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Zoological Journal of the Linnean Society, 2015, 174, 93–113. With 8 figures
Description of a new family, new genus, and two new
species of deep-sea Forcipulatacea (Asteroidea),
including the first known sea star from hydrothermal
vent habitats
CHRISTOPHER MAH1,2*, KATRIN LINSE3, JON COPLEY4, LEIGH MARSH4,
ALEX ROGERS5, DAVID CLAGUE6 and DAVID FOLTZ2
1
Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution,
Washington, DC 20013-7012, USA
2
Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA
3
British Antarctic Survey, High Cross, Madingley Road, Cambridge, CB3 0ET, UK
4
Ocean and Earth Science, University of Southampton, Waterfront Campus, Southampton,
SO14 3ZH, UK
5
Department of Zoology, University of Oxford, The Tinbergen Building, South Parks Road, Oxford,
OX1 3PS, UK
6
Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039, USA
Received 1 September 2014; revised 24 October 2014; accepted for publication 3 November 2014
Based on a phylogenetic analysis of undescribed taxa within the Forcipulatacea, a new family of deep-sea forcipulatacean
starfishes, Paulasteriidae fam. nov., is described from deep-sea settings. Paulasterias tyleri gen. et sp. nov. was observed at recently documented hydrothermal vents on the East Scotia Ridge, Southern Ocean. A second species,
Paulasterias mcclaini gen. et sp. nov. was observed in deep-sea settings in the North Pacific, more distant from
hydrothermal vents. Both species are multi-armed (with between six and eight arms), with a fleshy body wall,
and a poorly developed or absent adoral carina. Here, we include discussions of pedicellariae morphology, feeding
biology, and classification.
© 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 93–113.
doi: 10.1111/zoj.12229
ADDITIONAL KEYWORDS: Antarctica – deep sea – forcipulatacea – hydrothermal vent – North Pacific –
pedicellariae.
INTRODUCTION
Deep-sea chemosynthetic communities are ecologically and biologically significant settings that are host
to many associated but often undescribed taxa (e.g.
MacPherson, Jones & Segonzac, 2005). These habitats are predominantly composed of organisms fuelled
by the in situ primary production of chemosynthetic
microbes. At deep-sea hydrothermal vents, the source
*Corresponding author. E-mail: [email protected]
of energy for this microbial production is through the
oxidation of reduced inorganic chemicals found in high
concentrations in vent fluid effluent. Many of these
chemosynthetically sustained communities are composed of diverse invertebrate taxa, such as crustaceans, bivalves, and annelids (e.g. Desbruyères, Segonzac
& Bright, 2006), that often possess unusual adaptations for surviving in these extreme habitats.
Paradoxically, the Echinodermata, one of the most
primary inhabitants of deep-sea benthos in terms of
abundance and ecological importance (e.g. Gage & Tyler,
1991), are present with very little if any prominence
© 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 93–113
93
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C. MAH ET AL.
in chemosynthetic settings; however, echinoderms do
occur in these communities, albeit in different capacities with varying levels of abundance and diversity.
Our understanding of the roles that echinoderms occupy
in these faunal assemblages is in its infancy, as our
first steps include the discovery and description of these
taxa.
Asteroids have been recorded as having non-obligate
relationships with cold-seep habitats (Carney, 1994),
but, to date, no specimens have been collected as
primary members of hydrothermal vent settings. Asteroids show ecological importance in shallow water
settings (e.g. Paine, 1966, 1969), and although they
are also significant in deep-water habitats (e.g. Gale,
Hamel & Mercier, 2013), our understanding of their
role in the deep sea remains poorly understood. The
presence of asteroids as members of hydrothermal vent
assemblages is unprecedented, and the discovery of
not simply new species but also a new genus and
family from these isolated deep-sea habitats is also
remarkable.
NEWLY
DISCOVERED DEEP-SEA FORCIPULATES
This article was motivated by material collected during
two major marine research expeditions, including one
undertaken by the British Chemosynthetic Ecosystems in the Southern Ocean (ChEsSo) consortium, and
one undertaken by the Monterey Bay Aquarium Research Institute (MBARI).
The first species was collected during an exploration
of hydrothermal vent communities on the East Scotia
Ridge in the Southern Ocean by ChEsSo in 2010 (see
Fig. 1; Rogers et al. 2012, Marsh et al., 2012). The faunal
assemblages at two vent fields discovered on the East
Scotia Ridge were dominated by taxa such as anomuran
crabs, peltospiroid gastropods, eolepadid barnacles, and
actinostolid sea anemones, in abundance, several of which
were new to science (Marsh et al., 2012). Among the
animals observed and collected was a new species of
seven-rayed forcipulate asteroid, initially identified as
‘Stichasteridae sp. nov.’, which was among the visually representative vent fauna of the East Scotia Ridge
(Rogers et al., 2012). This species has since been shown
to have closer affinities with stemward forcipulataceans,
and is described and discussed herein.
The MBARI species was first identified from specimens collected during the 2009 Pacific Northwest Expedition (see Fig. 1; geological aspects outlined by Helo
et al., 2013). Both the East Scotia Ridge species and
the MBARI species were observed in situ, with data
gathered on their respective ecological settings. Further
data on phylogenetic and ecological affinities are
presented below.
MATERIAL AND METHODS
MATERIALS
Specimens examined herein were from ChEsSo collections hosted at the Natural History Museum, London
Figure 1. Map showing species occurrence of the Paulasteriidae in the North Pacific and the Southern Ocean.
© 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 93–113
PAULASTERIAS: HYDROTHERMAL VENT STARFISH
(NHM) and the National Museum of Natural History
in Washington, DC (NMNH). Scanning electron microscopy was performed using the Zeiss EVO MA 15
at the scanning electron microscopy (SEM) suite in the
National Museum of Natural History. The terminology used to describe pedicellariae morphology is taken
from Lambert, deVos & Jangoux (1984). Ossicle terminology is taken from Turner & Dearborn (1972).
METHODS
Most of the molecular data (for the mitochondrial 16S
rDNA, mitochondrial 12S rDNA, and nuclear earlystage histone H3 gene) have been previously reported
and analysed by Mah & Foltz (2011b). Mah & Foltz
(2011a, b) should be consulted for details on DNA extraction, polymerase chain reactions (PCRs), sequencing, contig assembly, GenBank accession numbers,
specimen voucher numbers, alignment methods, and
curation of alignments prior to phylogenetic analysis.
The new sequence data for Paulasterias tyleri
gen. et sp. nov. have GenBank accession numbers
JQ918326, JQ918344, and JQ918211 for the 16S, 12S,
and histone H3 gene regions, respectively. Sequence
data for Paulasterias mcclaini gen. et sp. nov. have been
published in the supplementary data table for Mah &
Foltz (2011b: S1) under ‘Pedicellasteridae nov. gen.,
nov. sp. #3’ for USNM 113787, 113788, and 113789. The
concatenated alignment contained 137 nucleotide
sequences and 1030 nucleotide positions. Some nonessential species with missing data in two of the outgroups (Asteriidae/Sclerasterias and Valvataceae) that
were previously analysed were excluded in the present
report.
Phylogenetic analysis was performed in MEGA 6.06
(Tamura et al., 2013) using the maximum-likelihood
method, based on the general time-reversible model
(Nei & Kumar, 2000). Initial tree(s) for the heuristic
search were obtained with the neighbour-joining method
and a matrix of maximum composite-likelihood pairwise
distances. A discrete (five categories) Gamma distribution was used to model evolutionary rate differences
among sites (Γ parameter estimate 0.4133). All nucleotide
positions with less than 95% site coverage in the concatenated alignment were eliminated; i.e. a maximum
of 5% alignment gaps, missing data, and ambiguous
bases were allowed at any position. There were a total
of 1005 positions in the analysed alignment. The tree
with the highest log likelihood (24165.83) was shown
in Figure 2, with bootstrap support values displayed
next to the branches (when greater than 0.7) and branch
lengths scaled to the number of substitutions per site.
RESULTS
We obtained sequence data for specimens of
P. tyleri gen. et sp. nov., as indicated below (Material
95
examined; Table 1), and merged them with the
Forcipulatacea data set from Mah & Foltz (2011b). The
tree with these species included differs in minor respects, but the topology in Figure 2 is essentially the
same topology as that presented by Mah & Foltz (2011b).
The taxon labelled ‘6-rayed pedicellasterid clade’ in Mah
& Foltz (2011b) is described below as Paulasterias
mcclaini gen. et sp. nov. Our data set further adds the
newly discovered Antarctic P. tyleri gen. et sp. nov. to
the data set, where it was supported as part of the
Paulasterias gen. nov. clade with 100% bootstrap support
(Fig. 2).
The position of Paulasterias in our three-gene tree
(Fig. 2) is identical with the three-gene topology presented by Mah & Foltz (2011b: fig. 3) for the
Forcipulatacea. The ‘6-rayed pedicellasterid’
(= Paulasterias) and Labidiaster annulatus Sladen,
1889 (Heliasteridae) were supported on the same
clade. The Paulasterias + Labidiaster annulatus
(Heliasteridae) branch is sister clade to the
Stichasteridae + ‘Ampheraster clade’ in both threegene trees (here and in Mah & Foltz 2011b). The addition of P. tyleri gen. et sp. nov. did not alter the topology
of the three-gene tree topology from that presented in
Mah & Foltz (2011b).
Although the topology was largely similar, there were
slight differences between the three-gene tree topology presented herein (Fig. 2) and the two-gene tree presented by Mah & Foltz (2011b: fig. 2), which used a
larger taxon sampling. The Mah & Foltz (2011b) twogene tree showed the ‘6-rayed pedicellasterid’
(= Paulasterias) clade as sister branch to a clade containing Heliasteridae (including Labidiaster and
Heliaster) + ‘Ampheraster clade’. The clade containing ‘6-rayed pedicellasterid’ + (Heliasteridae+
‘Ampheraster clade’) is sister to the Stichasteridae.
SYSTEMATICS
FORCIPULATACEA BLAKE 1987
PAULASTERIIDAE FAM. NOV.
Mah & Foltz 2011b: 649–653, 658; figures 2–3.
Type genus/species
Paulasterias tyleri gen. et sp. nov.
Diagnosis
Pedicellasterid-like forcipulataceans with small disc and
between six and eight arms. Reticulate skeleton, weakly
developed, concealed by fleshy body wall or dense
spinelets. Fleshy body wall with abactinal spinelets and/
or pedicellariae and furrow spines sheathed in tissue.
Adoral carina either minimal (one or two adambulacrals
abutting) or absent altogether. Madreporite encircled
by spines. One shared, crossed pedicellariae type, with
jagged teeth on valve edge and multiple shanks on valve
© 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 93–113
96
C. MAH ET AL.
100
Asteriidae [restricted] / Sclerasterias, N=23 species
98 Freyella sp. CASIZ 163058
100
Freyella sp. CASIZ 163025
83
82
98
94
Freyastera benthophila
Brisingidae
Astrostephane moluccana
99
Hymenodiscus sp. 1 MNHNP EcAH6036
Hymenodiscus sp. 2 USNM E47614
100 Paulasterias mcclaini CLM-314
100 Paulasterias mcclaini CLM-320
Paulasteriidae
Paulasterias tyleri
Labidiaster annulatus
100 Tarsaster alaskanus
100
Tarsastrocles verrilli
82
New genus new species #2 CLM-310
Cosmasterias lurida
99
Granaster nutrix
81
Stichaster australis
Stichaster striatus
100
Tarsaster galapagensis
100
Cosmasterias dyscrita
Stichasteridae
Pseudechinaster rubens
78
100 Neosmilaster steineni
Neosmilaster sp. CLM-37
100 Allostichaster farquhari
Allostichaster sp. CASIZ 174681
Smilasterias sp. CLM-214
Neomorphaster forcipatus
99 Zoroaster ophiactis
100
Zoroaster spinulosus
100
Zoroasteridae
Zoroaster fulgens
Myxoderma platyacanthum
Doraster constellatus
100
New genus new species #1 CLM-312
Hydrasterias sp. CLM-318
100
Pedicellasteridae
Pedicellaster magister
Pedicellaster
hypernotius
100
100
Valvataceae, N=74 species
84
0.05
Velatida, N=5 species
98
Figure 2. Phylogenetic tree for the Paulasteriidae and related taxa, based in large part on a three-gene data set from
Mah & Foltz (2011b). The scale bar shows the number of substitutions per site; see Material and methods for additional
details.
roof (sensu Lambert et al., 1984). Tube feet biserial or
quadraserial (distally biserial). Both known members
were collected from deep-sea settings below 2000 m in
depth, either from or in the vicinity of hydrothermal
vents.
ESTABLISHMENT
OF THE
COMPARISONS WITH THE
PAULASTERIIDAE AND
PEDICELLASTERIDAE
Based on the molecular evidence presented in Figure 2
and the morphological data outlined below, it is argued
that the two new species presented herein are members
of a new, previously undescribed clade, which we now
name as a new family, the Paulasteriidae, for the newly
described type genus Paulasterias. This clade represents the first new taxon (i.e. based on undescribed
or previously unknown material) within the
Forcipulatacea since the 1800s. Many of the newer families, such as the Pycnopodiidae Fisher, 1928 or the
Freyellidae Downey, 1986 have been based on, or
elevate, previously recognized taxa. Within the
Asteroidea as a whole, the two most recently
© 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 93–113
© 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 93–113
NHMUK 2014.10
USNM 1231372
NHMUK
2014.11–15
USNM 1231372
NHMUK
2014.16–18
NHMUK
2014.19–22
NHMUK 2014.23
NHMUK
2014.24–27
NHMUK 2014.28
USNM 1231374
NHMUK
2014.29–30
USNM 1097554
USNM 1087711
Holotype (DNA
voucher)
Paratype (DNA
voucher)
Paratype
Paratypes
Paratypes
Paratypes
Paratype
Paratypes
Paratype
Paratype
Paratypes
Paratype
Paratype
Specimen ID
Status
Kemp Caldera: start, −59.69955,
−28.3501; end, −59.69345, −28.3522
Kemp Caldera: start, −59.695, −28.351;
end, −59.6949, −28.3496
Kemp Caldera: start, −59.6935, −28.3537;
end, −59.6949, −28.3495
North of Saunders Island, South
Sandwich Islands, Scotia Sea:
57°39′00″S, 26°00′24″W.
Southern Ocean: 74°06′S, 175°05′W to
74°06′S, 174°58′W
Site E9, South Sandwich Islands: start,
−60.0428, −29.9815; end, −60.0427,
−29.4814
Site E9, South Sandwich Islands: start,
−60.0428, −29.9815; end, −60.0427,
−29.4814
Site E9, South Sandwich Islands: start,
−60.0428, −29.9815; end, −60.0427,
−29.4814
Site E9, South Sandwich Islands: start,
−60.0428, −29.9815; end, −60.0427,
−29.4814
Site E9: start, −60.0491, −29.9741; end,
−60.0426, −29.9813
Site E2, west of Dog’s Head: start,
−56.087, −30.31; end, −56.0884,
−30.3185
Site E2, west of Dog’s Head: start,
−56.087, −30.31; end, −56.0884,
−30.3185
Site E9, South Sandwich Islands: start,
−60.0428, −29.9815; end, −60.0427,
−29.4814
Locality and coordinates
Table 1. List of type specimens for Paulasterias tyleri
2350
2380–2609
1420–1435
1294–1424
1517-1421
2401–2402
2401–2402
2401–2402
2401–2402
2402
2401–2402
2606–2611
2606–2611
Depth
(in m)
Coll. RV Eltanin, Feb 8,
1968
JC-42-F-0755, dive 152,
Feb 11, 2010
JC-42-F-0697, dive 149,
Feb 8, 2010
JC-42-F-0754, dive 153,
Feb 12, 2010
Coll. RV Islas Orcadas,
May 27, 1975
JC-42-F-0460, dive 144,
Jan 30, 2010
JC-42-F-0339, dive 140,
Jan 30, 2010
JC-42-F-0385, dive 140,
Jan 30, 2010
JC-42-F-0316, dive 140,
Jan 30, 2010
Cruise JC42-F-0385, dive
140, Jan 30, 2010
JC 42-F-0270, dive 140,
Jan 30, 2010
JC 42-F-0219, dive 135,
Jan 25, 2010
JC 42-F-0219, dive 135,
Jan 25, 2010
Collection data
1 dry specimen, 7 arms,
R = 6.1 cm, r = 1.4 cm
5 wet specimens, 7 arms,
R = 5.5, 4.7, 5.0, 8.4, and
8.0 cm, r = 1.1, 1.1, 1.1, 1.6,
and 1.7 cm
2 dry specimens, 7 arms, R = 4.7
and ∼6.2 cm, r = 0.9 and
0.9 cm
3 wet specimens, 7 arms,
R = 6.1, 6.6, and 7.0 cm,
r = 1.0, 1.0, and 1.2 cm
4 wet specimens, 7 arms,
R = 6.0, 6.8, 7.2, and 8.2 cm,
r = 1.0, 1.4, 1.0, and 0.9 cm
1 wet specimen, 7 arms (6 arms
and 1 arm incipient),
R = 2.2 cm, r = 0.8 cm
4 wet specimens, 7 arms,
R = 7.9, 6.5, 9.0, and 7.6 cm,
r = 0.7, 0.4, 1.0, and 1.2 cm
1 wet specimen, 7 arms,
R = 6.6 cm, r = 1.3 cm
1 wet specimen, 8 arms,
R = 7.2 cm, r = 0.8 cm
2 wet specimens, 7 arms, R = 2.5
and 8.0 cm, r = 0.5 and 1.5 cm
1 dry specimen, 7 arms,
R = 4.6 cm, r = 0.9 cm
1 wet specimen, 7 arms,
R = 7.1 cm, r = 1.1 cm
1 wet specimen, 7 arms,
R = 5.4 cm, r = 1.3 cm
Specimen measurements, etc.
PAULASTERIAS: HYDROTHERMAL VENT STARFISH
97
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C. MAH ET AL.
described families include the Caymanostellidae, described by Belyaev (1974), and the Podosphaerasteridae
Fujita & Rowe (2002), although in the latter case, the
recognition of Podosphaeraster was made by Clark &
Wright (1962).
The clade discussed in the results section, including the ‘6-rayed pedicellasterid’ (sensu Mah &
Foltz, 2011b) and the ‘Antarctic stichasterid’ or
‘Stichasterid n. sp.’ (e.g. Rogers et al., 2012) included
in the analysis are supported as a distinct clade, previously unrecognized and separate from other
forcipulataceans. Some characters used in the description of the taxa, such as a weakly developed adoral
carina, occur among multiple forcipulatacean lineages, suggesting that these characters are convergent. Morphological synapomorphies for the group are
not abundant but there are diagnostic characters for
the lineage that further support its distinction as a
new family.
Prior classifications of the Forcipulatacea, when considering the Pedicellasteridae, focused on the characters that were most comparable with the Asteriidae,
the group to which pedicellasterids were most similar.
Characters such as tube foot rows, development of the
abactinal/marginal/actinal skeleton as well as the adoral
carina (= the number of adambulacral plates abutted
proximal to the oral plates) were the primary emphasis (e.g. Fisher, 1928). As indicated earlier, prior molecular data on forcipulataceans (Mah & Foltz, 2011b)
show that the Pedicellasteridae was not a monophyletic
group, being instead composed of several clades occupying stemward locations.
Although they occur on different clades within the
Forcipulatacea, comparisons between the Paulasteriidae
and various ‘pedicellasterid’ genera are inevitable given
the characters present, such as a minimal or absent
adoral carina, biserial tube foot rows, and fleshy body
tissue/weakly developed abactinal skeleton. Our results
(Fig. 2) show the Paulasteriidae as separated from other
pedicellasterids, including ‘Tarsaster’, which was present
on two different clades, and Pedicellaster and
Hydrasterias on another more distant clade.
In addition to the paraphyly of the group as a result
of the molecular trees presented by Mah & Foltz (2011b),
however, further taxonomic issues have since been discovered for taxa within the Pedicellasteridae (e.g.
paraphyletic genera, etc.). A more comprehensive
summary of diagnostic characters distinguishing
Paulasterias from other ‘Pedicellasteridae’ is being developed, but full treatment is beyond the scope of this
account. Thus, diagnostic treatments presented herein
should be considered only as a means of broadly distinguishing the Paulasteriidae from other members of
the Forcipulatacea. Comparisons between Paulasterias
tyleri gen. et sp. nov. and other Antarctic Asteriidae are
listed in Table 2.
PAULASTERIAS GEN. NOV.
Etymology
See below.
Key to species
1. Seven arms in most individuals examined (Fig. 3A–
D), with two specimens showing some variation (one
six-rayed individual with emerging seventh ray and
one seven-rayed individual with emerging eighth
ray; Fig. 3B). Abactinal, lateral surface covered by
dense thickets of spinelets (Fig. 3E,F). Welldeveloped septa present at internal arm junction
(Fig. 4D). Adoral carina composed with one or two
abutting plates (Fig. 4C). Tube foot rows weakly
quadraserial proximally (Figs 3D, 4C), becoming
biserial distally. Scotia Arc, Southern Ocean.
Paulasterias tyleri gen. et sp. nov.
1′. Six arms in all individuals examined (Fig. 7). Dense
thickets of spinelets absent (Fig. 7B,D). Few short
spines present. Spines widely distributed, rarely occurring on surface which is mostly covered by skin
and pedicellariae. No septa observed at internal arm
junction. Adoral carina absent, no adambulacral
plates in contact. Tube foot rows biserial along entire
arm distance. North Pacific.
Paulasterias mcclaini gen. et sp. nov.
PAULASTERIAS TYLERI GEN. ET SP. NOV.
FIGS 3A–F, 4A–E, 5A–D
Stichasteridae sp. (or ‘stichasterid asteroid’) Rogers et al.
2012: 7, table 2, figure 3E; Marsh et al., 2012: 1, 2, 6,
8, 15, figures 4, 5, table 1; Reid et al. 2013: 1, 6, 8, 9,
tables 3 and 5.
Etymology
The genus and species are named for Professor Paul
Tyler, Member of the Most Excellent Order of the British
Empire (MBE), National Oceanography Centre, at the
University of Southampton, in honor of his voluminous contributions to deep-sea biology.
Ecological observations
This species was observed towards the base of vent
chimneys and peripheral to areas of low-temperature
diffuse venting (Fig. 3A,B), and was classified as part
of the ‘peripheral assemblage’ as described by Marsh
et al. (2012). This species was observed individually
as well as in small aggregations of between two and
five individuals (with 0.11 m being the closest proximity between the centre points of the discs). Throughout the three ChEsSo cruises to the East Scotia Ridge
(2009 JR224 RRS James Clark Ross; 2010 JC42 RRS
© 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 93–113
FS, furrow spine.
Diplasterias spp.
(D. octoradiata
or D. radiata)
Saliasterias
brachiata
2
2
9 (10)
1
8
8–10
2 or 3
10 or 11
1 or 2?
9 (10)
Psalidaster
mordax rigidus
Lysasterias
heteractis
2 (3)
6–8 (7)
Paulasterias
tyleri gen.
et sp. nov.
Psalidaster
mordax mordax
FS
Arms
Species
Spinelets. Widely spaced.
Large, distinct, conical
spines in distinct series.
Spines, cylindrical to
pointed. Relatively few
distributed irregularly
over surface.
Dense, fleshy thicket.
Spinelets covered by
tissue.
Spinelets. Abundant but
evenly distributed.
Similar in size to
pedicellariae.
Large discrete spines.
Spination
Weakly developed.
Moderately
developed.
Weakly developed
but with
prominent
abactinal plate
clusters.
Strongly developed.
Moderately
developed.
Weakly developed.
Skeleton
Wrench-like. No
prominent
teeth.
Crossed with
multiple teeth.
Two-fanged with
beak.
Wrench-like. No
prominent
teeth.
Multiple teeth on
valves, no
fangs.
Two-fanged with
beak.
Pedicellariae
morphology
Table 2. Character comparisons between Paulasterias tyleri gen. et sp. nov. and Antarctic Asteriidae
18–845 m
Small (1/10th of spine
length). Centred
primarily around spines.
Present widely on body
surface.
27–647 m
110–402 m
15–319 m
160–3931 m
1294–2640 m
Depth
Small. Widely occurring on
body surface and around
marginal spines.
Large. Centred on spines.
Abundant on abactinal
surface. Straight peds
on adambulacrals.
Large (L ≥ spines)
abundant on abactinal
surface.
Pedicellariae location,
notes
PAULASTERIAS: HYDROTHERMAL VENT STARFISH
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C. MAH ET AL.
Figure 3. Paulasterias tyleri gen. et sp. nov., whole body and abactinal views. A, P. tyleri gen. et sp. nov. in situ from
Kemp Caldera. B, in situ image from the E9 segment of East Scotia Ridge showing an individual apparently feeding on
Kiwa sp. More specific details of this image can be found in Marsh et al. (2012). C, paratype NHMUK 204.11–15, aboral
surface, R = 8.0 cm, r = 1.7 cm. D, paratype NHMUK 204.11–15, oral surface. E, paratype NHMUK 204.11–15, close-up
of abactinal surface. F, paratype USNM 1231372, close-up of abactinal surface on dried specimen.
James Cook; 2011 JC55 RRS James Cook), four areas
of low-lying diffuse flow seabed at the E9 vent field
were imaged in subsequent years [Fig. 6; 2009 and 2011,
Seabed High Resolution Imaging Platform SHRIMP;
2010, remotely operated vehicle (ROV) Isis]. Within these
areas of observed seabed, absolute numbers of
P. tyleri gen. et sp. nov. remain constant, and using
seabed geological features for reference, the positions
© 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 93–113
PAULASTERIAS: HYDROTHERMAL VENT STARFISH
101
Figure 4. Paulasterias tyleri gen. et sp. nov., oral and skeletal views. All from paratype, USNM 1231372 (dried), except
for (E). A, lateral view of arm showing abactinal spination, marginals, and arm details. Scale bar: 0.5 cm. B, internal
view of body wall showing abactinal and marginal reticulate plate arrangement. Scale bar: 1.0 mm. C, oral view showing
mouth, tube foot grooves, adambulacral spination, and mouth spines. Scale bar: 0.5 cm. D, close-up of inter-radial septa
present between arms. Scale bar: 0.5 cm. E, ambulacral column from paratype USNM 1087711. Scale bar: 2.0 mm.
of individuals on the seafloor have changed by less than
1 m from the locations where they were first observed (Fig. 6).
Occurrence
East Scotia Ridge segments E2 and E9, South Sandwich Islands, Kemp Caldera to Ross Sea, 1420–
2609 m.
Taxonomic comments
Paulasterias tyleri gen. et sp. nov. displays a body form
similar to that of several different multi-armed
Antarctic asteriid taxa, all of which can be confused
with P. tyleri gen. et sp. nov., including species within
Psalidaster, Saliasterias, Lysasterias, and Diplasterias.
Differences between P. tyleri gen. et sp. nov. and these
species are outlined in Table 2.
Description
Between six and eight arms, but most specimens observed with seven; disc small (R/r = 3.78–9.00, but most
with ∼5–6, where R is the length from disk center to
end of arm and r is radius of the disc). One smaller
specimen (NHMUK 2014.23, R = 2.2 cm) has six arms,
with an incipient seventh growing between two other
arms.
Based on measurements of the disc size compared
with the R/r ratio, individuals with smaller discs show
a more strongly stellate body form, whereas arm length
varies between more strongly and weakly stellate
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C. MAH ET AL.
Figure 5. Paulasterias tyleri gen. et sp. nov., paratype USNM 1087711, crossed pedicellariae. All SEM images except
where noted. A, light-microscope image; total length ∼ 0.5 mm. B, articulated pedicellariae. Scale bar: 100 μm. C, Single
disarticulated pedicellariae valve. Scale bar: 100 μm. D, distal edge of pedicellariae valve showing teeth. Scale bar: 50 μm.
individuals. Arms proximally swollen, with distinct septa
present inter-radially at contact points between arms
(Fig. 4D). Spination absent from surface in this region.
Endoskeleton weakly calcified, with widely spaced
reticulation (observable when tissue is denuded;
Fig. 4B). Two types of pedicellariae present: straight
pedicellariae on arm surface and adambulacral plate
in tube foot furrow, with crossed-type pedicellariae
covering the majority of the abactinal/lateral surface
(Fig. 5).
Abactinal plates forming widely spaced reticulate
pattern. Surface covered by an abundance of dense
spinelets (Fig. 3E, F), fleshy tissue, and pedicellariae.
All abactinal plates (i.e. the reticulate patterns in
Fig. 4B) obscured. Spination forms a fur-like appearance to the surface (Fig. 3E, F). Spinelets, slender,
covered in a sheath of tissue (best observed in dry specimens), range in height from 0.5 to 1.0 mm (base to
tip) at densities of 20–30 along a 1.0-cm line (at R = 4.0–
6.0 cm, respectively). Individual plates with approximately between two and six spinelets, each arranged
in a crescentic or irregular series. Some individual
spinelets on single plates. Spinelet density heaviest on
abactinal and upper lateral surfaces (Fig. 3C, E, F).
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PAULASTERIAS: HYDROTHERMAL VENT STARFISH
103
Figure 6. Time series observations of Paulasterias tyleri gen. et sp. nov. from the E9 vent field over a 3-year period
(2009–2011). Individuals indicated by upward white arrows. Results presented from left to right in each image. Horizontal translocation distances: A–B, 0.48 and 0.00 m; C–D, 0.38 m; E–F, 0.46, 0.83, 0.85, and 0.22 m; G–H, 0.09 m. Laser
scale (i.e. two red dots produced by lasers for scale) in each image: 0.10 m. Laser scale in imagery was used to measure
absolute translocation distances (i.e. shortest distance travelled) of individual seastars between the years observed.
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C. MAH ET AL.
Abactinal plates are smaller (50–75% of the size) relative to the elongate and larger plates present in the
marginal plate/lateral arm region. Plates tightly reticulate, with very close articulation becoming almost
imbricate. Abactinal plates more irregularly arranged than those on marginal/lateral arm regions,
forming a continuum with the more regularly arranged plates present along the marginal/lateral arm
series (Fig. 4A, B). Abactinal plates reticulate, widely
arranged on the body surface, becoming more densely
arranged, almost imbricate, along marginal series. Gaps
between tightly articulated abactinal plates filled with
tissue often have between one and three (mostly single)
papula present between plates. Discrete carinal series
not observed.
Papulae are large and single but obscured among
spinelet-covered surface. Madreporite with deep sulci,
partially to completely covered and encircled by between
two and eight spinelets, arranged in a single series.
On some specimens, madreporite surface free of
spination.
Two types of pedicellariae observable on the abactinal
surface. Straight pedicellariae less abundant and not
observed on some individuals, present interadially
on the lateral arm surface but not observed on the
disc surface, similar in form but smaller (∼0.5 mm
in length) than those observed inter-radially in
P. mcclaini gen. et sp. nov. These present interadially
on the lateral arm surface but not observed on the disc
surface.
Most abundant crossed pedicellariae with rounded
valve edges (Fig. 5A–D). Pedicellariae width approximately <0.5 mm, present widely on body surface, interspersed among spines and papulae. Valves rounded with
multiple jagged edges. Pedicellariae on abactinal/
lateral surface crossed, and similar in form to those
observed in other forcipulataceans. Valves of these
pedicellariae articulate at their bases (Fig. 5A, B). The
distal part of the valve containing 25–40 sharp, conical
teeth, with smaller teeth at the distalmost edge and
larger teeth present more proximally on the roof. The
roof (i.e. present nearer to the base of the valve) of the
pedicellariae with 20–40 sharp conical teeth (Fig. 5C,
D). Numerous circular pores present where muscle and
tissue connect along the surface of each valve. Attachment area at proximal end of each valve with numerous fenestrae.
Marginal plate series partially obscured by spinelets
and fleshy tissue (Fig. 4A). Abactinal plates articulate with superomarginals elongate and forming
‘top edge’ of window-like spaces between each
superomarginal–inferomarginal pairing, with each containing papulae (Fig. 4B). Each of these large spaces
flanked by approximately between eight and 12 elongate, round- to rectangular-shaped, spine-bearing plates
forming a quadrate frame articulating with the
superomarginal series. Superomarginal plate series, imbricate, trilobate in shape, smaller than inferomarginals
(<50% of size), flanked by other imbricate plates
articulating with adjacent superomarginals.
Superomarginals + intermarginals with between one
and four large spines (Fig. 4A). Larger spines present
proximally, becoming smaller distally. Intermarginal
plates present between superomarginals and
inferomarginals, with between two and four
(mostly three) forming borders around papular
regions. Inferomarginals multilobate, larger than
superomarginals. Single, large spine present on
inferomarginals, decreasing in size proximally to distally. Papulae, between two and four, mostly three,
present between spaces formed by lobes between
superomarginal plates.
Inter-radial septa present between arms (Fig. 4D),
flanking large membrane-like window at proximal articulation between arms. Plates that form the septa
are large, scalar, and articulate with actinolateral and
adambulacral plates. Lower end of inter-radial septa
articulates via actinal plating with adjacent arm septa.
Actinal plates, individually diamond to polygonal in
shape. Present in series adjacent to adambulacrals along
arm. Actinal plates form irregular imbricate pavement inter-radially on disc. Adoral carina composed
of one or two abutted adambulacrals. Tissue present
between abutted contact along plates of adjacent
adambulacrals (implying no direct skeletal fusion).
Adoral carina with two abutting adambulacrals observed in slightly larger individuals (e.g. R = 6.1 cm,
USNM 1087711).
Each paired oral plate articulated with tissue, shieldshaped, with two spines present on surface (Fig. 4C).
In addition to these surficial oral spines, two more
elongate spines present on each oral plate project into
mouth, each with approximately a dozen straight
pedicellariae clustered around the base. These two
elongate oral spines are consistent in numeration and
morphology, with furrow spines present on each
adambulacral plate. Furrow spines, two per
adambulacral plate, are tissue-covered, thick, and round
in cross section. Approximately between four and a
dozen pedicellariae, beak-like, differing from those on
the abactinal surface, occur on the furrow-side of each
adambulacral plate at the base of each set of furrow
spines. Adambulacral plates quadrate in outline,
blockish, punctuated by tissue present between plates
(Fig. 4B).
Ambulacral ossicles compressed and wing-shaped
(Fig. 4E), but with relatively broad keel and wide wing
relative to Asteriidae. Tissue present between ossicles.
A well-developed cardiac stomach observed (Fig. 3D)
extruded in all Scotia Arc specimens.
Living colour of animal is white to light reddish
orange.
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PAULASTERIAS: HYDROTHERMAL VENT STARFISH
participate in the 2009 Pacific Northwest MBARI
expedition.
Material examined
See Table 1.
PAULASTERIAS
105
MCCLAINI GEN. ET SP. NOV.
FIGS 7–8
‘Six-rayed pedicellasterid’ Mah & Foltz, 2011b: 649–653,
658; Figs 2–3.
Etymology
This species is named for Dr Craig McClain, NESCENT,
Duke University, who invited the lead author to
Taxonomic comments
The surveyed literature revealed no other comparable Indian or Pacific taxa. Three Atlantic
pedicellasterid species, Hydrasterias ophiodon (Sladen
1889), Hydrasterias sexradiatus (Perrier in MilneEdwards 1882), and Ampheraster alaminos Downey,
1971 possess six arms. The skeletons of these three
taxa lack a fleshy body wall, however, and are
relatively well developed, with strongly expressed
Figure 7. Paulasterias mcclaini gen. et sp. nov. A, in situ image of USNM 1138789 from CoAxial North Seamount,
North Pacific; R = 3.5 cm, r = 0.4 cm. B, paratype USNM 1138789 (wet). Abactinal surface. C, madreporite with spiny
ring (paratype USNM 1138787). D, paratype USNM 1138787 (dry, R = 2.4 cm, r = 0.2 cm). Abactinal/lateral view showing
pedicellariae and spines on dry specimen. E, paratype USNM 1138789 (wet, scale as before). Oral surface. F, paratype
USNM 1138787 (dry, scale as before). Oral surface showing spines, adambulacral plates.
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C. MAH ET AL.
Figure 8. Paulasterias mcclaini gen. et sp. nov. Pedicellariae and skeletal anatomy from paratype USNM 1231371.
Scale bar: 50 μm. A, SEM of articulated crossed pedicellariae. B, SEM of single valve, disarticulated crossed pedicellariae.
C, abactinal, inter-radial region showing pedicellariae distribution; straight versus crossed. D, close-up of straight pedicellariae
in inter-radius. Scale bar: 1.0 mm. E, ambulacral ossicles (lateral view). Scale bar: 1.0 mm. F, widely reticulate abactinal
plates (viewed internally). Scale bar: 1.0 mm.
reticulation across the disc and arms, compared with
that of P. mcclaini gen. et sp. nov., which is reduced to
weakly expressed, with widely dispersed irregular reticulation. Marginal plates and accessory spines are
observable in Ampheraster and Hydrasterias, but are
not observable in P. mcclaini gen. et sp. nov.
ECOLOGICAL
NOTES
Unlike P. tyleri gen. et sp. nov., specimens of
P. mcclaini gen. et sp. nov. were not collected from active
hydrothermal vent regions, but from adjacent or proximal settings displaying related geological activity (e.g.
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PAULASTERIAS: HYDROTHERMAL VENT STARFISH
Clague et al., 2013 for Axial Seamount; Damm et al.,
2006 for Gorda Ridge). As indicated under the ‘Material examined’ section, some specimens were collected 0.2 km away from active vent regions, whereas others
were collected more distantly. Specimens were collected from both soft bottom and rock substrates. These
areas included pillow lavas covered by fine sediments and vent chimney fragments. One specimen
(USNM 1138787) was collected from an area covered
by yellow, hydrothermally altered clays interspersed
with white bacterial mat.
No direct evidence of feeding (e.g. gut contents) was
present, but stomachs in at least two of the specimens
were slightly distended and one specimen was observed to have a slightly depressed disc relative to the
arms, suggesting that its stomach was extended to the
substrate. It is possible that P. mcclaini gen. et sp. nov.
is a detritivore or perhaps feeds on the bacterial mats
present in the area.
Occurrence
CoAxial North Seamount, Juan deFuca Ridge; ‘North
Cleft’ pillow mounds, Gorda Ridge south to Taney Seamount, North Pacific Ocean, 2257.9–3321.8 m.
Description
Arms six, slender, elongate; disc small. Body strongly
stellate (R/r = 6.4–14.4).
Abactinal skeleton strongly minimized, especially in
the smaller specimen. Larger specimens with thicker,
fleshier skin. In smaller individuals, body surface paperthin on dried specimens. Abactinal skeleton nearly absent
except the primary circlet on the disc, carinal plates
expressed weakly and other tiny plates irregularly occurring on arms. Body surface covered by a layer of
fleshy, spongy tissue, obscuring plates in wet and unprepared dry specimens. Plates observed best in dry
specimens and obscured in living or wet-preserved individuals. Primary plates, polygonal, relatively large
present inter-radially, forming part of circular series
with smaller, rod-like plates extending between primary
circlet plates. Within the primary circlet, a series of
smaller, rod-like plates extends to the disc centre, forming
an irregular curve. Some minor, smaller quadrate plates
present at disc centre. Carinal plates present weakly,
each carinal plate lobate with four basal projections or
sometimes irregular in shape with a spine present on
the centre surface of each plate. Carinals not directly
articulated with primary circlet and weakly in contact
in series along arm. Carinal plates slender, overlapping. Thicker, more broad-based plates occurring regularly along carinal series where spines are present.
Slender, but irregularly shaped plates in short series
of ossicles forming weakly transverse ribs. Spines with
jagged tips. Abactinal plates particularly diffuse adradially,
becoming more defined closer to the marginal plate series.
107
Reticulation widely spaced, with prominent single papulae
present within plate openings. Pedicellariae covered
by pustular sheaths, occurring in the fleshy, dense covering on body surface.
Papulae not observed. Madreporite large, pentagonal in outline, strongly convex with well-developed sulci.
Madreporite thick and sitting above the plane of the
body surface. Basal madreporite region with spines.
Pedicellariae, three types present. Largest (length
∼1 mm) pedicellariae, straight with between three and
five jagged teeth on each valve, occuring heavily on the
inter-radial disc but also along the arm (Fig. 8C, D).
Second largest pedicellariae wrench-like, with curved
valves bearing small low-profile teeth (Fig. 8A,B), most
abundant covering abactinal and lateral surfaces of arm.
Smallest sized pedicellariae are straight and occur in
furrow at the base of each spine on each adambulacral
plate. These are similar in shape to the large, straight
pedicellariae, but more triangular in shape with fewer
teeth.
Marginal plates in incomplete series and obscured
by fleshy tissue, with individual plates often not in direct
contact but appearing to be in a discontinuous series
along lateral side to arm tip. Individual plates irregular in shape, some cruciform, others polygonal to lobate.
Some marginal plates directly in contact with
adambulacral plate series. Superomarginals relatively small, sometimes absent, especially in small individuals, cruciform to diamond in outline in weakly
defined series. Sometimes, when present, with a single
short pointed spine. Inferomarginals trilobate in shape,
each bearing a spine, easily between two and four times
larger than superomarginals, always present, overlapping onto adambulacral plate series. Inferomarginal
spines short, blunt round in cross section. Large straight
pedicellariae, equivalent in size and adjacent to
inferomarginal spine.
A series of single flattened imbricate plates extend
from the primary plates inter-radially from the abactinal
to the actinal surface, but absent in smaller individuals. Actinal clusters of plates composed of five or six
plates, some bearing a sharp spine and/or a large
straight pedicellariae, bearing multiple teeth on each
valve. Small gaps present between actinal plates filled
with skin. Papulae absent from actinal surface.
Furrow spines, one or two (mostly one) per
adambulacral plate, each with jagged tips. These spines
covered by fleshy, sacculate sheath. Single spines present
on first two adambulacral plates, remaining plates each
with two spines. Small furrow pedicellariae present (described above). Adambulacral plates wing-shaped, with
tissue-filled spaces between plates. First adambulacral
plates not in direct contact.
Cardiac stomach extended, muscular. Tube feet
biserial.
Colour of animal in life: white to light reddish orange.
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C. MAH ET AL.
Material examined
USNM 1231370 Holotype: Gorda Ridge, GR-14 Seacliff
Vent Field site, from 42.755725, −126.710512 to
42.755738, −126.71052, 2771.3–2771.5 m. Collected about
0.2 km from active venting, with black smokers and
Ridgeia sp. present, coll. D. Clague, MBARI, aboard RV
Western Flyer, using ROV Tiburon 8/23/2005 T884
A14+A15 (one wet specimen, R = 5.7 cm, r = −0.6 cm).
USNM 1231371 Paratype: Gorda Ridge, GR-14 Seacliff
Site, from 42.755725, −126.710512 to 42.755738,
−126.71052, 2771.3–2771.5 m. Collected about 0.2 km
from active venting, with black smokers and Ridgeia sp.
present. Coll. D. Clague, MBARI, aboard RV Western
Flyer, using ROV Tiburon 8/23/2005 T884 A14+A15 (one
dry specimen, R = 7.2 cm, r = 0.5 cm).
USNM 1138789 Paratype: CoAxial North seamount,
North Pacific, 46°31′00″N, 129°34′22″W, 2430.2 m, coll.
Clague/McClain, MBARI, aboard RV Western Flyer using
ROV Doc Ricketts D78-A4, 31 Aug, 2009. DNA sample
CLM 314 (one wet specimen R = 3.5 cm, r = 0.4 cm).
USNM 1138787 Paratype: North Cleft ‘1986 Pillow
mounds’, North Pacific, 45°1′54.1″N, 130°10′50.5″W,
2257.9 m, coll. Clague/McClain, MBARI, aboard RV
Western Flyer using ROV Doc Ricketts, D80-A1, 2 September 2009, DNA sample CLM D320 (one dry specimen, R = 2.4 cm, r = 0.2 cm).
USNM 1138788 Paratype: NESCA clam site, North
Pacific, 41°0′43.7″N, 127°29′28.5″W, 3321.8 m, coll.
Clague/McClain, MBARI, aboard RV Western Flyer using
ROV Doc Ricketts, D83-A10, 5 September 2009 (one wet
specimen, R = 2.9 cm, r = 0.45 cm)
Further occurence observations
Taney Seamount, 36.849706, −125.592912, 2840.6 m,
ROV Doc Ricketts, 8 August 2010, Dive D174-A30; Taney
Seamount 36.839267, −125.607463, 2427.1 m (images,
but no specimen collections verified).
DISCUSSION
ECHINODERMS AND THE PAULASTERIIDAE
IN
HYDROTHERMAL VENT SETTINGS
Hydrothermal vent environments, where geothermally
heated water produces sulfide-rich water in proximity to active underwater tectonics, were first documented on the Galapagos Rift in the late 1970s (Corliss
& Ballard, 1977; Lonsdale, 1977; Corliss et al., 1979).
These habitats host unusual communities, which have
been studied extensively (e.g. Gage & Tyler, 1991;
Desbruyères et al., 2006), and show a diverse invertebrate fauna, including several echinoderms inhab-
iting the primary vent areas. Desbruyères et al. (2006)
presented a brief overview of echinoderms occurring
in primary vent and adjacent regions. Six genera and
species of ophiuroids are documented from vent faunas
in the North Atlantic (Tyler et al., 1995; Stöhr &
Segonzac, 2005), as well as the East Pacific (Stöhr &
Segonzac, 2006) and Caribbean (Connelly et al., 2012).
Smirnov et al. (2000) described a species of sea cucumber from a primary vent habitat in the SouthEast Pacific Rise. Further accounts from Van Dover
et al. (1996) and Desbruyères et al. (2006) indicated
several echinoderm taxa, which occur peripherally to
the primary vent zones, including suspension-feeding
brisingid sea stars occurring on inert vent chimneys
(Desbruyères et al., 2006) and stalked crinoids on freshly
deposited basaltic rocks and other inactive geological
formations.
Paulasterias includes the first known member of the
Asteroidea to be directly present or closely associated with active hydrothermal vents; however, each species
seems to occur in different, if related, habitats.
Paulasterias tyleri gen. et sp. nov. shows a very close
relationship with the vent setting, as indicated by Marsh
et al. (2012), and was observed near the base of vent
chimneys and peripheral to areas of low-temperature
diffuse venting. It was classified as part of the ‘peripheral assemblage’, including the brisingid Freyella,
zoarcid fish, pycnogonids, individuals of the anomuran
‘Kiwa n. sp.’, and an unidentified octopodid. These represent taxa that occur at a distance away from visible
vent fluid exits. Although stable isotope values indicate nutrition ultimately derived from chemosynthetic
sources of carbon fixation, no clear chemosynthetic structure was apparent.
In contrast, P. mcclaini gen. et sp. nov. was observed much more distantly from active vent settings and was not observed in direct proximity to vent
communities. Some asteriid asteroids, such as
Sclerasterias, with Sclerasterias eructans (McKnight,
2006) identified as the synonym Rumbleaster by
McKnight (2006), have been observed in relatively high
abundance, crouched over and presumably feeding on
chemosynthetic clams in cold-seep settings (e.g. MacAvoy
et al., 2002; Cosel & Marshall, 2003; Gordon, 2010).
It is possible that Paulasterias shows a comparable relationship in hydrothermal settings: that is, they are
able to tolerate toxic environments long enough to feed
or derive nutrition from organisms or other prey supported by the primary vent setting.
Diagnostic for both members of the Paulasteriidae
is the fleshy body wall and highly reduced skeleton,
which appears to represent a synapomorphy for the
group, relative to the non-fleshy endoskeleton
observed in other closely related taxa (e.g. the Tarsaster
lineage and the Stichasteridae). The significance of the
fleshy body wall and reduced skeleton, if any, is unclear;
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PAULASTERIAS: HYDROTHERMAL VENT STARFISH
however, decalcified skeletons with fleshy body tissue
present are both characters observed on several highlatitude forcipulataceans, such as Lysasterias or
Diplasterias in the Southern Ocean or Icasterias in the
Arctic (Fisher, 1928, 1940, respectively).
Clear chemosynthetic structures were not
apparent; however, the dense spination on
P. tyleri gen. et sp. nov. shows a superficial resemblance to the dense setae on the hydrothermal vent
‘yeti crab’ Kiwa hirsuta Macpherson, Jones & Segonzac,
2005, which were observed harbouring filamentous bacteria (Goffredi et al., 2008). No bacteria were observed but microbial traces may not have endured
collection and preservation. Individuals occur outside
areas of visible hydrothermal fluid flow, where substrates for chemosynthesis may already be oxidised.
Dense spination is absent in P. maclaini, which was
not recorded from close proximity to a hydrothermal
vent, as P. tyleri gen. et sp. nov. had been. Heavier
spination in P. tyleri gen. et sp. nov. may reflect some
other function, such as defence within the context
of its closer proximity to the hydrothermal vent
community.
FEEDING
BIOLOGY
Reid et al. (2013) reported on carbon fixation pathways using stable isotopes to examine trophic relationships among food webs in this system, and reported
P. tyleri gen. et sp. nov. feeding on ‘Kiwa n. sp.’ (Marsh
et al., 2012: fig. 5H). Paulasterias tyleri gen. et sp. nov.
(identified in the paper as ‘stichasterid n. sp.’) was reported as a ‘vent macroconsumer’ that had a 13C indicative of mixed carbon sources (i.e. multiple nutritional
sources), which possibly also includes feeding on freeliving bacteria or other source nutritional material from
photosynthetic-derived carbon.
Paulasterias tyleri gen. et sp. nov., in addition to the
sea anemone Actinostola sp. and the pycnogonid
Colossendeis sp., were identified as having the highest
15
N values among taxa sampled from the vent settings, which suggests the highest trophic positions of
those predators sampled (Reid et al., 2013). Paulasterias
tyleri gen. et sp. nov. apparently possesses the highest
15
N value among the three predators sampled. ‘Kiwa sp.’
(sensu Reid et al. 2013) is not a predator but a primary
consumer in this instance.
In addition to the crab predation reported by Marsh
et al. (2012), other images (Fig. 3) also show several
different individuals with their disc hunched over, and
presumably feeding upon large patches of the
scalpelliform barnacle Vulcanolepas scotiaensis
(Buckeridge, Linse & Jackson, 2013). In situ images
show starfish attacking patches of Vulcanolepas from
different perspectives. Some are shown attacking the
smaller individuals along the edges, whereas others
109
are hunched over the more central, larger individuals in the central clusters.
In situ observations from Marsh et al. (2012) of
P. tyleri gen. et sp. nov. hunched over and apparently
feeding on ‘Kiwa n. sp.’ are consistent with these 15N
values; however, large, mobile crustaceans have not
been reported as food items for asteroids, except as
molts or moribund carcasses (e.g. Jangoux, 1982), and
in fact the opposite has been observed, as sea stars
are fed upon by large crabs and other decapods in shallower settings (e.g. summaries in Blake, 1983; Lawrence
& Vasquez, 1996). Reptant decapods in the periphery
of the East Scotia Ridge hydrothermal vent fields may
be comparatively torpid, however, as a result of the
effects of cold conditions on decapod physiology (e.g.
Wittmann et al., 2010). It may also be possible, given
the large number of individuals present, that
Paulasterias tyleri gen. et sp. nov. collectively feeds on
larger prey, as has been observed in the asteriid
Anasterias rupicola (Verrill, 1876) (Blankley & Branch,
1984).
Abundances of P. tyleri gen. et sp. nov. within areas
of the E9 seafloor observed over several years (2009–
2011) remained constant, with individuals observed
within <1 m radius of the locations where they were
first recorded (Fig. 6A–G). Asteroids from shallow water
and intertidal environments are known to ‘home’
(Scheibling, 1980), with seastar movement becoming
non-directional once patches of prey are encountered,
allowing individuals to remain in areas of high prey
density (McClintock & Lawrence, 1985). Whether such
behaviour also occurs among P. tyleri gen. et sp. nov. requires further investigation with the use of timelapse photography, assessed on both short- (i.e.
comparable with shallow water tidal cycles) and longterm (annual) time scales.
From the rocky intertidal, the asteroid Pisaster is
a renowned keystone species (Paine, 1966), exerting
top-down control on lower trophic levels, and preventing species at lower trophic levels from monopolizing
limiting resources (Paine, 1969). The role of predation in shaping vent communities is in its infancy,
with only one manipulative experiment (Micheli
et al., 2002) suggesting that vent-endemic predators,
such as zoarcid fish, exert ‘top-down’ control on vent
communities. Whether P. tyleri gen. et sp. nov. observed at the E9 vent field can be considered ‘vent
endemic’ is unclear; however, this species occupies the
highest trophic position at this vent field (Reid et al.,
2013), and has been observed actively predating on
‘Kiwa n. sp.’ (Marsh et al., 2012), but its potential influence on the overall patterns of species abundance
is unknown.
Paulasterias mcclaini gen. et sp. nov. was only observed individually and not in immediate proximity
to other faunal assemblages. One of the CoAxial
© 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 93–113
110
C. MAH ET AL.
specimens (USNM 1138789) displayed a distended
stomach during collection (Fig. 7E). Juniper et al. (1995)
reported significant quantities of microbial flocculence
in this region. It is possible that P. mcclaini gen. et sp. nov.
was feeding on this or other organic matter present in
the region.
PEDICELLARIAE
MORPHOLOGY AND FEEDING
The SEM images of pedicellariae observed in
Paulasterias indicate that a shared pedicellariae morphology is present. Pedicellariae observed in
paulasteriids display large numbers of teeth on the distal
edge of each valve. Prominent shanks were observed
on the roof (i.e. a more basal surface on each valve)
of the pedicellariae in each species. The SEM images
of crossed pedicellariae observed in Labidiaster
annulatus Sladen, 1889 by Dearborn, Edwards & Fratt
(1991) show that the overall valve morphology is similar
in shape to those observed in Paulasterias. This would
be consistent with the relatively close phylogenetic relationship observed between the Paulasteriidae clade
and Labidiaster (Fig. 2); however, shanks on the
pedicellariae roof and edge of the valve in Labidiaster
are larger, fewer in number, and are arranged in a single
row relative to those in the Paulasteriidae, which possesses numerous shanks in multiple rows on the valve
edge and pedicellariae roof.
One apparent similarity observed between three relatively distant forcipulataceans, Labidiaster, the brisingid
Novodinia (Emson & Young, 1994), and the so-called
‘fish catching’ starfish Stylasterias forreri (deLoriol, 1887)
(Chia & Amerongen, 1975), is that all three show the
presence of enlarged teeth on the distal edges of each
valve. These species have all been documented as
showing some form of pedicellariae-based benthopelagic
predation, suggesting that these enlarged teeth play
a role in holding mobile prey. This is considered in
contrast to a more generalized forcipulate, the asteriid
Marthasterias glacialis (Linnaeus, 1758), which shows
the absence of these enlarged valve teeth, but with
homogeneously sized shanks on the roof and on the
distal edge of each pedicellariae valve (Lambert et al.,
1984). Enlarged teeth on the distal valve edge are
absent from Paulasterias, with the overall morphology being more similar to the generalized pedicellariae
morphology observed in Marthasterias, implying that
the pedicellariae are not used for benthopelagic predation but are instead more generalized, perhaps occupying a defensive function.
DISTRIBUTION AND
DIVERSITY
The discovery of this clade underscores the potential
existence of significant new biodiversity in Antarctic
and deep-sea settings. Although only two taxa from
this group are included in our analysis, many more
members of this clade may remain to be discovered.
The collected specimens of P. mcclaini gen. et sp. nov.
are relatively small and have likely been overlooked
by prior submersible surveys, which are often attentive to larger, more prominent megafauna.
A six-rayed pink species with inflated arms has been
observed by the Okeanos Explorer on two ROV imaging
expeditions (C. Mah, pers. observ.), in the North
Atlantic (August 2013) and in the Gulf of Mexico
(April 2014). This species is possibly identified
as Ampheraster alaminos; however, it shows
superficially similar body colour and shape to
P. mcclaini gen. et sp. nov. No specimens have been
collected.
If P. mcclaini gen. et sp. nov. was a widely occurring deep-sea species, as several other asteroids are
(e.g. the Porcellanasteridae, see Madsen, 1961a, b),
it may represent a further occurrence of this species
in the Atlantic. The occurrence between both members
of this clade shows a substantial geographic distance
between the two species sampled. It is not unusual,
especially for asteroid groups in deep-sea and/or
cold-water settings to include members that occur widely,
e.g. across two hemispheres. The Poraniidae, for example
(Mah & Foltz, 2014), includes several genera that
occur at high latitudes in both hemispheres. In some
instances there are also examples of species
[e.g. Hippasteria phrygiana (Parelius, 1768)] that
occur broadly across a large distance (Foltz et al.,
2013).
PHYLOGENY
Our phylogenetic tree (Fig. 2) shows the Paulasteriidae
within the context of the larger Forcipulatacea data
set presented by Mah & Foltz (2011b), and shows the
group on the same clade as the Stichasteridae, the
Brisingidae, Labidiaster, the former pedicellasterid
Tarsaster, and the ‘asteriid’ Tarsastrocles. The original tree presented by Mah & Foltz (2011b) differs in
that the earlier tree shows the Brisingidae supported
as the sister clade to the younger and more derived
Asteriidae, rather than the older and more stemward
Stichasteridae. The primary occurrence of this group
in deep-sea settings (>1000 m) is consistent with the
presence of many stemward forcipulataceans (e.g.
Zoroasteridae and some stichasterids) at comparably
deep depths.
Although no molecular clock estimates were made
for the tree in Mah & Foltz (2011b), fossil occurrence
provided a hypothetical framework for timing within
the Forcipulatacea. For example, Blake, Breton & Gofas
(1996) described a pedicellasterid fossil from the Cretaceous of Africa. A Cretaceous stichasterid has been
described from California (Blake & Peterson, 1993).
© 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 174, 93–113
PAULASTERIAS: HYDROTHERMAL VENT STARFISH
Phylogenetically earlier taxa, such as the Zoroasteridae,
are consistent with Jurassic occurrences of zoroasteridlike forcipulataceans (Blake, 1990). This provides a
Mesozoic framework for the stemward history of
Forcipulataceans, including the Paulasteriidae.
The fleshy body wall in the Paulasteriidae has
not been observed in other known stemward
forcipulataceans (i.e. Stichasteridae, Zoroasteridae, and
Pedicellasteridae). This character occurs convergently
in different genera throughout the Asteriidae, primarily in high-latitude or cold-water taxa, including nearly
all the members of the Antarctic Asteriidae (e.g.
Lysasterias and Diplasterias), in addition to several
Arctic/sub-Arctic, cold-water genera, such as Pycnopodia,
Rathbunaster, Lysastrostroma, and Icasterias. Multiple arms (i.e. more than five) and abundant pedicellariae
are also commonly present in species with a fleshy
or decalcified body wall (e.g. Pycnopodia helianthoides
Brandt, 1835, Rathbunaster californicus Fisher, 1906,
and Lysasterias heteractis Fisher, 1940).
BIOGEOGRAPHY AND
THE
ANTARCTIC
Occurrence of the two taxa in cold-water settings (i.e.
deep sea and Antarctic) suggests a distribution similar
to several other asteroids, which includes closely related
deep-sea and high-latitude members at different taxonomic levels. For example, Odontaster (Odontasteridae)
includes several deep-sea species present in the Pacific
and Atlantic, in addition to multiple species in the
Antarctic region (Janosik & Halanych, 2013; Clark &
Downey, 1992). Two astropectinids, Bathybaster and
Psilaster, also include species in the Antarctic that
occur elsewhere in deep-sea settings (Clark & Downey,
1992). Other examples of closely related Antarctic/
deep-sea taxa include Rhopiella/Henricia and
Paralophaster/Lophaster (Clark, 1962). Taxon sampling in our data set did not provide any definitive
biogeographic inference.
Nearly all other forcipulataceans present in Antarctic settings display some kind of brooding behaviour,
as well as lecithotrophic larvae (Pearse & Bosch, 1994).
Brooding in multi-armed forcipulataceans varies,
as the brisingid Odinella possesses specialized brood
chambers versus asteriids, such as Psalidaster or
Saliasterias, which are not known to brood. The brooding of juveniles was not observed in any of the
Paulasteriidae.
Large yolky eggs, interpreted as lecithotrophic, are
observed in several widely occurring deep-sea asteroids, including brisingids and zoroasterids (Tyler et al.,
1984). Although yolky eggs were not confirmed in the
Paulasteriidae, its widespread occurrence would be consistent with previous hypotheses of dispersal for widely
occurring deep-sea asteroids with lecithotrophic eggs
(summary of these ideas by Pearse 1994).
111
ACKNOWLEDGEMENTS
C. Mah is extremely grateful to Dr Craig McClain and
Dr Dave Clague for their invitation to participate in
the 2009 MBARI Pacific Northwest Expedition. C. Mah
also thanks Lonny Lundsten, Linda Kuntz, the crew
of the RV Western Flyer and other personnel at MBARI
for their assistance. We extend thanks to the crew of
RRS James Cook and the staff of the UK National
Marine Facilities at NOC, especially the ROV Isis team,
for logistic, technical, and shipboard support during
JC42, as well the ChEsSo research programme, which
was funded by UK NERC Consortium Grant (NE/
DO1249X/1) under the lead of Professor Paul Tyler.
We gratefully acknowledge Will Reid, who provided us
with isotope data in advance of his paper (Reid et al.,
2013). Special appreciation is extended to Bob Ford
and Taylor Steed, Frederick Community College, and
Scott Whitaker, NMNH SEM Lab, for their help with
SEM logistics. For specimen cataloguing and logistics we thank Linda Ward and Paul Greenhall at the
NMNH, and Miranda Lowe and Andrew Cabrinovic
at the NHM. The original forcipulates sequence data
set was collected with support by NSF-Polar Programs Postdoctoral Fellowship OPP-0631245 to C. Mah,
and by an LSU Faculty Research Grant to D. Foltz.
The new molecular work was funded in part by NSF
award DEB-1036358 to D. Foltz and C. Mah. The manuscript benefitted from improvements provided by two
anonymous reviewers.
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