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Does the acanthocephalan parasite Polymorphus minutus modify the energy reserves and antitoxic defences of its intermediate host Gammarus roeseli?

Published online by Cambridge University Press:  12 March 2012

E. GISMONDI*
Affiliation:
Laboratoire des Interactions Ecotoxicologie Biodiversité Ecosystèmes (LIEBE) – CNRS UMR 7146, Université de Lorraine (UdL), Campus Bridoux, Bât. IBiSE, 8 Rue du Général Delestraint, 57070 Metz, France
C. COSSU-LEGUILLE
Affiliation:
Laboratoire des Interactions Ecotoxicologie Biodiversité Ecosystèmes (LIEBE) – CNRS UMR 7146, Université de Lorraine (UdL), Campus Bridoux, Bât. IBiSE, 8 Rue du Général Delestraint, 57070 Metz, France
J.-N. BEISEL
Affiliation:
Laboratoire des Interactions Ecotoxicologie Biodiversité Ecosystèmes (LIEBE) – CNRS UMR 7146, Université de Lorraine (UdL), Campus Bridoux, Bât. IBiSE, 8 Rue du Général Delestraint, 57070 Metz, France
*
*Corresponding author: Laboratoire des Interactions Ecotoxicologie Biodiversité Ecosystèmes (LIEBE)–CNRS UMR 7146, Université de Lorraine (UdL), Campus Bridoux, Bât. IBiSE, 8 Rue du Général Delestraint, 57070Metz, France. Tel: +33(0)387378500. Fax: +33(0)387378512. E-mail: [email protected]

Summary

In disturbed environments, infected organisms have to face both parasitic and chemical stresses. Although this situation is common, few studies have been devoted to the effects of infection on hosts' energy reserves and antitoxic defence capacities, while parasite survival depends on host survival. In this study, we tested the consequences of an infection by Polymorphus minutus on the energy reserves (protein, lipid and glycogen) and antioxidant defence capacities (reduced glutathione, γ-glutamylcysteine ligase activity) of Gammarus roeseli males and females, in the absence of chemical stress. Moreover, malondialdehyde concentration was used as a toxicity biomarker. The results revealed that in infected G. roeseli, whatever their gender and the sampling month, protein and lipid contents were lower, but glycogen contents were higher. This could be explained by the fact that the parasite diverts part of the host's energy for its own development. Moreover, glutathione concentrations and γ-glutamylcysteine ligase activity were both lower, which could lead to lower antitoxic defence in the host. These results suggest negative effects on individuals in the case of additional stress (e.g. pollutant exposure). In the absence of chemical stress, the lower malondialdehyde level in infected gammarids could imply a probable protective effect of the parasite.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Bakker, T. C., Mazzi, D. and Zala, S. (1997). Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78, 10981104.CrossRefGoogle Scholar
Baldauf, S. A., Thünken, T., Frommen, J. G., Bakker, T. C. M., Heupel, O. and Kullmann, H. (2007). Infection with an acanthocephalan manipulates an amphipod's reaction to a fish predator's odours. International Journal for Parasitology 37, 6165. doi:10.1016/j.ijpara.2006.09.003.Google Scholar
Barnard, J. L. and Barnard, C. M. (1983). Freshwater Amphipoda of the World I & II. Hayfield Associates, Mt. Vernon, VA, USA.Google Scholar
Barrett, J. and Butterworth, P. E. (1968). The carotenoids of Polymorphus minutus (Acanthocephala) and its intermediate host, Gammarus Pulex. Comparative Biochemistry and Physiology 27, 575581. doi:10.1016/0010-406X(68)90254-5.Google Scholar
Baudrimont, M., De Montaudouin, X. and Palvadeau, A. (2006). Impact of digenean parasite infection on metallothionein synthesis by the cockle (Cerastoderma edule): A multivariate field monitoring. Marine Pollution Bulletin 52, 494502. doi:10.1016/j.marpolbul.2005.09.035.CrossRefGoogle ScholarPubMed
Bauer, A., Trouvé, S., Grégoire, A., Bollache, L. and Cézilly, F. (2000). Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native and invader gammarid species. International Journal for Parasitology 30, 14531457. doi:10.1016/S0020-7519(00)00138-7.Google Scholar
Bauer, A., Haine, E. R., Perrot-Minnot, M. J. and Rigaud, T. (2005). The acanthocephalan parasite Polymorphus minutus alters the geotactic and clinging behaviours of two sympatric amphipod hosts: the native Gammarus pulex and the invasive Gammarus roeseli. Journal of Zoology 267, 3943. doi: 10.1017/S0952836905007223.Google Scholar
Behrens, W. and Madère, R. (1991). Malonaldehyde determination in tissues and biological fluids by ion-pairing high-performance liquid chromatography. Lipids 26, 232236. doi: 10.1007/BF02543977.CrossRefGoogle ScholarPubMed
Beisel, J. N. and Médoc, V. (2010). Bird and amphipod parasites illustrate a gradient from adaptation to exaptation in complex life cycle. Ethology Ecology and Evolution 22, 265270. doi:10.1080/03949370.2010.502321.Google Scholar
Bollache, L., Rigaud, T. and Cézilly, F. (2002). Effects of two acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea: Amphipoda). Journal of Invertebrate Pathology 79, 102110. doi:10.1016/S0022-2011(02)00027-7.Google Scholar
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254. doi:10.1016/0003-2697(76)90527-3.Google Scholar
Canesi, L., Viarengo, A., Leonzio, C., Filippelli, M. and Gallo, G. (1999). Heavy metals and glutathione metabolism in mussel tissues. Aquatic Toxicology 46, 6776. doi:10.1016/S0166-445X(98)00116-7.Google Scholar
Cargill, A. S., Cummin, K. W., Hanson, B. J. and Lowry, R. R. (1985). The role of lipids as feeding stimulants for shredding aquatic insects. Freshwater Biology 15, 455464. doi:10.1111/j.1365-2427.1985.tb00215.x.Google Scholar
Cézilly, F., Gregoire, A. and Bertin, A. (2000). Conflict between co-occurring manipulative parasites? An experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology 120, 625630.CrossRefGoogle ScholarPubMed
Cézilly, F. and Perrot-Minnot, M. J. (2005). Studying adaptive changes in the behaviour of infected hosts: a long and winding road. Behavioural Processes 68, 223228. doi:10.1016/j.beproc.2004.08.013.CrossRefGoogle ScholarPubMed
Cézilly, F., Thomas, F., Médoc, V. and Perrot-Minnot, M. J. (2010). Host-manipulation by parasites with complex life cycles: adaptive or not? Trends in Parasitology 26, 311317. doi: 10.1016/j.pt.2010.03.009.Google Scholar
Cornet, S., Franceschi, N., Bauer, A., Rigaud, T. and Moret, Y. (2009). Immune depression induced by acanthocephalan parasites in their intermediate crustacean host: Consequences for the risk of super-infection and links with host behavioural manipulation. International Journal for Parasitology 39, 221229. doi:10.1016/j.ijpara.2008.06.007.Google Scholar
Correia, A. D., Livingstone, D. R. and Costa, M. H. (2002). Effects of water-borne copper on metallothionein and lipid peroxidation in the marine amphipod Gammarus locusta. Marine Environmental Research 54, 357360. doi:10.1016/S0141-1136(02)00114-9.Google Scholar
Crompton, D. W. T. and Nickol, B. B. (1985). Biology of the Acanthocephala, Cambridge University Press, Cambridge, UK.Google Scholar
Dezfuli, B. S., Giari, L., Arrighi, S., Domeneghini, C. and Bosi, G. (2003). Influence of enteric helminths on the distribution of intestinal endocrine cells belonging to the diffuse endocrine system in brown trout, Salmo trutta L. Journal of Fish Diseases 26, 155166. doi:10.1046/j.1365-2761.2003.00446.x.Google Scholar
Dick, J. T. A., Armstrong, M., Clarke, H. C., Farnsworth, K. D., Hatcher, M. J., Ennis, M., Kelly, A. and Dunn, A. M. (2010). Parasitism may enhance rather than reduce the predatory impact of an invader. Biology Letters 6, 636638. doi: 10.1098/rsbl.2010.0171.Google Scholar
Doyotte, A., Cossu, C., Jacquin, M. C., Babut, M. and Vasseur, P. (1997). Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the digestive gland of the freshwater bivalve Unio tumidus. Aquatic Toxicology 39, 93110. doi:10.1016/S0166-445X(97)00024-6.Google Scholar
Griffith, O. W. (1999). Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radical Biology and Medicine 27, 922935. doi:10.1016/S0891-5849(99)00176-8.Google Scholar
Jazdzewski, K. (1980). Range extensions of some gammaridean species in european inland waters caused by human activity. Crustaceana 6, 84107.Google Scholar
Kennedy, C. R. (2006). Ecology of the Acanthocephala. Cambridge University Press, Cambridge, UK.Google Scholar
Lafferty, K. D. (1999). The evolution of trophic transmission. Parasitology 15, 111115. doi:10.1016/S0169-4758(99)01397-6.Google ScholarPubMed
Lagrue, C., Kaldonski, N., Perrot-Minnot, M. J., Motreuil, S. and Bollache, L. (2007). Modification of hosts' behavior by a parasite: field evidence for adaptive manipulation. Ecology 88, 28392847. doi:10.1890/06-2105.1.Google Scholar
Leroy, P., Nicolas, A., Thioudellet, C., Oster, T., Wellman, M. and Siest, G. (1993). Rapid liquid chromatographic assay of glutathione in cultured cells. Biomedical Chromatography 7, 8689. doi:10.1002/bmc.1130070208.Google Scholar
Mantiri, D. M. H., Negre-Sadargues, G., Charmantier, G., Trilles, J. P., Milicua, J. C. G. and Castillo, R. (1996). Nature and metabolism of carotenoid pigments during the embryogenesis of the European Lobster Homarus gammarus (Linne, 1758). Comparative Biochemistry and Physiology Part A: Physiology 115, 237241. doi:10.1016/0300-9629(96)00054-0.Google Scholar
Maynard, B. J., Wellnitz, T. A., Zanini, N., Wright, W. G. and Dezfuli, B. S. (1998). Parasite-altered behavior in a crustacean intermediate host : field and laboratory studies. Journal of Parasitology 84, 11021106.Google Scholar
McCahon, C. P., Maund, S. J. and Poulton, M. J. (1991). The effect of the acanthocephalan parasite (Pomphorhynchus laevis) on the drift of its intermediate host (Gammarus pulex). Freshwater Biology 25, 507513. doi:10.1111/j.1365-2427.1991.tb01393.x.Google Scholar
Médoc, V., Bollache, L. and Beisel, J. N. (2006). Host manipulation of a freshwater crustacean (Gammarus roeseli) by an acanthocephalan parasite (Polymorphus minutus) in a biological invasion context. International Journal for Parasitology 36, 13511358. doi:10.1016/j.ijpara.2006.07.001.Google Scholar
Médoc, V., Rigaud, T., Bollache, L. and Beisel, J. N. (2009). A manipulative parasite increasing an antipredator response decreases its vulnerability to a nonhost predator. Animal Behaviour 77, 12351241. doi:10.1016/j.anbehav.2009.01.029.CrossRefGoogle Scholar
Médoc, V. and Beisel, J. N. (2009). Field evidence for non-host predator avoidance in a manipulated amphipod. Naturwissenschaften 96, 513523. doi: 10.1007/s00114-008-0503-8.CrossRefGoogle Scholar
Médoc, V., Piscart, C., Maazouzi, C., Simon, L. and Beisel, J.-N. (2011). Parasite-Induced Changes in the Diet of a Freshwater Amphipod: Field and Laboratory Evidence. Parasitology 138, 537546. doi: 10.1017/S0031182010001617.Google Scholar
Neuparth, T., Correia, A. D., Costa, F. O., Lima, G. and Costa, M. H. (2005). Multi-level assessment of chronic toxicity of estuarine sediments with the amphipod Gammarus locusta: I. Biochemical endpoints. Marine Environmental Research 60, 6991. doi:10.1016/j.marenvres.2004.08.006.Google Scholar
Neves, C. A., Sampedro, , Pastor, M. P., Nery, L. E. M. and Santos, E. A. (2004). Effects of the parasite Probopyrus ringueleti (Isopoda) on glucose, glycogen and lipid concentration in starved Palaemonetes argentinus (Decapoda). Diseases of Aquatic Organisms 58, 209213.Google Scholar
Parmentier, C., Leroy, P., Wellman, M. and Nicolas, A. (1998). Determination of cellular thiols and glutathione-related enzyme activities: versatility of high-performance liquid chromatography–spectrofluorimetric detection. Journal of Chromatography B: Biomedical Sciences and Applications 719, 3746. doi:10.1016/S0378-4347(98)00414-9.Google Scholar
Perrot-Minnot, M. J. (2004). Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala). International Journal for Parasitology 34, 4554. doi:10.1016/j.ijpara.2003.10.005.Google Scholar
Perrot-Minnot, M. J., Kaldonski, N. and Cézilly, F. (2007). Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected amphipod. International Journal for Parasitology 37, 645651. doi:10.1016/j.ijpara.2006.12.005.CrossRefGoogle Scholar
Plaistow, S. J., Troussard, J. P. and Cézilly, F. (2001). The effect of the acanthocephalan parasite Pomphorhynchus laevis on the lipid and glycogen content of its intermediate host Gammarus pulex. International Journal for Parasitology 31, 346351. doi:10.1016/S0020-7519(01)00115-1.Google Scholar
Poulin, R. (1995). “Adaptive” changes in the behaviour of parasitized animals: A critical review. International Journal for Parasitology 25, 13711383. doi:10.1016/0020-7519(95)00100-X.Google Scholar
Sparkes, T. C., Keogh, D. P. and Pary, R. A. (1996). Energetic costs of mate guarding behavior in male stream-dwelling isopods. Oecologia 106, 166171. doi: 10.1007/BF00328595.CrossRefGoogle ScholarPubMed
Sroda, S. and Cossu-Leguille, C. (2011 a). Seasonal variability of antioxidant biomarkers and energy reserves in the freshwater gammarid Gammarus roeseli. Chemosphere 83, 538544. doi:10.1016/j.chemosphere.2010.12.023.CrossRefGoogle ScholarPubMed
Sroda, S. and Cossu-Leguille, C. (2011 b). Effects of sublethal copper exposure on two gammarid species: which is the best competitor?. Ecotoxicology 20, 264273. doi: 10.1007/s10646-010-0578-9.Google Scholar
Stentiford, G. D., Neil, D. M. and Coombs, G. H. (2001). Development and application of an immunoassay diagnostic technique for studying Hematodinium infections in Nephrops norvegicus populations. Diseases of Aquatic Organisms 46, 223229.Google Scholar
Sures, B., Dezfuli, B. S. and Krug, H. F. (2003). The intestinal parasite Pomphorhynchus laevis (Acanthocephala) interferes with the uptake and accumulation of lead (210Pb) in its fish host chub (Leuciscus cephalus). International Journal for Parasitology 33, 16171622. doi:10.1016/S0020-7519(03)00251-0.Google Scholar
Sures, B. and Siddall, R. (1999). Pomphorhynchus laevis: The intestinal Acanthocephalan as a lead sink for its fish host, chub (Leuciscus cephalus). Experimental Parasitology 93, 6672. doi:10.1006/expr.1999.4437.CrossRefGoogle ScholarPubMed
Sures, B., Taraschewski, H. and Jackwerth, E. (1994). Lead accumulation in Pomphorhynchus laevis and its host. Journal of Parasitology 80, 355357. doi: 10.2307/3283403.Google Scholar
Sures, B. and Radszuweit, H. (2007). Pollution induced heat shock protein expression in the amphipod Gammarus roeseli is affected by larvae of Polymorphus minutus (Acanthocephala). Journal of Helminthology 81, 191197. doi: 10.1017/S0022149X07751465.Google Scholar
Sutcliffe, D. W. (1993). Reproduction in Gammarus (Crustacea Amphipoda): female strategies. Freshwater Forum 3, 2665.Google Scholar
Taraschewski, H. (2000). Host-parasite interactions in acanthocephalan: a morphological approach. Advances in Parasitology 46, 1179.Google Scholar
Vasseur, P. and Leguille, C. (2004). Defense systems of benthic invertebrates in response to environmental stressors. Environmental Toxicology 19, 433436. doi: 10.1002/tox.20024.Google Scholar
Yan, T., Teo, L. H. and Sin, Y. M. (1997). Effects of mercury and lead on tissue glutathione of the green mussel, Perna viridis L. Bulletin of Environmental Contamination and Toxicology 58, 845850. doi: 10.1007/s001289900411.CrossRefGoogle ScholarPubMed