds at 5 - 8 m water depth off Mallorca Island, Deudero et al. (2011, 2014) found
Pelogenia arenosa to have 15N enrichment comparable to levels in lumbrinerids, again indicative
of carnivory.
The single sigalionid analyzed for fatty acids by Würzberg et al. (2011) from the abyssal
Weddell Sea had high fatty alcohol concentration with clear markers for phytodetritus. We
suspect that, like the goniadid also analyzed, this sigalionid obtained those markers indirectly by
preying on species that consume phytodetritus.
Guild membership
We list Sigalionidae as carnivores. Sthenelais berkeley sits and waits; whether other species
do the same or hunt more actively is unknown, but sit-and-wait predation is expected in tubebuilding Sthenelanella spp. S. berkeley buries itself but feeds on passing epifauna. Comparable
information for other species is lacking. Judging from its habitat distribution, the pisionid
morphotype probably feeds primarily on interstitial protists and metazoans.
Research questions and opportunities
• Functions of the projecting notoacicula of Pisione remain to be determined.
• Motility remains to be quantified.
• Prey preferences and realized diets remain to be determined.
• It may be possible to relate anterior chaetal structure (the “snorkel”) to sit-and-wait predation
on epifauna (Pernet 2005).
Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
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Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
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Diet of worms emended: an update of polychaete feeding guilds
Jumars, Dorgan & Lindsay
07 November 2014
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Please e-mail corrections and additions to Kelly Dorgan <[email protected]>.
A286
Sigalionidae
Supplemental Material: Annu. Rev. Mar. Sci. 2015. 7:497–520
doi: 10.1146/annurev-marine-010814-020007
Diet of worms emended: an u