Biology of a “Babysitting” Symbiosis in Brittle Stars: Analysis of The
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Invertebrate Biology 126(4): 385–395. r 2007, The Authors Journal compilation r 2007, The American Microscopical Society, Inc. DOI: 10.1111/j.1744-7410.2007.00108.x Biology of a ‘‘babysitting’’ symbiosis in brittle stars: analysis of the interactions between Ophiomastix venosa and Ophiocoma scolopendrina Didier Fourgon,1 Michel Jangoux,1,2,3 and Igor Eeckhaut2,3,a 1 Marine Biology, Free University of Brussels, 1050 Brussels, Belgium 2 Marine Biology, University of Mons-Hainaut, 7000 Mons, Belgium 3 Aqua-Lab, Institut Halieutique et des Sciences Marines, BP 141 Toliara, Madagascar Abstract. ‘‘Babysitting’’ symbioses between brittle star species involve juveniles of one species and adults of another. During this phenomenon, reported from many localities in the Indo- Pacific Ocean, juveniles are attached to the disk or lie in the bursa of the adults. The symbiosis between members of Ophiomastix venosa and their host, Ophiocoma scolopendrina, was in- vestigated on the Great Barrier Reef of Toliara (Madagascar) during a 14-month period. The population of O. scolopendrina only occurs on rocky spurs that frequently emerge at low tide, while the population of O. venosa lies in adjacent surge channels that are always immersed. Only juveniles of O. venosa associated with adults of O. scolopendrina may occur on the rocky spurs. Analyses conducted on the populations of the two species showed that (1) the sym- biosis is facultative and that symbiotic juveniles migrate into the channels when they reach a disc diameter of 6 mm, and (2) recruitment in the channels occurs in April. Host choice ex- periments, Y-tube experiments, and experiments assessing the resistance of the ophiuroids to air-drying were conducted in the laboratory. The experiments clearly demonstrated that (1) symbiotic juveniles of O. venosa specifically recognize adults of O. scolopendrina, while free juveniles of the same size do not, and (2) juveniles of O. venosa would not survive air-drying conditions similar to those observed on the spurs at low tides if they were not in symbiosis with adults of O. scolopendrina. Additional key words: symbiosis, commensalisms, echinoderm, ophiuroid ‘‘Babysitting’’ symbiosis in brittle stars concerns subtidal. According to Hendler et al. (1999), symbi- juveniles of one species and adults of another species. otic ophiuroids must avoid desiccation, overheating, During this phenomenon, reported from many local- and isolation. It would seem advantageous for these ities in the Indo-Pacific Ocean, juveniles are attached juveniles to take refuge within large, abundant, wide- to the disk or lie in the bursa of the adults. ‘‘Baby- spread, mobile, calcified animals that occupied moist, sitting’’ symbiosis between the subtidal populations sheltered crevices. Their results, however, do not al- of Ophiomastix annulosa and the intertidal popula- low them to find selective advantages that would ex- tions of Ophiocoma scolopendrina (LAMARCK 1816) plain why it is advantageous for subtidal symbiotic was first studied by Hendler et al. (1999) at Sesoko ophiuroids to recruit to the intertidal. Island (Okinawa, Japan). These authors found that A similar inter-ophiuroid symbiosis was observed juveniles of O. annulosa were usually in the bursae of on the barrier reef of Toliara (Madagascar) between the hosts while a few others were attached to their juveniles of Ophiomastix venosa PETERS 1851 and disk. They suggested that members of Ophiomastix adults of O. scolopendrina. Investigations made on species in general would be found to be associated the reproductive cycles of both ophiuroids indicated with members of Ophiocoma species, and that juve- that members of O. scolopendrina reproduce contin- niles of O. annulosa may always be symbiotic with uously and that they have a planktotrophic larva, adults of O. scolopendrina before they move into the while individuals of O. venosa breed once a year in the austral summer, mainly in January–February (Fourgon 2006). Members of O. venosa have a le- a Author for correspondence. citotrophic larva that metamorphoses spontaneously E-mail: [email protected] after 2 d of development in cultures (Fourgon et al. 386 Fourgon, Jangoux, & Eeckhaut 2005). Yet, analyses of the natural abundance of car- bon and nitrogen stable isotopes were performed to investigate the feeding habits of the two ophiuroids and their symbiotic juveniles (Fourgon et al., 2006). The results suggest that symbiotic juveniles steal ne- uston from their host, O. scolopendrina. The present article aims to explain why juveniles of the subtidal species, O. venosa, are found in associa- tion with adults of the intertidal species, O. scolopen- drina and it explores the reasons why this symbiosis is specific. It presents the results of a 14-month survey conducted on the populations of the two species. It also further investigates this symbiosis by laboratory experiments that were conducted to study (1) the host choice shown by ophiuroid symbionts, (2) the degree of recognition of host odors by ophiuroid symbionts, and (3) the tolerance of ophiuroid symbionts to air- drying conditions similar to those they face in the in- tertidal. Methods In situ observations Members of Ophiomastix venosa and Ophiocoma scolopendrina occur in the boulder tract of the barrier reef of Toliara (Madagascar) (Fig. 1; see Clausade et al. 1971 for a detailed description of the Toliara bar- Fig. 1. A. Map of the Great Barrier Reef of Toliara with rier reef). There, rocky spurs alternate with surge the location of transect sites (A–E). B. Schematic transverse channels, in parallel to each other and perpendicular section of study site C. c, channel; s, spur; fr, fringing reef; to the external reef slope. Spurs and surge channels grt, Great Barrier Reef of Toliara; wl, water level at low tide. continue r20 m deep into the subtidal. At the inter- tidal level, spurs are B100 m long and 10 m wide. They consist of rocks of dead corals emerging at low and the southern adjacent spur. This site was then tides. Surge channels are permanently immersed investigated monthly from March 2000 to April 2001 (channel width: B30 m; water height at low tide: at low tide: each month, eight 1-m2 quadrats were B50 cm) and their bottom consists of sand with liv- placed on the spur and eight others in the channel; all ing and dead corals. the ophiuroid species, as well as the occurrence of Ophiuroids were collected at low tide by hand. At symbiotic juveniles of O. venosa on adults of O. first, transects were performed at five different sites scolopendrina or other species were recorded. Disc along the barrier reef in February 2000 (Fig. 1A–E). diameters (DDs) of symbionts and hosts were mea- Each of the transects consisted of four 1-m2 quadrats sured in the field using a calliper and the number of haphazardly placed on the spurs and four others in symbionts per host was noted. Yet, each month, the the channels (40 quadrats in total). All dead coral DD of the individuals that were found in one (for O. rocks were removed and analyzed to ensure that all scolopendrina) to up to ten quadrats (for O. venosa) ophiuroids were counted. The occurrence of the in- was measured (4180 individuals of both species were ter-ophiuroid symbiosis was recorded and the prev- measured each month). Yet, because juveniles of O. alence (i.e., the percentage of hosts associated with at venosa were also found in the host’s bursae, and be- least one symbiont individual) was calculated. The cause it was difficult to dissect individuals in the field, prevalences were statistically equal in transects A, B, a minimum of 180 individuals of O. scolopendrina D, and E, but significantly higher in transect C was dissected monthly in the laboratory, and the bur- (Mann–Whitney U Test, po0.05). The latter was sal infestation was recorded. thus selected as the study site for the inter-ophiuroid To determine recruitment events in the popula- symbiosis. The investigated area comprises a channel tion of O. venosa, monthly disk-size frequency Invertebrate Biology vol. 126, no. 4, fall 2007 Babysitting brittle star symbiosis 387 distributions were generated by pooling individuals were conducted using 120 ophiuroids (30 ophiuroids in size classes of 2 mm. Size-frequency data were first for each of the four types). Each trial lasted 15 h, at tested against a normal distribution (Kolmogorov– the end of which the position of the juvenile in rela- Smirnov test); any deviation from normality would tion to the co-occurring adults was recorded. Juve- indicate possible multimodality. When multimodality niles tested could be found (1) alone without was suspected, separation of the observed polymodal touching any of the two adults, (2) in loose contact length–frequency distributions into component nor- with any part of any of the two adults, or (3) firmly mal distributions (subgroups) was achieved by attached to any part of any of the two adults. C.A.MAN program (Bo¨hning et al. 1992: freely Y-tube experiments. This assessed the ability of ju- available at www.medizin.fu-berlin.de/sozmed/caman. veniles of O. venosa to recognize water flows condi- html). This program estimates finite mixtures of dis- tioned by either O. scolopendrina or O. venosa. The tributions using the maximum-likelihood method. experimental system used was a Y-tube system adapt- Information such as the number of population sub- ed from Davenport (1950). It consisted in a Y-shaped groups, their mean values, and relative sizes ex- glass tube, 3 cm in diameter, whose branches each pressed as weights, was extracted from the length– measured 10 cm long. The paired branches were con- frequency data. The information generated by nected to two separate aquaria (17 Â 17 Â 10 cm; C.A.MAN was used as initial values in the MIX pro- aquaria A and B; Fig.