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Presence of a seawater-filled caecum in Echinocardium cordatum (Echinoidea: Spatangoida)

Published online by Cambridge University Press:  31 August 2011

Gauthier Rolet ,
Alexander Ziegler  and
Chantal De Ridder
Gauthier Rolet*
Affiliation:
Laboratoire de Biologie Marine (CP160/15), Université Libre de Bruxelles, 50 Avenue Franklin D. Roosevelt, 1050 Bruxelles, Belgium
Alexander Ziegler
Affiliation:
Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA
Chantal De Ridder
Affiliation:
Laboratoire de Biologie Marine (CP160/15), Université Libre de Bruxelles, 50 Avenue Franklin D. Roosevelt, 1050 Bruxelles, Belgium
*
Correspondence should be addressed to: G. Rolet, Laboratoire de Biologie Marine (CP160/15), Université Libre de Bruxelles, 50 Avenue Franklin D. Roosevelt, 1050 Bruxelles, Belgium email: grolet@ulb.ac.be
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Abstract

Heart urchins (Echinoidea: Spatangoida) are considered infaunal, deposit feeding sea urchins that utilize the surrounding sediment as a source of nutrients. Sediment occupies most of the digestive tract lumen but never enters the gastric caecum, a prominent structure that is filled with a transparent fluid. The aim of this study was to shed light on the nature of the fluid found inside the gastric caecum of a well-studied spatangoid species, Echinocardium cordatum. Our conclusions are based on a three-step-approach: firstly, by following the movement of dyed seawater from the mouth up to the caecal lumen; secondly, by comparing the osmolarity of various body fluids; and thirdly, by describing the particulate content of the gastric caecum. In addition, we employed magnetic resonance imaging (MRI) to reveal the absence of sediment within the gastric caecum. Our osmolarity measurements show that the coelomic fluid is significantly more concentrated than the caecal fluid, which in turn has an osmolarity similar to seawater. MRI reveals that the gastric caecum, in contrast to the rest of the digestive tract, is always devoid of sediment. Light and electron microscopy observations reveal the presence of a variety of detrital particles suspended in the caecal fluid that are identical to those occurring in seawater sampled over the seafloor. We argue that the fluid filling the gastric caecum must be predominantly seawater, and we propose a scenario that explains seawater circulation in E. cordatum. In this context, the gastric caecum could act as an internal trap for suspended particulate organic matter. We hypothesize that spatangoid sea urchins could have adopted internal suspension feeding as a secondary feeding mode in addition to deposit feeding.

Keywords

EchinoideaIrregulariaSpatangoidaEchinocardiumgastric caecumgut contenttrophic statussuspension feedingdeposit feeding
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 92 , Issue 2 , March 2012 , pp. 379 - 385
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

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References

REFERENCES

Agassiz, A. (1872–1874) Revision of the Echini. Illustrated Catalogue of the Museum of Comparative Zoology 7.Google Scholar
Bromley, R.G. and Asgaard, U. (1975) Sediment structures produced by a spatangoid echinoid: a problem of preservation. Bulletin of the Geological Society of Denmark 24, 261–281.Google Scholar
Buchanan, J.B. (1966) The biology of Echinocardium cordatum (Echinodermata: Spatangoidea) from different habitats. Journal of the Marine Biological Association of the United Kingdom 46, 97–114.CrossRefGoogle Scholar
Buchanan, J.B. (1969) Feeding and control of volume within the tests of regular sea-urchins. Journal of Zoology 159, 51–64.CrossRefGoogle Scholar
Buchanan, J.B., Brown, B.E., Coombs, T.L., Pirie, B.J.S. and Allen, J.A. (1980) The accumulation of ferric iron in the guts of some spatangoid echinoderms. Journal of the Marine Biological Association of the United Kingdom 60, 631–640.CrossRefGoogle Scholar
Chesher, R.H. (1963) The morphology and function of the frontal ambulacrum of Moira atropos (Echinoidea: Spatangoida). Bulletin of Marine Science of the Gulf and Caribbean 13, 549–573.Google Scholar
Chia, F.S. (1969) Some observations on the locomotion and feeding of the sand dollar Dendraster excentricus (Eschscholtz). Journal of Experimental Marine Biology and Ecology 3, 162–170.Google Scholar
Cramer, A. (1991) Observations on spatial distribution, metabolism and feeding strategy of Echinocardium cordatum (Pennant) (Echinodermata) and the implications for its energy budget, in Metabolic activity at frontal systems in the North Sea. PhD thesis. Universiteit Amsterdam, The Netherlands.Google Scholar
Cuénot, L. (1948) Anatomie, éthologie et systématique des échinodermes. In Grassé, P.P. (ed.) Traité de Zoologie, Volume 11. Paris: Masson, pp. 1–363.Google Scholar
De Amaral, P., Nunes, C.D.A.P. and Jangoux, M. (2007) Larval growth and perimetamorphosis in the echinoid Echinocardium cordatum (Echinodermata): the spatangoid way to become a sea urchin. Zoomorphology 126, 103–119.CrossRefGoogle Scholar
De Ridder, C. (1987) Mécanique digestive chez l'échinide fouisseur Echinocardium cordatum (Echinodermata). Bulletin de la Société des Sciences Naturelles de l'Ouest de la France Supplement HS, 65–71.Google Scholar
De Ridder, C., Jangoux, M. and Van Impe, E. (1985) Food selection and absorption efficiency in the spatangoid echinoid, Echinocardium cordatum (Echinodermata). In Keegan, B. and O'Connor, B. (eds) Proceedings of the 5th International Echinoderm Conference, Galway 1984. Rotterdam: A.A. Balkema Press, pp. 245–251.Google Scholar
De Ridder, C., Jangoux, M. and De Vos, L. (1987) Frontal ambulacral and peribuccal areas of the spatangoid echinoid Echinocardium cordatum (Echinodermata): a functional entity in feeding mechanism. Marine Biology 94, 613–624.CrossRefGoogle Scholar
De Ridder, C. and Jangoux, M. (1993) The digestive tract of the spatangoid echinoid Echinocardium cordatum (Echinodermata): morphofunctional study. Acta Zoologica 74, 337–351.CrossRefGoogle Scholar
De Ridder, C. and Lawrence, J. (1982) Food and feeding mechanisms: Echinoidea. In Jangoux, M. and Lawrence, J. (eds) Echinoderm nutrition. Rotterdam: A.A. Balkema Press, pp. 97–115.Google Scholar
Egglishaw, H.J. (1972) An experimental study of the breakdown of cellulose in fast-flowing streams. In Melchiorri-Santolini, U. and Hopton, J.W. (eds) Detritus and its role in aquatic ecosystems. Proceedings of an IBP-UNESCO symposium. Memorie dell'Istituto Italiano di Idrobiologia 29, pp. 406–428.Google Scholar
Fechter, H. (1972) Untersuchung über den Wasserwechsel der Seeigel und seine Bedeutung für Atmung und Exkretion. Helgoländer Wissenschaftliche Meeresuntersuchungen 23, 80–99.CrossRefGoogle Scholar
Ferguson, J.C. (1969) Feeding, digestion and nutrition in Echinodermata. In Florkin, M. and Scheer, B.T. (eds) Chemical Zoology 3, 71–100.Google Scholar
Foster-Smith, R.L. (1978) An analysis of water flow in tube-living animals. Journal of Experimental Marine Biology and Ecology 34, 73–95.CrossRefGoogle Scholar
Hendey, N.I. (1974) A revised check-list of British marine diatoms. Journal of the Marine Biological Association of the United Kingdom 54, 277–300.CrossRefGoogle Scholar
Higgins, R.C. (1974) Specific status of Echinocardium cordatum, E. australe and E. zealandicum (Echinoidea: Spatangoida) around New Zealand, with comments on the relation of morphological variation to environment. Journal of Zoology 173, 451–475.CrossRefGoogle Scholar
Holland, N.D. and Ghiselin, M.T. (1970) A comparative study of gut mucous cells in thirty-seven species of the class Echinoidea (Echinodermata). Biological Bulletin. Marine Biological Laboratory, Woods Hole 138, 286–305.CrossRefGoogle ScholarPubMed
Hollertz, K. (1999) The response of Brissopsis lyrifera (Echinoidea: Spatangoida) to organic matter on the sediment surface. In Proceedings of the 5th European Conference on Echinoderms. Rotterdam: A.A. Balkema Press, pp. 19–24.Google Scholar
Hollertz, K. and Duchêne, J.C. (2001) Burrowing behaviour and sediment reworking in the heart urchin Brissopsis lyrifera Forbes (Spatangoida). Marine Biology 139, 951–957.Google Scholar
Horner, R.A. (2002) A taxonomic guide to some common marine phytoplankton. Dorchester, UK: Biopress Limited and Dorset Press.Google Scholar
Kanazawa, K. (1992) Adaptation of test shape for burrowing and locomotion in spatangoid echinoids. Palaeontology 35, 733–750.Google Scholar
Margalef, R. (1967) Laboratory analogues of estuarine plankton systems. In Lauff, G.H. (ed.) Estuaries: perspectives in ecological theory. American Association for the Advancement of Science Publication No. 83, pp. 515–521.Google Scholar
M'Harzi, A. (1999) Phytoplankton community structuring in some areas of the North Sea. PhD thesis. Vrije Universiteit Brussel, Belgium.Google Scholar
Muller, Y. (2004) Faune et flore du littoral du Nord, du Pas-de-Calais et de la Belgique: inventaire. Commission Régionale de Biologie de la Région Nord Pas-de-Calais.Google Scholar
Nichols, D. (1959a) Changes in the chalk heart-urchin Micraster interpreted in relation to living forms. Philosophical Transactions of the Royal Society London 242, 347–437.Google Scholar
Nichols, D. (1959b) The histology of the tube-feet and clavulae of Echinocardium cordatum. Quarterly Journal of Microscopical Science 100, 73–87.Google Scholar
Nichols, D. (1959c) Mode of life and taxonomy in irregular sea-urchins. In Nichols, D. (ed.) Taxonomy and geography, a symposium. Systematics Association Publication No. 3, pp. 61–80.Google Scholar
Osinga, R., Kop, A.J., Malschaert, J.F.P. and Van Duyl, F.C. (1997) Effects of the sea urchin Echinocardium cordatum on bacterial production and carbon flow in experimental benthic systems under increasing organic loading. Journal of Sea Research 37, 109–121.CrossRefGoogle Scholar
Péquignat, C.E. (1970) Biologie des Echinocardium cordatum (Pennant) de la Baie de Seine. Forma et Functio 2, 121–168.Google Scholar
Smith, A.B. (1980) The structure and arrangement of echinoid tubercles. Philosophical Transactions of the Royal Society B 289, 1–54.Google Scholar
Stott, F.C. (1955) The food canal of the sea-urchin Echinus esculentus L. and its functions. Proceedings of the Zoological Society of London 125, 63–86.CrossRefGoogle Scholar
Telford, M. and Mooi, R. (1996) Podial particle picking in Cassidulus caribaearum (Echinodermata: Echinoidea) and the phylogeny of sea urchin feeding mechanisms. Biological Bulletin. Marine Biological Laboratory, Woods Hole 191, 209–223.CrossRefGoogle ScholarPubMed
Thorsen, M.S. (1998) Microbial activity, oxygen status and fermentation in the gut of the irregular sea urchin Echinocardium cordatum (Spatangoida: Echinodermata). Marine Biology 132, 423–433.CrossRefGoogle Scholar
Thorsen, M.S. (1999) Abundance and biomass of the gut-living microorganisms in the irregular sea urchin Echinocardium cordatum (Spatangoida: Echinodermata). Marine Biology 133, 353–360.CrossRefGoogle Scholar
Timko, P.L. (1976) Sand dollars as suspension feeders: a new description of feeding in Dendraster excentricus. Biological Bulletin. Marine Biological Laboratory, Woods Hole 151, 247–259.CrossRefGoogle Scholar
Turquier, Y. (1989) L'organisme dans son milieu. Tome 1: les fonctions de nutrition. Paris: Editions Doin.Google Scholar
Warnau, M., Temara, A., Ameye, L. and Jangoux, M. (1998) The excretory function of the posteriormost part of the echinoid and holothuroid gut (Echinodermata). Comparative Biochemistry and Physiology A 120, 687–691.CrossRefGoogle Scholar
Wilkinson, L. (1988) Systat 5.2.1: the system for statistics. Evanton, IL: Systat.Google Scholar
Ziegler, A., Faber, C., Mueller, S. and Bartolomaeus, T. (2008) Systematic comparison and reconstruction of sea urchin (Echinoidea) internal anatomy: a novel approach using magnetic resonance imaging. BMC Biology 6, 33.CrossRefGoogle ScholarPubMed
Ziegler, A., Mooi, R., Rolet, G. and De Ridder, C. (2010) Origin and evolutionary plasticity of the gastric caecum in sea urchins (Echinodermata: Echinoidea). BMC Evolutionary Biology 10, 313.CrossRefGoogle ScholarPubMed