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Notice: ©1976 The Society for Integrative and Comparative Biology. This is an electronic version of an article published in American Zoologist http://icb.oxfordjournals.org/ and may be cited as: Rice, M. E. (1976). Larval development and metamorphosis in Sipuncula. American Zoologist, 16(3), 563‐571.

AMER. ZOOL., 16:56 3- 571 ( 1976).

Larval Development and Metamorphosis in Sipuncula

MARY E. RICE

Department of Invertebrate Zoology, National Mu seum of Natural H istory, Smithsonian Institution, Washington, D.C. 20560

SYNOPSI S. In a br ief review of development of the phylum Sipuncul a, fo ur patterns of develop ment are recogni zed: (1) dir ect with no pelagic stage; (2) on e larval stage, a lecitho­ trophic tro ch ophore ; (3) two larval stages, a lecithotrophic trochophore and a lecithotrophic pelagospher a; (4) two lar val stages, a lecith otrophic trochophore and a planktotrophic pel agosphera. Lar val types and th eir metam orphoses are described , with special attention to the d evelopment and morphologyofthe larval cut icle. In the majority ofspecies stud ied, the egg en velope is tr an sformed into the larval cuticle a t metam orphosis of th e tr ochophore. T he cuticle ofman y planktotrophic pel agosphera lar vae is cha rac terized by su rface papill ae ofdiverse form and pattern. The underl ying cuticle in some species is compo sed oflayers of fiber s at right angles to one anothe r.

INTRODUCTION scribed, bringing the total number of species studied to 18 (Rice, 1967, 1973, The first description of spiral cleavage in 1975a,b). the Sipuncula appeared in a publication by In this paper a brief resume will be pre­ Gerould (1907) on cell lineage and larval sented of current knowledge on larval d e­ development in Phascolopsis gouldi and velopment and metamorphosis in the Goljingia vulgaris. In earlier studies Selenka Sipuncula, including some previously un­ (1875) gave an abbreviated account of the published information on morphology, development of Goljingia elongata, and cuticle structure and metamorphosis of Hatschek (1883) reported in detail the em­ open-ocean planktotrophic larvae. For bryogenesis and organogenesis of Sipun­ more detailed accou n ts of development culus nudus. Although these earlier reports and com plete bibliographies, the reader is on sip u ncu lan s did not include studies of referred to several recent reviews (Hall and early cleavage, the authors recognized cer­ Scheltema, 1975; Rice, 1967, 1975a,b). tain developmental similarities to annelids, echiurans and molluscs, and thus estab­ lished the basis for the consideration of DEVELOPMENTAL PATTERNS sipunculans as members of the Spiralia. Following the reports of Gerould (1903, Four patterns of development are now 1907), there were no studies on sipunculan recognized in the Sipuncula (Table 1). development until 1958 when Akesson Three species develop directl y with no published a treatise on the nervous system pelagic larval stage. Two species exhibit a of sipunculans in which he considered the short lecithotrophic trochophore stage development of two species, Phascolion which gradually transforms into a ver­ strombi and Goljingia minuta. Later he re­ miform stage, then into the juvenile form. peated Selenka's observations on Goljingia In a third developmental pattern, charac­ elongata and investigated the development teristic of four species, there are two larval of neurosecretory ce lls in this species stages, a lecithotrophic trochophore an d a (~kesson, 1961a). More recently, develop­ lecithotrophic pelagosphera. One species, ment of additional species has been de- Themiste lageniformis, listed in category 111in Table 1 does not completely fit the defini­ tion in that it lacks a swimming trochophore .t T his paper is Co ntribu tio n No. 41 of the Harbor stage, developing directly into a lecitho­ Br an ch Foundation, Inc., Science Lab oratory. trophic pelagosphera (Williams, 1972).

563 564 M ARY E. RICE

TABLE J. Patterns of development in Sipuncula. patterns have eggs relatively higher in yolk conten t th an th ose species in the fo urth Direct Development de velopmental category, asjudged by opac­ I. Egg --+ Ver mi fo rm Stage --+ Juvenile ity in th e livin g egg and concen tration of Golfingia minuta" yo lk granules in sec tio ned material. All Phascolion cryptus' species in the first th ree categories pass Th emiste pyroidesc through a ver miform stage, i.e., a craw ling Indirec r Develop ment lecithotrophic form, which undergoes a

II. Egg --+ Trocho phore --+ Vermiform Stage --+ grad ual transformation into a feeding Juvenile juvenile. The only clearly metamorphic Phascolion strombi» change in the first three categories is from Phascolopsis gouldi" the lecithotrophic troch ophore to the lecithotrophic pelagosphera. The latter III. Egg --+ Trochophore --+ Lecith o tr ophic larval form swims fo r a relati vely short time Pelagosph era --+ Vermiform Stage --+ Juvenile before undergoing a gradual transforma­ Golfingia elongatah. h tion in to the vermifo r m stage. In th e fo urth Golfingia pugettensis" Golfingia uulgaris" devel opmental category th e vermiform Them iste alutacea' stage is absent and there are two distin ct Th emiste lagen iformis' . •. j metamorphoses, one from the trochophore to th e planktotrophic pelagosphera and th e I V. Egg --+ Trochophore --+ Planktotrop hic oth er from the p ela g o spher a to the Pe lagosphera --+ Juve nile j u venile. It has not been possible thus far to Aspidosiphon paruuluss rear larvae in category 4 in the lab orat ory Golfingia pellucidar Paraspidosiphonfischeri' fro m th e eg g through two metamorphose s. Phascolosoma agassizii» In most studies of development, obse rva ­ Phascolosoma antillarum' tio ns have been made throu gh metam or­ Pha scolosoma perlu cens' phosis of th e troch ophore and resulting Phascalosoma varians! Sipunculus nud us" pelagospheras have been maintained in some instan ces fo r several months in cul­ a Akesson, 1958. ture wit hou t undergoing a secon d b Akesson, 1961 a. metamorphosis (Rice, 1967). Metamor­ c Gerould , 1907. d Hat sch ek , 1883. phosis from the pela go spher a to the c Rice , 1967. j uvenile has been stud ied only in ocean ic ! Rice, 1975b. pelagospheras collected in plankton sam­ • Rice, Un published . ples (Hall and Schel te ma, 1975). h Selenka, 1875. The term pelagosphera was first used by I Williams, 1972. j De vel ops di rectly from egg to lecithotrophic Mingazinni (1905) to design at e wha t he be­ pelag osphera , without a troch ophore stage. lieved to be a new genus and species of Sipunculan, "Pelagosphaera aloysii" . This was The majority of species fall into a fourth later shown to be a larval rather th an ad ult developmental classification similar to the form; however, the name pelagosphera th ird with two pelagic stages, but differing persisted in th e literature in reference to by ha vin g a planktotrophic pelagosphera certa in oceanic sip unc ula n larvae. In ligh t larva whi ch often remains in th e plankton of r ecent st ud ies it has been rede fined as a fo r several months. Numerous reports of lar val stage unique to the Sipuncul a which planktotrophic pelagospheras of unknown succeeds the troch ophore and is distin­ species from oceanic plankton are found in guished by a prominent metatroch al ciliary the lit erature (see reviews of H all and band and a loss or reduction of th e proto­ Scheltema, 197 5; Rice 197 Sa). tro ch (Rice, 1967). A close interrelationship is appa re nt be­ tween the yolk cont ent of an egg and its CLEAVAGE ens uing devel opmental pattern.Species Cleavage in all sipu nc ulan eggs is spiral, ex h ibiting the first three developmental holoblastic, and unequal (Fig. 1). In spe cies - m

-7

ma 2 / bo

·~~.·~~WifA~ - m ~I ~ .'Ig

3 8'--__

FIGS. 1-6. Developmental stag es of Phascolosoma var­ alutacea 2 da ys. Dor sal view. Head partially retracted . ians. Scale, 25 JLm. Scale, 25 JLm. 1. T wo-cell stage. 2-4. T ro chophor es. No te d evelo ping g ut , prototroch , a n d a pica l tuft. 5. Be ginning FI G. 8. Planktotrophic pelagosphera of Golfingia pel­ metam orphosis. Four da ys. 6. Recently metam or­ lucida, 7 days. Later al view. Scale, 25 JLm. phosed . Planktotrophic pelagosphera, 5 days. a, a nus ; bo, bu ccal orga n ; I, lower lip ; Ig,lip gland ; m, rnet atroch ; rno, mouth; s, stomach; to, terminal organ FIG. 7. Lecithotrophic pelagosphera of Th emiste 566 MARY E. RICE with lecithotrophic development and yolk­ Metamorphosis of the trochophore may rich eggs, the micromeres in the A, B, and C result in either a lecithotrophic or a quadrants at the 8-cell stage may be larger planktotrophic larva (Figs. 4-6, 7-9). In than the macromeres. The greater size of both cases metamorphic alterations consist the micromeres is reflected in the excep­ of elongation of the posttrochal body, for­ tionally large prototroch cells which serve mation or expansion of the coelom, reduc­ as a source of nutrition to the developing tion in the prototroch and formation or larva by releasing yolk granules into the enlargement of the metatroch as the pri­ coelom usually at the time of metamor­ mary locomotory organ. Usually a terminal phosis of the trochophore. attachment organ is formed at the posterior The apical plate at the 48-cell stage in extremity. At the time of metamorphosis Goljingia vulgaris, as reported by Gerould the egg envelope is ruptured in the region (1907), consists ofrosette cells (Iq Ill), cross of the stomodaeum, the outer portion of cells (lqI21.122), and intermediate cells which is everted to form the ventral ciliated (lq112). The cross cells are in the frontal and surface of the head. Part of the prototroch sagittal planes, the radial position of the immediately above the stomodaeum is lost molluscan cross. There are 19 cells in the and the remainder is usually retained to prototrochal band ofG. vulgaris; 16 are de­ form a horseshoe-shaped band on the dor­ rived from the trochoblasts (Iq") and 3 are sal head. Retractor muscles become func­ secondary, later additions probably from tional at metamorphosis and the anterior divisions of intermediate cells. "In the pos­ body, including head and metatroch, is re­ terior hemisphere the descendants of the tractable into the posterior trunk. 2d cells give rise to the somatic plate and most of the ectoderm of the trunk. Micro­ PELAGOSPHERA LARVA meres of the third quartette also form ec­ toderm and the macromeres 3A-3D give In the lecithotrophic pelagosphera (Fig. rise to both endoderm and mesoderm. 7), the lumen ofthe gut is not complete, the Mesoderm of the trochophore is derived anus not open and, even though the mouth from descendants of the 4d cell formed by a may be formed, the gut is not functional. laeotropic division of the 3D cell at the 64­ Larvae, as observed in the laboratory, may cell stage. swim through the water, or they ma y re­ main quiescent on the bottom or attached TROCHOPHORE LARVA to the substratum. Attachment is ac­ complished by the terminal organ, orin the The trochophore larva of sipunculans is absence ofthat organ, as in Themistealuta cea lecithotrophic, enclosed by the thick en­ (Fig. 7), the larva attaches presumably velope of the egg (Figs. 2, 3). It is charac­ through an adhesive secretion from glands, terized by an apical tuft and an equatorial not yet described, in the posterior body. band of prototrochal cilia. A pair of red After a pelagic or benthopelagic period ofa eyespots is present in a dorsolateral posi­ few days to two weeks, the larva loses its tion in the pretrochal hemisphere and in rnetatrochal cilia and gradually transforms the posttrochal hemisphere the ventral into the vermiform stage, finally assuming stomodaeum occurs just below the proto­ the form of the juvenile. troch. Differing from many pol ychaetes At the time of metamorphosis of the and so me molluscs, the sipunculan trochophore to the planktotrophic trochophore does not possess a protone­ pelagosphera, the mouth and anus are phridium. The trochophore of one species, opened with the rupture of the overlying Sipunculus nudus, is unique in that it is en­ egg envelope, and the gut, with lumen tirely enclosed by a layer of ciliated cells completed in initial metamorphic stages, is lying just beneath the egg envelope then full y de veloped (Figs. 8, 9). A ventral (Hatschek, 1883). Gerould (1903) has in­ ciliated groove extends from the anterior terpreted these cells to be homologous to end ofthe head to the mouth, resulting in a the prototroch of other species. bilobate ventral head. Ventral to the mouth F IG . 9. Planktotrophic pelagosphera larva from head of planktotrophic pelagosphera from open­ open-ocean plankton. Sipunculus sp. Live specimen. ocean plankton, te ntatively identified as be longing to Note extended head and expanded metatroch. Scale, the genus Siphonosoma. Scale, 50 u st». 3.0 mm . FIG . 12. Scanning electron micrograph of head of re­ FIG . 10. Scanning electron micrograph of ventral cently metamorphosed larva ofsame type as in Figure head of planktotrophic pelagosphera from open­ 8. Tentacles have developed from the ciliated larval ocean plan kton. Aspidosiphon sp. Scale, 50 /-L m . lobes surrounding the mo uth region. Scale, 50 /-L m. bo , buccal organ; 1, lip; Ig, pore of lip gland; mo , FIG. I I. Scanning e lectron micrograph of ven tral mouth; t, tentacles. 568 M ARY E. RICE is a pro truding lower lip which is usually Fisher (1947), usi ng number of muscle extende d at right angles to the head (Figs. bands as a taxonomic character, identified a 8, 10, II ). Two organs associated with the large, tran sparent pelagosphera from the mouth are the buccal organ and the lip Gulf Stream off Ca pe Hatte ras, North glands (Figs. 8, II). T he lip glan ds consist Carolin a as Sipuneulus polymyotus. Later of2 to 4 pe ndu lous lobes, sus pe nde d within Murina (1 96 5) id entifi ed two p el a go­ the coelom by a d uct ope ning to th e surface spheras, one from the Gulf of Aden as of the distal lip through a pore. A ciliated Sipunculus aequabilis a nd one from the groove between the pore and the mo uth Northwest Pacific as S. norvegieus. In a bifu rcates the vent ral lip . Secretion of th e com pa rative study of the morphology of lip gland has not been characterized. T he o pen-ocean p el agos pheras, H all an d bu ccal organ, a protrus ible muscul ar struc­ Schelte ma (1975) descri bed 10 larvae, but tu re located o n the floor of the mouth, has did no t make specific identificatio ns . been implicated in swa llowing of foo d as Cha racters by whic h larval forms ma y be well as in rejection of unwanted particles distinguish ed are size, sha pe, be havioral and in loosening of food mat erial from th e patterns, pigmentat ion patter ns, number su bstratu m prior to in gestion Uagersten, of eyes pots, arrangeme nt ofbody wall mus­ 1963; Rice, 1973). A well-defined, bulbous ' culatu re, numb er ofretractor muscles, and stomach is unique to th e plan ktotroph ic th e p re ~ e n c e and form ofcuticular papillae. pelagosp hera. T he intestine is looped , de­ For specific identification larvae must usu­ scendi ng posteriorly from the stomach, ally be reared to the post-juvenile stage. then anteriorly to the d orsal anus. In some larvae a pair of saccifo r m glands of un­ FO RMATION AND MORPHOLOGY OF LARVAL kn own fu nct ion ope ns on either side of th e CUT ICLE anus. T he re is a pair ofpigmented nephrid­ ia with openings to the exterior by way of Oceanic pelagosphera larvae have been ventrolateral nephridiopores and to the .grouped by J agersten (1963) as "ro ugh" or coelo m th ro ugh ciliated coelo mic fu n nels. "smooth" dependin g o n the presence or A single unpaired ventral nerve cord di­ absence of cutic ular elevations (Figs. 9, 13, vides in th e region of the lip glands to form 14). In "rough" larvae cuticular papillae are the circumesop hageal connectives which found in a variety of forms and patterns, continue dorsally to unite with the su pra­ each characteristic of a specific larval type esophageal gang lio n. Retractor muscles, (Figs. 13, 15, 16). T he form may be do me­ u sually fo u r in number, extend from th e shaped and smooth or mammiform with head region to the body wall ofthe trunk. A a pica l nipples, or papillae may consist of metatrocha l co llar, when fully ex panded as two or more tiers with flattened, ro unde d in swimming, is the widest part ofthe lar val or ta pered a pices, with either smooth or bod y; posteriorly it is bounded by a post­ rugose surfaces. met atroch al sph incte r (Fig. 9). A retracta­ In laborat ory stu dies of sip unc ula n d e­ ble term in al organ, usu all y se rv ing for velop ment it has been fo u nd that in 15 of a temporar y at tach ment to th e substratum, is total of 18 spec ies the cuticle of the lar va or present in most larvae. Planktotrophic vermifo rm stage is formed all, or at least in pelagosphera larvae have been reared in part, from transformation of th e egg en­ th e laboratory as long as 7 months at which velo pe. T wo of th e exceptions are Golfingia tim e th ey have atta ine d the size and fo rm of vu lgaris and Phaseolopsis gouldi, re ported to oceanic larvae. Me ta mo r phosis, however, shed the egg e nvelo pe at the time of has not been obse rve d in lab orator y-reared m etamo r phosi s of the trochopho r e planktotro phic larvae, but only in th ose col­ (Gerould, 1907). In Phascolion eryptus, a lected fr om ope n-ocean plankton (Fig. 12). species which d evelops directly, the pre­ Of th e numer ous reports on oceanic lar­ trochal egg envelope is lost as the embryo vae, only two have a ttem pted to assign transforms into th e ver miform stage while spec ific designat ions (See literat ure reviews the posttroch al envelo pe is retained as the by H all and Scheltema , 197 5; Rice, 1975a). cu ticle (Rice, 1975b). With th e exce p tion of DEVELOPMENT AND METAMORPHOSIS IN SIPUNCULA 569

FIGS. 13-14. Scanning electron micrographs of open-ocean plankton. Metamorphosis occurred in the planktotrophic pelagosphera larva and recently laboratory. Scale , 100 /Lm. metamorphosed juvenile of Aspidosiphon sp. From

Sipunculus nudus, all planktotrophic face elevations in the form of pa pillae simi­ pelagospheras retain the egg envelope as lar to those of later pelagosphera larvae of the larval cuticle. Sipunculus nudus is unique the open-ocean (Rice, 1973). in that the trochoblast cells spread an­ In sectioned material papillae appear teriorly and posteriorly on the inside ofthe different in composition from the underly­ egg envelope to surround the embryo with ing cuticle, as indicated by differences in a ciliated covering or "serosa" (Hatschek, staining and microstructure (Fig. 17). The 1883; Gerould, 1903). At trochophoral underlying cuticle of two oceanic larvae metamorphosis the entire serosa, cells and identified by rearing through metamor­ egg envelope, is cast off. phosis as species of Aspidosiphon and Para­ The egg envelope of all sipunculans is spidosiphon, when examined by transmis­ comprised of two or more layers and per­ sion and scanning electron microscopy re­ forated by pores. When retained at vealed an arrangement of fibers in layers metamorphosis of the trochophore, it un­ perpendicular to one another (Fig. 18). A dergoes a posttrochal elongation, losing its similar arrangement has been reported for lamellation and porosity; from the thick the cuticle of the adult sipunculan, Phasco­ rigid covering, with the characteristic shape lion strombi (Moritz and Storch, 1970) . In a ofthe egg, it is transformed into theexceed­ third oceanic larva, tentatively identified as ingly extensible and flexible cuticle of the a species of GolJingia, fibers are scattered early pelagosphera (Figs. 1-6). In species of irregularly throughout the underlying Phascolosorna studied in early development cuticle in no obvious pattern. Functional from laboratory spawnings, the cuticle in significance ofcuticular form and structure larvae of 3 to 4 weeks of age develops sur- remains to be investigated. 570 MARY E. RICE

FIG . 15. Scanning electron microgr aph of sur face Paraspidosiphon sp, Embedded in Epo n; staine d in cuticular papilla e of planktotrophic pel ag osphera methyen e blu e and Azure II. Note longitudinal mus­ from open-ocean plankton tentativel y identified as be­ cles (1m), circ ular muscl es (em) , epidermis (ep ) with longing to the gen us Phascolosoma. Scale, 2 /Lm. epidermal organ exte nding to the surface and lightly staining cut icle (cu) with darkly staining surface cuticu­ FIG. 16. Scanning electron micrograph of cuticular lar pap illae (p), Scale, 10 /Lm . papillae of ope n-oc ea n pel agosphera larva of As­ pidosiphon sp. The smaller papilla contains the duct of FI G. 18. Scanning electron micr ograph of a section, an epidermal o rga n, similar to that shown in Figure cut with razor, through the cuticle of a n ope n-ocea n 17. Scale, 5 /Lm. pelagosphera la rva, Aspidosiphon sp.(sa me type as in Fig. 16). No te surface papill ae (p) and underl ying cuti­ FIG. 17. Light micrograph ofa o ne-micro n sectlon of cle co mposed oflayers of cross ing fibers. Scale, 2/Lm. the body wall of an open-ocean pelagosphera larva,

METAM ORPHOSIS OF T HE PELAGOSPH ERA lower lip regresses and larval organs such as terminal organ, buccal organ, and lip Metamorphosis of the planktotrophic glands disappear, their fate not deter­ pelagosphera to the juvenile sipunculan is mined. It has been suggested that the duct marked by a loss of metatrochal cilia and an for th e lip glands ma y become the canal of elongation and growth ofthe body anterior the ventral sensory organ fou nd in the to the postmetatrochal sphincter to become adult ofman y species, but thi s remains to be the retractable introvert which in many verified (Akesson, 196Ib). species develops characteristic spines and The period of time over which these hooks (Figs. 13, 14). The mouth assu mes a metamorphic changes take place may vary terminal rather than ventral position and from I to 5 days. The specific or generic tentacular lobes are formed, usually around characters of the ad ult ma y not develop the rim of the mouth (Figs. II, 12). The full y, under laboratory conditions, for sev- DEVELOPMENT AND METAMORPHOSIS IN S IPUNCULA 57 1

eral weeks to several months after Fisher, W. K. 1947. New genera and species of metamorphos is. For example, the anterior echiuroid and sipunculoid worms. Proc. U.S. Nat. Mus . 97 (3218):351-372. and posterior horny shields characteristic Gerould,j. H . 1903. Studies on the embryology of the of the genera ofAspidosiphon and Paraspido­ Sipunculidae, I. The embryonal envelope and its siphon may require months to develop homologue. Mark Anniversary Volume, 439-452. (Scheltema and H all , 1965). And many Gerould ,J . H . 1907. Studies on the embryology of the species in which the absence of hooks is Sipunculidae, II . The development ofPhascolosoma . Zool. Jahrb. Abt. Anat. Ontog. Thiere 23 :77-162. used as a taxonomic character in the adult Hal l, j. R. and R. S. Scheltema. 1975 . Comparative possess h oo ks o n the introvert in the morphology ofopen-ocean peiagosphaera.In M. E. j u ven ile stage. Rice and M. Todorovic (eds.), Proceedings ofthe inter­ national symposium on the biology of the Sipuncula and Echiura, Vo!.-- I, pp. i83-197. Naucno Delo, CONCLUDING REMARKS Belgrade. Hatschek, B. 1883 . Ueber Entwicklung von Sipunculus Typical of other Spiralia, the Sipuncula nudus. Arb. Zool. Inst. Univ. Wien und Zool. Sta . exhibit spiral cleavage followed by a Triest 5:61 -140. Jagersten, G. 1963 . On the morphology and behavior trochophore larva. In yolk-rich eggs the of Pelagosphaera larvae (Sipunculoidea). Zool. Bid. micromeres may be larger t han the Fran Uppsala 36 : 27-35. macromeres in the A, B, and C quadrants, Mingazinni, P. 1905. Un Gefireo pelagico. Pelago­ the la rger size being related in later de ­ sphaera Aloysii n. gen., n. sp .Rendiconti delle sedute velopment to the n utritive function of solenni della R. Academia Nacionale dei Lincei 14: 713 -720 . yo lk-fi lled prototroch cells . Uniq ue to Moritz, K. and V. Storch. 1970. Uber den Aufbau des Sipuncula is a second lar val form whic h Integumentes der Priapuliden und der Sipunculi­ follows the trochophore in two of four de ­ den. Zeit. Zellforsch. mikrosk. Anat. 105: 55-64. velopmental patterns in the group, includ ­ Murina, V. V. 1965 . Some data on the structure of pelagospheres-sipunculid larvae. Zool. Zhurnal. ing the majority of species studied. This 44(1 1):16 10-1619. (In Russian) larva is the pelagosphera and may be either Rice, M. E. 1967 . A comparative study of the develop­ lecithotro phi c or planktotrophic. Plankto­ ment of Phascolosoma agassizii, Golfingia pugettensis, trophic pelagosphera lar vae may live in the and Them iste pyroides with a discussion of develop­ open ocean for prolonged periods. Some of mental patterns in the Sip uncula. Ophelia 4: 143­ 171. these lar vae are characterized by cuticu lar Rice, M. E. 1973 . Morphology, be havior, and his­ papillae of distinctive form and pattern. I n togenesis of the pe lagosphera larva of Phas colosoma the development of species with plankto­ agassizii (Sipuncula). Smithsonian Contributions to trophic pelagosphera larvae, there are two Zoology , No. 132: I-51. Rice, M. E. 1975a. Sipuncula.In A. C. Giese and j. S. distinct metamorphoses, one from the Pearse (eds .), Reproduction ofmarine invertebrates, Vol. trochophore to the pelagosphera and the II , Chapter 4, pp . 67-127. Academic Press, Inc., second from the pelagosphera to the New York. j uvenile. Rice, M. E. 1975b. Observations on the development of six species of Caribbean Sipuncula with a review of REFERENCES development in the phy lum. In M. E. Rice and M. Todorovic (eds .), Proceedings ofthe internationalsym­ Akesson, B. 1958. A studyof the nervous system ofthe posium on the biology of the Sipuncula and Echiura, Sipunculoideae with some remarks on the develop­ Vol. I, pp . 141-160 . Naucno Delo, Belgrade. ment of two species Phascolion strombi Montagu and Scheltema, R. S. and j. R. Ha ll. 1965 . Trans-oceanic Goljingia minuta Keferstein. Undersokningar over transport of sipunculid larvae belonging to the Oresund 38: 1-249. genus Phascolosoma. Amer. Zool. 5(2) :100 . (Abstr.) Akesson, B. 196 1a. The development ofGoljingia elon­ Selenka, E. 1875 . Eifurchung und larvenbildung von gata Keferstein (Sipunculidea) with som e remarks Phascolosoma elonga tu m Kef. Zeit. wiss . Zoo!' on the development of neurosecretory cells in 25:442-449. sipunculids. Ark. Zool. (Ser. 2) 13 (2): 511-53 1. Williams, J . 1972. Development of a rock burrowing Akesson, B. 196 1b. Some observations on Pelago­ sipunculid inhabiting stony coral. Amer. Zool. sphaera larva. Galathea Report 5:7- 17. 12(4):72 3. (Abstr.) ",