150 million years old isopods on fishes: a possible case of palaeo-parasitism

 

Authors: Nagler C, Haug C, Resch U Kriwet J, Haug JT

Published in: Bulletin of Geosciences, volume 91, issue 1; pages: 1 - 12; Received 7 September 2015; Accepted in revised form 31 October 2015; Online 4 December 2015

Keywords: palaeo-parasitology, fossil Cymothoida, Nerocila, host-parasite interaction,

full text (PDF, 8 MB)

Export to RIS

 

Abstract

Parasites are found in all habitats and within all groups of animals, and their influence on food webs, ecosystems and evolutionary development is significant. However, the fossil record of direct parasitism is very scarce. We present here probable examples of parasitic isopods on fishes from the Upper Jurassic Solnhofen Lithographic Limestones (150 million years old, southern Germany). Individual fishes appear to be infested with one to three isopods each. All specimens were documented with up-to-date imaging methods (macrophotography, stereo-photography, composite imaging). Position, orientation and other aspects clearly indicate that the isopods were already attached to the fishes before they died and hence do not represent scavengers but (more or less permanently) attached parasites. While the morphology of the specimens is somewhat uninformative about the systematic position of the isopods, their specific type of parasitism is an indicator for a position in the early lineage towards Cymothoidae. This would represent the first fossil record of this group of obligate fish parasites.

References

AGASSIZ, L. 1837-1843. Recherches sur les poissons fossiles. 3. Contenant l’histoire de l’ordre des Placoides. 422 pp. Petitpierre, Neuchâtel.

ARILLO, A. 2007. Paleoethology: fossilized behaviours in amber. Geologica Acta 5, 159-166.

BAUMILLER, T.K. & GAHN, F.J. 2002. Fossil record of parasitism on marine invertebrates with special emphasis on the platyceratid-crinoid interaction. Paleontological Society Papers 8, 195-210.View article

BLAINVILLE, H. de 1818. Mémoire sur la classe des Sétipodes, partie des Vers a sang rouge de M. Cuvier, et des Annélides de M. de Lamarck. Bulletin des Sciences, par la Société Philomatique de Paris 1818, 78-85.

BOWMAN, T.E. 1960. Description and notes on the biology of Lironeca puhi n. sp. (Isopoda: Cymothoidae) parasite of the Hawaiian Moray Eel, Gymnothorax eurostus (Abbott). Crustaceana 1, 82-91.View article

BOWMAN, T.E. 1981. Thermosphaeroma milleri and T. smithi, new sphaeromatid isopod crustaceans from hot springs in Chihuahua, Mexico, with a review of the genus. Journal of Crustacean Biology 1, 105-122.View article

BOYKO, C.B., MOSS, J., WILLIAMS, J.D. & SHIELDS, J.D. 2013. A molecular phylogeny of Bopyroidea and Cryptoniscoidea (Crustacea: Isopoda), Systematics and Biodiversity 11, 495-506.View article

BRACKEN-GRISSOM, H.D., AHYONG, S.T., WILKINSON, R.D., FELDMANN, R.M., SCHWEITZER, C.E., BREINHOLT, J.W., BENDALL, M., PALERO, F., CHAN, T.Y., FELDER, D.L., ROBLES, R., CHU, K.H., TSANG, L.M., KIM, D., MARTIN, J.W. & CRANDALL, K.A. 2014. Emergence of lobsters: phylogenetic relationships, morphological evolution and divergence time comparisons of an ancient group (Decapoda: Achelata, Astacidea, Glypheidea, Polychelida). Systematic Biology 63(4), 1-23.View article

BRANDT, A. & POORE, G.C.B. 2003. Higher classification of the flabelliferan and related Isopoda based on a reappraisal of relationships. Invertebrate Systematics 17, 893-923.View article

BRETT, C.E. 1978. Hostspecific pitforming epizoans on Silurian crinoids. Lethaia 11, 217-231.View article

BRETT, C.E. 1985. Tremichnus: A new ichnogenus of circular parabolic pits in fossil echinoderms. Journal of Paleontology 59(3), 625-635.

BRUSCA, R.C. 1981. A monograph on the Isopoda Cymothoidae (Crustacea) of the eastern Pacific. Zoological Journal of the Linnean Society 73, 117-199.View article

BRUSCA, R.C., COELHO, V. & TAITI, S. 2001. A Guide to the Coastal Isopods of California. http://tolweb.org/notes/?note_id=3004, downloaded November 2014.

BUNCKLEY-WILLIAMS, L., WILLIAMS, E.H. & BASHIRULLAH, A.K.M. 2006. Isopods (Isopoda: Aegidae, Cymothoidae, Gnathiidae) associated with Venezuelan marine fishes (Elasmobranchii, Actinopterygii). Revista de Biological Tropical 54, 175-188.

CARLE, E. 1969. The very hungry caterpillar. 22 pp. World Publishing Company, Cleveland.

CASTELLANI, C., MAAS, A., WALOSZEK, D. & HAUG, J.T. 2011. New pentastomids from the Late Cambrian of Sweden - deeper insight of the ontogeny of fossil tongue worms. Palaeontographica, Abteilung A: Palaeozoology-Stratigraphy 293(4-6), 95-145.View article

CONWAY MORRIS, S. 1981. Parasites and the fossil record. Parasitology 82, 489-509.View article

CRESSEY, R. & BOXSHALL, G. 1989. Kabatarina pattersoni, a fossil parasitic copepod (Dichelesthiidae) from a lower Cretaceous fish. Micropaleontology 35(2), 150-167.View article

DE BAETS, K., KLUG, C. & KORN, D. 2011. Devonian pearls and ammonoid-endoparasite coevolution. Acta Palaeontologica Polonica 56, 159-180.View article

DONOGHUE, M.J., DOYLE, J.A., GAUTHIER, J., KLUGE, A.G. & ROWE, T. 1989. The importance of fossils in phylogeny reconstruction. Annual Review of Ecology and Systematics 20, 431-460.View article

EDGECOMBE, G.D. 2010. Palaeomorphology: fossils and the inference of cladistic relationships. Acta Zoologica 91, 72-80.View article

FRICKHINGER, K.A. 1999. Die Fossilien von Solnhofen. Dokumentation der aus den Plattenkalken bekannten Tiere und Pflanzen 2. 333 pp. Goldschneck, Wiebelsheim.

GAO, T.P., SHIH, C.K., XU, X., WANG, S. & REN, D. 2012. Mid-Mesozoic flea-like ectoparasites of feathered or haired vertebrates. Current Biology 22, 732-735.View article

HANSEN, T. & HANSEN, J. 2010. First fossils of the isopod genus Aega Leach, 1815. Journal of Paleontology 84, 141-147.View article

HAUG, C., KUTSCHERA, V., AHYONG, S.T., VEGA, F.V., MAAS, A., WALOSZEK, D. & HAUG, J.T. 2013. Re-evaluation of the Mesozoic mantis shrimp Ursquilla yehoachi based on new material and the virtual peel technique. Palaeontologia Electronica, http://palaeo-electronica.org/content/2013/495-ursquilla-and-virtual-peel, 16.2.5T.

HAUG, C., MAYER, G., KUTSCHERA, V., WALOSZEK, D., MAAS, A. & HAUG, J.T. 2011. Imaging and documenting gammarideans. International Journal of Zoology, 380829.View article

HAUG, C., VAN ROY, P., LEIPNER, A., FUNCH, P., RUDKIN, D.M., SCHÖLLMANN, L.& HAUG, J.T. 2012a. A holomorph approach to xiphosuran evolution - a case study on the ontogeny of Euproops. Development Genes and Evolution 222, 253-268.View article

HAUG, J.T., HAUG, C., MAAS, A., KUTSCHERA, V. & WALOSZEK, D. 2010. Evolution of mantis shrimps (Stomatopoda, Malcostraca) in the light of new Mesozoic fossils. BMC Evolutionary Biology 10, 290.View article

HAUG, J.T., MAYER, G., HAUG, C. & BRIGGS, D.E.G. 2012b. A Carboniferous non-onychophoran lobopodian reveals long-term survival of a Cambrian morphotype. Current Biology 22, 1673-1675.View article

KLOMPMAKER, A.A., ARTAL, P., VAN BAKEL, B.W.M., FRAAIJE, R.H.B. & JAGT, J.W.M. 2014. Parasites in the fossil record: a Cretaceous fauna with isopod-infested decapod crustaceans, infestation patterns through time, and a new ichnotaxon. Plos One 9, e92551.View article

KLOMPMAKER, A.A. & BOXSHALL, G. 2015. Fossil Crustaceans as Parasites and Hosts. In DE BAETS, K. & LITTLEWOOD, T. (eds) Advances in Parasitology. Elsevier, Amsterdam.View article

KLOMPMAKER, A.A., SCHWEITZER, C.E., FELDMANN, R.M. & KOWALEWSKI, M. 2013. The influence of reefs on the rise of Mesozoic marine crustaceans. Geology 41, 1179-1182.View article

LEACH, W.E. 1818. Cymothoadées, 338-354. In CUVIER, F. (ed.) Dictionnaire des sciences naturelles, Vol. 12. F.G. Levrault & Le Normant, Paris & Strasbourg.

LESTER, R.J.G. 2005. Isopoda, 138-144. In RHODE, K. (ed.) Marine Parasitology. CSIRO Publishing, Clayton South.

LINCOLN, R.J. 1971. Isopod fish parasites. Marine Observations 41, 184-186.

MAAS, A. & WALOSZEK, D. 2001. Cambrian Derivates of the early arthropod stem lineage, Pentastomids, Tardigrades and Lobopodians - an “Orsten” perspective. Zoologischer Anzeiger 240, 451-459.View article

MCKIERNAN, J.P., GRUTTER, A.S. & DAVIES, A.J. 2005. Reproductive feeding ecology of parasitic gnathiid isopods of epaulette sharks (Hemiscyllium ocellatum) with consideration of their role in the transmission of a haemogregarine. International Journal for Parasitology 35, 19-27.View article

MUENSTER, G. Graf zu 1832. Ueber die Planuliten und Gonititen im Uebergangs-Kalk des Fichtelgebirges. 38 pp. Birner, Bayreuth.

NAGLER, C. & HAUG, J.T. 2015 (accepted). From fossil parasitoids to vectors: Insects as parasites and hosts. In DE BAETS, K. & LITTLEWOOD, T. (eds) Advances in Parasitology. Elsevier, Amsterdam. View article

PERRICHOT, V., BEAUCOURNU, J.C. & VELTEN, J. 2012. First extinct gens of a flea (Siphonaptera: Pulicidae) in Miocene amber from the Dominican Republic. Zootaxa 3438, 54-61.View article

POINAR, G.P. 1985. Fossil evidence of insect parasitism by mites. International Journal of Acarology 11, 37-38.View article

POLZ, H. 2004. Asselansammlung auf einer Wasserwanze aus den Solnhofener Plattenkalken. Archaeopteryx 22, 51-60.

POLZ, H., SCHWEIGERT, G. & MAISCH, M.W. 2006. Two new species of Palaega (Isopoda: Cymothoida: Cirolanidae) from the Upper Jurassic of Swabian Alb, South Germany. Stuttgarter Beiträge zur Naturkunde 362, 1-17.

RADWANSKA, U. & POIROT, E. 2010. Copepod-infest Bathonian (Middle Jurassic) echinoids from northern France. Acta Geologica Polonica 60, 549-555.

RADWANSKA, U. & RADWANSKI, A. 2005. Myzostomid and copepod infestation of Jurassic echinoderms: A general approach, some new occurrences, and/or re-interpretation of previous reports. Acta Geologica Polonica 55, 109-130.

RAVICHANDRAN, S., RAMESHKUMAR, G. & KUMARAVEL, K. 2009. Variation in the morphological features of isopod fish parasites. World Journal of Fish and Marine Sciences 1, 137-140.

ROCHE, D.G., STRONG, L.E. & BINNING, S.A. 2013. Prevalence of the parasitic cymothoid isopod Anilocra nemipteri on its fish host at Lizard Island, Great Barrier Reef. Australian Journal of Zoology 60, 330-333.View article

ROMESTAND, B., THUET, P. & TRILLES, J.P. 1982. Some aspects of nutritional mechanisms in the isopod Ceratothoa oestroides Risso, 1826 parasite of fishes. Annales de Parasitologie Humaine et Comparee 57, 79-89.View article

RUST, J. 2007. Die Bedeutung von Fossilien fu¨r phylogenetische Rekonstruktionen. Species, Phylogeny and Evolution 1, 73-87.

SCHRAM, F.R. 1977. Paleozoography of late Paleozoic and Triassic Malacostraca. Systematic Biology 26, 367-379.View article

SCHWEIGERT, G. 2007. Ammonite biostratigraphy as a tool for dating Upper Jurassic lithographic limestones from South Germany - first results and open questions. Neues Jahrbuch der geologischen paläontologischen Abhandlungen 245, 117-125.View article

SERRANO-SÁNCHEZ, M.D.L., NAGLER, C., HAUG, C., HAUG, J.T., CENTENO-GARCÍA, E. & VEGA, F.J. in review. The first fossil record of larval stages of parasitic isopods: cryptoniscus larvae preserved in Miocene amber. Neues Jahrbuch für Geologie und Paläontologie.

SMIT, J.N., BRUCE, N.L. & HADFIELD, K.A. 2014. Global diversity of fish parasitic isopod crustaceans of the family Cymotoidae. International Journal for Parasitology: Parasites and Wildlife 3, 188-197.

STRONG, L. 2012. Effects of a cymothoid ectoparasite on the turning behavior (lateralization) of the bridled monocle bream Scolopsis bilineata. Independent Study Project (ISP) Collection 1267.

THIOLLIERE, V. 1852. Troisieme notice sur les gisements a poissons fossiles situés dans le Jura du départment de l’Ain. Annales (Extrait des Proces-Verbaux), des Societe royale d’Agriculture, d’Histoire naturelle et Arts utiles de Lyon 4, 352-446.

TSAI, M.L., LI, J.J. & DAI, C.F. 1999. Why selection favors protandrous sex change for the parasitic isopod, Ichthyoxenus fushanensis (Isopoda: Cymothoidae). Evolutionary Ecology 13, 327-338.View article

WALOSSEK, D. & MÜLLER, K.J. 1994. Pentastomid parasites from the Lower Palaeozoic of Sweden. Transactions of the Royal Society of Edinburgh: Earth Sciences 85(01), 1-37.View article

WALOSSEK, D., REPETSKI, J.E. & MÜLLER, K.J. 1994. An exceptionally preserved parasitic arthropod, Heymonsicambria taylori n.sp. (Arthropoda incertae sedis: Pentastomida), from Cambrian-Ordovician boundary beds of Newfoundland, Canada. Canadian Journal of Earth Sciences 31(11), 1664-1671.View article

WILLIAMS, E.H. JR. & WILLIAMS, L.B. 1985. Cuna insularis n. gen. and n. sp. (Isopoda: Cymothoidae) from the gill chamber of the sergeant major, Abudefduf saxatilis Linnaeus (Osteichthyes) in the West Indies. Journal of Parasitology 71, 209-214.View article

WILLIAMS, J.D. & BOYKO, C.B. 2012. The global diversity of parasitic isopods associated with crustacean hosts (Isopoda: Bopyroidea and Cryptoniscoidea). PLoS ONE 7, e35350.View article

WILSON, G.D.F, PATERSON, J.R. & KEAR, B.P. 2011. Fossil isopod associated with a fish skeleton from the Lower Cretaceous of Queensland, Australia - direct evidence of a scavenging lifestyle in Mesozoic Cymothoida. Palaeontology 54, 1053-1068.View article

YESMIN, S. & KHANUM, H. 2011. On the studies of parasites infestation in Clarias batrachus (Linneaeus) and Clarias gariepinus (Burchell). Proceedings of 22nd National Congress on Parasitology, 30.10.2010-01.11.2010, West Bengal, India, 252-259.