Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-24T23:52:30.889Z Has data issue: false hasContentIssue false
  • English
  • Français

Multiple isotope analyses of the pike tapeworm Triaenophorus nodulosus reveal peculiarities in consumer–diet discrimination patterns

Published online by Cambridge University Press:  22 January 2014

J. Behrmann-Godel  and
E. Yohannes
J. Behrmann-Godel
Affiliation:
Limnological Institute, University of Konstanz, Mainaustrasse 252, D-78464, Konstanz, Germany
E. Yohannes*
Affiliation:
Limnological Institute, University of Konstanz, Mainaustrasse 252, D-78464, Konstanz, Germany
*
*E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Previous studies of dietary isotope discrimination have led to the general expectation that a consumer will exhibit enriched stable isotope levels relative to its diet. Parasite–host systems are specific consumer–diet pairs in which the consumer (parasite) feeds exclusively on one dietary source: host tissue. However, the small numbers of studies previously carried out on isotopic discrimination in parasite–host (ΔXP-HT) systems have yielded controversial results, showing some parasites to be isotopically depleted relative to their food source, while others are enriched or in equilibrium with their hosts. Although the mechanism for these deviations from expectations remains to be understood, possible influences of specific feeding niche or selection for only a few nutritional components by the parasite are discussed. ΔXP-HT for multiple isotopes (δ13C, δ15N, δ34S) were measured in the pike tapeworm Triaenophorus nodulosus and two of its life-cycle fish hosts, perch Perca fluviatilis and pike Esox lucius, within which T. nodulosus occupies different feeding locations. Variability in the value of ΔXP-HT calculated for the parasite and its different hosts indicates an influence of feeding location on isotopic discrimination. In perch liver ΔXP-HT was relatively more negative for all three stable isotopes. In pike gut ΔXP-HT was more positive for δ13C, as expected in conventional consumer–diet systems. For parasites feeding on pike gut, however, the δ15N and δ34S isotope values were comparable with those of the host. We discuss potential causes of these deviations from expectations, including the effect of specific parasite feeding niches, and conclude that ΔXP-HT should be critically evaluated for trophic interactions between parasite and host before general patterns are assumed.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 2 , March 2015 , pp. 238 - 243
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barrett, J. (1981) Biochemistry of parasitic helminths. 380 pp. London, MacMillan.Google Scholar
Boag, B., Neilson, R., Robinson, D., Scrimgeour, C.M. & Handley, L.L. (1998) Wild rabbit host and some parasites show trophic-level relationships for delta 13C and delta 15N: a first report. Isotopes in Environmental and Health Studies 34, 81–85.Google Scholar
Bryant, C. & Behm, C. (1989) Biochemical adaptations in parasites. 259 pp. London, Chapman & Hall.Google Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Cocheret de la Morinière, E., Pollux, B.J.A., Nagelkerken, I., Hemminga, M.A., Huiskes, A.H.L. & van der Velde, G. (2003) Ontogenic dietary changes of coral reef fishes in the mangrove– seagrass– reef continuum: stable isotopes and gut-content analysis. Marine Ecology. Progress Ser. 246, 279–289.Google Scholar
Deudero, S., Pinnegar, J.K. & Polunin, N.V. (2002) Insights into fish host–parasite trophic relationships revealed by stable isotope analysis. Disease of Aquatic Organisms 7, 77–86.CrossRefGoogle Scholar
Doucett, R., Giberson, D. & Power, G. (1999) Parasitic association of Nanocladius (Diptera: Chironomidae) and Pteronarcys biloba (Plecoptera: Pteronarcyidae): insights from stable-isotope analysis. Journal of the North American Benthological Society 18, 514–523.CrossRefGoogle Scholar
Gresty, K.A. & Quarmby, C. (1991) The trophic level of Mytilicola intestinalis Steuer (Copepoda: Poecilostomatoida) in Mytilus edulis L., as determined from stable isotope analysis. Proceedings of the Fourth International Conference on Copepoda. Bulletin of the Plankton Society of Japan Special volume, 363–371.Google Scholar
Iken, K., Brey, T., Wand, U., Voigt, J. & Junghans, P. (2001) Food web structure of the benthic community at the Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis. Progress in Oceanography 50, 383–405.Google Scholar
Ingram, T., Mathews, B., Harrod, C., Stephens, T., Grey, J. & Markel, R. (2007) Lipid extraction has little effect on the δ15N of aquatic consumers. Limnology and Oceanography Methods 5, 338–343.CrossRefGoogle Scholar
Kennedy, C.R. (1976) Ecological aspects of parasitology. 474 pp. Amsterdam, North Holland Publishing.Google Scholar
Kling, G.W., Fry, B. & O'Brien, W.J. (1992) Stable isotopes and planktonic trophic structure in arctic lakes. Ecology 73, 561–566.Google Scholar
Kuperman, B.I. (1973) Tapeworms of the genus Triaenophorus – parasites of fish. 222 pp. New Delhi, India, Amerind Publication.Google Scholar
Logan, J.M., Jardine, T.D., Miller, T.J., Bunn, S.E., Cunjak, R.A. & Lutcavage, M.E. (2008) Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modeling methods. Journal of Animal Ecology 77, 838–846.Google Scholar
Minagawa, M. & Wada, E. (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48, 1135–1140.Google Scholar
Navarro, J., Albo-Puigserver, M., Coll, M., Saez, R., Forero, M.G. & Kutcha, R. (2013) Isotopic discrimination of stable isotopes of nitrogen (δ15N) and carbon (δ13C) in a host-specific holocephalan tapeworm. Journal of Helminthology doi:10.1017/S0022149X13000126.Google Scholar
Neilson, R. & Brown, D.J.F. (1999) Feeding on different host plants alters the natural abundances of δ13C and δ15N in Longidoridae (Nemata). Journal of Nematology 31, 20–26.Google Scholar
Neilson, R., Boag, B. & Hartely, G. (2005) Temporal host-parasite relationships of the wild rabbit, Oryctolagus cuniculus (L.) as revealed by stable isotope analyses. Parasitology 131, 279–285.Google Scholar
O'Grady, S.P. & Dearing, M.D. (2006) Isotopic insight into host-endosymbiont relationships in Liolaemid lizards. Oecologia 150, 355–361.CrossRefGoogle ScholarPubMed
Peterson, B.J. & Fry, B. (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293–320.Google Scholar
Pinnegar, J., Campbell, N. & Polunin, N. (2001) Unusual stable isotope fractionation patterns observed for fish host-parasite trophic relationships. Journal of Fish Biology 59, 494–503.Google Scholar
Post, D.M. (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.Google Scholar
Power, M. & Klein, G. (2004) Fish host-cestode parasite stable isotope enrichment patterns in marine, estuarine and freshwater fishes from northern Canada. Isotopes in Environmental Health Studies 40, 257–266.Google Scholar
Richards, M.P., Fuller, B.T., Sponheimer, M., Robinson, T. & Ayliffe, L. (2003) Sulphur isotopes in palaeodietary studies: a review and results from a controlled feeding experiment. International Journal of Osteoarchaeology 13, 37–45.Google Scholar
Schleuter, D. & Eckmann, R. (2008) Generalist versus specialist: the performances of perch and ruffe in a lake of low productivity. Ecology of Freshwater Fish 17, 86–99.CrossRefGoogle Scholar
Sokal, R.R. & Rohlf, F.J. (2000) Biometry. 3rd edn.New York, W.H. Freeman.Google Scholar
Svanbäck, R. & Eklöv, P. (2004) Morphology in perch affects habitat specific feeding efficiency. Functional Ecology 18, 503–510.Google Scholar
Tielens, A.G.M & Van Hellemond, J.J. (2006) Unusual aspects of metabolism in flatworm parasites. pp. 387–405in Maule, A.G. & Narks, J.N. (Eds) Parasitic flatworms: molecular biology, biochemistry, immunology and physiology. King's Lynn, Biddles Ltd.CrossRefGoogle Scholar
Vander Zanden, M.J. & Rasmussen, J.B. (2001) Variation in delta N-15 and delta C-13 trophic fractionation: Implications for aquatic food web studies. Limnology and Oceanography 46, 2061–2066.Google Scholar
Xu, J., Zhang, M. & Xie, P. (2007) Trophic relationship between the parasitic isopod Ichthyoxenus japonensis and the fish Carassius auratus auratus as revealed by stable isotopes. Journal of Freshwater Ecology 22, 238–333.CrossRefGoogle Scholar