Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-24T12:33:36.218Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  04 March 2013

J. Navarro ,
M. Albo-Puigserver ,
M. Coll ,
R. Saez ,
M.G. Forero  and
R. Kutcha
J. Navarro*
Affiliation:
Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta 37-49, 08003Barcelona, Spain
M. Albo-Puigserver
Affiliation:
Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta 37-49, 08003Barcelona, Spain
M. Coll
Affiliation:
Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta 37-49, 08003Barcelona, Spain
R. Saez
Affiliation:
Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta 37-49, 08003Barcelona, Spain
M.G. Forero
Affiliation:
Estación Biológica de Doñana (EBD-CSIC), C/Américo Vespucio s/n, 41092, Sevilla, Spain
R. Kutcha
Affiliation:
Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05Ceské Budejovice, Czech Republic
*
*Fax: +34 932309555 E-mail: joan@icm.csic.es
Get access Rights & Permissions [Opens in a new window]

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.

Type
Short Communications
Information
Journal of Helminthology , Volume 88 , Issue 3 , September 2014 , pp. 371 - 375
Copyright
Copyright © Cambridge University Press 2013 

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

Bandoni, S. & Brooks, D. (1987) Revision and phylogenetic analysis of the Gyrocotylidea Poche, 1926 (Platyhelminthes: Cercomeria: Cercomeromorpha). Canadian Journal of Zoology 65, 2369–2389.Google Scholar
Barrett, J. (1981) Biochemistry of parasitic helminths. 380 pp. London, MacMillan.Google Scholar
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, 185–189.Google Scholar
Boyer, P., Lardy, H. & Myraback, K. (1962) The enzymes. Vol. 6. New York, Academic Press.Google Scholar
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, 119–124.Google Scholar
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, 529–538.Google Scholar
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, 443–453.CrossRefGoogle Scholar
Cornwell, W., Schwilk, D. & Ackerly, D. (2006) A trait-based test for habitat filtering: convex hull volume. Ecology 87, 1465–1471.CrossRefGoogle ScholarPubMed
de Niro, M.J. & Epstein, S. (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351.Google Scholar
Dienske, H. (1968) A survey of the metazoan parasites of the rabbit-fish, Chimaera monstrosa L. (Holocephali). Netherlands Journal of Sea Research 4, 32–58.Google 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.Google Scholar
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, 65–77.Google Scholar
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, 337–343.Google Scholar
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, 130–142.Google Scholar
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, 277–292.CrossRefGoogle Scholar
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, 186–194.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
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, 291–300.Google Scholar
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, 515–518.CrossRefGoogle ScholarPubMed
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, 533–546.Google Scholar
Layman, C., Arrington, D., Montaña, C. & Post, D. (2007) Can stable isotope ratios provide quantitative measures of trophic diversity within food webs? Ecology 88, 42–48.Google Scholar
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, 545–562.Google Scholar
Macko, S., Estep, M., Engel, M. & Hare, P. (1986) Kinetic fractionation of stable nitrogen isotopes during amino acid transamination. Geochimica et Cosmochimica Acta 50, 2143–2146.Google Scholar
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, 516–523.Google Scholar
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, 441–452.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
Poddubnaya, L., Bruňanská, M., Kuchta, R. & Scholz, T. (2006) First evidence of the presence of microtriches in the Gyrocotylidea. Journal for Parasitology 92, 703–707.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
Robbins, C.T., Felicetti, L.A. & Sponheimer, M. (2005) The effects of dietary protein quality on nitrogen discrimination in mammals and birds. Oecologia 144, 534–540.Google Scholar
Williams, H.H., Colin, J.A. & Halvorsen, O. (1987) Biology of gyrocotylideans with emphasis on reproduction, population ecology and phylogeny. Parasitology 95, 173–207.Google Scholar
Wolf, N., Carleton, S.A. & Martínez, C. (2009) Ten years of experimental animal isotopic ecology. Functional Ecology 23, 17–26.Google Scholar