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Planktonic Dispersal of Juvenile Brittle Stars (Echinodermata: Ophiuroidea) on a Caribbean Reef

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Planktonic Dispersal of Juvenile Brittle Stars (Echinodermata: Ophiuroidea) on a Caribbean Reef BULLETIN OF MARINE SCIENCE, 65(1): 283–288, 1999 CORAL REEF PAPER PLANKTONIC DISPERSAL OF JUVENILE BRITTLE STARS (ECHINODERMATA: OPHIUROIDEA) ON A CARIBBEAN REEF Gordon Hendler, Carole C. Baldwin, David G. Smith and Christine E. Thacker ABSTRACT Juveniles of four species of shallow water ophiuroids were captured in a plankton net tethered on the reef flat at Carrie Bow Cay, Belize: Ophiothrix orstedii, Ophiothrix angulata, Ophiocoma wendtii, and Ophiactis savignyi. These water-borne animals were similar in size to the smallest benthic conspecifics found on the reef, but considerably larger than newly metamorphosed postlarvae. Thus, this first report of planktonic dis- persal by juvenile coral reef ophiuroids suggests that they reenter the plankton and drift, or perhaps raft on algal fragments, after first having recruited to the benthos. The occur- rence of water-borne juveniles in species with planktotrophic and abbreviated larval de- velopment, and with clonal, asexual reproduction suggests that postlarval drifting may augment larval dispersal in some ophiuroid species and substitute for it in others. It has been suggested that rafting dispersal, by adult marine invertebrates clinging to buoyant objects, prevails in cool waters where drift algae are abundant and float for long distances before deteriorating (Highsmith, 1985; Johannesson, 1988; Parker and Tunnicliffe, 1994). Long-distance larval dispersal may prevail in tropical waters where larvae can survive and delay metamorphosis for extended periods (Pechenik, 1980; Scheltema, 1995; Palumbi et al., 1997; Lessios et al., 1998). However, the geographic patterns of rafting and larval dispersal are more complex than suggested by that simplis- tic temperate-tropical dichotomy. They are shaped by the behavior and physiology of larvae and postlarvae (Yamaguchi, 1977; Pechenik, 1990) and other factors such as direc- tions and speeds of oceanic currents (Palumbi et al., 1997; Lessios et al., 1998). More- over, clonal and direct-developing organisms that lack larvae evidently depend largely on rafting for dispersal (Highsmith, 1985; Jackson, 1986; Johannesson, 1988). Thus, the question arises as to how benthic invertebrates with direct or clonal develop- ment disperse in the tropics where large drifting algae such as kelps are unavailable. The present report considers this situation for echinoderms, and describes a previously unre- ported phenomenon of planktonic dispersal by juvenile ophiuroids. In the discussion, the water-borne, juvenile ophiuroids are compared to “plantigrade” and “planktonic postlarva” stages (sensu Baker and Mann, 1997) of other marine invertebrates. MATERIALS AND METHODS The study site was at Carrie Bow Cay, a small coral-fringed island on the Belize Barrier Reef. A plankton net was fished off a pier on the reef flat seaward of the island in less than 1 m of water. The net was of 505 μm mesh, with a 1.0 × 0.5 m mouth that remained on or near the bottom. At that site, the bottom shoals and compresses the water layer flowing across the reef, thereby funneling most of the water column through the net. Samples, intended to capture larval and postlarval fishes, were taken at approximately 30–40 min intervals between sunset and midnight. Approximately 70 collections were taken from 5 to 15 September 1997 and examined for the presence of ophiuroids. We did not measure the speed 283 284 BULLETIN OF MARINE SCIENCE, VOL. 65, NO. 1, 1999 of the water flow and the volume of water sampled, but current speed near the study site averages 6 cm s−1 (Greer and Kjerfve, 1982). Catches of larval fishes were sparse compared to previous years, in part perhaps due to the short period between moonset and sunrise during the present study (Baldwin, Smith and Thacker, unpub. observ.). RESULTS Fish larvae, invertebrate holoplankters and meroplankters, and small pieces of algae and seagrass were the dominant items in the samples. The organisms captured were all planktonic. Benthic fauna such as decapods and polychaetes were not entrained in the net, nor did sediment accumulate. Five of 70 sets of the net on the reef flat yielded one individual each of juvenile Ophiothrix orstedii Lütken, Ophiothrix angulata (Say), and Ophiocoma wendtii Müller and Troschel, and two individuals of Ophiactis savignyi (Müller and Troschel) (Table 1). Most speci- mens were identified by comparing their pigmentation patterns and disk armament to that of adults of the respective species (Hendler et al., 1995), but O. wendtii was identi- fied by comparison with a growth series of that species. Unlike conspecific adults, it had a completely blackish-brown disk devoid of round granules, and arms uniformly stippled with reddish-brown. The water-borne individuals of the four species had a more intense coloration than is usually found in newly metamorphosed postlarval ophiuroids, which are sparsely pig- mented (Balser and Emlet, pers. comm.; Hendler, unpub. observ.). All the captured indi- viduals had juvenile morphological features such as the first ventral arm plates set out- side the mouth rather than enclosed within the oral slit as in adults. However, the mouth and stomach were sufficiently developed for the juveniles to feed. The ophiuroids collected in the plankton were larger in size than the smallest individu- als collected from benthic substrates. Table 1 shows the size of each specimen captured in this study and the range of size of conspecifics that were found in the alga Halimeda opuntia (Linnaeus) Lamouroux elsewhere on the same reef. The previously unpublished data on benthic individuals in algae are from the study by Hendler and Littman (1986), who found that clumps of Halimeda serve as an initial refuge habitat for small ophi- uroids. The individuals captured in reef plankton were considerably larger than the re- cently metamorphosed postlarval ophiuroids found in offshore plankton tows in the North Atlantic, which have a maximum disk diameter of 0.9 mm, an arm length of 2.0 mm, and up to five arm joints (Hendler, 1975). Table 1. The body dimensions of juvenile ophiuroids captured in plankton samples during this study at Carrie Bow Cay, Belize, and the sizes of benthic conspecifics found in Halimeda opuntia at the same study site by Hendler and Littman (1986). Sepecies Dat Disk Ahrm lengt Arm joints Size of collected diameter (mm) (no.) conspecifics (mm (mm) disk diam.) Ophiothrix angulata 141 Sept. 97 12. 66. 250. −6.6 Ophiothrix orstedii 165 Sept. 97 14. 70. 350. −8.7 Ophiactis savignyi 54Sept. 97 14. 69. 220. −2.8 Ophiactis savignyi 54Sept. 97 12. 63. 320. −2.8 Ophiocoma wendtii 114 Sept. 97 26. 86. 250. −13.0 HENDLER ET AL.: DRIFTING BRITTLE STARS 285 DISCUSSION A review of the relevant literature reveals that adult asteroids [A], echinoids [E], holothuroids [H], and ophiuroids [O], raft in cool waters as predicted by Highsmith (1985) and Johannesson (1988). Adult echinoderms on floating macroalgae have been reported from off Tasmania (Amphipholis squamata (Delle Chiaje) [O], Ophiothrix caespitosa Lyman [O], Pentacta australis (Ludwig) [H]); off the Auckland Islands (Amphiura magellanica (Ljungman)[O], Calvasterias suteri (de Loriol) [A]); off South Georgia Is- land (Amphiura lymani Studer [O]); and off Washington, USA (A. squamata [O], Leptosynapta clarki Heding [H])(Mortensen, 1925; Fell, 1953; Smirnov, 1979; Highsmith,1985; Edgar, 1987). In addition, kelp carried in the Benguela Current has transported South African echinoderm species to the tropical Atlantic vicinity of St. Hel- ena (Ophiothrix triglochis Müller and Troschel [O], Ophiactis carnea Ljungman [O], Parechinus angulosus (Leske) [E]) (Arnaud et al., 1976; but compare Mortensen, 1933). A number of ophiuroid species metamorphose before settling, giving rise to the post- larval ophiuroids that are found drifting in open water plankton. But these postlarvae, mentioned above, are not yet identified to species and are much smaller and less fully developed than benthic juveniles (Hendler 1975, 1991, and refs. therein). Thus, the ques- tion remains whether juvenile tropical echinoderms can disperse by rafting or drifting. Prior to this report, evidence for floating tropical ophiuroids was limited to the surprising reports of phoresy by Ophiocnemis marmorata (Lamarck) on several species of Indo- Pacific scyphomedusae (Marsh, 1998) and the occurrence of adult ophiuroids in rolling, demersal clumps of algae in the Gulf of Mexico (Holmquist, 1994). Our observations augment accumulating evidence that the life histories of some benthic invertebrates deviate from the classical two-phase pattern composed of a dispersing, plank- tonic larval stage that metamorphoses to a sedentary, bottom-dwelling juvenile stage. Currently, there are reports of a facultative, functionally distinct dispersal stage following metamorphosis and preceding the sedentary phase in numerous species of bivalves and polychaetes, some gastropods, several sea anemones, and a hermatypic coral (Levin, 1982; Richmond, 1985; Butman, 1987; Martel and Chia, 1991; Baker and Mann, 1997; Ri- emann-Zürneck, 1998). In some of these cases, the dispersers are non-planktonic, crawl- ing postlarvae (“plantigrade stage”) that are suspended in bedload sediment or in the water column. In other instances they are drifting “planktonic postlarvae”, kept in sus- pension by mucous or byssal threads (sensu Baker and Mann, 1997). The pigmentation of the small ophiuroids we collected and their size, approximately twice that of postlarvae that have metamorphosed in the water column (compare Hendler,
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