FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. 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).