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FAU Institutional Repository FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1975 Elsevier Inc. This manuscript is an author version and may be cited as: Rice, M. E. (1975). Sipuncula. In A. C. Giese and J. S. Pearse (Eds.), Reproduction of marine invertebrates: Vol. 2. Entoprocts and lesser coelomates (67‐127). New York: Academic Press. Reprinted from: RE:PRODUCTIONREPRODUCTION OF MARINE INVERTEBRATES, VOLVOl. II @1975©1975 ACADEMIC PRESS, INC.INC N*wH_ YwkYork SonSan Fronci>cOFrancisco LoiIcIolILoado« Chapter 4 SIPUNCULA Mary E. Rice 4.1 Introduction......................................Introduction .............. 67 4.2 Asexual Reproduction ..... ....................................... 69 K 44..3..3 Sexual Reproduction ............................................. 71 4.3.1 Sexual Dimorphism 71 ^ 4.3.2 Hermaphroditism 72 4.3.3 Anatomy of the Reproductive System 72 4.3.4 Origin of the Germ Cells 74 4.3.5 CytodifferentiationCytodifierentiation of the Gametes ........................... 74 4.3.6 Gametogenic Cycles 85 4.3.7 Factors Influencing Gametogenesis 90 4.3.8 Spawning and Breeding Periods 91 4.4 Development 96 4.4.1 Fertilization 96 4.4.2 Embryonic Development 97 4.4.3 Larvae 112 4.4.4 Summary of Developmental Patterns 123 Acknowledgments 124 4.5 References 125 4.1 Introduction The phylum SipullculaSipuncula is a simtllsmall group of unsegmentedunsegmcnted coelomcoelomateate marine worms noted for its lack of morphological diversity. Comprised of 17 recognized gClleragenera and approximately 320.320 species, the group is distributed throughout the polar, temperate, and tropical oceans (Stephen and Edmonds, 1972). The worms dwell in benthic habitats, ranging from intertidal shores to abyssal depths. Commonly they burrow into sand, mud, or gravel and, in the tropics, are frequently found inin • burrows within dead coral or other calcareous rock. Some species inhabit discarded mollusc shells and others live under rocks or wedge themselves into crevices. 67 68 MARY E. RICE :1 FIG. 1.I. Dissected specimen of Themiste lissllm.lUsnm. A, anus; FF,, F"Fj, F"F,,, fixing muscles " of the digestive tract; G, gomld;gonad; 1\,\, nephridium; NC, nerve cord; Rlvl,RM, retractor muscle; T, tentacles; INd, descending intt'stine;intestine; INa,I\'a, ascending intestine.intestine, (Redrawn from Fisher, 1952.)1952. ) I I The adult body consists of an elongated cylindrical trunk with slendcrslender anterior introvert which may be vvithdrawnwithdrawn into thcthe trunk by the contrac­contrac- .I tion of one or more pairs of retractor muscles. The introV<'rtintrovert is usually terminated by tentacles surrounding or dorsal to thcthe mouth. The esscntialessential features of sipunculan anatomy are illustrated in Fig. 1, a dissecteddi.ssected specimen of Themiste lissum. A long narrow csophagus,esophagus, extending the length of the introvert, is continuous with the intestinal spiral in the trunk. Recurved, with descending and ascending limbs typicallytypicallv coiled about oneOne another, the intestine opens to the exterior in a dorsal anusamis commonlycommonlv located on the anterior trunk. Two nephridia, reduced in some species to one, open through ventrolateral pores usually at the .., apprOXimateapproximate level of the anus. ThcThe ncrvousnervous system includes a supraeso­supraeso- phagcal ganglion, circumesophagealcireumesophageal connectives, and a ventral, un-un­ f paired and unsegmented n1l'uianmedian nerve cord. The gonad is commonlycommonlv locatedlocatc>d at the base of the ventral retractor muscles. The Sipuncula are classificdclassified as coelomate protostomes. CleavagcCleavage is spiral, the mouth forms in the position of the blastopore, and the coelom l , 4. SIPUl\'CULASIPU,\CULA 69 is formed by schizocoely. Characteristically there is a trochophore larva which in some species may behe followed by a second larval type, the pelagosphera. A protonephridium,protonephridimn, found in developmental stages of many protostomes, is absent in sipunculans. The complete lack of seg­seg- mentation either during development or in the adult, distinguishes the Sipuncula from the Annelida and, in the opinion of most contemporary zoologists, justifies the recognition of the group as a separate phylum. 4.2 Asexual Reproduction Asexual reproduction is known to occur in two species of sipunculans. A small, rock-boring species from the Caribbean Sea, Aspidosiphon brocki,hrocki, reproduces asexually, dividing into two unequal parts (Rice, 197D).1970). A constriction separates the smaller posterior daughter portion from the larger parent at a distance approximately one-fifth of the total length of the trunk from the posterior extremity (Fig. 2a). Before the completion of fission, the parent portion and the daughter portion each regencratesregenerates the structures essential to the formation of a new individual. In the case of the daughter the regenerated structures includcinclude thcthe entire anterior body and introvert, anterior gut, retractor muscles, and neph­neph- ridia. Adult structures contributed bybv the parent and incorporated into the daughter are one or two coils of the posterior intestinal spiral, poste­poste- rior parts of the spindle muscle and ventral nerve cord, and coelomocytes (Fig. 3). ThcThe formation of the juvenile is completed at the time of detachment from the adult or shortly.shortly thereafter when the newly regener­regener- ated introvcrtintrovert is everted (Fig. 2c). The parent regenerates only the posterior body wall which is formed as an invagination anterior to the constriction and is everted at the time the daughter individual is de­de- tached. Asexual reproduction is a naturally occurring phenomenon in AspidosiphonAspidosipllOH hrocki and has heenbeen found in 1.5ÍÍ15~t of the specimens col­col- lected in a population in KeyKev Largo, Florida. Sexual reproduction has not been observed in this species, although gonadal tissue is present in most individuals at the basehase of the retractor muscles. A second ascxuallyasexually reproducing species, Si/JUIlClIlllsSipiinciihts rolmsllls,rohusUis, has been ... reported to reproduce both by transversctransverse fission and lateral Imddingbudding (Rajulu and Krishnan, 1969; Hajulu,Rajulu, 1975). The posterior third of the animal may constrict off by transvcrsetransverse fission to form a new individual or the posterior one-half or two-thirds may give rise to as many as 5 incli­indi- viclualsviduals Simultaneously.simultaneously. The newly formed organs and structurcsstructures of the daughter dcvelopdevelop from a blastema composed of coclomocytescoelomocytes and pro- --------_._-------------------------------_.. -, 70 MARY~IARY E. RICE FIG.Fic:. 2. Asexual reproduction in i\sl'idosipllOnAspidosiphon brocki. (a) Animal showing posterior coastriction.L'onstri<:tion. (b)( b ) Recently separated parent amIand daughter.daughter, :-':oleXote everted.everted, newlyne\\'ly regeneratedf(;,gl'nerated posterior end of parent and black anterior cupcap of daughter.daughter, (e)(c) Parent and juvenile, 2 days after separation,separation. Regenerated anterior end of juvenile has \)el'nbeen everted.everted, (d) Posterior end of parent and daughter individual in process of separation,separation. Regenerated posterior of parent haslias heenbeen evertede\erted and daughter remains attached only hyby fragments of the hlaekblack material of the collar. A, anus; AS,.AS, anterior shield; C, collar on constricted animal or cap on daughter individual and juvenil*';juvenile; I, introvert. (From Rice, 1970.) liferations of epidermal and giltgut cells of the parent. MostMo.st of the internal organs are formed beforcbefore fission, but tentacles, introvert, and anus de­de- velop after clctachmcnl'.detacliment. Lat('ralLateral buds maymav hchv formed illin the region pos­pos- terior to the anus, and at the time of separation from the parent the daughter individual is compkklycompletely formed. Asexual reproduction inin ... S-iJlunculllsSipunculus rolJUstusrohuslus has be'enbeen observed only under conditions of stress such as maintl'nancemaintenance of animals inin stalestal(> sea water in the laboratory.laboratorv. Although asexual reproduction has becnbeen onlyonlv recentlyrecentlv reportedrc-portcd in si­si- puneulans, their regenerative eapahilitic.~capabilities havchave been recognizedrc>cognizcd for some.some time. :n~n cxnerimcntaJlyexnerimentally indncedinduced reg('nerationregeneration of the introvert of severalsevenal species, formation of anterior gut, retractor muscles, and brain have heenbeen 4.4. SI1>UNCUJ.ASIPUNCULA 7171 " Fifi.l'J(;. 3. Diaj^raniDia~ral11 of dissected posterior end of constricted AspidnsiphonAspidosipholl brockihrocki illustrating intcrnalinternal stl'1lclurcsslniclures of daughter and I'0sl"riorposterior portion of parent. C, collar; E, esophagus;csopha~lls; EP,lOP, epidermal ill\'agination;invagination; C, gonad; INa, ascending intestine; I:--Jcl,INd, cl('secndingdescending intt'stine;intestine; N, nephridium;ncphridiinii; ::\'C,\C, nerve cord; n,H, rectum; R\l,RM, retractor lllllSCIe;muscle; S, internalinternal noncellularnoneelhilar sheet of constriction; S\I,SM, spindle lIlllscle.nuiscle. (From Rice, HJiO.)1970.) observedob.scrved (Schleip.(Schleip, 1934; 'Wegener,Wegcncr, 193R).193S). EdodcnnalEctodermal clementselements have becnbeen presumed to formform from a strandstrand of regenerative ('('liseells illin thetlie nerve con1cord and mesodermalmesoderm;d elellwntselements fromfrom
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