BULLETIN OF MARINE SCIENCE, 48(2): 500-516,1991
SEXUAL REPRODUCTIVE MODES IN POLYCHAETES:
CLASSIFICATION AND DIVERSITY
W Herbert Wilson
ABSTRACT
A two-factor classification system for types of reproductive modes within the Polychaeta
is described. The classification is based on the type ofIarval development and the fate of the
female gametes (free-spawned or brooded in a variety of ways). A compilation ofinformation
from the literature allowed the classification of 306 species. The Orders Phyllodocida and
Spionida show the greatest diversity of reproductive modes. The most common reproductive
mode involves the free spawning of gametes and the development of planktotrophic larvae.
It is apparent that there has been multiple evolution of many reproductive modes during the
course of polychaete evolution. This plasticity is argued to exceed that of the Classes Gastropoda, Bivalvia and Malacostraca.
Polychaetes display an extraordinary diversity of reproductive traits (Schroeder
and Hermans, 1975). It is not uncommon for congeneric species to possess radically different means of reproduction. For example, the maldanid Axiothella
mucosa produces gelatinous egg masses attached to the female tube (Bookhout
and Hom, 1949). Sibling species of A. rubrocincta brood their young inside their
tube and free spawn demersal eggs, respectively (Wilson, 1983). The plasticity of
polychaete life histories has undoubtedly contributed to their success in the marine
environment (Knox, 1977).
Although a considerable literature exists on the reproductive traits of polychaetes (see references in Table 2), there has been no effort to survey the distribution of reproductive modes across orders and families. Fauchald (1983) divided
polyaetes generally into three general reproductive life styles, although intermediate species that are difficult to classify are common. My approach involves a
finer classification of reproductive modes. Each class incorporates two aspects of
reproduction. The first concerns the fate of the ova, particularly whether they are
spawned freely into the seawater or afforded some type of brood protection or
encapsulation. The second aspect concerns the type oflarval development: planktotrophic (having planktonic feeding larvae), lecithotrophic (having planktonic,
non-feeding larvae) or direct (having no free-swimming larval phase) (Thorson,
1950). The distribution of these modes across the orders and families of the
Polychaeta are examined, using data from 306 species.
MATERIALS AND METHODS
I surveyed the literature for descriptions of the reproductive biology ofpolychaetes. To be classified
in my scheme, information had to be provided on the fate ofthe ova (whether they are free-spawned
or brooded) and the type of larval development (planktotrophic, lecithotrophic or direct). The classification system that I have developed (Table 1) represents all combinations of six ova fate classes
and the three larval development classes. The ova fate classes were developed based on my own
knowledge of polychaete reproductive biology and are strictly applicable only to polychaetes. Each
class is presumed to require specific morphological and physiological adaptations peculiar to that
class, e.g., the ability to produce gelatinous egg capsules or the evolution of structures on the body for
brooding. The larval developmental classes (Thorson, 1946; 1950) were selected a priori. These larval
developmental classes can be applied to all marine invertebrates. The abbreviations given in Table I
are used extensively in the text. The ova fate classes are: 1) free spawning, 2) brooding on the body,
3) brooding within the body (viviparity), 4) brooding in capsules within the tube, 5) brooding along
the linings of the tube and 6) encapsulation in a gelatinous mass. The classification incorporates the
notion of "mixed" development (Pechenik, 1979) in which embryos are sequestered for some portion
500
WILSON: POLYCHAETE
REPRODUCTIVE
MODES
SOl
Table I. List of the reproductive modes of polychaetes, based on the criteria of the fate of the ova
and the type of larval development (Abbreviations for each mode are used throughout the text)
Abbreviation
FS-PLK
FS-LEC
FS-DIR
BR-EXT-PLK
BR-EXT-LEC
BR-EXT-DIR
BR-INT-PLK
BR-INT-LEC
BR-INT-DIR
BR-TUBE-PLK
BR-TUBE-LEC
BR-TUBE-DIR
BR-CAP-PLK
BR-CAP-LEC
BR-CAP-DIR
GEL-PLK
GEL-LEC
GEL-DIR
Description
Free spawning with planktotrophic larvae
Free spawning with lecithotrophic larvae
Free spawning with entirely benthic development
Brooding on the outside of the body with release of planktotrophic larvae
Brooding on the outside of the body with release of lecithotrophic larvae
Brooding on the outside of the body with direct development
Brooding inside the body with release of planktotrophic larvae
Brooding inside the body with release of lecithotrophic larvae
Brooding inside the body with direct development
Brooding inside the tube with release of planktotrophic larvae
Brooding inside the tube with release of lecithotrophic larvae
Brooding inside the tube with direct development
Brooding of encapsulated embryos inside the tube with release of planktotrophic larvae
Brooding of encapsulated embryos inside the tube with release of lecithotrophic larvae
Brooding of encapsulated embryos inside the tube with direct development
Encapsulation of embryos in a gelatinous mass with release of planktotrophic
larvae
Encapsulation of embryos in a gelatinous mass with release of lecithotrophic
larvae
Encapsulation of embryos in a gelatinous mass with direct development
of early development in an encapsulating structure or other brood structure after which, in different
species, the embryos may be released as planktotrophic larvae, as lecithotrophic larvae, or as benthic
juveniles. I do not distinguish between the production of nurse eggs (exogenous yolk) and the production
of endogenous yolk. There are numerous pathways for each (Eckel barger, 1988) and there is insufficient
information to classify most species.
The classification presented herein addresses only sexual reproduction and hence excludes the various
types of asexual reproduction observed in polychaetes (Schroeder and Hermans, 1975). The larvae of
some arabellid polychaetes are parasitic in other polychaetes (Richards, 1967); these are not considered
in this paper.
In reviewing the literature, I was able to find descriptions of the reproduction of 306 polychaetes
which were sufficiently detailed to allow unambiguous classification of reproductive mode in my
system. Many descriptions of other species had to be eliminated from the compendium because the
investigators were unable to discriminate between planktotrophic and lecithotrophic larvae. Other
descriptions did not indicate if early development involves free-spawned gametes or some type of
brood protection. Nevertheless, the 307 species analyzed provide a summary of our knowledge of the
distribution of reproductive modes across the higher taxa of the Polychaeta. The ordinal classification
scheme given in Fauchald (1977) is used to group families; however, I do not consider his arrangement
of orders to reflect polychaete phylogeny. Some families have received far more attention by reproductive biologists than other taxa; hence, better studied families may show a greater diversity of
reproductive modes. Therefore, the 307 species classified do not constitute a random sample. This
bias significantly reduces one's ability to make strong inferences about the relative diversities of
reproductive modes between families and orders.
RESULTS
Table 2 presents the taxonomic compilation of polychaete species whose reproductive mode could be determined. For ease of search, taxa are arranged
alphabetically; I make no assertion about polychaete phylogeny in this paper. The
Amphinomida is listed first solely because this order comes first alphabetically,
not because I consider it primitive. The 306 species classified belong to 36 families.
Twenty-three species are classified into more than one category. Such plasticity
may arise from geographic variation, from unrecognized sibling speciation or
502
BULLETIN OF MARINE SCIENCE, VOL. 48, NO.2, 1991
from poecilogony (Thorson, 1950). The reason for the variability is not important
for purposes here; each mode represents a type found within the family and order
to which the species belongs. Table 3 is a ranking of the frequency of occurrence
of each reproductive mode from the data in Table 2. The FS-PLK mode (see
Table I for a key to the abbreviations) occurs in 79 species, belonging to 22
families and seven orders. BR- TUBE-DIR is found in 39 species, distributed in
II families and eight orders. FS-'LEC occurs in 34 species spread across 16 families
and eight orders. Although BR-CAP-PLK is reported 24 times, all occurrences
are in the family Spionidae. The next most common modes, BR-INT-DIR, GELLEC, BR-EXT-DIR and BR-CAP-DIR are spread across six, two, one and two
order(s), respectively. The remaining modes are represented less than 15 times in
the compilation. The only reproductive mode which is not represented at least
once is BR-INT-PLK.
A comparison of the orders well-represented in the compilation (Table 2) reveals
that 9 reproductive modes are represented among the 21 species of the Order
Capitellida. Within the order, four modes are found in the Arenicolidae (five
species), seven modes are found in the Capitellidae (13 species) and four modes
in the Maldanidae (eight species). Eight modes are found in the Order Eunicida
with five modes in the Dorvilleidae (nine species) and six modes in the Onuphidae
(14 species). Within the Phyllodocida (97 species), II modes are represented within
the Hesionidae-(1l species), the Nereidae (23 species) and the Syllidae (22 species)
showing five, six, and four reproductive modes, respectively. A pattern is evident
within the Syllidae with external brooding common in the Autolytinae, Eusyllinae
and Exogoninae but internal brooding common in the Syllinae. A total of seven
reproductive modes are seen in the Order Sabellida (28 species) with the greatest
diversity in the SabeIlidae (5 modes among 18 species). Within the Sabellidae,
four modes occur in the Sabellinae while three occur in the Fabricinae, predominantly BR- TUBE-DIR. The Order Spionida demonstrates the highest diversity
of reproductive modes with 14, distributed among 86 species. The Cirratulidae
is remarkably variable with eight modes found in 18 species. The Spionidae (63
species) exhibit 10 reproductive modes. Within the Spionidae, four modes, primarily FS-PLK occur in the Scolelepinae; five modes occur in the Laonicinae and
five occur in the Spioninae. With the exception of a single species in the Scolelepinae (Scolelepis yamaguchi), brooding in capsules is restricted to the Spioninae.
Finally, nine reproductive modes are found among the 22 species of the Terebellida with four modes found in the four species of the Ampharetidae and five
modes in the seven species of the TerebeIlidae.
DISCUSSION
The classification and compilation of polychaete reproductive modes confirms
the instincts of polychaete biologists that the diversity of reproductive types is
high within the class. Several of the orders (Eunicida, Phyllodocida, Spionida)
show great variability of reproductive types (Table 2). A number of families are
notably diverse (Spionidae, Cirratulidae, Nereidae, Onuphidae, Dorvilleidae and
Sabellidae) (Table 2).
It seems that polychaetes have few phylogenetic/morphological
constraints on
the evolution of reproductive mode (Stearns, 1983). In other words, the possession
of one type of reproductive mode does not seem to preclude closely related species
from evolving a vastly different suite of reproductive characteristics; reproductive
modes are labile, even at the genus level. The Nephtyidae and Sabellariidae may
be exceptions in demonstrating no variability in reproductive mode (Table 2).
WILSON: POLYCHAETE
REPRODUCTIVE
503
MODES
Table 2. Compilation of polychaete reproductive modes from the primary literature and reviews of
the primary literature (Abbreviations to the different modes are explained in Table I)
Order Amphinomida
Amphinomidae
Hipponoe gaudichaudi
Order Capitellida
Arenicolidae
Arenicola brasiliensis
Arenicola claparedii
Arenicola cristala
Arenicola marina
Abarenicola pacifica
Capitellidae
Capitella capitala sp. I
Capitella
Capitella
Capitella
Capitella
capitala
capilala
capitata
capitata
sp.
sp.
sp.
sp.
la
II
III
IlIa
Capitella capitata complex
Capitella capitata complex
Capitella hermaphrodita
Dasybranchus caducus
Heteromastus filiformis
Mediomaslus ambiseta
Mediomaslus fragilis
Notomastus latericeus
Maldanidae
Axiolhella mucosa
Axiolhella rubrocincla
Axiolhella rubrocincta
Axiothella serrata
Boguea enigmatica
Clymenella torquata
Clymenella torquata
Clymenura clypeata
Order Eunicida
Dorvilleidae
Dorvillea rudolphi
Ophryotrocha bacci
Ophryotrocha diadema
Ophryotrocha hartmanni
Ophryotrocha labronica
Ophryotrocha maculata
Ophryotrocha notoglandulata
Ophryotrocha puerilis
Ophryotrocha vivipara
Eunicidae
Eunice harassii
Eunice schemecephala
Marphysa borradailei
Lumbrineridae
Lumbrineris brevicirra
Lumbrineris impatiens
Lumbrineris latreilfi
Lumbrineris tenuis
Lumbrineris zonata
Onuphidae
Brevibrachium maculatum
Diopatra cuprea
BR-EXT-DIR
Kudenov,
GEL-LEC
FS-LEC
GEL-DIR
BR-TUBE-DIR
BR-TUBE-DIR
Okada, 1941; Bailey-Brock, 1984
Okuda, 1946
Wilson, 1883
Farke and Berghuis, 1979
Healy and Wells, 1959
BR- TUBE-LEC
BR-TUBE-LEC
BR-TUBE-DIR
BR-TUBE-LEC
GEL-LEC
FS-PLK
FS-PLK
GEL-PLK
FS-LEC
Grassle and Grassle, 1976; Reish,
1980
Grassle and Grassle, 1976
Grass1e and Grassle, 1976
Grass1e and Grassle, 1976
Grass1e and Grassle, 1976; Reish,
1980
Rasmussen, 1956; Reish, 1974
Rasmussen, 1956
Boletzky and Dohle, 1967
Bookhout, 1957
Shaffer, 1983
Grassle and Grassle, 1985
Rasmussen, 1956
Wilson, 1933
GEL-DIR
BR-TUBE-DIR
FS-DIR
BR-TUBE-DIR
BR-TUBE-DIR
GEL-DIR
FS-DIR
FS-LEC
Bookhout and Horn, 1949
Wilson, 1983
Wilson, 1983
Read, 1984
Wolf, 1983
Wilson, 1883
Newell, 1951
Cazaux, 1972
FS-LEC
BR-TUBE-PLK
BR-TUBE-DIR
BR-TUBE-PLK
BR-TUBE-PLK
FS-PLK
BR-TUBE-PLK
BR- TUBE-PLK
BR-INT-DIR
Richards, 1967; Blake, 1975a
Akesson, 1973a
Akkeson, 1976
Akesson, 1973a
Akesson, 1973a
Akesson, 1973b
Akesson, 1973a
Akesson, 1973a
Banse, 1963
FS-PLK
FS-PLK
GEL-LEC
Herpin, 1925
Richards, 1967
PilIai,1958
BR- TUBE-DIR
GEL-PLK
BR- TUBE-DIR
GEL-LEC
BR-TUBE-DIR
Bhaud and Cazaux, 1987
Cazaux, 1972
Richards, 1967
Richards, 1967
Richards, 1967
BR- TUBE-DIR
GEL-DIR
Smith and Jensz, 1968
Allen, 1959
BR-TUBE-PLK
BR-TUBE-LEC
BR-TUBE-PLK
BR-TUBE-DIR
1977
504
BULLETIN OF MARINE SCIENCE, VOL. 48, NO.2, 1991
Table 2, Continued
Diopatra neapolitana
Diopatra variabi/is
Diopatra sp,
Hyalinoecia araucana
Kinbergonuphis simoni
Mooreonuphis jonesi
Nothria elegans
Nothria nolialis
Onuphis magna
Onuphis stigmatis
Paraonuphis antarctica
Paraonuphis bermudensis
Order F1abelligerida
F1abelligeridae
Flabelligera mundata
Order Opheliida
Opheliidae
Armandia brevis
Euzonus mucronatus
Ophelia bicornis
Ophelia bicornis
Order Orbiniida
Orbiniidae
Phylo Joetida
Phylo Joetida atlantica
Leitoscoloplos kerguelensis
Leitoscoloplos pugeftensis
Leitoscoloplos robustus
Naineris laevigata
Scoloplos acmeceps
Scoloplos armiger
GEL-LEC
GEL-DIR
BR-TUBE-DIR
BR-TUBE-DIR
BR- TUBE-LEC
BR- TUBE-LEC
FS-LEC
BR-TUBE-DIR
GEL-LEC
BR-TUBE-DIR
BR-TUBE-DIR
BR-INT-DIR
Choe,1960
Krishnan, 1936
Monro, 1924
Carrasco, 1983
Hsieh and Simon, 1987
Fauchald, 1982
Blake, 1975b
Hartman, 1967a; 1967b
Andrews, 1891'; Hartman,
Wilson, unpublished
Hartman, 1967a; 1976b
Hartman, 1965
BR-EXT-DIR
Gravier, 1923
FS-PLK
Hermans, 1966
FS-PLK
FS-LEC
FS-PLK
Dales, 1952
Wilson, 1948
Riser, 1987
GEL-DIR
FS-LEC
FS-LEC
GEL-DIR
FS-LEC
GEL-LEC
FS-LEC
GEL-DIR
Seoloplos simplex
Order Phyllodocida
Aphroditidae
Aphrodita aculeata
Chrysopetalidae
Chrysopetalum debile
Paleanotus bellis
Glyceridae
Glycera convoluta
Goniadidae
Glycinde armigera
Goniada emerita
Hesionidae
Gyptis ?brunnea
Gyptis rosea
Hesionides arenaria
Hesionides gohari
Microphthalmus aberrans
Microphthalmus sczelkowii
Nereimyra punctata
Ophiodromus j/exuosus
Ophiodromus obscura
Ophiodromus pugeftensis
Syllidia armata
Nephtyidae
Nephtys caeca
Nephtys ciliata
Nephtys coeca
GEL-LEC
Salensky, 1883
Cazaux,1972
Okuda, 1946
Blake, 1980
Hom and Bookhout,1950
Okuda, 1946
Blake, 1980
Anderson, 1959; Chapman,
Gibbs, 1968
Anderson, 1961
FS-DIR
Thorson, 1946
FS-PLK
FS-PLK
Cazaux, 1968
Blake, 1975a
FS-PLK
Cazaux,1967
FS-LEC
FS-PLK
Blake, 1975a
Cazaux, 1972
FS-LEC
FS-PLK
FS-DIR
FS-DIR
GEL-PLK
GEL-DIR
FS-PLK
FS-PLK
FS-PLK
FS-LEC
FS-PLK
Blake, 1975a
Haaland and Schram, 1983a
Westheide, 1967; 1970
Westheide, 1967; 1970
Westheide, 1967; 1970
We~heide, 1967; 1970
Schram and Haaland, 1984
Haaland and Schram, 1983b
Treadwall, 1898; 1901
Blake, 1975a
Rasmussen, 1956
FS-PLK
FS-PLK
FS-PLK
Bentley et ai" 1984
Thorson, 1946
Thorson, 1946
1945
1965;
WILSON: POLYCHAETE
REPRODUCfIVE
505
MODES
Table 2. Continued
Nephtys hombergi
Nereididae
Ceratonereis aequisetis
Ceratonereis costae
Ceratonereis erythraeensis
Ceratonereis limnetica
Laeonereis culveri
Leptonereis glauca
Micronereis nanaimoensis
Micronereis variegata
Nereis arenaceodentata
Nereis diversicolor
Nereis Jalcaria
Nereis grubei
Nereis irrorata
Nereis limnicola
Nereis pelagica
Nereis pelagica
Nereis vexillosa
Nicon aestuariensis
Perinereis cultrifera
Platynereis canaliculata
Platynereis dumeri/ii
FS-PLK
Thorson, 1946; Bentley et a!.,
1984
BR-TUBE-DIR
BR-TUBE-DIR
FS-PLK
BR-TUBE-DIR
FS-DIR
BR- TUBE-DIR
GEL-LEC
GEL-LEC
BR- TUBE-DIR
FS-LEC
GEL-LEC
FS-PLK
FS-PLK
BR-INT-DIR
FS-LEC
FS-DIR
GEL-LEC
FS-LEC
FS-PLK
FS-LEC
FS-LEC
Dorsey, 1981
Durchon, 1956
Hutchings and Turvey, 1982
Glasby, 1986
Mazurkiewicz, 1975
Thorson, 1946
Reish, 1957
Reish,1957
Reish, 1957; Pesch et aI., 1987
Dales, 1950
Read, 1974
Reish,1954
Cazaux, 1968
Smith, 1950
Wilson, 1932
Herpin, 1925
Johnson, 1943
Estcourt, 1966
Cazaux, 1968
Blake,1975a
Hauenschild and Fischer, 1969;
Cazaux, 1969
Thorson, 1946
Pfannenstiel et aI., 1987
Pfannenstiel et aI., 1987
Platynereis dumeri/ii
Platynereis dumeri/ii
Platynereis massiliensis
Phyllodocidae
Eteone barbata
Eteone dilatae
Eteone longa
Eulalia sanguinea
FS-DIR
FS-PLK
BR- TUBE-DIR
Eulalia viridis
Phyllodoce (Anaitides) groenlandica
Phyllodoce laminosa
Phyllodoce (Anaitides) maculata
Phyllodoce (Anaitides) mucosa
Phyllodoce maculata
Phyllodoce (Anaitides) williamsi
Polynoidae
Acholoe astericola
Halosydna brevisetosa
Halosydna gelatinosa
H alosydna johnsoni
Harmothoe imbricata
Harmothoe imbricata
Harmothoe longisetis
Harmothoe lunu/ata
Lagisca extenuata
Lepidonotus clava
Lepidonotus squamatus
Sigalionidae
Pholoe assimi/is
Pholoe balthica
Pholoe inornata
Pholoe min uta
GEL-PLK
GEL-PLK
Ph%e swedmarki
Ph%e synophtha/mica
GEL-PLK
GEL-PLK
GEL-PLK
GEL-PLK
Thorson, 1946
Blake, 1975a
Rasmussen, 1956
Thorson, 1946; Bhaud and
Cazaux, 1987
Thorson, 1946
Thorson, 1946
Bhaud and Cazaux, 1987
Thorson, 1946; Cazaux, 1969
Thorson, 1946, Cazaux, 1969
Thorson, 1946
Blake,1975a
FS-PLK
FS-PLK
FS-PLK
FS-PLK
BR-EXT-PLK
FS-PLK
FS-PLK
FS-PLK
FS-PLK
FS-PLK
FS-PLK
Bhaud and Cazaux,
Blake,1975a
Bhaud and Cazaux,
Reish, 1980
Blake, 1975a
Cazaux, 1968
Bhaud and Cazaux,
Bhaud and Cazaux,
Bhaud and Cazaux,
Bhaud and Cazaux,
Bhaud and Cazaux,
FS-PLK
FS-PLK
FS-PLK
FS-PLK
Christie, 1982
Petersen, M. E., in prep.
Rasmussen, 1956
Blake, 197Sa; Heffernan and Keegan, 1988
Laubier, 1975
Cazaux, 1968
FS-LEC
FS-PLK
FS-PLK
FS-PLK
FS-PLK
BR-INT-DIR
FS-PLK
1987
1987
1987
1987
1987
1987
1987
506
BULLETIN OF MARINE SCIENCE, VOL. 48, NO.2,
1991
Table 2. Continued
Sthenelais baa
Genus A
Syllidae
Auto1ytinae
Autalytus edwardsi
Autalytus fasciatus
Autolytus prollfer
Autolytus prolifer x brachycephalus
Eusyllinae
Parapionosyllis gestans
Exogoninae
Brania limbata
Exogone gemmifera
Exogone hebes
Exogone longicornis
Exagone lourei
Exogone naidina
Exogone occidentalis
Sphaerosyllis bulbosa
Sphaerosyllis erinaceus
Sphaerosyllis hystrix
Syllinae
Dentatisyllis brevicirra
Syllis incisa
Syllis nepiotica
Syllis parturiens
Syllis variegata
Syllis vivipara
Order Sabellida
Sabellidae
Fabricinae
Chane echaudata
Dasychone bombyx
Fabricia limnicola
Fabricia sabella
Fabriciola chilensis
Manayunkia aestuarina
Manayunkia baicalensis
Manayunkia caspica
Oriopsis alata
Oriopsis ehlersi
Myxicolinae
Myxicola infundibulum
Sabellinae
Amphiglena mediterranea
Eudistylia vancouveri
Megalomma vesiculosum
Pomataceros triqueter
Potamilla myriops
Potamilla neglecta
Sabella media
Schizobranchia ins ignis
Serpulidae
Ficopomatus enigmaticus
Microserpula infiata
Serpula vermicularis
Spirorbidae
Janua (Dexiospira) brasiliensis
Spirorbis ambilateralis
Spirorbis borealis
Spirorbis granulatus
FS-PLK
BR-INT-DIR
Bhaud and Cazaux, 1987
Wo1f,1984
BR-EXT-DIR
BR-EXT-PLK
BR-EXT-LEC
FS-EXT-PLK
Allen, 1964
Allen, 1964
Dales, 1951 b
Schiedges, 1979
BR-EXT-DIR
Cazaux, 1969
BR-EXT-DIR
BR-EXT-DIR
BR-INT-DIR
BR-EXT-DIR
BR-EXT-DIR
BR-EXT-DIR
Cazaux, 1972
Thorson, 1946
Pocklington and Hutcheson,
Westheide, 1974
Levin, 1984a
Oersted, 1845
BR-EXT-DIR
Westheide, 1974
BR-EXT-DIR
BR-EXT-DIR
BR-EXT-DIR
Cazaux, 1972
Cazaux, 1972
Cazaux, 1972
BR-INT-DIR
BR-INT-DIR
BR-INT-DIR
BR-INT-DIR
BR-EXT-PLK
BR-INT-DIR
Russell, pers. comm.
Augener, 1929
Caullery and Mesni1, 1916
Ben-E1iahu, 1975
Cazaux, 1969
Goodrich, 1900
GEL-LEC
GEL-DIR
BR-TUBE-DIR
BR-TUBE-DIR
BR-TUBE-DIR
BR-TUBE-DIR
BR-TUBE-DIR
BR- TUBE-DIR
BR-TUBE-DIR
BR- TUBE-DIR
Okuda, 1946
Thorson, 1946
Levin, 1984a
Thorson, 1946
McEuen et a1., 1983
Forsman, 1956
B1iakher, 1959
Marinescu, 1964
McEuen et a1., 1983
McEuen et a1., 1983
FS-LEC
Dean et al., 1987
BR-TUBE-DIR
FS-LEC
FS-LEC
FS-PLK
FS-LEC
BR- TUBE-DIR
GEL-LEC
FS-LEC
McEuen et a1.,
McEuen et al.,
Wilson, 1936a
Thorson, 1946
Okuda, 1946
McEuen et al.,
McEuen, et al.,
Lee, 1975
FS-PLK
BR-TUBE-LEC
FS-PLK
Dixon, 1981
Dons, 1933
Thorson, 1946
BR-EXT-LEC
BR-EXT-LEC
BR-TUBE-LEC
BR-EXT-LEC
Reish, 1980
Potswald, 1965
Thorson, 1946
Thorson, 1946
1983
1983
1983
1983
1983
WILSON: POLYCHAETE
REPRODUCTIVE
507
MODES
Table 2. Continued
Spirorbis marchi
Spirorbis racemosus
Spirorbis spirillum
Spirorbis vitreus
Order Spionida
Chaetopteridae
Chaetopterus norveticus
Chaetopterus pergamentaceus
Spiochaetopterus ocu/atus
Cirratulidae
Cau//erie//a Jragi/is
Cau//erie//a n. sp.
Chaetozone setosa complex
Cirratu/us cirratus
Cirratu/us cirratus
Cirratu/us cirratus
Cirratu/us sp.
Cirriformia /uxuriosa
Cirriformia spirabrancha
Cirriformia tentacu/ata
Dodecaceria ater
Dodecaceria caul/eryi
Dodecaceria concharum
Dodecaceria concharum
Tharyx marioni
Tharyx marioni
Tharyx vivipara
Tharyx n. sp.
Ctenodrilidae
Raphidrilus nemasoma
Poecilochaetidae
Poeci/ochaetus serpens
Spionidae
Laonicinae
Laonice cirrata
Streblospio benedicti
Streb/ospio benedicti
Streb/ospio benedicti
Streb/ospio shrubsoli
Scolelepinae
Aonides oxycepha/a
Aonides paucibranchiata
Ma/acoceros ciliata
M a/acoceros Juligi nosa
Ma/acoceros girardi
Prionospio cirrifera
Prionospio ma/mgreni
Prionospio steenstrupi
Rhynchospio areninco/a
Sco/e/epis Joliosa
Sco/e/epis squamata
Sco/e/epis tridentata
Sco/e/epis yamaguchi
Sco/e/epis sp. I
Sco/e/epis sp. II
Spioninae
Boccardia acus
Boccardia acus
Boccardia androgyna
Boccardia chilensis
Boccardia hamata
BR-EXT-LEC
BR-EXT-LEC
BR- TUBE-LEC
BR- TUBE-LEC
Potswald,
Potswald,
Potswald,
Potswald,
FS-PLK
FS-PLK
FS-PLK
Thorson, 1946
Wilson, 1883
Wilson, 1883
BR- TUBE-DIR
BR-INT-DIR
FS-LEC
GEL-DIR
GEL-LEC
BR-EXT-DIR
BR-INT-DIR
FS-LEC
FS-LEC
FS-LEC
BR-INT-LEC
FS-PLK
FS-PLK
GEL-LEC
FS-DIR
FS-LEC
BR-INT-DIR
BR-TUBE-DIR
Petersen, M. E., in prep.
Petersen, M. E., in prep.
Christie, 1985
Okuda, 1946
Cunningham and Ramage, 1888
Fauvel, 1916
Claparede and Mecznikow, 1868
Reish, 1980
Blake, 1975c; Reish, 1980
Wilson, 1936b
Caullery and Mesnil, 1898
Gibson and Clark, 1976
Caullery and Mesnil, 1898
Gibson, 1977
Cazaux, 1972; Dales, 1951a
Gibbs, 1971
Christie, 1984
Petersen, M. E., in prep.
BR-INT-DIR
Monticelli, 1910
FS-PLK
Hannerz, 1956
FS-PLK
BR-EXT-PLK
BR-EXT-LEC
BR-EXT-DIR
BR- TUBE-DIR
Hannerz, 1956
Dean, 1965
FS-LEC
FS-LEC
FS-PLK
FS-PLK
FS-PLK
FS-PLK
FS-PLK
FS-PLK
BR-EXT-PLK
FS-PLK
FS-PLK
FS-PLK
BR-CAP-PLK
FS-PLK
FS-PLK
Hannerz, 1956
Hannerz, 1956
Hannerz, 1956
Day, 1934
Hannerz,1956
Hannerz, 1956
Hannerz, 1956
Hannerz, 1956
Levin, 1984a
Hannerz, 1956
Hannerz, 1956
Hannerz, 1956
Imajima,1959
Hannerz, 1956
Hannerz, 1956
BR-CAP-DIR
BR-CAP-PLK
BR-CAP-PLK
BR-CAP-PLK
BR-CAP-PLK
Read,
Read,
Read,
Blake
Dean
1965
1965
1965
1965
Levin, 1984b
Levin, 1984b
Cazaux, 1985
1975
1975
1975
and Kudenov, 1981
and Blake, 1966
508
BULLETIN OF MARINE SCIENCE, VOL 48, NO.2,
1991
Table 2. Continued
Boccardia
Boccardia
Boccardia
Boccardia
Boccardia
Boccardia
Boccardia
Boccardia
knoxi
magniovata
natrix
otakouica
polybranchia
polybranchia
proboscidea
proboscidea
Boccardia syrtis
Boccardia wellingtonensis
Microspio atlantica
Polydora aggregata
Polydora commensalis
Polydora concharum
Polydora giardi
Polydora hermaphroditica
Polydora hoplura
Polydora hoplura
Polydora ligni
Polydora ligni
Polydora nuchalis
Polydora quadricirrata
Polydora quadrilobata
Polydora quadrilobata
Polydora socialis
Polydora websteri
Pseudopolydora kempi
Pseudopolydora kempi
Pseudopolydora paucibranchiata
Pygospio elegans
Pygospio elegans
Pygospio elegans
Spio filicornis
Spio martinensis
Spio setosa
Spio setosa
Spiophanes bombyx
Spiophanes kroyeri
Order Terebellida
Ampharetidae
Alkmaria romijni
Ampharete grubei
H obsonia florida
Melinna cristata
Pectinariidae
Pectinaria auricoma
Pectinaria koreni
Sabellariidae
Lygdamus indicus
Lygdamus muratus
Phragmatopoma lapidosa
Phragmatopoma calijornica
Sabel/aria alveolata
Sabel/aria floridensis
Sabel/aria spinulosa
Sabel/aria vulgaris
Terebellidae
Artacama proboscidea
Eupolymnia heterobranchia
BR-CAP-DIR
BR-CAP-DIR
BR-INT-DIR
BR-CAP-PLK
BR-CAP-LEC
BR-CAP-DIR
BR-CAP-PLK
BR-CAP-DIR
BR-CAP-PLK
BR-CAP-DIR
BR-CAP-LEC
BR-CAP-PLK
BR-CAP-PLK
BR-CAP-DIR
BR-CAP-PLK
FS-PLK
FS-PLK
Read, 1975
Read,1975
Soderstrom, 1920
Read,1975
Read, 1975
Duchene, 1984
Woodwick, 1977
Reish, 1980; Blake and Kudenov,
1981
Read, 1975
Read, 1975
Hannerz,1956
Blake, 1969
Blake, 1969
Blake 1969
Day and Blake, 1979
Hannerz, 1956
Wilson, 1928
Read, 1975
Blake, 1969; Rice, 1980
Zajac, 1985
Woodwick, 1960
Read, 1975
Blake, 1969
Blake, 1969
Carrasco, 1976
Blake, 1969
Blake and Woodwick, 1975
Myohara, 1979
Blake and Woodwick, 1975;
Myohara, 1980
Hannerz, 1956
Hannerz, 1956
Hannerz, 1956
Hannerz, 1956
Hannerz, 1956
Simon, 1967
Simon, 1968
Hannerz, 1956
Hannerz, 1956
BR-INT-DIR
FS-DIR
BR- TUBE-DIR
FS-LEC
Wesenberg-Lund,
Thorson, 1946
Zottoli, 1974
Nyholm, 1950
FS-PLK
FS-PLK
Thorson, 1946
Watson, 1928; Wilson, 1936c
FS-PLK
FS-PLK
FS-PLK
FS-PLK
FS-PLK
FS-PLK
FS-PLK
FS-PLK
Bhaud, 1975
Wilson, 1929
Eckelbarger, 1976
Eckelbarger, 1977
Wilson, 1929
Eckelbarger, 1977
Wilson, 1929
Eckelbarger, 1975
FS-LEC
BR-TUBE-DIR
Thorson, 1946
Wilson, unpublished obs.
BR-CAP-PLK
BR-CAP-DIR
BR-CAP-PLK
BR-CAP-PLK
BR-CAP-PLK
BR-CAP-PLK
BR-CAP-PLK
BR-CAP-LEC
BR-CAP-DIR
BR-CAP-DIR
BR-CAP-PLK
BR-CAP-DIR
BR-CAP-DIR
BR-CAP-PLK
BR-CAP-PLK
BR-CAP-DIR
BR-CAP-PLK
BR-CAP-PLK
BR-CAP-DIR
BR-CAP-PLK
BR-CAP-PLK
1934
WILSON: POLYCHAETE
REPRODUCTIVE
509
MODES
Table 2. Continued
Eupolymnia nebulosa
Eupolymnia nebulosa
Nicolea zoslericola
Ramex californiensis
Thelepus crisp us
Trichobranchidae
Terebe//ides stroemi
FS-LEC
BR-TUBE-LEC
GEL-DIR
BR-CAP-DIR
BR-TUBE-DIR
Gremare, 1986
Gremare, 1986
Eckelbarger, 1974
Blake, 1989
Wilson, unpublished obs.
GEL-DIR
Thorson, 1946
Jagersten (1972) argues that the primitive means of reproduction in the protostomes occurs by spawning gametes freely into the seawater with subsequent
development of planktotrophic larvae. This pattern corresponds to the FS-PLK
class in my system. It is therefore not surprising that FS-PLK is represented in
more families and orders than any other mode (Tables 2, 3). From this plesiomorphic condition, the repeated radiation of other reproductive modes has occurred.
From Table 3, it is parsimonious to claim, for instance, that BR-TUBE-DIR, a
major shift from the primitive FS-PLK, must have evolved at least eight times
because it appears in eight different orders, each of which retains the plesiomorphic
FS-PLK in some species. Similarly, GEL-DIR and GEL-LEe both occur in six
orders. The appearance of each mode, other than the presumed plesiomorphic
FS-PLK, in an order is likely to have been an independent evolutionary event.
A comparison of the reproductive variability ofthe Polychaeta with other major
benthic taxa is intriguing. The classification scheme adopted here is specifically
designed to accommodate polychaete reproductive modes and hence is not completely comparable for other taxa. For instance, gastropods, because they do not
build tubes, cannot brood their young within a tube. However, there is sufficient
information to determine the taxonomic level at which most reproductive plasticity occurs in other major protostome groups. Within the prosobranch gastropods, the archaeogastropods uniformly spawn eggs freely into the seawater, ultimately producing either planktotrophic or lecithotrophic larvae (Fretter, 1984).
Table 3. The distribution of reproductive modes within the Polychaeta (Number of species, orders
and families in which each mode occurs are given; data are compiled from Table 2)
Reproductive mode
FS-PLK
BR-TUBE-DIR
FS-LEC
BR-CAP-PLK
BR-INT-DIR
GEL-LEC
BR-EXT-DIR
BR-CAP-DIR
GEL-DIR
BR-TUBE-LEC
GEL-PLK
FS-DIR
BR-TUBE-PLK
BR-EXT-LEC
BR-EXT-PLK
BR-CAP-LEC
BR-INT-LEC
BR-INT-PLK
Species
79
39
34
24
17
16
15
15
13
II
10
10
7
7
6
3
I
0
Orders
7
8
8
I
2
6
I
2
6
4
3
4
2
3
2
I
2
0
Families
22
II
16
I
4
9
I
2
7
5
4
6
2
3
3
I
2
0
510
BULLETIN OF MARINE SCIENCE, VOL. 48. NO.2.
1991
Among the mesogastropod and neogastropod prosobranch snails, virtually all
species encapsulate their young in leathery capsules (Fretter, 1984). The young
hatch as planktotrophic larvae, lecithotrophic larvae or benthic juveniles. A few
species brood their young inside the reproductive tract but within leathery capsules, releasing either planktotrophic larvae or benthic juveniles (Fretter, 1984).
The pattern then appears to be a switch at the ordinal level from free-spawning
to dependence upon the production of capsules for sequestering the embryos, a
switch requiring but one evolutionary event, the acquisition of the ability to secrete
leathery capsules. The Opisthobranchia encapsulate their young in gelatinous
ribbons from which planktotrophic larvae, lecithotrophic larvae or juveniles may
emerge (Thompson, 1976). Again, the diversity of reproductive modes below the
level of order is low. Species of the Bivalvia either spawn gametes freely which
develop as planktotrophic or lecithotrophic larvae (rarely demersal development)
or brood embryos within the female mantle cavity (morphologically, an external
brood chamber) for all of embryonic development (Mackie, 1984). Brooding has
arisen several times, always associated with small size; however, brooding tends
to characterize families rather than higher taxa (Strathmann and Strathmann,
1982). Larger bivalves are invariably free-spawners (Mackie, 1984). Finally, virtually all members of the crustacean class Malacostraca, a taxon far more diverse
than the Polychaeta with 18,000 species (Barnes, 1987), display only three basic
reproductive modes: free-spawning eggs followed by planktotrophic development,
brooding eggs externally with the release of planktotrophic larvae, or brooding
eggs externally for all of embryonic development (Schram, 1986). There is virtually
no variability below the level offamily. For instance, the entire superorder Peracarida brood their young externally with no larval stage (Barnes, 1987). Within
the decapods, only the penaeid shrimps spawn their eggs freely; all remaining taxa
in this order brood their young on the abdomen, releasing planktotrophic larvae
(Schram, 1986). These examples show that other major taxa of prot ostomes seem
to have less potential for changing basic attributes of their reproductive biology.
The remarkable plasticity of the polychaetes derives in part from the relative
simplicity of the reproductive system, which seems to place few restrictions on
further evolutionary change (Dales, 1967). There is a striking contrast with the
complicated reproductive system of gastropods (Thompson, 1976; Fretter, 1984)
which certainly places great morphological constraints on evolutionary change.
The plasticity of reproductive mode in the polychaetes likely played a major role
in their success in benthic habitats of the oceans.
ACKNOWLEDGMENTS
I would like to thank several polychaetologists who provided encouragement as well as references
and information on the life histories of various polychaetes, particularly J. Blake, B. Brown, K.
Fauchald, P. Hutchings, L. Levin, D. Reish, D. Russell, H. ten Hove and especially, M. Petersen. I
am grateful to B. Brown, K. Fauchald, D. McHugh and S. Woodin for discussion or comments on
the manuscript. The anonymous reviewers made many useful comments on the manuscript for which
I am thankful. I continue to add to this compendium; I would appreciate information on species which
could be added.
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DATEACCEPTED: November 6, 1990.
ADDRESS: Department of Zoology, NJ-15, University of Washington, Seattle, Washington 98195;
PRESENTADDRESS:Department of Biology, Colby College, Waterville, Maine 04901.