Sipuncula (Peanut Worms) from Bocas Del Toro, Panama

Home , Aspidosiphonidae, Aspidosiphon elegans, Phascolosomatidae

Sipuncula (Peanut Worms) from Bocas del Toro, Panama

ANJA SCHULZE

Smithsonian Marine Station, 701 Seaway Drive, Fort Pierce, FL 34949; [email protected] or [email protected]

ABSTRACT.—In a survey of sipunculan diversity in the Bocas del Toro (Panama) region, sipunculans were collected from 10 stations, ranging in depth from intertidal to 37 m. Nineteen species of adult sipunculans were collected. In addition, two types of pelagic sipunculan larvae were retrieved from plankton tows. Thirteen of the adult sipunculan species were inhabitants of hard substrate, either in crevices or burrowing into rocks. These included representatives of the genera Antillesoma, Aspidosiphon, Golfingia, Nephasoma, Phascolosoma, Phascolion and Themiste. An unidentified Phascolion, an unidentified Aspidosiphon and Antillesoma antillarum (the latter usually an inhabitant of rock crevices) were retrieved from gastropod shells. Sipunculidae sp., Sipunculus sp., Phascolion sp. and Nephasoma cf. eremita were recovered by trawling in soft mud. While the hard-substrate sipunculans are all well-known and widely distributed species, three of the four soft-substrate inhabitants were morphologically unusual and/or unexpected in tropical waters.

KEYWORDS.—Peanut worms, invertebrate, Caribbean, larvae, pelagosphera, diversity

INTRODUCTION burrows in coral or other rocks and in a variety of abandoned mollusc shells, Sipuncula (common name: peanut worms) polychaete tubes and foraminiferan tests are exclusively marine worm-like animals. (Cutler 1994). One species has been re- The body consists of an unsegmented trunk ported from decaying whale bones (Gibbs and a retractable introvert, usually with an 1987). array of tentacles at its distal end. Sipun- Many sipunculans have long-lived cula are currently recognized as a phylum planktotrophic larvae, enabling them to and seem to be most closely related to disperse over long distances (Rice 1981). molluscs and/or annelids although sister Larvae are morphologically diverse but group relationships have not yet been un- only a few are currently identifiable to spe- ambiguously resolved (Maxmen et al. cies (Fisher 1947; Hall and Scheltema 1966). 2003). With only ca. 150 recognized species; This contribution is the first survey of there is relatively low within-phylum di- sipunculan diversity including larvae and versity. Although Sipuncula are known adults from Bocas del Toro, Panama. from all major oceans, depths and climatic zones (Cutler 1994), tropical and subtropi- cal shallow waters probably show the high- MATERIALS AND METHODS est sipunculan diversity, often with a few species in very high abundance (Rice 1975; Sampling was conducted during the sec- Rice et al. 1983, 1995). Despite high abun- ond Invertebrate Taxonomy workshop Au- dance, Sipuncula are often neglected in fau- gust 2-12, 2004 and by trawling from the nal surveys, mainly due to two facts: 1. R/V Urraca on Aug. 30, 2004. The adults They inhabit cryptic habitats and 2. Species collected during the invertebrate workshop identification can be challenging for non- were, with three exceptions, retrieved from experts. Sipunculans have been reported coral rubble. Pieces of rubble were picked from sand and mud, crevices in or under- up by wading in the intertidal zone or, if neath rocks, within algal masses and deeper, by snorkeling or scuba diving. sponges, mangrove and seagrass roots, Sipuncula were removed either from crev- 523 524 ANJA SCHULZE ices underneath the rocks or from burrows Family Golfingiidae inside the rock. The burrowing specimens were extracted by cracking the rocks with Golfingia elongata (Keferstein, 1862): see hammer and chisel and removing the Plate 1 (top) for description, distribution worms with forceps. Abandoned gastro- and notes. pod shells were also examined for the pres- Nephasoma cf. eremita (Sars, 1851) ence of sipunculans. Larvae were retrieved from two plankton tows near the dock of Trunk 30-40 mm long, max. 5 mm wide, the Smithsonian field station. For collecting smooth. Introvert about as long as trunk stations, see Table 1 and Fig. 1. The samples and without hooks. Two introvert retractor collected during the R/V Urraca cruise were musles. Approximately 40 tentacles. collected by trawling. Notes.—The two specimens found match the descriptions of N. eremita given by Cut- ler (1994) and Stephen and Edmonds (1972) RESULTS but the species has only been recorded from cold, deep water before. Its known Nineteen species of adult Sipuncula and distribution comprises the arctic and tem- two types of planktonic larvae were col- perate North Atlantic as well as the Antarc- lected in the Bocas del Toro area (Table 1). tic and Subantarctic below 80 m.

Family Sipunculidae Nephasoma pellucidum (Keferstein, 1865) Sipunculidae sp. Trunk up to 25 mm, introvert slightly shorter than trunk. Scattered hooks usually Trunk approximately 50 mm long and 10 present. 20-30 tentacles. Body uniformly mm wide. Body wall of trunk transparent covered with papillae. with distinct longitudinal and circular Distribution.—Widespread in the Indo- muscle bands. Midsection of trunk with Pacific, western Atlantic and Caribbean; bulbous papillae or coelomic extensions, fairly common. arranged regularly along the circular muscle bands and between the longitudinal muscle bands. Introvert approximately 10 Family Phascolionidae mm and with numerous large, scale-like Phascolion (Isomya) gerardi Rice, 1993: see papillae pointing posteriorly. Large num- Plate 1 (2nd from top) for description, dis- bers of short tentacles. tribution and notes. Notes.—The organization of the body wall musculature places the species in the Phascolion (Isomya) sp. Sipunculidae but the texture of the body Trunk 50 mm long, introvert longer than wall and the tentacles do not match the de- trunk. Body wall very thick, strongly scriptions of any of the genera. wrinkled with large scattered papillae. Color tan with patchy black pigment, espe- Sipunculus sp. cially on introvert. No tentacles or hooks observed. Body wall musculature split into Only posterior fragment recovered. Body strongly anastomosing bands. wall with longitudinal and circular muscu- Notes.—Although the presence of only a lature in bands. 28 longitudinal muscle single nephridium and the fusion of the re- bands. tractor muscles into one dorsal and one Notes.—It is likely that the fragment be- ventral muscle of approximately equal longs to one of the Sipunculus species re- strength place the single recovered speci- ported from the Caribbean. The number of men into Phascolion (Isomya), the large size longitudinal muscle bands suggests that it of the animal and the structure of the body is S. nudus or S. robustus. wall are very unusual. TABLE 1. Collecting stations for adult Sipuncula in Bocas del Toro and species collected. sp. sp. IUCL RMBCSDLTR 525 TORO DEL BOCAS FROM SIPUNCULA sp. sp. sp.

Depth

Station Date Location name Habitat (m) Latitude Longitude Antillesoma antillarum Aspidosiphon elegans Aspidosiphon fischeri Aspidosiphon laevis Aspidosiphon parvulus Aspidosiphon steenstrupii Aspidosiphon Golfingia elongata Lithacrosiphon cristatus Nephasoma cf. eremita Nephasoma pellucidum Phascolosoma nigrescens Phascolosoma perlucens Phascolion gerardi Phascolion (Isomya) Phascolion (Lesenka) Sipunculidae Sipunculus Themiste alutacea 2 8/2/04 Hospital Point Coral rubble 2-3 N 09°20.011Ј W 082°13.113Ј xxx x 3 8/2/04 Mangrove Inn Coral rubble 2-5 N 09°19.876Ј W 082°15.295Ј xxxxx 5 8/3/04 Almirante pilings Gastropod shell 0-1 N 09°16.218Ј W 082°23.382Ј x with pagurid 9 8/3/04 Solarte Norte Coral rubble 2-6 N 09°21.071Ј W 082°15.423Ј xx xx (= Cayo Nancy) 16 8/5/04 Playa del Drago Coral rubble 2-4 N 09°25.605Ј W 082°19.501Ј x xx x xxxx x 21 8/6/04 Crawl Cay Coral rubble 4-5 N 09°15.261Ј W 082°07.787Ј xx xxx 22 8/6/04 Zapatilla Coral rubble 5-9 N 09°15.891Ј W 082°03.460Ј xxx x 41 8/9/04 Emilio’s Beach Nassarius shell 0-1 N 09°22.050Ј W 082°14.341Ј x 42 8/9/04 Drago, off resort Coral rubble, 0-1 N 09°25.605Ј W 082°19.501Ј xxxxxxxxx area gastropod shell Urraca 8/30/04 Mud 33-37 N 09°28.472’- W 082°18.329Ј- xxxx Stn.5 N09°28.260Ј W 082°17.969Ј 526 ANJA SCHULZE

Aspidosiphon (Paraspidosiphon) steenstrupii Diesing, 1859: Plate 2, bottom

Aspidosiphon sp.

Trunk 6 mm. Body wall transparent without obvious longitudinal muscle bands. Anal shield with longitudinal grooves, caudal shield with radial grooves. Hooks or tentacles not observed. Notes.—The single specimen shared an abandoned gastropod shell with a pagurid. Although several Aspidosiphon species inhabit discarded gastropod shells, an asso- ciation with hermit crabs has never been reported.

Lithacrosiphon cristatus (Sluiter, 1902): Plate 3, top FIG. 1. Maps of Panama and of the Bocas del Toro area with collecting stations as in Table 1. Phascolion (Lesenka) sp. Family Phascolosomatidae

Small sipunculan (trunk 10 mm), recov- Antillesoma antillarum (Grübe and Oersted, ered from a gastropod shell. The subgenus 1858): Plate 3, 2nd from top is characterized by the complete fusion of Phascolosoma nigrescens (Keferstein, 1865): the four introvert retractor muscles. The Plate 3, 3rd from top only specimen recovered in Bocas del Toro Phascolosoma perlucens (Baird, 1868): Plate 3, bears abundant papillae on the base of the bottom introvert and anterior trunk but no hard- ened holdfast papillae that are otherwise Larvae common in the shell-inhabiting representatives of this genus. Approximately 10 ten- Sipunculan pelagosphera larvae can be tacles and scattered hooks on anterior in- relatively easily recognized by the follow- trovert. ing characteristics: 1. Retractable head, 2. A single transverse ciliary band (meta- Family Themistidae troch), 3. Head with a lower lip. Two larval types were collected from plankton tows in Themiste alutacea (Grübe and Oersted, Bocas del Toro: 1858): see Plate 1 (3rd from top) for description, distribution and notes. Small Transparent larva

Family Aspidosiphonidae This larval type is about 1 mm long, with a more or less spherical trunk and a strong Aspidosiphon elegans (Chamisso and Eysen- constriction between the trunk and the hardt, 1851): Plate 1, bottom head. The body wall is transparent and the Aspidosiphon (Paraspidosiphon) fischeri ten body wall musculature is organized in Broeke, 1925: Plate 2, top bands, although not easily discernible. The Aspidosiphon (Paraspidosiphon) laevis de larva corresponds to the “Type B” larva of Quatrefages, 1865: Plate 2, 2nd from top Hall and Scheltema (1975) and to the Aspidosiphon (Paraspidosiphon) parvulus Ger- “Smooth” larva type “A” of Jägersten ould, 1913: Plate 2, 3rd from top (1963). The species is unknown. SIPUNCULA FROM BOCAS DEL TORO 527

Transverse Groove larva tion for supporting my collecting efforts. I also thank all participants of the second This larval type varies in color from Invertebrate Taxonomy workshop for help translucent yellow-tan to blue-green. It is in the field and cheerful company. Mary E. 1-1.5 mm long with an elongated body and Rice, José Ignacio Saiz Salinas and an without a deep constriction between head anonymous reviewer provided helpful and trunk. The body wall forms incomplete comments on the manuscript (Smithsonian transverse grooves. This larval type corre- Marine Station at Fort Pierce contribution sponds to “Type E” by Hall and Scheltema number 612). (1975) and belongs to Siphonosoma cumanense (Rice, 1988). LITERATURE CITED The Sipuncula. Their systematics, biol- DISCUSSION Cutler, E. B. 1994. ogy and evolution. Ithaca, N.Y.: Cornell Univ. Press. The thirteen species that were retrieved Fisher, W. K. 1947. New genera and species of Echiu- ridae and Sipunculid worms. Proc. USNM, Smiths. from hard substrates are all well known Inst. 97:351-372. and widespread in the Caribbean and be- Gibbs, P. E. 1987. A new species of Phascolosoma yond. The only unusual observation was (Sipuncula) associated with a decaying whale’s the presence of a single individual of An- skull trawled at 880 m depth in the South-west tillesoma antillarum in a gastropod shell Pacific. N.Z. J. Zool. 14:135-137. (Stn. 41, Table 1). The other two inhabitants Hall, J. R., and R. S. Scheltema. 1966. Morphology of North Atlantic sipunculid larvae. Amer. Zool. 6:193. of gastropod shells could not be identified Hall, J. R., and R. S. Scheltema. 1975. Comparative to species, but the habitat is common for morphology of open-ocean pelagosphera. In Pro- members of their respective genera. Of the ceedings of the International Symposium on the Biology four soft-substrate inhabiting species, only of the Sipuncula and Echiura, ed. M. E. Rice, and M. the occurrence of a Sipunculus was ex- Todorovic´, 183-197. Kotor: Naucˇno Delo Press. pected. The other three species were either Jägersten, G. 1963. On morphology and behavior of morphologically unusual or outside of their pelagosphaera larvae (Sipunculoidea). Zool. Bidr. Uppsala 36:27-36. known geographical range. Maxmen, A. B., B. F. King, E. B. Cutler, and G. Giribet. During the workshop, there was a sam- 2003. Evolutionary relationships within the proto- pling bias toward hard substrates. It is pos- stome phylum Sipuncula; a molecular analysis of sible that more shallow-water sand- ribosomal genes and histone H3 sequence data. borrowing species are present in the area Mol. Phylogenet. Evol. 27:489-503. but have not been recovered. Attempts to Rice, M. E. 1975. Survey of the Sipuncula of the coral retrieve sipunculans from sandy and and beach rock communities of the Caribbean Sea. In Proceedings of the International Symposium of muddy substrates around the Smithsonian Sipuncula and Echiura, ed. M. E. Rice, and dock and Mangrove Inn (Stn. 3) were fruit- M. Todorovic´, 35-49. Belgrade: Naucˇno Delo Press. less. Sand-borrowing sipunculans usually Rice, M. E. 1981. Larvae adrift: patterns and problems occur in lower density than hard-substrate in life histories of sipunculans. Am. Zool. 21:605- species, making collection efforts less effi- 619. cient. Rice, M. E. 1988. Observations on development and The presence of the Transverse Groove metamorphosis of Siphonosoma cumanense with comparative remarks on Sipunculus nudus (Sipun- larva suggests that the common sand- cula, Sipunculidae). Bull. Mar. Sci. 42:1-15. burrowing Siphonosoma cumanense might be Rice, M. E., J. Piraino, and H. F. Reichardt. 1983. Ob- present in the area. However, the larvae servations on the ecology and reproduction of the might have originated in other parts of the sipunculan Phascolion cryptus in the Indian River Caribbean and might have drifted into the Lagoon. Fla. Sci. 46:382-396. archipelago. Rice, M. E., J. Piraino, and H. F. Reichardt. 1995. A survey of the Sipuncula of the Indian River La- goon. Bull. Mar. Sci. 57:128-135. Acknowledgments.—Many thanks to Stephen, A. C., and S. J. Edmonds. 1972. The phyla Rachel Collin and the competent and Sipuncula and Echiura. London: Trustees British friendly staff at the Bocas del Toro field sta- Mus. (Nat. Hist.).