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BULLETIN OF MARINE SCIENCE, 48(2): 500-516,1991

SEXUAL REPRODUCTIVE MODES IN : 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 . The Orders and 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 evolution. This plasticity is argued to exceed that of the Classes Gas- tropoda, Bivalvia and Malacostraca.

Polychaetes display an extraordinary diversity of reproductive traits (Schroeder and Hermans, 1975). It is not uncommon for congeneric species to possess rad- ically 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 poly- chaetes (see references in Table 2), there has been no effort to survey the distri- bution of reproductive modes across orders and families. Fauchald (1983) divided polyaetes generally into three general reproductive life styles, although interme- diate 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: plank- totrophic (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 clas- sification 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 . 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 Description FS-PLK Free spawning with planktotrophic larvae FS-LEC Free spawning with lecithotrophic larvae FS-DIR Free spawning with entirely benthic development BR-EXT-PLK Brooding on the outside of the body with release of planktotrophic larvae BR-EXT-LEC Brooding on the outside of the body with release of lecithotrophic larvae BR-EXT-DIR Brooding on the outside of the body with direct development BR-INT-PLK Brooding inside the body with release of planktotrophic larvae BR-INT-LEC Brooding inside the body with release of lecithotrophic larvae BR-INT-DIR Brooding inside the body with direct development BR-TUBE-PLK Brooding inside the tube with release of planktotrophic larvae BR-TUBE-LEC Brooding inside the tube with release of lecithotrophic larvae BR-TUBE-DIR Brooding inside the tube with direct development BR-CAP-PLK Brooding of encapsulated embryos inside the tube with release of plankto- trophic larvae BR-CAP-LEC Brooding of encapsulated embryos inside the tube with release of lecitho- trophic larvae BR-CAP-DIR Brooding of encapsulated embryos inside the tube with direct development GEL-PLK Encapsulation of embryos in a gelatinous mass with release of planktotrophic larvae GEL-LEC Encapsulation of embryos in a gelatinous mass with release of lecithotrophic larvae GEL-DIR 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 repro- ductive 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 re- productive 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 . The next most common modes, BR-INT-DIR, GEL- LEC, 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 . Within the order, four modes are found in the (five species), seven modes are found in the (13 species) and four modes in the (eight species). Eight modes are found in the Order with five modes in the (nine species) and six modes in the (14 species). Within the Phyllodocida (97 species), II modes are represented within the -(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 (28 species) with the greatest diversity in the SabeIlidae (5 modes among 18 species). Within the , four modes occur in the Sabellinae while three occur in the Fabricinae, predom- inantly BR- TUBE-DIR. The Order Spionida demonstrates the highest diversity of reproductive modes with 14, distributed among 86 species. The is remarkably variable with eight modes found in 18 species. The Spionidae (63 species) exhibit 10 reproductive modes. Within the Spionidae, four modes, pri- marily 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 Scole- lepinae (Scolelepis yamaguchi), brooding in capsules is restricted to the Spioninae. Finally, nine reproductive modes are found among the 22 species of the Tere- bellida 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 level. The Nephtyidae and Sabellariidae may be exceptions in demonstrating no variability in reproductive mode (Table 2). WILSON: POLYCHAETE REPRODUCTIVE MODES 503

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 BR-EXT-DIR Kudenov, 1977 Order Capitellida Arenicolidae brasiliensis GEL-LEC Okada, 1941; Bailey-Brock, 1984 Arenicola claparedii FS-LEC Okuda, 1946 Arenicola cristala GEL-DIR Wilson, 1883 Arenicola marina BR-TUBE-DIR Farke and Berghuis, 1979 BR-TUBE-DIR Healy and Wells, 1959 Capitellidae Capitella capitala sp. I BR- TUBE-LEC Grassle and Grassle, 1976; Reish, 1980 Capitella capitala sp. la BR-TUBE-PLK Grassle and Grassle, 1976 Capitella capilala sp. II BR-TUBE-LEC Grass1e and Grassle, 1976 Capitella capitata sp. III BR-TUBE-PLK Grass1e and Grassle, 1976 Capitella capitata sp. IlIa BR-TUBE-DIR Grass1e and Grassle, 1976; Reish, 1980 Capitella capitata complex BR-TUBE-LEC Rasmussen, 1956; Reish, 1974 Capitella capitata complex BR-TUBE-DIR Rasmussen, 1956 Capitella hermaphrodita BR-TUBE-LEC Boletzky and Dohle, 1967 Dasybranchus caducus GEL-LEC Bookhout, 1957 Heteromastus filiformis FS-PLK Shaffer, 1983 Mediomaslus ambiseta FS-PLK Grassle and Grassle, 1985 Mediomaslus fragilis GEL-PLK Rasmussen, 1956 Notomastus latericeus FS-LEC Wilson, 1933 Maldanidae Axiolhella mucosa GEL-DIR Bookhout and Horn, 1949 Axiolhella rubrocincla BR-TUBE-DIR Wilson, 1983 Axiolhella rubrocincta FS-DIR Wilson, 1983 Axiothella serrata BR-TUBE-DIR Read, 1984 Boguea enigmatica BR-TUBE-DIR Wolf, 1983 Clymenella torquata GEL-DIR Wilson, 1883 Clymenella torquata FS-DIR Newell, 1951 Clymenura clypeata FS-LEC Cazaux, 1972 Order Eunicida Dorvilleidae Dorvillea rudolphi FS-LEC Richards, 1967; Blake, 1975a bacci BR-TUBE-PLK Akesson, 1973a Ophryotrocha diadema BR-TUBE-DIR Akkeson, 1976 Ophryotrocha hartmanni BR-TUBE-PLK Akesson, 1973a Ophryotrocha labronica BR-TUBE-PLK Akesson, 1973a Ophryotrocha maculata FS-PLK Akesson, 1973b Ophryotrocha notoglandulata BR-TUBE-PLK Akesson, 1973a Ophryotrocha puerilis BR- TUBE-PLK Akesson, 1973a Ophryotrocha vivipara BR-INT-DIR Banse, 1963 Eunicidae Eunice harassii FS-PLK Herpin, 1925 Eunice schemecephala FS-PLK Richards, 1967 Marphysa borradailei GEL-LEC PilIai,1958 Lumbrineridae Lumbrineris brevicirra BR- TUBE-DIR Bhaud and Cazaux, 1987 Lumbrineris impatiens GEL-PLK Cazaux, 1972 Lumbrineris latreilfi BR- TUBE-DIR Richards, 1967 Lumbrineris tenuis GEL-LEC Richards, 1967 Lumbrineris zonata BR-TUBE-DIR Richards, 1967 Onuphidae Brevibrachium maculatum BR- TUBE-DIR Smith and Jensz, 1968 Diopatra cuprea GEL-DIR Allen, 1959 504 BULLETIN OF MARINE SCIENCE, VOL. 48, NO.2, 1991

Table 2, Continued

Diopatra neapolitana GEL-LEC Choe,1960 Diopatra variabi/is GEL-DIR Krishnan, 1936 Diopatra sp, BR-TUBE-DIR Monro, 1924 Hyalinoecia araucana BR-TUBE-DIR Carrasco, 1983 Kinbergonuphis simoni BR- TUBE-LEC Hsieh and Simon, 1987 Mooreonuphis jonesi BR- TUBE-LEC Fauchald, 1982 Nothria elegans FS-LEC Blake, 1975b Nothria nolialis BR-TUBE-DIR Hartman, 1967a; 1967b Onuphis magna GEL-LEC Andrews, 1891'; Hartman, 1945 Onuphis stigmatis BR-TUBE-DIR Wilson, unpublished Paraonuphis antarctica BR-TUBE-DIR Hartman, 1967a; 1976b Paraonuphis bermudensis BR-INT-DIR Hartman, 1965 Order F1abelligerida F1abelligeridae Flabelligera mundata BR-EXT-DIR Gravier, 1923 Order Opheliida Opheliidae Armandia brevis FS-PLK Hermans, 1966 Euzonus mucronatus FS-PLK Dales, 1952 Ophelia bicornis FS-LEC Wilson, 1948 Ophelia bicornis FS-PLK Riser, 1987 Order Orbiniida Orbiniidae Phylo Joetida GEL-DIR Salensky, 1883 Phylo Joetida atlantica FS-LEC Cazaux,1972 Leitoscoloplos kerguelensis FS-LEC Okuda, 1946 Leitoscoloplos pugeftensis GEL-DIR Blake, 1980 Leitoscoloplos robustus FS-LEC Hom and Bookhout,1950 Naineris laevigata GEL-LEC Okuda, 1946 Scoloplos acmeceps FS-LEC Blake, 1980 Scoloplos armiger GEL-DIR Anderson, 1959; Chapman, 1965; Gibbs, 1968 Seoloplos simplex GEL-LEC Anderson, 1961 Order Phyllodocida aculeata FS-DIR Thorson, 1946 debile FS-PLK Cazaux, 1968 Paleanotus bellis FS-PLK Blake, 1975a Glyceridae Glycera convoluta FS-PLK Cazaux,1967 Goniadidae Glycinde armigera FS-LEC Blake, 1975a Goniada emerita FS-PLK Cazaux, 1972 Hesionidae Gyptis ?brunnea FS-LEC Blake, 1975a Gyptis rosea FS-PLK Haaland and Schram, 1983a Hesionides arenaria FS-DIR Westheide, 1967; 1970 Hesionides gohari FS-DIR Westheide, 1967; 1970 Microphthalmus aberrans GEL-PLK Westheide, 1967; 1970 Microphthalmus sczelkowii GEL-DIR We~heide, 1967; 1970 Nereimyra punctata FS-PLK Schram and Haaland, 1984 Ophiodromus j/exuosus FS-PLK Haaland and Schram, 1983b Ophiodromus obscura FS-PLK Treadwall, 1898; 1901 Ophiodromus pugeftensis FS-LEC Blake, 1975a Syllidia armata FS-PLK Rasmussen, 1956 Nephtyidae Nephtys caeca FS-PLK Bentley et ai" 1984 Nephtys ciliata FS-PLK Thorson, 1946 Nephtys coeca FS-PLK Thorson, 1946 WILSON: POLYCHAETE REPRODUCfIVE MODES 505

Table 2. Continued

Nephtys hombergi FS-PLK Thorson, 1946; Bentley et a!., 1984 Ceratonereis aequisetis BR-TUBE-DIR Dorsey, 1981 Ceratonereis costae BR-TUBE-DIR Durchon, 1956 Ceratonereis erythraeensis FS-PLK Hutchings and Turvey, 1982 Ceratonereis limnetica BR-TUBE-DIR Glasby, 1986 Laeonereis culveri FS-DIR Mazurkiewicz, 1975 Leptonereis glauca BR- TUBE-DIR Thorson, 1946 Micronereis nanaimoensis GEL-LEC Reish, 1957 Micronereis variegata GEL-LEC Reish,1957 arenaceodentata BR- TUBE-DIR Reish, 1957; Pesch et aI., 1987 Nereis diversicolor FS-LEC Dales, 1950 Nereis Jalcaria GEL-LEC Read, 1974 Nereis grubei FS-PLK Reish,1954 Nereis irrorata FS-PLK Cazaux, 1968 Nereis limnicola BR-INT-DIR Smith, 1950 Nereis pelagica FS-LEC Wilson, 1932 Nereis pelagica FS-DIR Herpin, 1925 Nereis vexillosa GEL-LEC Johnson, 1943 Nicon aestuariensis FS-LEC Estcourt, 1966 Perinereis cultrifera FS-PLK Cazaux, 1968 Platynereis canaliculata FS-LEC Blake,1975a Platynereis dumeri/ii FS-LEC Hauenschild and Fischer, 1969; Cazaux, 1969 Platynereis dumeri/ii FS-DIR Thorson, 1946 Platynereis dumeri/ii FS-PLK Pfannenstiel et aI., 1987 Platynereis massiliensis BR- TUBE-DIR Pfannenstiel et aI., 1987 Eteone barbata FS-LEC Thorson, 1946 Eteone dilatae FS-PLK Blake, 1975a Eteone longa FS-PLK Rasmussen, 1956 sanguinea FS-PLK Thorson, 1946; Bhaud and Cazaux, 1987 Eulalia viridis GEL-PLK Thorson, 1946 (Anaitides) groenlandica GEL-PLK Thorson, 1946 Phyllodoce laminosa FS-PLK Bhaud and Cazaux, 1987 Phyllodoce (Anaitides) maculata GEL-PLK Thorson, 1946; Cazaux, 1969 Phyllodoce (Anaitides) mucosa GEL-PLK Thorson, 1946, Cazaux, 1969 Phyllodoce maculata GEL-PLK Thorson, 1946 Phyllodoce (Anaitides) williamsi GEL-PLK Blake,1975a Acholoe astericola FS-PLK Bhaud and Cazaux, 1987 Halosydna brevisetosa FS-PLK Blake,1975a Halosydna gelatinosa FS-PLK Bhaud and Cazaux, 1987 Halosydna johnsoni FS-PLK Reish, 1980 Harmothoe imbricata BR-EXT-PLK Blake, 1975a Harmothoe imbricata FS-PLK Cazaux, 1968 Harmothoe longisetis FS-PLK Bhaud and Cazaux, 1987 Harmothoe lunu/ata FS-PLK Bhaud and Cazaux, 1987 Lagisca extenuata FS-PLK Bhaud and Cazaux, 1987 clava FS-PLK Bhaud and Cazaux, 1987 FS-PLK Bhaud and Cazaux, 1987 Sigalionidae Pholoe assimi/is FS-PLK Christie, 1982 Pholoe balthica FS-PLK Petersen, M. E., in prep. Pholoe inornata FS-PLK Rasmussen, 1956 Pholoe min uta FS-PLK Blake, 197Sa; Heffernan and Kee- gan, 1988 Ph%e swedmarki BR-INT-DIR Laubier, 1975 Ph%e synophtha/mica FS-PLK Cazaux, 1968 506 BULLETIN OF MARINE SCIENCE, VOL. 48, NO.2, 1991

Table 2. Continued

Sthenelais baa FS-PLK Bhaud and Cazaux, 1987 Genus A BR-INT-DIR Wo1f,1984 Syllidae Auto1ytinae Autalytus edwardsi BR-EXT-DIR Allen, 1964 Autalytus fasciatus BR-EXT-PLK Allen, 1964 Autolytus prollfer BR-EXT-LEC Dales, 1951 b Autolytus prolifer x brachycephalus FS-EXT-PLK Schiedges, 1979 Eusyllinae Parapionosyllis gestans BR-EXT-DIR Cazaux, 1969 Exogoninae Brania limbata BR-EXT-DIR Cazaux, 1972 Exogone gemmifera BR-EXT-DIR Thorson, 1946 Exogone hebes BR-INT-DIR Pocklington and Hutcheson, 1983 Exogone longicornis BR-EXT-DIR Westheide, 1974 Exagone lourei BR-EXT-DIR Levin, 1984a Exogone naidina BR-EXT-DIR Oersted, 1845 Exogone occidentalis BR-EXT-DIR Westheide, 1974 Sphaerosyllis bulbosa BR-EXT-DIR Cazaux, 1972 Sphaerosyllis erinaceus BR-EXT-DIR Cazaux, 1972 Sphaerosyllis hystrix BR-EXT-DIR Cazaux, 1972 Syllinae Dentatisyllis brevicirra BR-INT-DIR Russell, pers. comm. Syllis incisa BR-INT-DIR Augener, 1929 Syllis nepiotica BR-INT-DIR Caullery and Mesni1, 1916 Syllis parturiens BR-INT-DIR Ben-E1iahu, 1975 Syllis variegata BR-EXT-PLK Cazaux, 1969 Syllis vivipara BR-INT-DIR Goodrich, 1900 Order Sabellida Sabellidae Fabricinae Chane echaudata GEL-LEC Okuda, 1946 Dasychone bombyx GEL-DIR Thorson, 1946 Fabricia limnicola BR-TUBE-DIR Levin, 1984a Fabricia sabella BR-TUBE-DIR Thorson, 1946 Fabriciola chilensis BR-TUBE-DIR McEuen et a1., 1983 Manayunkia aestuarina BR-TUBE-DIR Forsman, 1956 Manayunkia baicalensis BR-TUBE-DIR B1iakher, 1959 Manayunkia caspica BR- TUBE-DIR Marinescu, 1964 Oriopsis alata BR-TUBE-DIR McEuen et a1., 1983 Oriopsis ehlersi BR- TUBE-DIR McEuen et a1., 1983 Myxicolinae Myxicola infundibulum FS-LEC Dean et al., 1987 Sabellinae Amphiglena mediterranea BR-TUBE-DIR McEuen et a1., 1983 vancouveri FS-LEC McEuen et al., 1983 Megalomma vesiculosum FS-LEC Wilson, 1936a Pomataceros triqueter FS-PLK Thorson, 1946 Potamilla myriops FS-LEC Okuda, 1946 Potamilla neglecta BR- TUBE-DIR McEuen et al., 1983 Sabella media GEL-LEC McEuen, et al., 1983 insignis FS-LEC Lee, 1975 Ficopomatus enigmaticus FS-PLK Dixon, 1981 Microserpula infiata BR-TUBE-LEC Dons, 1933 Serpula vermicularis FS-PLK Thorson, 1946 Spirorbidae Janua (Dexiospira) brasiliensis BR-EXT-LEC Reish, 1980 ambilateralis BR-EXT-LEC Potswald, 1965 Spirorbis borealis BR-TUBE-LEC Thorson, 1946 Spirorbis granulatus BR-EXT-LEC Thorson, 1946 WILSON: POLYCHAETE REPRODUCTIVE MODES 507

Table 2. Continued

Spirorbis marchi BR-EXT-LEC Potswald, 1965 Spirorbis racemosus BR-EXT-LEC Potswald, 1965 Spirorbis spirillum BR- TUBE-LEC Potswald, 1965 Spirorbis vitreus BR- TUBE-LEC Potswald, 1965 Order Spionida Chaetopterus norveticus FS-PLK Thorson, 1946 Chaetopterus pergamentaceus FS-PLK Wilson, 1883 Spiochaetopterus ocu/atus FS-PLK Wilson, 1883 Cirratulidae Cau//erie//a Jragi/is BR- TUBE-DIR Petersen, M. E., in prep. Cau//erie//a n. sp. BR-INT-DIR Petersen, M. E., in prep. Chaetozone setosa complex FS-LEC Christie, 1985 Cirratu/us cirratus GEL-DIR Okuda, 1946 Cirratu/us cirratus GEL-LEC Cunningham and Ramage, 1888 Cirratu/us cirratus BR-EXT-DIR Fauvel, 1916 Cirratu/us sp. BR-INT-DIR Claparede and Mecznikow, 1868 Cirriformia /uxuriosa FS-LEC Reish, 1980 Cirriformia spirabrancha FS-LEC Blake, 1975c; Reish, 1980 Cirriformia tentacu/ata FS-LEC Wilson, 1936b Dodecaceria ater BR-INT-LEC Caullery and Mesnil, 1898 Dodecaceria caul/eryi FS-PLK Gibson and Clark, 1976 Dodecaceria concharum FS-PLK Caullery and Mesnil, 1898 Dodecaceria concharum GEL-LEC Gibson, 1977 Tharyx marioni FS-DIR Cazaux, 1972; Dales, 1951a Tharyx marioni FS-LEC Gibbs, 1971 Tharyx vivipara BR-INT-DIR Christie, 1984 Tharyx n. sp. BR-TUBE-DIR Petersen, M. E., in prep. Ctenodrilidae Raphidrilus nemasoma BR-INT-DIR Monticelli, 1910 Poeci/ochaetus serpens FS-PLK Hannerz, 1956 Spionidae Laonicinae Laonice cirrata FS-PLK Hannerz, 1956 BR-EXT-PLK Dean, 1965 Streb/ospio benedicti BR-EXT-LEC Levin, 1984b Streb/ospio benedicti BR-EXT-DIR Levin, 1984b Streb/ospio shrubsoli BR- TUBE-DIR Cazaux, 1985 Scolelepinae Aonides oxycepha/a FS-LEC Hannerz, 1956 Aonides paucibranchiata FS-LEC Hannerz, 1956 Ma/acoceros ciliata FS-PLK Hannerz, 1956 M a/acoceros Juligi nosa FS-PLK Day, 1934 Ma/acoceros girardi FS-PLK Hannerz,1956 Prionospio cirrifera FS-PLK Hannerz, 1956 Prionospio ma/mgreni FS-PLK Hannerz, 1956 Prionospio steenstrupi FS-PLK Hannerz, 1956 Rhynchospio areninco/a BR-EXT-PLK Levin, 1984a Sco/e/epis Joliosa FS-PLK Hannerz, 1956 Sco/e/epis squamata FS-PLK Hannerz, 1956 Sco/e/epis tridentata FS-PLK Hannerz, 1956 Sco/e/epis yamaguchi BR-CAP-PLK Imajima,1959 Sco/e/epis sp. I FS-PLK Hannerz, 1956 Sco/e/epis sp. II FS-PLK Hannerz, 1956 Spioninae Boccardia acus BR-CAP-DIR Read, 1975 Boccardia acus BR-CAP-PLK Read, 1975 Boccardia androgyna BR-CAP-PLK Read, 1975 Boccardia chilensis BR-CAP-PLK Blake and Kudenov, 1981 Boccardia hamata BR-CAP-PLK Dean and Blake, 1966 508 BULLETIN OF MARINE SCIENCE, VOL 48, NO.2, 1991

Table 2. Continued

Boccardia knoxi BR-CAP-DIR Read, 1975 Boccardia magniovata BR-CAP-DIR Read,1975 Boccardia natrix BR-INT-DIR Soderstrom, 1920 Boccardia otakouica BR-CAP-PLK Read,1975 Boccardia polybranchia BR-CAP-LEC Read, 1975 Boccardia polybranchia BR-CAP-DIR Duchene, 1984 Boccardia proboscidea BR-CAP-PLK Woodwick, 1977 Boccardia proboscidea BR-CAP-DIR Reish, 1980; Blake and Kudenov, 1981 Boccardia syrtis BR-CAP-PLK Read, 1975 Boccardia wellingtonensis BR-CAP-DIR Read, 1975 Microspio atlantica BR-CAP-PLK Hannerz,1956 aggregata BR-CAP-PLK Blake, 1969 Polydora commensalis BR-CAP-PLK Blake, 1969 Polydora concharum BR-CAP-PLK Blake 1969 Polydora giardi BR-CAP-PLK Day and Blake, 1979 Polydora hermaphroditica BR-CAP-LEC Hannerz, 1956 Polydora hoplura BR-CAP-DIR Wilson, 1928 Polydora hoplura BR-CAP-DIR Read, 1975 Polydora ligni BR-CAP-PLK Blake, 1969; Rice, 1980 Polydora ligni BR-CAP-DIR Zajac, 1985 Polydora nuchalis BR-CAP-DIR Woodwick, 1960 Polydora quadricirrata BR-CAP-PLK Read, 1975 Polydora quadrilobata BR-CAP-PLK Blake, 1969 Polydora quadrilobata BR-CAP-DIR Blake, 1969 Polydora socialis BR-CAP-PLK Carrasco, 1976 Polydora websteri BR-CAP-PLK Blake, 1969 Pseudopolydora kempi BR-CAP-DIR Blake and Woodwick, 1975 Pseudopolydora kempi BR-CAP-PLK Myohara, 1979 Pseudopolydora paucibranchiata BR-CAP-PLK Blake and Woodwick, 1975; Myohara, 1980 elegans BR-CAP-PLK Hannerz, 1956 BR-CAP-DIR Hannerz, 1956 Pygospio elegans BR-CAP-LEC Hannerz, 1956 Spio filicornis BR-CAP-PLK Hannerz, 1956 Spio martinensis BR-CAP-PLK Hannerz, 1956 Spio setosa BR-CAP-DIR Simon, 1967 Spio setosa BR-CAP-PLK Simon, 1968 Spiophanes bombyx FS-PLK Hannerz, 1956 Spiophanes kroyeri FS-PLK Hannerz, 1956 Order Ampharetidae Alkmaria romijni BR-INT-DIR Wesenberg-Lund, 1934 Ampharete grubei FS-DIR Thorson, 1946 H obsonia florida BR- TUBE-DIR Zottoli, 1974 Melinna cristata FS-LEC Nyholm, 1950 auricoma FS-PLK Thorson, 1946 Pectinaria koreni FS-PLK Watson, 1928; Wilson, 1936c Sabellariidae Lygdamus indicus FS-PLK Bhaud, 1975 Lygdamus muratus FS-PLK Wilson, 1929 Phragmatopoma lapidosa FS-PLK Eckelbarger, 1976 Phragmatopoma calijornica FS-PLK Eckelbarger, 1977 Sabel/aria alveolata FS-PLK Wilson, 1929 Sabel/aria floridensis FS-PLK Eckelbarger, 1977 Sabel/aria spinulosa FS-PLK Wilson, 1929 Sabel/aria vulgaris FS-PLK Eckelbarger, 1975 Artacama proboscidea FS-LEC Thorson, 1946 Eupolymnia heterobranchia BR-TUBE-DIR Wilson, unpublished obs. WILSON: POLYCHAETE REPRODUCTIVE MODES 509

Table 2. Continued

Eupolymnia nebulosa FS-LEC Gremare, 1986 Eupolymnia nebulosa BR-TUBE-LEC Gremare, 1986 Nicolea zoslericola GEL-DIR Eckelbarger, 1974 Ramex californiensis BR-CAP-DIR Blake, 1989 Thelepus crispus BR-TUBE-DIR Wilson, unpublished obs. Trichobranchidae Terebe//ides stroemi GEL-DIR Thorson, 1946

Jagersten (1972) argues that the primitive means of reproduction in the pro- tostomes 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 plesiomor- phic 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 com- pletely 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 plas- ticity occurs in other major protostome groups. Within the prosobranch gastro- pods, the archaeogastropods uniformly spawn eggs freely into the seawater, ul- timately 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 Species Orders Families

FS-PLK 79 7 22 BR-TUBE-DIR 39 8 II FS-LEC 34 8 16 BR-CAP-PLK 24 I I BR-INT-DIR 17 2 4 GEL-LEC 16 6 9 BR-EXT-DIR 15 I I BR-CAP-DIR 15 2 2 GEL-DIR 13 6 7 BR-TUBE-LEC II 4 5 GEL-PLK 10 3 4 FS-DIR 10 4 6 BR-TUBE-PLK 7 2 2 BR-EXT-LEC 7 3 3 BR-EXT-PLK 6 2 3 BR-CAP-LEC 3 I I BR-INT-LEC I 2 2 BR-INT-PLK 0 0 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 cap- sules, 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, vir- tually 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 Pera- carida 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 .

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.