Skip to main content
×
Home
    • Aa
    • Aa

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

  • E. GISMONDI (a1), C. COSSU-LEGUILLE (a1) and J.-N. BEISEL (a1)
Summary
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.

Copyright
Corresponding author
*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: eric.gismondi@hotmail.fr
References
Hide All
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.
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.
Barnard J. L. and Barnard C. M. (1983). Freshwater Amphipoda of the World I & II. Hayfield Associates, Mt. Vernon, VA, USA.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Crompton D. W. T. and Nickol B. B. (1985). Biology of the Acanthocephala, Cambridge University Press, Cambridge, UK.
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.
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.
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.
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.
Jazdzewski K. (1980). Range extensions of some gammaridean species in european inland waters caused by human activity. Crustaceana 6, 84107.
Kennedy C. R. (2006). Ecology of the Acanthocephala. Cambridge University Press, Cambridge, UK.
Lafferty K. D. (1999). The evolution of trophic transmission. Parasitology 15, 111115. doi:10.1016/S0169-4758(99)01397-6.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Sutcliffe D. W. (1993). Reproduction in Gammarus (Crustacea Amphipoda): female strategies. Freshwater Forum 3, 2665.
Taraschewski H. (2000). Host-parasite interactions in acanthocephalan: a morphological approach. Advances in Parasitology 46, 1179.
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.
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.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 2
Total number of PDF views: 6 *
Loading metrics...

Abstract views

Total abstract views: 102 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 22nd October 2017. This data will be updated every 24 hours.