SEXUAL REPRODUCTIVE MODES IN POLYCHAETES

BULLETIN OF MARINE SCIENCE 48(2) 500-5161991

SEXUAL REPRODUCTIVE MODES IN POLYCHAETESCLASSIFICATION AND DIVERSITY

W Herbert Wilson

ABSTRACTA 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 thefemale gametes (free-spawned or brooded in a variety of ways) A compilation ofinformationfrom the literature allowed the classification of 306 species The Orders Phyllodocida andSpionida show the greatest diversity of reproductive modes The most common reproductivemode involves the free spawning of gametes and the development of planktotrophic larvaeIt is apparent that there has been multiple evolution of many reproductive modes during thecourse of polychaete evolution This plasticity is argued to exceed that of the Classes Gas-tropoda Bivalvia and Malacostraca

Polychaetes display an extraordinary diversity of reproductive traits (Schroederand Hermans 1975) It is not uncommon for congeneric species to possess rad-ically different means of reproduction For example the maldanid Axiothellamucosa produces gelatinous egg masses attached to the female tube (Bookhoutand Hom 1949) Sibling species of A rubrocincta brood their young inside theirtube and free spawn demersal eggs respectively (Wilson 1983) The plasticity ofpolychaete life histories has undoubtedly contributed to their success in the marineenvironment (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) dividedpolyaetes generally into three general reproductive life styles although interme-diate species that are difficult to classify are common My approach involves afiner classification of reproductive modes Each class incorporates two aspects ofreproduction The first concerns the fate of the ova particularly whether they arespawned freely into the seawater or afforded some type of brood protection orencapsulation The second aspect concerns the type oflarval development plank-totrophic (having planktonic feeding larvae) lecithotrophic (having planktonicnon-feeding larvae) or direct (having no free-swimming larval phase) (Thorson1950) The distribution of these modes across the orders and families of thePolychaeta are examined using data from 306 species

MATERIALS AND METHODS

I surveyed the literature for descriptions of the reproductive biology ofpolychaetes To be classifiedin my scheme information had to be provided on the fate ofthe ova (whether they are free-spawnedor 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 classesand the three larval development classes The ova fate classes were developed based on my ownknowledge of polychaete reproductive biology and are strictly applicable only to polychaetes Eachclass is presumed to require specific morphological and physiological adaptations peculiar to thatclass eg the ability to produce gelatinous egg capsules or the evolution of structures on the body forbrooding The larval developmental classes (Thorson 1946 1950) were selected a priori These larvaldevelopmental classes can be applied to all marine invertebrates The abbreviations given in Table Iare used extensively in the text The ova fate classes are 1) free spawning 2) brooding on the body3) brooding within the body (viviparity) 4) brooding in capsules within the tube 5) brooding alongthe linings of the tube and 6) encapsulation in a gelatinous mass The classification incorporates thenotion 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 ovaand the type of larval development (Abbreviations for each mode are used throughout the text)

Abbreviation

FS-PLKFS-LECFS-DIRBR-EXT-PLKBR-EXT-LECBR-EXT-DIRBR-INT-PLKBR-INT-LECBR-INT-DIRBR-TUBE-PLKBR-TUBE-LECBR-TUBE-DIRBR-CAP-PLK

BR-CAP-LEC

BR-CAP-DIRGEL-PLK

GEL-LEC

GEL-DIR

Description

Free spawning with planktotrophic larvaeFree spawning with lecithotrophic larvaeFree spawning with entirely benthic developmentBrooding on the outside of the body with release of planktotrophic larvaeBrooding on the outside of the body with release of lecithotrophic larvaeBrooding on the outside of the body with direct developmentBrooding inside the body with release of planktotrophic larvaeBrooding inside the body with release of lecithotrophic larvaeBrooding inside the body with direct developmentBrooding inside the tube with release of planktotrophic larvaeBrooding inside the tube with release of lecithotrophic larvaeBrooding inside the tube with direct developmentBrooding of encapsulated embryos inside the tube with release of plankto-

trophic larvaeBrooding of encapsulated embryos inside the tube with release of lecitho-

trophic larvaeBrooding of encapsulated embryos inside the tube with direct developmentEncapsulation of embryos in a gelatinous mass with release of planktotrophic

larvaeEncapsulation of embryos in a gelatinous mass with release of lecithotrophic

larvaeEncapsulation of embryos in a gelatinous mass with direct development

of early development in an encapsulating structure or other brood structure after which in differentspecies the embryos may be released as planktotrophic larvae as lecithotrophic larvae or as benthicjuveniles I do not distinguish between the production of nurse eggs (exogenous yolk) and the productionof endogenous yolk There are numerous pathways for each (Eckel barger 1988) and there is insufficientinformation to classify most species

The classification presented herein addresses only sexual reproduction and hence excludes the varioustypes of asexual reproduction observed in polychaetes (Schroeder and Hermans 1975) The larvae ofsome arabellid polychaetes are parasitic in other polychaetes (Richards 1967) these are not consideredin this paper

In reviewing the literature I was able to find descriptions of the reproduction of 306 polychaeteswhich were sufficiently detailed to allow unambiguous classification of reproductive mode in mysystem Many descriptions of other species had to be eliminated from the compendium because theinvestigators were unable to discriminate between planktotrophic and lecithotrophic larvae Otherdescriptions did not indicate if early development involves free-spawned gametes or some type ofbrood protection Nevertheless the 307 species analyzed provide a summary of our knowledge of thedistribution of reproductive modes across the higher taxa of the Polychaeta The ordinal classificationscheme given in Fauchald (1977) is used to group families however I do not consider his arrangementof 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 ofreproductive modes Therefore the 307 species classified do not constitute a random sample Thisbias significantly reduces ones ability to make strong inferences about the relative diversities ofreproductive 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 arrangedalphabetically I make no assertion about polychaete phylogeny in this paper TheAmphinomida is listed first solely because this order comes first alphabeticallynot because I consider it primitive The 306 species classified belong to 36 familiesTwenty-three species are classified into more than one category Such plasticitymay arise from geographic variation from unrecognized sibling speciation or

502 BULLETIN OF MARINE SCIENCE VOL 48 NO2 1991

from poecilogony (Thorson 1950) The reason for the variability is not importantfor purposes here each mode represents a type found within the family and orderto which the species belongs Table 3 is a ranking of the frequency of occurrenceof each reproductive mode from the data in Table 2 The FS-PLK mode (seeTable I for a key to the abbreviations) occurs in 79 species belonging to 22families and seven orders BR- TUBE-DIR is found in 39 species distributed inII families and eight orders FS-LEC occurs in 34 species spread across 16 familiesand eight orders Although BR-CAP-PLK is reported 24 times all occurrencesare in the family Spionidae The next most common modes BR-INT-DIR GEL-LEC BR-EXT-DIR and BR-CAP-DIR are spread across six two one and twoorder(s) respectively The remaining modes are represented less than 15 times inthe compilation The only reproductive mode which is not represented at leastonce is BR-INT-PLK

A comparison of the orders well-represented in the compilation (Table 2) revealsthat 9 reproductive modes are represented among the 21 species of the OrderCapitellida Within the order four modes are found in the Arenicolidae (fivespecies) seven modes are found in the Capitellidae (13 species) and four modesin the Maldanidae (eight species) Eight modes are found in the Order Eunicidawith five modes in the Dorvilleidae (nine species) and six modes in the Onuphidae(14 species) Within the Phyllodocida (97 species) II modes are represented withinthe Hesionidae-(1l species) the Nereidae (23 species) and the Syllidae (22 species)showing five six and four reproductive modes respectively A pattern is evidentwithin the Syllidae with external brooding common in the Autolytinae Eusyllinaeand Exogoninae but internal brooding common in the Syllinae A total of sevenreproductive modes are seen in the Order Sabellida (28 species) with the greatestdiversity in the SabeIlidae (5 modes among 18 species) Within the Sabellidaefour modes occur in the Sabellinae while three occur in the Fabricinae predom-inantly BR- TUBE-DIR The Order Spionida demonstrates the highest diversityof reproductive modes with 14 distributed among 86 species The Cirratulidaeis remarkably variable with eight modes found in 18 species The Spionidae (63species) exhibit 10 reproductive modes Within the Spionidae four modes pri-marily FS-PLK occur in the Scolelepinae five modes occur in the Laonicinae andfive occur in the Spioninae With the exception of a single species in the Scole-lepinae (Scolelepis yamaguchi) brooding in capsules is restricted to the SpioninaeFinally 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 fivemodes in the seven species of the TerebeIlidae

DISCUSSION

The classification and compilation of polychaete reproductive modes confirmsthe instincts of polychaete biologists that the diversity of reproductive types ishigh within the class Several of the orders (Eunicida Phyllodocida Spionida)show great variability of reproductive types (Table 2) A number of families arenotably diverse (Spionidae Cirratulidae Nereidae Onuphidae Dorvilleidae andSabellidae) (Table 2)

It seems that polychaetes have few phylogeneticmorphological constraints onthe evolution of reproductive mode (Stearns 1983) In other words the possessionof one type of reproductive mode does not seem to preclude closely related speciesfrom evolving a vastly different suite of reproductive characteristics reproductivemodes are labile even at the genus level The Nephtyidae and Sabellariidae maybe 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 ofthe primary literature (Abbreviations to the different modes are explained in Table I)

Order AmphinomidaAmphinomidae

Hipponoe gaudichaudi BR-EXT-DIR Kudenov 1977Order Capitellida

ArenicolidaeArenicola brasiliensis GEL-LEC Okada 1941 Bailey-Brock 1984Arenicola claparedii FS-LEC Okuda 1946Arenicola cristala GEL-DIR Wilson 1883Arenicola marina BR-TUBE-DIR Farke and Berghuis 1979Abarenicola pacifica BR-TUBE-DIR Healy and Wells 1959

CapitellidaeCapitella capitala sp I BR- TUBE-LEC Grassle and Grassle 1976 Reish

1980Capitella capitala sp la BR-TUBE-PLK Grassle and Grassle 1976Capitella capilala sp II BR-TUBE-LEC Grass1e and Grassle 1976Capitella capitata sp III BR-TUBE-PLK Grass1e and Grassle 1976Capitella capitata sp IlIa BR-TUBE-DIR Grass1e and Grassle 1976 Reish

1980Capitella capitata complex BR-TUBE-LEC Rasmussen 1956 Reish 1974Capitella capitata complex BR-TUBE-DIR Rasmussen 1956Capitella hermaphrodita BR-TUBE-LEC Boletzky and Dohle 1967Dasybranchus caducus GEL-LEC Bookhout 1957Heteromastus filiformis FS-PLK Shaffer 1983Mediomaslus ambiseta FS-PLK Grassle and Grassle 1985Mediomaslus fragilis GEL-PLK Rasmussen 1956Notomastus latericeus FS-LEC Wilson 1933

MaldanidaeAxiolhella mucosa GEL-DIR Bookhout and Horn 1949Axiolhella rubrocincla BR-TUBE-DIR Wilson 1983Axiolhella rubrocincta FS-DIR Wilson 1983Axiothella serrata BR-TUBE-DIR Read 1984Boguea enigmatica BR-TUBE-DIR Wolf 1983Clymenella torquata GEL-DIR Wilson 1883Clymenella torquata FS-DIR Newell 1951Clymenura clypeata FS-LEC Cazaux 1972

Order EunicidaDorvilleidae

Dorvillea rudolphi FS-LEC Richards 1967 Blake 1975aOphryotrocha bacci BR-TUBE-PLK Akesson 1973aOphryotrocha diadema BR-TUBE-DIR Akkeson 1976Ophryotrocha hartmanni BR-TUBE-PLK Akesson 1973aOphryotrocha labronica BR-TUBE-PLK Akesson 1973aOphryotrocha maculata FS-PLK Akesson 1973bOphryotrocha notoglandulata BR-TUBE-PLK Akesson 1973aOphryotrocha puerilis BR- TUBE-PLK Akesson 1973aOphryotrocha vivipara BR-INT-DIR Banse 1963

EunicidaeEunice harassii FS-PLK Herpin 1925Eunice schemecephala FS-PLK Richards 1967Marphysa borradailei GEL-LEC PilIai1958

LumbrineridaeLumbrineris brevicirra BR- TUBE-DIR Bhaud and Cazaux 1987Lumbrineris impatiens GEL-PLK Cazaux 1972Lumbrineris latreilfi BR- TUBE-DIR Richards 1967Lumbrineris tenuis GEL-LEC Richards 1967Lumbrineris zonata BR-TUBE-DIR Richards 1967

OnuphidaeBrevibrachium maculatum BR- TUBE-DIR Smith and Jensz 1968Diopatra cuprea GEL-DIR Allen 1959

504

Table 2 Continued

BULLETIN OF MARINE SCIENCE VOL 48 NO2 1991

Diopatra neapolitana GEL-LEC Choe1960Diopatra variabiis GEL-DIR Krishnan 1936Diopatra sp BR-TUBE-DIR Monro 1924Hyalinoecia araucana BR-TUBE-DIR Carrasco 1983Kinbergonuphis simoni BR- TUBE-LEC Hsieh and Simon 1987Mooreonuphis jonesi BR- TUBE-LEC Fauchald 1982Nothria elegans FS-LEC Blake 1975bNothria nolialis BR-TUBE-DIR Hartman 1967a 1967bOnuphis magna GEL-LEC Andrews 1891 Hartman 1945Onuphis stigmatis BR-TUBE-DIR Wilson unpublishedParaonuphis antarctica BR-TUBE-DIR Hartman 1967a 1976bParaonuphis bermudensis BR-INT-DIR Hartman 1965

Order F1abelligeridaF1abelligeridae

Flabelligera mundata BR-EXT-DIR Gravier 1923Order Opheliida

OpheliidaeArmandia brevis FS-PLK Hermans 1966Euzonus mucronatus FS-PLK Dales 1952Ophelia bicornis FS-LEC Wilson 1948Ophelia bicornis FS-PLK Riser 1987

Order OrbiniidaOrbiniidae

Phylo Joetida GEL-DIR Salensky 1883Phylo Joetida atlantica FS-LEC Cazaux1972Leitoscoloplos kerguelensis FS-LEC Okuda 1946Leitoscoloplos pugeftensis GEL-DIR Blake 1980Leitoscoloplos robustus FS-LEC Hom and Bookhout1950Naineris laevigata GEL-LEC Okuda 1946Scoloplos acmeceps FS-LEC Blake 1980Scoloplos armiger GEL-DIR Anderson 1959 Chapman 1965

Gibbs 1968Seoloplos simplex GEL-LEC Anderson 1961

Order PhyllodocidaAphroditidae

Aphrodita aculeata FS-DIR Thorson 1946Chrysopetalidae

Chrysopetalum debile FS-PLK Cazaux 1968Paleanotus bellis FS-PLK Blake 1975a

GlyceridaeGlycera convoluta FS-PLK Cazaux1967

GoniadidaeGlycinde armigera FS-LEC Blake 1975aGoniada emerita FS-PLK Cazaux 1972

HesionidaeGyptis brunnea FS-LEC Blake 1975aGyptis rosea FS-PLK Haaland and Schram 1983aHesionides arenaria FS-DIR Westheide 1967 1970Hesionides gohari FS-DIR Westheide 1967 1970Microphthalmus aberrans GEL-PLK Westheide 1967 1970Microphthalmus sczelkowii GEL-DIR We~heide 1967 1970Nereimyra punctata FS-PLK Schram and Haaland 1984Ophiodromus jexuosus FS-PLK Haaland and Schram 1983bOphiodromus obscura FS-PLK Treadwall 1898 1901Ophiodromus pugeftensis FS-LEC Blake 1975aSyllidia armata FS-PLK Rasmussen 1956

NephtyidaeNephtys caeca FS-PLK Bentley et ai 1984Nephtys ciliata FS-PLK Thorson 1946Nephtys coeca FS-PLK Thorson 1946

Table 2 Continued

WILSON POLYCHAETE REPRODUCfIVE MODES 505

Nephtys hombergi

NereididaeCeratonereis aequisetisCeratonereis costaeCeratonereis erythraeensisCeratonereis limneticaLaeonereis culveriLeptonereis glaucaMicronereis nanaimoensisMicronereis variegataNereis arenaceodentataNereis diversicolorNereis JalcariaNereis grubeiNereis irrorataNereis limnicolaNereis pelagicaNereis pelagicaNereis vexillosaNicon aestuariensisPerinereis cultriferaPlatynereis canaliculataPlatynereis dumeriii

Platynereis dumeriiiPlatynereis dumeriiiPlatynereis massiliensis

PhyllodocidaeEteone barbataEteone dilataeEteone longaEulalia sanguinea

Eulalia viridisPhyllodoce (Anaitides) groenlandicaPhyllodoce laminosaPhyllodoce (Anaitides) maculataPhyllodoce (Anaitides) mucosaPhyllodoce maculataPhyllodoce (Anaitides) williamsi

PolynoidaeAcholoe astericolaHalosydna brevisetosaHalosydna gelatinosaHalosydna johnsoniHarmothoe imbricataHarmothoe imbricataHarmothoe longisetisHarmothoe lunuataLagisca extenuataLepidonotus clavaLepidonotus squamatus

SigalionidaePholoe assimiisPholoe balthicaPholoe inornataPholoe min uta

Phe swedmarkiPhe synophthamica

FS-PLK

BR-TUBE-DIRBR-TUBE-DIRFS-PLKBR-TUBE-DIRFS-DIRBR- TUBE-DIRGEL-LECGEL-LECBR- TUBE-DIRFS-LECGEL-LECFS-PLKFS-PLKBR-INT-DIRFS-LECFS-DIRGEL-LECFS-LECFS-PLKFS-LECFS-LEC

FS-DIRFS-PLKBR- TUBE-DIR

FS-LECFS-PLKFS-PLKFS-PLK

GEL-PLKGEL-PLKFS-PLKGEL-PLKGEL-PLKGEL-PLKGEL-PLK

FS-PLKFS-PLKFS-PLKFS-PLKBR-EXT-PLKFS-PLKFS-PLKFS-PLKFS-PLKFS-PLKFS-PLK

FS-PLKFS-PLKFS-PLKFS-PLK

BR-INT-DIRFS-PLK

Thorson 1946 Bentley et a1984

Dorsey 1981Durchon 1956Hutchings and Turvey 1982Glasby 1986Mazurkiewicz 1975Thorson 1946Reish 1957Reish1957Reish 1957 Pesch et aI 1987Dales 1950Read 1974Reish1954Cazaux 1968Smith 1950Wilson 1932Herpin 1925Johnson 1943Estcourt 1966Cazaux 1968Blake1975aHauenschild and Fischer 1969

Cazaux 1969Thorson 1946Pfannenstiel et aI 1987Pfannenstiel et aI 1987

Thorson 1946Blake 1975aRasmussen 1956Thorson 1946 Bhaud and

Cazaux 1987Thorson 1946Thorson 1946Bhaud and Cazaux 1987Thorson 1946 Cazaux 1969Thorson 1946 Cazaux 1969Thorson 1946Blake1975a

Bhaud and Cazaux 1987Blake1975aBhaud and Cazaux 1987Reish 1980Blake 1975aCazaux 1968Bhaud and Cazaux 1987Bhaud and Cazaux 1987Bhaud and Cazaux 1987Bhaud and Cazaux 1987Bhaud and Cazaux 1987

Christie 1982Petersen M E in prepRasmussen 1956Blake 197Sa Heffernan and Kee-

gan 1988Laubier 1975Cazaux 1968

506

Table 2 Continued


Sthenelais baaGenus A

SyllidaeAuto1ytinaeAutalytus edwardsiAutalytus fasciatusAutolytus prollferAutolytus prolifer x brachycephalus

EusyllinaeParapionosyllis gestans

ExogoninaeBrania limbataExogone gemmiferaExogone hebesExogone longicornisExagone loureiExogone naidinaExogone occidentalisSphaerosyllis bulbosaSphaerosyllis erinaceusSphaerosyllis hystrix

SyllinaeDentatisyllis brevicirraSyllis incisaSyllis nepioticaSyllis parturiensSyllis variegataSyllis vivipara

Order SabellidaSabellidae

FabricinaeChane echaudataDasychone bombyxFabricia limnicolaFabricia sabellaFabriciola chilensisManayunkia aestuarinaManayunkia baicalensisManayunkia caspicaOriopsis alataOriopsis ehlersi

MyxicolinaeMyxicola infundibulum

SabellinaeAmphiglena mediterraneaEudistylia vancouveriMegalomma vesiculosumPomataceros triqueterPotamilla myriopsPotamilla neglectaSabella mediaSchizobranchia ins ignis

SerpulidaeFicopomatus enigmaticusMicroserpula infiataSerpula vermicularis

SpirorbidaeJanua (Dexiospira) brasiliensisSpirorbis ambilateralisSpirorbis borealisSpirorbis granulatus

FS-PLKBR-INT-DIR

BR-EXT-DIRBR-EXT-PLKBR-EXT-LECFS-EXT-PLK

BR-EXT-DIR

BR-EXT-DIRBR-EXT-DIRBR-INT-DIRBR-EXT-DIRBR-EXT-DIRBR-EXT-DIRBR-EXT-DIRBR-EXT-DIRBR-EXT-DIRBR-EXT-DIR

BR-INT-DIRBR-INT-DIRBR-INT-DIRBR-INT-DIRBR-EXT-PLKBR-INT-DIR

GEL-LECGEL-DIRBR-TUBE-DIRBR-TUBE-DIRBR-TUBE-DIRBR-TUBE-DIRBR-TUBE-DIRBR- TUBE-DIRBR-TUBE-DIRBR- TUBE-DIR

FS-LEC

BR-TUBE-DIRFS-LECFS-LECFS-PLKFS-LECBR- TUBE-DIRGEL-LECFS-LEC

FS-PLKBR-TUBE-LECFS-PLK

BR-EXT-LECBR-EXT-LECBR-TUBE-LECBR-EXT-LEC

Bhaud and Cazaux 1987Wo1f1984

Allen 1964Allen 1964Dales 1951bSchiedges 1979

Cazaux 1969

Cazaux 1972Thorson 1946Pocklington and Hutcheson 1983Westheide 1974Levin 1984aOersted 1845Westheide 1974Cazaux 1972Cazaux 1972Cazaux 1972

Russell pers commAugener 1929Caullery and Mesni1 1916Ben-E1iahu 1975Cazaux 1969Goodrich 1900

Okuda 1946Thorson 1946Levin 1984aThorson 1946McEuen et a1 1983Forsman 1956B1iakher 1959Marinescu 1964McEuen et a1 1983McEuen et a1 1983

Dean et al 1987

McEuen et a1 1983McEuen et al 1983Wilson 1936aThorson 1946Okuda 1946McEuen et al 1983McEuen et al 1983Lee 1975

Dixon 1981Dons 1933Thorson 1946

Reish 1980Potswald 1965Thorson 1946Thorson 1946

Table 2 Continued


Spirorbis marchiSpirorbis racemosusSpirorbis spirillumSpirorbis vitreus

Order SpionidaChaetopteridae

Chaetopterus norveticusChaetopterus pergamentaceusSpiochaetopterus ocuatus

CirratulidaeCaueriea JragiisCaueriea n spChaetozone setosa complexCirratuus cirratusCirratuus cirratusCirratuus cirratusCirratuus spCirriformia uxuriosaCirriformia spirabranchaCirriformia tentacuataDodecaceria aterDodecaceria cauleryiDodecaceria concharumDodecaceria concharumTharyx marioniTharyx marioniTharyx viviparaTharyx n sp

CtenodrilidaeRaphidrilus nemasoma

PoecilochaetidaePoeciochaetus serpens

SpionidaeLaonicinaeLaonice cirrataStreblospio benedictiStrebospio benedictiStrebospio benedictiStrebospio shrubsoli

ScolelepinaeAonides oxycephaaAonides paucibranchiataMaacoceros ciliataM aacoceros Juligi nosaMaacoceros girardiPrionospio cirriferaPrionospio mamgreniPrionospio steenstrupiRhynchospio arenincoaScoeepis JoliosaScoeepis squamataScoeepis tridentataScoeepis yamaguchiScoeepis sp IScoeepis sp II

SpioninaeBoccardia acusBoccardia acusBoccardia androgynaBoccardia chilensisBoccardia hamata

BR-EXT-LECBR-EXT-LECBR- TUBE-LECBR- TUBE-LEC

FS-PLKFS-PLKFS-PLK

BR- TUBE-DIRBR-INT-DIRFS-LECGEL-DIRGEL-LECBR-EXT-DIRBR-INT-DIRFS-LECFS-LECFS-LECBR-INT-LECFS-PLKFS-PLKGEL-LECFS-DIRFS-LECBR-INT-DIRBR-TUBE-DIR

BR-INT-DIR

FS-PLK

FS-PLKBR-EXT-PLKBR-EXT-LECBR-EXT-DIRBR- TUBE-DIR

FS-LECFS-LECFS-PLKFS-PLKFS-PLKFS-PLKFS-PLKFS-PLKBR-EXT-PLKFS-PLKFS-PLKFS-PLKBR-CAP-PLKFS-PLKFS-PLK

BR-CAP-DIRBR-CAP-PLKBR-CAP-PLKBR-CAP-PLKBR-CAP-PLK

Potswald 1965Potswald 1965Potswald 1965Potswald 1965

Thorson 1946Wilson 1883Wilson 1883

Petersen M E in prepPetersen M E in prepChristie 1985Okuda 1946Cunningham and Ramage 1888Fauvel 1916Claparede and Mecznikow 1868Reish 1980Blake 1975c Reish 1980Wilson 1936bCaullery and Mesnil 1898Gibson and Clark 1976Caullery and Mesnil 1898Gibson 1977Cazaux 1972 Dales 1951aGibbs 1971Christie 1984Petersen M E in prep

Monticelli 1910

Hannerz 1956

Hannerz 1956Dean 1965Levin 1984bLevin 1984bCazaux 1985

Hannerz 1956Hannerz 1956Hannerz 1956Day 1934Hannerz1956Hannerz 1956Hannerz 1956Hannerz 1956Levin 1984aHannerz 1956Hannerz 1956Hannerz 1956Imajima1959Hannerz 1956Hannerz 1956

Read 1975Read 1975Read 1975Blake and Kudenov 1981Dean and Blake 1966

508

Table 2 Continued


Boccardia knoxiBoccardia magniovataBoccardia natrixBoccardia otakouicaBoccardia polybranchiaBoccardia polybranchiaBoccardia proboscideaBoccardia proboscidea

Boccardia syrtisBoccardia wellingtonensisMicrospio atlanticaPolydora aggregataPolydora commensalisPolydora concharumPolydora giardiPolydora hermaphroditicaPolydora hopluraPolydora hopluraPolydora ligniPolydora ligniPolydora nuchalisPolydora quadricirrataPolydora quadrilobataPolydora quadrilobataPolydora socialisPolydora websteriPseudopolydora kempiPseudopolydora kempiPseudopolydora paucibranchiata

Pygospio elegansPygospio elegansPygospio elegansSpio filicornisSpio martinensisSpio setosaSpio setosaSpiophanes bombyxSpiophanes kroyeri

Order TerebellidaAmpharetidae

Alkmaria romijniAmpharete grubeiH obsonia floridaMelinna cristata

PectinariidaePectinaria auricomaPectinaria koreni

SabellariidaeLygdamus indicusLygdamus muratusPhragmatopoma lapidosaPhragmatopoma calijornicaSabelaria alveolataSabelaria floridensisSabelaria spinulosaSabelaria vulgaris

TerebellidaeArtacama proboscideaEupolymnia heterobranchia

BR-CAP-DIRBR-CAP-DIRBR-INT-DIRBR-CAP-PLKBR-CAP-LECBR-CAP-DIRBR-CAP-PLKBR-CAP-DIR

BR-CAP-PLKBR-CAP-DIRBR-CAP-PLKBR-CAP-PLKBR-CAP-PLKBR-CAP-PLKBR-CAP-PLKBR-CAP-LECBR-CAP-DIRBR-CAP-DIRBR-CAP-PLKBR-CAP-DIRBR-CAP-DIRBR-CAP-PLKBR-CAP-PLKBR-CAP-DIRBR-CAP-PLKBR-CAP-PLKBR-CAP-DIRBR-CAP-PLKBR-CAP-PLK

BR-CAP-PLKBR-CAP-DIRBR-CAP-LECBR-CAP-PLKBR-CAP-PLKBR-CAP-DIRBR-CAP-PLKFS-PLKFS-PLK

BR-INT-DIRFS-DIRBR- TUBE-DIRFS-LEC

FS-PLKFS-PLK

FS-PLKFS-PLKFS-PLKFS-PLKFS-PLKFS-PLKFS-PLKFS-PLK

FS-LECBR-TUBE-DIR

Read 1975Read1975Soderstrom 1920Read1975Read 1975Duchene 1984Woodwick 1977Reish 1980 Blake and Kudenov

1981Read 1975Read 1975Hannerz1956Blake 1969Blake 1969Blake 1969Day and Blake 1979Hannerz 1956Wilson 1928Read 1975Blake 1969 Rice 1980Zajac 1985Woodwick 1960Read 1975Blake 1969Blake 1969Carrasco 1976Blake 1969Blake and Woodwick 1975Myohara 1979Blake and Woodwick 1975

Myohara 1980Hannerz 1956Hannerz 1956Hannerz 1956Hannerz 1956Hannerz 1956Simon 1967Simon 1968Hannerz 1956Hannerz 1956

Wesenberg-Lund 1934Thorson 1946Zottoli 1974Nyholm 1950

Thorson 1946Watson 1928 Wilson 1936c

Bhaud 1975Wilson 1929Eckelbarger 1976Eckelbarger 1977Wilson 1929Eckelbarger 1977Wilson 1929Eckelbarger 1975

Thorson 1946Wilson unpublished obs

Table 2 Continued


Eupolymnia nebulosaEupolymnia nebulosaNicolea zoslericolaRamex californiensisThelepus crispus

TrichobranchidaeTerebeides stroemi

FS-LECBR-TUBE-LECGEL-DIRBR-CAP-DIRBR-TUBE-DIR

GEL-DIR

Gremare 1986Gremare 1986Eckelbarger 1974Blake 1989Wilson unpublished obs

Thorson 1946

Jagersten (1972) argues that the primitive means of reproduction in the pro-tostomes occurs by spawning gametes freely into the seawater with subsequentdevelopment of planktotrophic larvae This pattern corresponds to the FS-PLKclass in my system It is therefore not surprising that FS-PLK is represented inmore families and orders than any other mode (Tables 2 3) From this plesiomor-phic condition the repeated radiation of other reproductive modes has occurredFrom Table 3 it is parsimonious to claim for instance that BR-TUBE-DIR amajor shift from the primitive FS-PLK must have evolved at least eight timesbecause it appears in eight different orders each of which retains the plesiomorphicFS-PLK in some species Similarly GEL-DIR and GEL-LEe both occur in sixorders The appearance of each mode other than the presumed plesiomorphicFS-PLK in an order is likely to have been an independent evolutionary event

A comparison of the reproductive variability ofthe Polychaeta with other majorbenthic taxa is intriguing The classification scheme adopted here is specificallydesigned to accommodate polychaete reproductive modes and hence is not com-pletely comparable for other taxa For instance gastropods because they do notbuild tubes cannot brood their young within a tube However there is sufficientinformation 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 ordersand families in which each mode occurs are given data are compiled from Table 2)

Reproductive mode Species Orders Families

FS-PLK 79 7 22BR-TUBE-DIR 39 8 IIFS-LEC 34 8 16BR-CAP-PLK 24 I IBR-INT-DIR 17 2 4GEL-LEC 16 6 9BR-EXT-DIR 15 I IBR-CAP-DIR 15 2 2GEL-DIR 13 6 7BR-TUBE-LEC II 4 5GEL-PLK 10 3 4FS-DIR 10 4 6BR-TUBE-PLK 7 2 2BR-EXT-LEC 7 3 3BR-EXT-PLK 6 2 3BR-CAP-LEC 3 I IBR-INT-LEC I 2 2BR-INT-PLK 0 0 0


Among the mesogastropod and neogastropod prosobranch snails virtually allspecies encapsulate their young in leathery capsules (Fretter 1984) The younghatch as planktotrophic larvae lecithotrophic larvae or benthic juveniles A fewspecies 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-spawningto dependence upon the production of capsules for sequestering the embryos aswitch requiring but one evolutionary event the acquisition of the ability to secreteleathery capsules The Opisthobranchia encapsulate their young in gelatinousribbons from which planktotrophic larvae lecithotrophic larvae or juveniles mayemerge (Thompson 1976) Again the diversity of reproductive modes below thelevel of order is low Species of the Bivalvia either spawn gametes freely whichdevelop as planktotrophic or lecithotrophic larvae (rarely demersal development)or brood embryos within the female mantle cavity (morphologically an externalbrood chamber) for all of embryonic development (Mackie 1984) Brooding hasarisen several times always associated with small size however brooding tendsto characterize families rather than higher taxa (Strathmann and Strathmann1982) Larger bivalves are invariably free-spawners (Mackie 1984) Finally vir-tually all members of the crustacean class Malacostraca a taxon far more diversethan the Polychaeta with 18000 species (Barnes 1987) display only three basicreproductive modes free-spawning eggs followed by planktotrophic developmentbrooding eggs externally with the release of planktotrophic larvae or broodingeggs externally for all of embryonic development (Schram 1986) There is virtuallyno variability below the level offamily For instance the entire superorder Pera-carida brood their young externally with no larval stage (Barnes 1987) Withinthe decapods only the penaeid shrimps spawn their eggs freely all remaining taxain this order brood their young on the abdomen releasing planktotrophic larvae(Schram 1986) These examples show that other major taxa of prot ostomes seemto have less potential for changing basic attributes of their reproductive biologyThe remarkable plasticity of the polychaetes derives in part from the relativesimplicity of the reproductive system which seems to place few restrictions onfurther evolutionary change (Dales 1967) There is a striking contrast with thecomplicated reproductive system of gastropods (Thompson 1976 Fretter 1984)which certainly places great morphological constraints on evolutionary changeThe plasticity of reproductive mode in the polychaetes likely played a major rolein their success in benthic habitats of the oceans

ACKNOWLEDGMENTS

I would like to thank several polychaetologists who provided encouragement as well as referencesand information on the life histories of various polychaetes particularly J Blake B Brown KFauchald P Hutchings L Levin D Reish D Russell H ten Hove and especially M Petersen Iam grateful to B Brown K Fauchald D McHugh and S Woodin for discussion or comments onthe manuscript The anonymous reviewers made many useful comments on the manuscript for whichI am thankful I continue to add to this compendium I would appreciate information on species whichcould be added

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DATEACCEPTED November 6 1990

ADDRESS Department of Zoology NJ-15 University of Washington Seattle Washington 98195PRESENTADDRESSDepartment of Biology Colby College Waterville Maine 04901

WILSON POLYCHAETE REPRODUCTIVE MODES SOl

Table I List of the reproductive modes of polychaetes based on the criteria of the fate of the ovaand the type of larval development (Abbreviations for each mode are used throughout the text)

Abbreviation

FS-PLKFS-LECFS-DIRBR-EXT-PLKBR-EXT-LECBR-EXT-DIRBR-INT-PLKBR-INT-LECBR-INT-DIRBR-TUBE-PLKBR-TUBE-LECBR-TUBE-DIRBR-CAP-PLK

BR-CAP-LEC

BR-CAP-DIRGEL-PLK

GEL-LEC

GEL-DIR

Description

Free spawning with planktotrophic larvaeFree spawning with lecithotrophic larvaeFree spawning with entirely benthic developmentBrooding on the outside of the body with release of planktotrophic larvaeBrooding on the outside of the body with release of lecithotrophic larvaeBrooding on the outside of the body with direct developmentBrooding inside the body with release of planktotrophic larvaeBrooding inside the body with release of lecithotrophic larvaeBrooding inside the body with direct developmentBrooding inside the tube with release of planktotrophic larvaeBrooding inside the tube with release of lecithotrophic larvaeBrooding inside the tube with direct developmentBrooding of encapsulated embryos inside the tube with release of plankto-

trophic larvaeBrooding of encapsulated embryos inside the tube with release of lecitho-

trophic larvaeBrooding of encapsulated embryos inside the tube with direct developmentEncapsulation of embryos in a gelatinous mass with release of planktotrophic

larvaeEncapsulation of embryos in a gelatinous mass with release of lecithotrophic

larvaeEncapsulation of embryos in a gelatinous mass with direct development

of early development in an encapsulating structure or other brood structure after which in differentspecies the embryos may be released as planktotrophic larvae as lecithotrophic larvae or as benthicjuveniles I do not distinguish between the production of nurse eggs (exogenous yolk) and the productionof endogenous yolk There are numerous pathways for each (Eckel barger 1988) and there is insufficientinformation to classify most species

The classification presented herein addresses only sexual reproduction and hence excludes the varioustypes of asexual reproduction observed in polychaetes (Schroeder and Hermans 1975) The larvae ofsome arabellid polychaetes are parasitic in other polychaetes (Richards 1967) these are not consideredin this paper

In reviewing the literature I was able to find descriptions of the reproduction of 306 polychaeteswhich were sufficiently detailed to allow unambiguous classification of reproductive mode in mysystem Many descriptions of other species had to be eliminated from the compendium because theinvestigators were unable to discriminate between planktotrophic and lecithotrophic larvae Otherdescriptions did not indicate if early development involves free-spawned gametes or some type ofbrood protection Nevertheless the 307 species analyzed provide a summary of our knowledge of thedistribution of reproductive modes across the higher taxa of the Polychaeta The ordinal classificationscheme given in Fauchald (1977) is used to group families however I do not consider his arrangementof 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 ofreproductive modes Therefore the 307 species classified do not constitute a random sample Thisbias significantly reduces ones ability to make strong inferences about the relative diversities ofreproductive 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 arrangedalphabetically I make no assertion about polychaete phylogeny in this paper TheAmphinomida is listed first solely because this order comes first alphabeticallynot because I consider it primitive The 306 species classified belong to 36 familiesTwenty-three species are classified into more than one category Such plasticitymay arise from geographic variation from unrecognized sibling speciation or




DISCUSSION

















504

Table 2 Continued
















Table 2 Continued


Nephtys hombergi








FS-PLK







BR-INT-DIRFS-PLK









506

Table 2 Continued













FS-PLKBR-INT-DIR


BR-EXT-DIR




FS-LEC






Cazaux 1969




Dean et al 1987




Table 2 Continued












FS-PLKFS-PLKFS-PLK


BR-INT-DIR

FS-PLK







Monticelli 1910

Hannerz 1956




508

Table 2 Continued














FS-PLKFS-PLK


FS-LECBR-TUBE-DIR








Table 2 Continued





GEL-DIR


Thorson 1946








ACKNOWLEDGMENTS


LITERATURE CITED


































559-572



















































































































































DISCUSSION

















504

Table 2 Continued
















Table 2 Continued


Nephtys hombergi








FS-PLK







BR-INT-DIRFS-PLK









506

Table 2 Continued













FS-PLKBR-INT-DIR


BR-EXT-DIR




FS-LEC






Cazaux 1969




Dean et al 1987




Table 2 Continued












FS-PLKFS-PLKFS-PLK


BR-INT-DIR

FS-PLK







Monticelli 1910

Hannerz 1956




508

Table 2 Continued














FS-PLKFS-PLK


FS-LECBR-TUBE-DIR








Table 2 Continued





GEL-DIR


Thorson 1946








ACKNOWLEDGMENTS


LITERATURE CITED


































559-572






























































































































































504

Table 2 Continued
















Table 2 Continued


Nephtys hombergi








FS-PLK







BR-INT-DIRFS-PLK









506

Table 2 Continued













FS-PLKBR-INT-DIR


BR-EXT-DIR




FS-LEC






Cazaux 1969




Dean et al 1987




Table 2 Continued












FS-PLKFS-PLKFS-PLK


BR-INT-DIR

FS-PLK







Monticelli 1910

Hannerz 1956




508

Table 2 Continued














FS-PLKFS-PLK


FS-LECBR-TUBE-DIR








Table 2 Continued





GEL-DIR


Thorson 1946








ACKNOWLEDGMENTS


LITERATURE CITED


































559-572
















































































































































504

Table 2 Continued
















Table 2 Continued


Nephtys hombergi








FS-PLK







BR-INT-DIRFS-PLK









506

Table 2 Continued













FS-PLKBR-INT-DIR


BR-EXT-DIR




FS-LEC






Cazaux 1969




Dean et al 1987




Table 2 Continued












FS-PLKFS-PLKFS-PLK


BR-INT-DIR

FS-PLK







Monticelli 1910

Hannerz 1956




508

Table 2 Continued














FS-PLKFS-PLK


FS-LECBR-TUBE-DIR








Table 2 Continued





GEL-DIR


Thorson 1946








ACKNOWLEDGMENTS


LITERATURE CITED


































559-572
















































































































































Table 2 Continued


Nephtys hombergi








FS-PLK







BR-INT-DIRFS-PLK









506

Table 2 Continued













FS-PLKBR-INT-DIR


BR-EXT-DIR




FS-LEC






Cazaux 1969




Dean et al 1987




Table 2 Continued












FS-PLKFS-PLKFS-PLK


BR-INT-DIR

FS-PLK







Monticelli 1910

Hannerz 1956




508

Table 2 Continued














FS-PLKFS-PLK


FS-LECBR-TUBE-DIR








Table 2 Continued





GEL-DIR


Thorson 1946








ACKNOWLEDGMENTS


LITERATURE CITED


































559-572
















































































































































506

Table 2 Continued













FS-PLKBR-INT-DIR


BR-EXT-DIR




FS-LEC






Cazaux 1969




Dean et al 1987




Table 2 Continued












FS-PLKFS-PLKFS-PLK


BR-INT-DIR

FS-PLK







Monticelli 1910

Hannerz 1956




508

Table 2 Continued














FS-PLKFS-PLK


FS-LECBR-TUBE-DIR








Table 2 Continued





GEL-DIR


Thorson 1946








ACKNOWLEDGMENTS


LITERATURE CITED


































559-572
















































































































































Table 2 Continued












FS-PLKFS-PLKFS-PLK


BR-INT-DIR

FS-PLK







Monticelli 1910

Hannerz 1956




508

Table 2 Continued














FS-PLKFS-PLK


FS-LECBR-TUBE-DIR








Table 2 Continued





GEL-DIR


Thorson 1946








ACKNOWLEDGMENTS


LITERATURE CITED


































559-572
















































































































































508

Table 2 Continued














FS-PLKFS-PLK


FS-LECBR-TUBE-DIR








Table 2 Continued





GEL-DIR


Thorson 1946








ACKNOWLEDGMENTS


LITERATURE CITED


































559-572
















































































































































Table 2 Continued





GEL-DIR


Thorson 1946








ACKNOWLEDGMENTS


LITERATURE CITED


































559-572


















































































































































ACKNOWLEDGMENTS


LITERATURE CITED


































559-572














































































































































































559-572










































































































































































































































































































































































































































































































































































Documents

SEXUAL REPRODUCTIVE MODES IN POLYCHAETES