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Isotopic discrimination of stable isotopes of nitrogen (δ15N) and carbon (δ13C) in a host-specific holocephalan tapeworm

  • J. Navarro (a1), M. Albo-Puigserver (a1), M. Coll (a1), R. Saez (a1), M.G. Forero (a2) and R. Kutcha (a3)...

Abstract

During the past decade, parasites have been considered important components of their ecosystems since they can modify food-web structures and functioning. One constraint to the inclusion of parasites in food-web models is the scarcity of available information on their feeding habits and host–parasite relationships. The stable isotope approach is suggested as a useful methodology to determine the trophic position and feeding habits of parasites. However, the isotopic approach is limited by the lack of information on the isotopic discrimination (ID) values of parasites, which is pivotal to avoiding the biased interpretation of isotopic results. In the present study we aimed to provide the first ID values of δ15N and δ13C between the gyrocotylidean tapeworm Gyrocotyle urna and its definitive host, the holocephalan Chimaera monstrosa. We also test the effect of host body size (body length and body mass) and sex of the host on the ID values. Finally, we illustrate how the trophic relationships of the fish host C. monstrosa and the tapeworm G. urna could vary relative to ID values. Similar to other studies with parasites, the ID values of the parasite–host system were negative for both isotopic values of N (Δδ15N = − 3.33 ± 0.63‰) and C (Δδ13C = − 1.32 ± 0.65‰), independent of the sex and size of the host. By comparing the specific ID obtained here with ID from other studies, we illustrate the importance of using specific ID in parasite–host systems to avoid potential errors in the interpretation of the results when surrogate values from similar systems or organisms are used.

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*Fax: +34 932309555 E-mail: joan@icm.csic.es

References

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Bandoni, S. & Brooks, D. (1987) Revision and phylogenetic analysis of the Gyrocotylidea Poche, 1926 (Platyhelminthes: Cercomeria: Cercomeromorpha). Canadian Journal of Zoology 65, 23692389.
Barrett, J. (1981) Biochemistry of parasitic helminths. 380 pp. London, MacMillan.
Berland, B., Bristow, G.A. & Grahl-Nielsen, O. (1990) Chemotaxonomy of Gyrocotyle (Platyhelminthes: Cercomeria) species, parasites of chimaerid fish (Holocephali), by chemometry of their fatty acids. Marine Biology 105, 185189.
Boyer, P., Lardy, H. & Myraback, K. (1962) The enzymes. Vol. 6. New York, Academic Press.
Bristow, G. (1992) On the distribution, ecology and evolution of Gryocotyle urna, G. confusa and G. nybelini (Cercomeromorpha: Gyrocotylidea) and their host Chimaera monstrosa (Holocephalida: Chimaeridae) in Norwegian waters, with a review of the species question. Sarsia 77, 119124.
Butterworth, K.G., Li, W. & McKinley, R.S. (2004) Carbon and nitrogen stable isotopes: a tool to differentiate between Lepeophtheirus salmonis and different salmonid host species? Aquaculture 241, 529538.
Caut, S., Angulo, E. & Courchamp, F. (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46, 443453.
Cornwell, W., Schwilk, D. & Ackerly, D. (2006) A trait-based test for habitat filtering: convex hull volume. Ecology 87, 14651471.
de Niro, M.J. & Epstein, S. (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341351.
Dienske, H. (1968) A survey of the metazoan parasites of the rabbit-fish, Chimaera monstrosa L. (Holocephali). Netherlands Journal of Sea Research 4, 3258.
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, 514523.
Dubois, S.Y., Savoye, N., Sauriau, P.-G., Billy, I., Martinez, P. & de Montaudouin, X. (2009) Digenean trematodes–marine mollusc relationships: a stable isotope study. Diseases of Aquatic Organisms 84, 6577.
Focken, U. & Becker, K. (1998) Metabolic fractionation of stable carbon isotopes: implications of different proximate compositions for studies of the aquatic food webs using δ13C data. Oecologia 115, 337343.
Halvorsen, O. & Williams, H. (1968) Studies of the helminth fauna of Norway. IX. Gyrocotyle. (Platyhelminthes) in Chimaera monstrosa from Olso Fjord. Nytt Magasin for Zoology 15, 130142.
Hare, P., Fogel, M., Stafford, T., Mitchell, A. & Hoering, T. (1991) The isotopic composition of carbon and nitrogen in individual amino acids isolated from modern and fossil proteins. Journal of Archaeological Science 18, 277292.
Hatcher, M.J., Dick, J.T. & Dunn, A.M. (2012) Diverse effects of parasites in ecosystems: linking interdependent processes. Frontiers in Ecology and the Environment 10, 186194.
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, 383405.
Kéfi, S., Berlow, E., Wieters, E., Navarrete, S., Petchey, O., Wood, S., Boit, A., Joppa, L., Lafferty, K., Williams, R., Martinez, N., Menge, B., Blachette, C., Iles, A. & Brose, U. (2012) More than a meal … integrating non-feeding interactions into food webs. Ecology Letters 15, 291300.
Kuris, A.M., Hechinger, R.F., Shaw, J.C., Whitney, K.L., Aguirre-Macedo, L., Boch, C.A., Dobson, A.P., Dunham, E.J., Fredensborg, B.L., Huspeni, T.C., Lorda, J., Mababa, L., Mancini, F.T., Mora, A.B., Pickering, M., Talhouk, N.L., Torchin, M.E. & Lafferty, K.D. (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515518.
Lafferty, K.D., Allesina, S., Arim, M., Briggs, C.J., de Leo, G., Dobson, A.P., Dunne, J.A., Johnson, P.T.J., Kuris, A.M., Marcogliese, D.J., Martinez, N.D., Memmott, J., Marquet, P.A., McLaughlin, J.P., Mordecai, E.A., Pascual, M., Poulin, R. & Thieltges, D.W. (2008) Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533546.
Layman, C., Arrington, D., Montaña, C. & Post, D. (2007) Can stable isotope ratios provide quantitative measures of trophic diversity within food webs? Ecology 88, 4248.
Layman, C., Araújo, M., Boucek, R., Hammerschlag-Peyer, C., Harrison, E., Jud, Z.R., Matich, P., Rosenblatt, A., Vaudo, J., Yeager, L., Post, D. & Bearhop, S. (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biological Reviews 87, 545562.
Macko, S., Estep, M., Engel, M. & Hare, P. (1986) Kinetic fractionation of stable nitrogen isotopes during amino acid transamination. Geochimica et Cosmochimica Acta 50, 21432146.
Pearson, S.F., Levey, D.J., Greenberg, C.H. & Martínez del Rio, C. (2003) Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia 135, 516523.
Persson, M.E., Larsson, P. & Stenroth, P. (2007) Fractionation of δ15N and δ13C for Atlantic salmon and its intestinal cestode Eubothrium crassum . Journal of Fish Biology 71, 441452.
Pinnegar, J., Campbell, N. & Polunin, N. (2001) Unusual stable isotope fractionation patterns observed for fish host–parasite trophic relationships. Journal of Fish Biology 59, 494503.
Poddubnaya, L., Bruňanská, M., Kuchta, R. & Scholz, T. (2006) First evidence of the presence of microtriches in the Gyrocotylidea. Journal for Parasitology 92, 703707.
Post, D.M. (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703718.
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, 257266.
Robbins, C.T., Felicetti, L.A. & Sponheimer, M. (2005) The effects of dietary protein quality on nitrogen discrimination in mammals and birds. Oecologia 144, 534540.
Williams, H.H., Colin, J.A. & Halvorsen, O. (1987) Biology of gyrocotylideans with emphasis on reproduction, population ecology and phylogeny. Parasitology 95, 173207.
Wolf, N., Carleton, S.A. & Martínez, C. (2009) Ten years of experimental animal isotopic ecology. Functional Ecology 23, 1726.

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