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First fossil record of parasitism in Devonian calcareous sponges (stromatoporoids)

Published online by Cambridge University Press:  03 August 2010

MIKOŁAJ K. ZAPALSKI  and
BENOÎT L. M. HUBERT
MIKOŁAJ K. ZAPALSKI*
Affiliation:
Institute of Paleobiology PAS, Twarda 51/55, 00-818 Warsaw, Poland
BENOÎT L. M. HUBERT
Affiliation:
Laboratoire de Paléontologie stratigraphique, ISA-FLST, Geosystemes FRE 3298 CNRS, 41 rue du Port F-59046 Lille cedex, France
*
*Corresponding author: Institute of Paleobiology PAS, Twarda 51/55, 00-818 Warsaw, Poland. Tel: +48 22 697 88 73. Fax: +48 22 620 62 25. E-mail: m.zapalski@twarda.pan.pl
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Summary

Introduction. Palaeozoic calcareous sponges (stromatoporoids) are common bio-constructing fossils; they are sometimes found in association with helicoidal structures of unknown biological affinities. The interaction between the tube-forming organisms has usually been classified as commensalism. Methods. About 260 stromatoporoid skeletons from the Middle Devonian (Givetian) of the Mont d'Haurs section near Givet (Champagne-Ardenne, France) were thin-sectioned and analysed under transmitted light. Results. Approximately 10% of the examined stromatoporoids (mainly belonging to the genera Actinostroma, Stromatopora and Stromatoporella) contain tubes classified as Torquaysalpinx sp. The Torquaysalpinx organisms penetrated the skeletons of stromatoporoids in vivo (as evidenced by skeletal overgrowths); around the infesting organisms, growth bands are bent down. Conclusion. Diminished growth rates around the infesting organism demonstrate a negative influence on the host, similar to that seen in the modern demosponge–polychaete association of Verongia–Haplosyllis. This is demonstrated by changes in growth bands. As in the above-mentioned association, the endosymbiont might have been feeding directly upon the tissues of the host. The Torquaysalpinx organisms were gaining habitat and possibly also food resources – for them this interaction was clearly positive. This long-term association can therefore be classified as parasitism. This is the first evidence for parasitism in Palaeozoic sponges.

Keywords

stromatoporoidcalcareous spongeendobiontparasitismDevonianGivetianTorquaysalpinxfossil record
Type
Research Article
Information
Parasitology , Volume 138 , Issue 1 , January 2011 , pp. 132 - 138
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Bassett, M. G., Popov, L. E. and Holmer, L. E. (2004). The oldest-known metazoan parasite? Journal of Paleontology 78, 1214–1216.2.0.CO;2>CrossRefGoogle Scholar
Casadevall, A. and Pirofski, L.-A. (2000). Host-pathogen interactions: basic concepts of microbial commensalism, colonization, infection and disease. Infection and Immunity 68, 6511–6518.CrossRefGoogle ScholarPubMed
Cheney, K. L. and Côté, I. (2005). Mutualism or parasitism? The variable outcome of cleaning symbioses. Biology Letters 1, 162–165. doi: 10.1098/rsbl.2004.0288.CrossRefGoogle ScholarPubMed
Combes, C. (2001). Parasitism: The Ecology and Evolution Intimate Interactions. University of Chicago Press, Chicago, IL, USA.Google Scholar
Cook, A. G. (1999). Stromatoporoid palaeoecology and systematic from the Middle Devonian Fanning River Group, North Queensland. Memoirs of the Queensland Museum 43, 463–551.Google Scholar
Dawkins, R. (1982). The Extended Phenotype. W. H. Freeman, Oxford, UK.Google Scholar
Drake, W. P. (2008). When a commensal becomes a pathogen. Sarcoidosis Vasculitis and Diffuse Lung Diseases 25, 10–11.Google Scholar
Hill, D. (1981). Tabulata. In Treatise on Invertebrate Paleontology. Part F. Coelenterata (ed. Moore, R. C. and Teichert, C.), pp. F430–F762. Geological Society of America, Boulder, and University of Kansas Press, Lawrence, KA, USA.Google Scholar
Hubert, B. L. M. (2008). Detailed lithology and faunal abundance of the historical Givetian section: the fortifications of the Mont d'Haurs (Givet, France). Annales de la Société Géologique du Nord 15 (2ème série), 45–57.Google Scholar
Hubert, B. L. M., Zapalski, M. K., Nicollin, J.-P., Mistiaen, B. and Brice, D. (2007). Selected benthic faunas from the Devonian of the Ardennes: an estimation of palaeobiodiversity. Acta Geologica Polonica 57, 223–262.Google Scholar
Insalaco, E. (1996). The use of Late Jurassic coral growth bands as palaeoenvironmental indicators. Palaeontology 39, 413–431.Google Scholar
Kershaw, S. (1980). Cavities and cryptic faunas beneath non-reef stromatoporoids. Lethaia 13, 327–338. doi: 10.1111/j.1502-3931.1980.tb01059.x.CrossRefGoogle Scholar
Krug, P. J. (2006). Defense of benthic invertebrates against surface colonization by larvae: a chemical arms race. In Antifouling Compounds (ed. Fusetani, N. and Clare, A. S.). Progress in Molecular and Subcellular Biology 42, 1–53.CrossRefGoogle Scholar
Lecompte, M. (1951). Les stromatoporoïdes du Dévonien moyen et supérieur du Bassin de Dinant. Première partie. Mémoires - Institut royal des Sciences naturelles de Belgique 116, 1–216.Google Scholar
Lecompte, M. (1952). Les stromatoporoïdes du Dévonien moyen et supérieur du Bassin de Dinant. Deuxième partie. Mémoires - Institut royal des Sciences naturelles de Belgique 117, 217–259.Google Scholar
Leung, T. L. F. and Poulin, R. (2008). Parasitism, commensalism, and mutualism: exploring the many shades of symbioses. Vie et Milieu – Life and Environment 58, 107–115.Google Scholar
Littlewood, D. T. J. and Donovan, S. K. (2003). Fossil parasites: a case of identity. Geology Today 19, 136–142.CrossRefGoogle Scholar
Nishi, E. and Nishihira, M. (1996). Age-estimation of the Christmas Tree worm Spirobranchus giganteus (Polychaeta, Serpulidae) living buried in the coral skeleton from the coral-growth band of the host coral. Fisheries Science 62, 400–403.CrossRefGoogle Scholar
Oekentorp, K. (1969). Kommensalismus bei Favositiden. Münster Forschungen zur Geologie und Paläontologie 12, 165–217.Google Scholar
Oekentorp, K. (2001). Review on diagenetic microstructures in fossil corals – a controversial discussion. Bulletin of the Tohoku University Museum 1, 193–209.Google Scholar
Oekentorp, K. (2007). The microstructure concept – coral research in the conflict of controversial opinions. Bulletin of Geosciences 82, 95–97.CrossRefGoogle Scholar
Pisera, A. (2006). Palaeontology of sponges – a review. Canadian Journal of Zoology 84, 242–261. doi: 10.1139/Z05–169.CrossRefGoogle Scholar
Plusquellec, Y. (1968). Commensaux des Tabulés et Stromatoporoïdes du Dévonien armoricain. Annales de la Societe Géologique du Nord 88, 47–56.Google Scholar
Poinar, G. Jr. and Boucot, A. J. (2006). Evidence of intestinal parasites of dinosaurs. Parasitology 133, 245–249. doi: 10.1017/S0031182006000138CrossRefGoogle ScholarPubMed
Poinar, G. Jr. and Poinar, R. (2004). Paleoleishmania proterus n. gen., n. sp., (Trypanosomatidae: Kinetoplastida) from Cretaceous Burmese Amber. Protist 155, 305–310. doi: 10.1078/1434461041844259.CrossRefGoogle Scholar
Reiswig, H. M. (1973). Population dynamics of three Jamaican Demospongiae. Bulletin of Marine Science 23, 191–226.Google Scholar
Riding, R. and Kershaw, S. (1977). Nature of stromatoporoids. Nature, London 268, 178.CrossRefGoogle Scholar
Sachs, J. L. and Wilcox, T. P. (2006). A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum. Proceedings of the Royal Society of London, B 273, 425–429. doi: 10.1098/rspb.2005.3346.Google ScholarPubMed
Sokolov, B. S. (1948). Commensalism among the favositids. Izvestia Akademii Nauk SSSR, Seria Biologicheskaya 1, 101–110. (In Russian.)Google Scholar
Stearn, C. W., Webby, B. D., Nestor, H. and Stock, C. W. (1999). Revised classification and terminology of Palaeozoic stromatoporoids. Acta Palaeontologica Polonica 44, 1–70.Google Scholar
Stel, J. H. (1976). The Palaeozoic hard substrate trace fossils Helicosalpinx, Chaetosalpinx and Torquaysalpinx. Neues Jahrbuch für Geologie und Paläontologie, Monatshefte 1976, 726–744.Google Scholar
Tapanila, L. (2005). Palaeoecology and diversity of endosymbionts in Palaeozoic marine invertebrates: trace fossil evidence. Lethaia 38, 89–99. doi: 10.1080/00241160510013123.CrossRefGoogle Scholar
Tapanila, L. (2006). Macroborings and bioclaustrations in a late Devonian reef above the Alamo Impact Breccia, Nevada, USA. Ichnos 13, 129–134. doi: 10.1080/10420940600850893.CrossRefGoogle Scholar
Tapanila, L. (2008). Direct evidence of ancient symbiosis using trace fossils. In From Evolution to Geobiology: Research Questions Driving Paleontology at the Start of a New Century, Paleontological Society Short Course, October 4, 2008 (ed. Kelley, P. H. and Bambach, R. K.), pp. 271–287. Paleontological Society Papers 14. The Paleontolgical Society, Ithaca, New York, USA.Google Scholar
Taylor, P. D. and Wilson, M. A. (2003). Palaeoecology and evolution of marine hard substrate communities. Earth Science Reviews 62, 1–103. doi: 10.1016/S0012-8252(02)00131-9.CrossRefGoogle Scholar
Vinn, O. and Isakar, M. (2007). The tentaculitid affinities of Anticalyptraea from the Silurian of Baltoscandia. Palaeontology 50, 1385–1390. doi: 10.1111/j.1475-4983.2007.00715.xCrossRefGoogle Scholar
Vinn, O. and Mutvei, H. (2009). Calcareous tubeworms of the Phanerozoic. Estonian Journal of Earth Sciences 58, 286–296.CrossRefGoogle Scholar
Vinn, O., Ten Hove, H. A., Mutvei, H. and Kirsimäe, K. (2008). Ultrastructure and mineral composition of serpulid tubes (Polychaeta, Annelida). Zoological Journal of the Linnean Society 154, 633–650. doi: 10.1111/j.1096-3642.2008.00421.xCrossRefGoogle Scholar
Weedon, M. J. (1991). Microstructure and affinity of the enigmatic Devonian tubular fossil Trypanopora. Lethaia 24, 227–234.CrossRefGoogle Scholar
Wulff, J. L. (2006). Ecological interactions of marine sponges, Canadian Journal of Zoology 84, 146–166. doi: 10.1139/Z06-019.CrossRefGoogle Scholar
Young, G. A. and Kershaw, S. (2005). Classification and controls of internal banding in Palaeozoic stromatoporoids and colonial corals. Palaeontology 48, 623–651. doi: 10.1111/j.1475-4983.2005.00480.xCrossRefGoogle Scholar
Zapalski, M. K. (2007). Parasitism versus commensalism – the case of tabulate endobionts. Palaeontology 50, 1375–1380. doi: 10.1111/j.1475-4983.2007.00716.x.CrossRefGoogle Scholar
Zapalski, M. K. (2009). Parasites in Emsian–Eifelian Favosites (Anthozoa, Tabulata) from the Holy Cross Mountains (Poland): changes of distribution within colony. In Palaeozoic Reefs and Bioaccumulations: Devonian Change. Case Studies in Palaeogeography and Palaeoecology (ed. Königshof, P.), pp. 125–129. Geological Society, London, Special Publications 314. doi: 10.1144/SP314.6.Google Scholar
Zapalski, M. K. (2010). Tabulate corals from the Givetian and Frasnian of the Southern Region of the Holy Cross Mountains (Poland). Special Papers in Palaeontology (in the Press).Google Scholar
Zapalski, M. K., Hubert, B. L. M., Nicollin, J.-P., Mistiaen, B. and Brice, D. (2007 a). The palaeobiodiversity of stromatoporoids, tabulates and brachiopods in the Devonian of the Ardennes – changes through time. Bulletin de la Société Géologique de France 178, 383–390.CrossRefGoogle Scholar
Zapalski, M. K., Hubert, B. L. M. and Mistiaen, B. (2007 b). Estimation of palaeoenvironmental changes: can analysis of distribution of tabulae in tabulates be a tool? In Palaeozoic Reefs and Bioaccumulations: Climatic and Evolutionary Controls (ed. Álvaro, J. J., Aretz, M., Boulvain, F., Munnecke, A., Vachard, D. and le Vennin, E.), pp. 275–281. Geological Society, London, Special Publications 275.Google Scholar
Zapalski, M. K., Pinte, E. and Mistiaen, B. (2008). Late Famennian? Chaetosalpinx in Yavorskia (Tabulata): the youngest record of tabulate endobionts. Acta Geologica Polonica 58, 321–324.Google Scholar