symbiosis; echinoderms; chemical communication; stable isotopes; Madagascar
Abstract :
[en] Tuleariocaris holthuisi and Arete indicus are two ectocommensal shrimps closely associated with the tropical sea urchin Echinometra mathaei. This study provides a comparison of these two E. mathaei symbiotic crustaceans and particularly focuses on the relationship between T. holthuisi and its host’s pigments (i.e. spinochromes), and its dependency on its host. While all the analyses underline a close association between A. indicus and E. mathaei, they reveal a particularly close interaction between T. holthuisi and its host. Chemical analyses reveal that these shrimps present the same spinochrome composition as E. mathaei, and have similar colouration, allowing camouflage. Isotopic composition and pigment loss after host separation suggest that these pigments are certainly assimilated upon feeding on the urchin. Moreover, symbiont isolation experiments demonstrate the high dependency of T. holthuisi on its host and the importance of the host’s pigments on their survival capacity. Finally, some host recognition mechanisms are investigated for T. holthuisi and show the probable implication of spinochromes in host selection, through chemical recognition. Hence, all the results suggest the essential roles of spinochromes for T. holthuisi, which, in turn, suggests the potential implication of these pigments in the shrimps’ metabolism.
Research Center/Unit :
MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Parmentier, E. & Michel, L. Boundary lines in symbiosis forms. Symbiosis 60, 1–5 (2013)
De Bary, A. Die Erscheinung der Symbiose (ed. Trübner, V. V. K. J.) (Strassburg, 1879)
Paracer, S. & Ahmadjian, V. Symbiosis: An Introduction to Biological Associations (Oxford University Press, 2000)
Olsen Wilford, O. Animal Parasites: Their Life Cycles and Ecology (Dover Publications, 1986)
Baker, A. C. Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34, 661–689 (2003)
Gherardi, F. Eco-ethological aspects of the symbiosis between the shrimp Athanas indicus (Coutière 1903) and the sea urchin Echinometra mathaei (de Blainville 1825). Trop. Zool. 4, 107–128 (1991)
Moyses, C. R. S., Spadacci-Morena, D. D., Xavier, J. G., Antonucci, A. M. & Lallo, M. A. Ectocommensal and ectoparasites in goldfish Carassius auratus (Linnaeus, 1758) in farmed in the State of São Paulo. Rev. Bras. Parasitol. Veterinária 24, 283–289 (2015)
Ross, D. M. The biology of Crustacea. (ed. Bliss, D.) 163–212 (Academic Press Inc., 1983)
De Grave, S. Biogeography of lndo-Pacific Pontoniinae (Crustacea, Decapoda): a PAE analysis. J. Biogeogr. 28, 1239–1253 (2007)
Suzuki, H. Taxonomic review of four alpheid shrimps belonging to the genus Athanas with reference to their sexual phenomena. Sci. Reports Yokohama Natl. Univ. Sect. II 1–52 (1970)
Hipeau-Jacquotte, R. Notes de faunistique et de biologie marines de Madagascar. III. Un nouveau decapode nageur (Pontoniinae) associé aux oursins dans la région de Tulear: Tuleariocaris holthuisi nov. gen. et nov. sp. Recl. des Trav. la Stn. Mar. d’Endoume 37, 247–259 (1965)
Marin, I. & Anker, A. On the Presence of the Pontoniine Shrimp, Tuleariocaris Holthuisi Hipeau-Jacquotte, 1965 (Decapoda, Pontoniinae) on the Pacific Coast of Panama. Crustaceana 82, 505–508 (2009)
Fourgon, D., Lepoint, G. & Eeckhaut, I. Assessment of trophic relationships between symbiotic tropical ophiuroids using C and N stable isotope analysis. J. Mar. Biol. Assoc. UK 86, 1443 (2006)
Caulier, G., Lepoint, G., Van Nedervelde, F. & Eeckhaut, I. 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)
Parmentier, E. & Das, K. Commensal vs. parasitic relationship between Carapini fish and their hosts: some further insight through δ13C and δ15N measurements. J. Exp. Mar. Bio. Ecol. 310, 47–58 (2004)
Vaïtilingon, D., Eeckhaut, I., Fourgon, D. & Jangoux, M. Population dynamics, infestation and host selection of Vexilla vexillum, an ectoparasitic muricid of echinoids, in Madagascar. Dis. Aquat. Organ. 61, 241–255 (2004)
Davenport, D., Camougis, G. & Hickok, J. F. Analyses of the behaviour of commensals in host-factor. 1. A hesioned polychaete and a pinnotherid crab. Anim. Behav. 8, 209–218 (1960)
Dimock, R. V. J. & Davenport, D. Behavioral Specificity and the Induction of Host Recognition in a Symbiotic Polychaete. Biol. Bull. 141, 472–484 (1971)
Vandenspiegel, D., Eeckhaut, I. & Jangoux, M. Host selection by Synalpheus stimpsoni (De Man), an ectosymbiotic shrimp of comatulid crinoids, inferred by a field survey and laboratory experiments. J. Exp. Mar. Bio. Ecol. 225, 185–196 (1998)
Fourgon, D., Jangoux, M. & Eeckhaut, I. Biology of a ‘babysitting’ symbiosis in brittle stars: analysis of the interactions between Ophiomastix venosa and Ophiocoma scolopendrina. Invertebr. Biol. 126, 385–395 (2007)
Miyazaki, S., Ichiba, T., Reimer, J. D. & Tanaka, J. Chemoattraction of the pearlfish Encheliophis vermicularis to the sea cucumber Holothuria leucospilota. Chemoecology 24, 121–126 (2014)
Van Meter, V. B. & Ache, B. W. Host location by the pearlfish Carapus bermudensis. Mar. Biol. 26, 379–383 (1974)
Caulier, G., Flammang, P., Gerbaux, P. & Eeckhaut, I. When a repellent becomes an attractant: harmful saponins are kairomones attracting the symbiotic Harlequin crab. Sci. Rep. 3, 2639 (2013)
Gage, J. Experiments with the behaviour of the bivalves Montacuta substriata and M. ferruginosa, ‘commensals’ with spatangoids. J. Mar. Biol. Assoc. United Kingdom 46, 71 (1966)
Gray, I. E., McCloskey, L. R. & Weihe, S. C. The Commensal Crab Dissodactylus mellitae and Its Reaction to Sand Dollar Host-Factor. J. Elisha Mitchell Sci. Soc. 84, 472–481 (1968)
De Bruyn, C., De Ridder, C., Rigaud, T. & David, B. Chemical host detection and differential attraction in a parasitic pea crab infecting two echinoids. J. Exp. Mar. Bio. Ecol. 397, 173–178 (2011)
Ache, B. W. & Davenport, D. The Sensory Basis of Host Recognition by Symbiotic Shrimps, Genus Betaeus. Biol. Bull. 143, 94–111 (1972)
Dix, T. G. Association between the echinoid Evechinus chloroticus (Val.) and the clingfish Dellichthys morelandi Briggs. Pacific Sci. 23, 332–336 (1969)
Van Dyck, S. et al. The triterpene glycosides of Holothuria forskali: usefulness and efficiency as a chemical defense mechanism against predatory fish. J. Exp. Biol. 214, 1347–1356 (2011)
Kornprobst, J. -M. Substances naturelles d’origine marine - Tome 2 (Lavoisier S.A.S., 2005)
Anderson, H. A., Mathieson, J. W. & Thomson, R. H. Distribution of spinochrome pigments in echinoids. Comp. Biochem. Physiol. 28, 333–345 (1969)
Thomson, R. H. Naturally Occuring Quinones (Academic Press Inc., 1971)
Stekhova, S. I., Shentsova, E. B., Kol’tsova, E. B. & Kulesh, N. I. Antimicrobial activity of polyhydroxynaphthoquinones from sea urchins. Antibiot. Khimioter. 33, 831–833 (1988)
Haug, T. et al. Antibacterial activity in Strongylocentrotus droebachiensis (Echinoidea), Cucumaria frondosa (Holothuroidea), and Asterias rubens (Asteroidea). J. Invertebr. Pathol. 81, 94–102 (2002)
Shankarlal, S., Prabu, K. & Natarajan, E. Antimicrobial and Antioxidant Activity of Purple Sea Urchin Shell (Salmacis virgulata L. Agassiz and Desor 1846). Am. J. Sci. Res. 6, 178–181 (2011)
Zhou, D.-Y. et al. Extraction and antioxidant property of polyhydroxylated naphthoquinone pigments from spines of purple sea urchin Strongylocentrotus nudus. Food Chem. 129, 1591–1597 (2011)
Li, D.-M. et al. Extraction, structural characterization and antioxidant activity of polyhydroxylated 1,4-naphthoquinone pigments from spines of sea urchin Glyptocidaris crenularis and Strongylocentrotus intermedius. Eur. Food Res. Technol. 237, 331–339 (2013)
Powell, C., Hughes, A. D., Kelly, M. S., Conner, S. & McDougall, G. J. Extraction and identification of antioxidant polyhydroxynaphthoquinone pigments from the sea urchin, Psammechinus miliaris. LWT - Food Sci. Technol. 59, 455–460 (2014)
Sciani, J. M. et al. Pro-inflammatory effects of the aqueous extract of Echinometra lucunter sea urchin spines. Exp. Biol. Med. 236, 277–280 (2011)
Gonzalez-Aravena, M. et al. Immune response of the Antarctic sea urchin Sterechinus neumayeri: cellular, molecular and physiological approach. Rev. Biol. Trop. 63, 309–320 (2015)
Majeske, A. J., Bayne, C. J. & Smith, L. C. Aggregation of Sea Urchin Phagocytes Is Augmented In Vitro by Lipopolysaccharide. PLoS One 8, e61419 (2013)
Shikov, A. N., Pozharitskaya, O. N., Krishtopina, A. S. & Makarov, V. G. Naphthoquinone pigments from sea urchins: chemistry and pharmacology. Phytochem. Rev. 17, 509–534 (2018)
Pasotti, F. et al. Benthic Trophic Interactions in an Antarctic Shallow Water Ecosystem Affected by Recent Glacier Retreat. PloS ONE 10, e0141742 (2015)
Caulier, G., Brasseur, L., Gerbaux, P., Flammang, P. & Eeckhaut, I. Crinoid anthraquinones are kairomones allowing host selection for the symbiotic snapping shrimp Synalpheus stimpsoni. submitted (2018)
Eeckhaut, I. et al. Effects of Holothuroid Ichtyotoxic Saponins on the Gills of Free-Living Fishes and Symbiotic Pearlfishes. Biol. Bull. 228, 253–65 (2015)
Kuwahara, R. et al. Antioxidant property of polyhydroxylated naphthoquinone pigments from shells of purple sea urchin Anthocidaris crassispina. LWT - Food Sci. Technol. 42, 1296–1300 (2009)
Egorov, E. A. et al. Histochrome, a new antioxidant, in the treatment of ocular diseases. Vestn. Oftalmol. 115, 34–35 (1999)
Brasseur, L. et al. Identification and quantification of spinochromes in body compartments of Echinometra mathaei’s colored types. R. Soc. Open Sci. 5, 171213 (2018)
Logan, J. M. et al. Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. J. Anim. Ecol. 77, 838–846 (2008)
Coplen, T. B. Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun. Mass Spectrom. 25, 2538–2560 (2011)
Similar publications
Sorry the service is unavailable at the moment. Please try again later.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.