Abstract
The present paper characterizes, for the first time, the diet of the Harlequin crab Lissocarcinus orbicularis, an obligate symbiotic crab that associates with sea cucumbers (holothuroids) belonging to the genera Thelenota, Bohadschia and Holothuria. These tropical holothuroids host a rich symbiotic community in the Indo-West Pacific Ocean of which the Harlequin crab is the best known. The diet of L. orbicularis was characterized by analyzing the microscopic, molecular and isotopic signatures obtained from its gastric content. The presence of sea cucumber ossicles in the gastric mills of the crabs suggests that symbionts eat the superficial integument of their host and this was supported by the fact that Holothuroid DNA was detected in the stomach of L. orbicularis after DGGE and sequencing of the 18S rDNA gene. The stable isotopic δ13C and δ15N values of crab tissues were compared with diverse potential food sources including three holothuroids, three algae, one sea grass as well as the organic matter contained in the water column, in the sediment, and the second most abundant symbiont, the polychaete Gastrolepidia clavigera. The low δ15N values of crabs suggests that the crabs do not exclusively feed on sea cucumber tissue but assimilate diverse food sources such as sea grasses and organic matter contained in sediment that have similar δ13C values. There were no differences between the feeding of males and females but there was a positive correlation between the carapace length and the stable isotopic values indicating a shift of the food source as crabs grow larger.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2
Bliss DE, Mantel LH (1985) Integument, pigments and hormonal processes. In: Bliss DE (ed) The biology of crustaceans. Academic, New York, p 549
Bodin N, Le Loc’h F, Hily C (2007) Effect of lipid removal on carbon and nitrogen stable isotope ratios in crustacean tissues. J Exp Mar Biol Ecol 341:168–175. doi:10.1016/j.jembe.2006.09.008
Britaev TA, Lyskin SA (2002) Feeding of the symbiotic polychaete Gastrolepidia clavigera (polynoidae) and its interactions with its hosts. Dokl Biol Sci 385:352–356. doi:10.1023/a:1019964918471
Caulier G, Parmentier E, Lepoint G, Van Nedervelde F, Eeckhaut I (2012) Characterization of the population of the Harlequin crab, Lissocarcinus orbicularis Dana, 1852, an obligate symbiont of holothuroids, in Toliara bay (Madagascar). In: Kroh A, Reich M (eds) Echinoderm Research 2010: Proceedings of the Seventh European Conference on Echinoderms, Göttingen, Germany, 2–9 October 2010. Zoosymposia, 7, pp 316
Caulier G, Flammang P, Gerbaux P, Eeckhaut I (2013) When a repellent becomes an attractant: harmful saponins are kairomones attracting the symbiotic Harlequin crab. Sci Rep 3:2639. doi:10.1038/srep02639
De Bruyn C, Rigaud T, David B, De Ridder C (2009) Nature and consequences of the symbiotic relationship between the crab Dissodactylus primitivus and its echinoid host Meoma ventricosa. Mar Ecol Prog Ser 375:173–183. doi:10.3354/meps07733
Deniro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351. doi:10.1016/0016-7037(81)90244-1
Diez B, Pedrós-Alió C, Marsh TL, Massana R (2001) Application of denaturing gradient gel electrophoresis (DGGE) to study the diversity of marine picoeukaryotic assemblages and comparison of DGGE with other molecular techniques. Appl Environ Microbiol 67:2942–2951. doi:10.1128/aem.67.7.2942-2951.2001
Eeckhaut I, Jangoux M (1993) Integument and epidermal sensory structures of Myzostoma cirriferum (myzostomida). Zoomorphology 113:33–45. doi:10.1007/bf00430975
Eeckhaut I, Parmentier E, Becker P, Gomez da silva S, Jangoux M (2004) Parasites and biotic disease in field and cultivated sea cucumbers. In: Lovatelli A (ed) Advances in sea cucumber aquaculture and management. pp 311–326. FAO Technical Paper, Roma
Gotto RV (1979) The association of copepods with marine invertebrates. Adv Mar Biol 16:1–109
Jangoux M (1984) Diseases of echinoderms. Helgoländer Meeresun 37:207–216. doi:10.1007/bf01989305
Jossart Q, David B, De Bruyn C, De Ridder C, Rigaud T, Wattier RA (2013) No evidence of host specialization in a parasitic pea-crab exploiting two echinoid hosts. Mar Ecol Prog Ser 475:167–176. doi:10.3354/meps10131
Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27. doi:10.1139/cjz-78-1-1
Kornienko ES, Korn OM (2004) Morphological features of the larvae of spider crab Pugettia quadridens (decapoda: Majidae) from the northwestern sea of japan. Russ J Mar Biol 30:402–413. doi:10.1007/s11179-005-0027-4
Lee SY (1995) Cheliped size and structure: the evolution of a multi-functional decapod organ. J Exp Mar Biol Ecol 193:161–176. doi:10.1016/0022-0981(95)00116-6
Loc’h FL, Hily C (2005) Stable carbon and nitrogen isotope analysis of Nephrops norvegicus / Merluccius merluccius fishing grounds in the bay of biscay (northeast atlantic). Can J Fish Aquat Sci 62:123–132. doi:10.1139/f04-242
Mccutchan JH Jr, Lewis WM Jr, Kendall C, Mcgrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390
Ng PKL, Jeng MS (1999) The brachyuran crabs (crustacea: Decapoda: Eumedonidae and portunidae) symbiotic with echinoderms in taiwan. Zool Stud 38:268–274
Parmentier E, Das K (2004) Commensal vs. Parasitic relationship between carapini fish and their hosts: some further insight through δ13C and δ15N measurements. J Exp Mar Biol Ecol 310:47–58. doi:10.1016/j.jembe.2004.03.019
Parmentier E, Michel L (2013) Boundary lines in symbiosis forms. Symbiosis 60:1–5. doi:10.1007/s13199-013-0236-0
Telford M (1982) Echinoderm spine structure, feeding and host relationships of four species of Dissodactylus (brachyura: Pinnotheridae). Bull Mar Sci 32:584–594
Vaïtilingon D, Eeckhaut I, Fourgon D, Jangoux M (2004) Population dynamics, infestation and host selection of Vexilla vexillum, an ectoparasitic muricid of echinoids, in Madagascar. Dis Aquat Org 61:241–255. doi:10.3354/dao061241
Vandenspiegel D, Ovaere A, Massin C (1992) On the association between the crab Hapalonotus reticulatus (Crustacea, Brachyura, Eumedonidae) and the sea cucumber Holothuria (Metriatyla) scabra (Echinodermata, Holothuridae). Bull K Belg Inst Nat Wet 62:167–177
Vannini M, Innocenti G (2000) Research on the coast of Somalia. Portunidae (crustacea brachyura). Trop Zool 13:251–298. doi:10.1080/03946975.2000.10531136
Warner GF (1977) The biology of crabs. Elek Science, London, 202pp
Westblad E (1949) On Meara stichopi (Bock) Westblad, a new representative of turbellaria archoophora. Ark Zool 1:43–54
Acknowledgments
The authors kindly thank Dr. Claude Massin for holothuroids ossicles identification and Prof. David Richardson for improving the english of this manuscript. GC benefited from a Fonds National de la Recherche Scientifique (FRIA) grant and a FNRS travel grant. G.L. is Research Associate at FRS-FNRS. This work is a contribution of the CIBIM (University of Mons, Brussels, Liège (Belgium), the Polyaquaculture Research Unit (IH.SM, Toliara, Madagascar)) and the MARE center (University of Liège).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Caulier, G., Lepoint, G., Van Nedervelde, F. et al. The diet of the Harlequin crab Lissocarcinus orbicularis, an obligate symbiont of sea cucumbers (holothuroids) belonging to the genera Thelenota, Bohadschia and Holothuria . Symbiosis 62, 91–99 (2014). https://doi.org/10.1007/s13199-014-0274-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-014-0274-2