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Biological invasion and parasitism: invaders do not suffer from physiological alterations of the acanthocephalan Pomphorhynchus laevis

Published online by Cambridge University Press:  21 September 2009

S. CORNET ,
G. SORCI  and
Y. MORET
S. CORNET*
Affiliation:
Université de Bourgogne, UMR CNRS 5561 Biogéosciences, Equipe Ecologie Evolutive, 6 Bd Gabriel, 21000 Dijon, France
G. SORCI
Affiliation:
Université de Bourgogne, UMR CNRS 5561 Biogéosciences, Equipe Ecologie Evolutive, 6 Bd Gabriel, 21000 Dijon, France
Y. MORET
Affiliation:
Université de Bourgogne, UMR CNRS 5561 Biogéosciences, Equipe Ecologie Evolutive, 6 Bd Gabriel, 21000 Dijon, France
*
*Corresponding author: Tel: +33 380399157. Fax: +33 380396231. E-mail: stephane.cornet@u-bourgogne.fr
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Summary

Biological invasions expose parasites to new invasive hosts in addition to their local hosts. However, local parasites are often less successful in infecting and exploiting their new hosts. This may have major consequences for the competitive ability of hosts, and finally on the fate of the parasite-host community. In Burgundy (Eastern France), the acanthocephalan parasite, Pomphorhynchus laevis, infects 2 amphipod species living in sympatry: the native Gammarus pulex and the invasive Gammarus roeseli. While P. laevis affects the behaviour and the immunity of G. pulex, G. roeseli seems unaffected by the infection. In this study, we examined in detail the ability of the parasite to affect the immune system and resource storage of both gammarid species. We found that the infection was associated with a general decrease of the prophenoloxidase activity, haemocyte density, resistance to an artificial bacterial infection and level of sugar reserves in G. pulex, but not in G. roeseli. These results demonstrate a differential ability of P. laevis to exploit its local and its invasive gammarid hosts. Potential mechanisms of these differential physiological alterations and their potential consequences on the coexistence of both gammarid species in sympatry are discussed.

Keywords

acanthocephalandisease resistanceGammarus pulexGammarus roeselihaemocyteslocal adaptationphenoloxidasePomphorhynchus laevis
Type
Research Article
Information
Parasitology , Volume 137 , Issue 1 , January 2010 , pp. 137 - 147
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Bollache, L., Dick, J. T. A., Farnsworth, K. D. and Montgomery, W. I. (2008). Comparison of the functional responses of invasive and native amphipods. Biology Letters 4, 166–169.Google Scholar
Bollache, L., Kaldonski, N., Troussard, J.-P., Lagrue, C. and Rigaud, T. (2006). Spines and behaviour as defences against fish predators in an invasive freshwater amphipod. Animal Behaviour 72, 627–633.Google Scholar
Bonneaud, C., Mazuc, J., Guillermo, G., Haussy, C., Chastel, O., Faivre, B. and Sorci, G. (2003). Assessing the cost of mounting an immune response. American Naturalist 161, 367–379.CrossRefGoogle ScholarPubMed
Cerenius, L., Bangyeekhun, E., Keyser, P., Soderhall, I. and Soderhall, K. (2003). Host prophenoloxidase expression in freshwater crayfish is linked to increased resistance to the crayfish plague fungus, Aphanomyces astaci. Cellular Microbiology 5, 353–357.Google Scholar
Cerenius, L., Lee, B. L. and Söderhäll, K. (2008). The proPO-system: pros and cons for its role in invertebrate immunity. Trends in Immunology 29, 263–271.CrossRefGoogle ScholarPubMed
Cerenius, L. and Söderhäll, K. (2004). The prophenoloxidase-activating system in invertebrates. Immunological Reviews 198, 116–126.CrossRefGoogle ScholarPubMed
Cézilly, F., Grégoire, A. and Bertin, A. (2000). Conflict between co-occuring manipulative parasites? An experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology 120, 625–630.CrossRefGoogle Scholar
Colautti, R. I., Ricciardi, A., Grigorovich, I. A. and Macisaac, H. J. (2004). Is invasion success explained by the enemy release hypothesis? Ecology Letters 7, 721–733.CrossRefGoogle Scholar
Cornet, S., Biard, C. and Moret, Y. (2009 a). Variation in immune defence among populations of Gammarus pulex (Crustacea: Amphipoda). Oecologia 159, 257–269.CrossRefGoogle ScholarPubMed
Cornet, S., Franceschi, N., Bauer, A., Rigaud, T. and Moret, Y. (2009 b). 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, 221–229.CrossRefGoogle ScholarPubMed
Cox, F. E. G. (2001). Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl), S23–S38.CrossRefGoogle ScholarPubMed
Damian, R. T. (1997). Parasite immune evasion and exploitation: reflections and projections. Parasitology 115 (Suppl), S169–S175.Google Scholar
De Jong-Brink, M. (1995). How schistosomes profit from the stress responses they elicit in their hosts. Advances in Parasitology 35, 177–256.CrossRefGoogle ScholarPubMed
Dezfuli, B. S., Simoni, E., Duclos, L. and Rossetti, E. (2008). Crustacean-acanthocephalan interaction and host cell-mediated immunity: parasite encapsulation and melanization. Folia Parasitologica 55, 53–59.CrossRefGoogle ScholarPubMed
Drake, J. M. (2003). The paradox of the parasites: implications for biological invasion. Proceedings of the Royal Society of London B 270, S133–S135.CrossRefGoogle ScholarPubMed
Dunn, A. M. and Dick, J. T. A. (1998). Parasitism and epibiosis in native and non-native gammarids in freshwater in Ireland. Ecography 21, 593–598.CrossRefGoogle Scholar
Ebert, D. (1994). Virulence and local adaptation of a horizontally transmitted parasite. Science 265, 1084–1086.CrossRefGoogle ScholarPubMed
Emblidge Fromme, A. and Dybdahl, M. F. (2006). Resistance in introduced populations of a freshwater snail to native range parasites. Journal of Evolutionary Biology 19, 1948–1955.Google Scholar
Ferguson, H. M. and Read, A. F. (2002). Genetic and environmental determinants of malaria parasite virulence in mosquitoes. Proceedings of the Royal Society of London, B 269, 1217–1224.Google Scholar
Franz, K. and Kurtz, J. (2002). Altered host behaviour: manipulation or energy depletion in tapeworm-infected copepods? Parasitology 125, 187–196.Google Scholar
Genner, M. J., Michel, E. and Todd, J. A. (2008). Resistance of an invasive gastropod to an indigenous trematode parasite in Lake Malawi. Biological Invasions 10, 41–49.CrossRefGoogle Scholar
Gomes, S. A. O., Feder, D., Garcia, E. S. and Azambuja, P. (2003). Suppression of the prophenoloxidase system in Rhodnius prolixus orally infected with Trypanosoma rangeli. Journal of Insect Physiology 49, 829–837.CrossRefGoogle ScholarPubMed
Graham, A. L. (2008). Ecological rules governing helminth microparasite coinfection. Proceedings of the National Academy of Sciences, USA 105, 566–570.Google Scholar
Grenfell, B. T. and Dobson, A. P. (1995). Ecology of Infectious Diseases in Natural Populations, Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Hatcher, M. J., Dick, J. T. A. and Dunn, A. M. (2006). How parasites affect interactions between competitors and predators. Ecology Letters 9, 1253–1271.CrossRefGoogle ScholarPubMed
Hudson, P. J., Dobson, A. P. and Lafferty, K. D. (2006). Is a healthy ecosystem one that is rich in parasites? Trends in Ecology & Evolution 21, 381–385.CrossRefGoogle Scholar
Humbert, E. and Coustau, C. (2001). Refractoriness of host haemocytes to parasites immunosuppressive factors as a putative resistance mechanism in the Biomphlaria glabrata-Echinostoma caproni system. Parasitology 122, 651–660.CrossRefGoogle Scholar
Jazdzewski, K. and Roux, A.-L. (1988). Biogéographie de Gammarus roeseli Gervais en Europe en particulier répartition en France et en Pologne. Crustaceana 13 (Suppl.), S272–S277.Google Scholar
Kaldonski, N., Lagrue, C., Motreuil, S., Rigaud, T. and Bollache, L. (2008). Habitat segregation mediates predation by the benthic fish Cottus gobio on the exotic amphipod species Gammarus roeseli. Naturwissenschaften 95, 839–844.CrossRefGoogle ScholarPubMed
Kaldonski, N., Perrot-Minnot, M.-J. and Cezilly, F. (2007). Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host. Animal Behaviour 74, 1311–1317.Google Scholar
Kaltz, O. and Shykoff, J. (1998). Local adaptation in host-parasite systems. Heredity 81, 361–370.CrossRefGoogle Scholar
Karaman, G. S. and Pinkster, S. (1977). Freshwater Gammarus species from Europe, North Africa and adjacent regions of Asia (Crustacea-Amphipoda). Part II. Gammarus roeseli-group and related species. Bijdragen Tot de Dierkunde 47, 165–196.CrossRefGoogle Scholar
Kennedy, C. R. (2006). Ecology of the Acanthocephala, Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Kuo, C.-H., Corby-Harris, V. and Promislow, D. E. L. (2008). The unavoidable costs and unexpected benefits of parasitism: Population and metapopulation models of parasite-mediated competition. Journal of Theoretical Biology 250, 244–256.Google Scholar
Labbé, P. and Little, T. J. (2009). ProPhenolOxidase in Daphnia magna: cDNA sequencing and expression in relation to resistance to pathogens. Developmental & Comparative Immunology 33, 674–680.Google Scholar
Lagrue, C., Kaldonski, N., Perrot-Minnot, M. J., Motreuil, S. and Bollache, L. (2007). Modification of host's behavior by a parasite: field evidence for adaptive manipulation. Ecology 88, 2839–2847.CrossRefGoogle ScholarPubMed
Lee, K. A. and Klasing, K. C. (2004). A role for immunology in invasion biology. Trends in Ecology & Evolution 19, 523–529.Google Scholar
Lee, K. A., Martin Ii, L. B. and Wikelski, M. (2005). Responding to inflammatory challenges is less costly for a successful avian invader, the hous sparrow (Passer domesticus), than its less-invasive congener. Oecologia 145, 244–251.Google Scholar
Lemaître, J.-F., Rigaud, T., Cornet, S. and Bollache, L. (2009). The effect of sperm depletion on male mating behaviour and reproductive “time-out” in Gammarus pulex (Crustacea). Animal Behaviour 77, 49–54.CrossRefGoogle Scholar
Loker, E. S. (1994). On being a parasite in an invertebrate host: a short survival course. Journal of Parasitology 80, 728–747.Google Scholar
Loukas, A. and Maizels, R. M. (2000). Helminth C-type lectins and host-parasite interactions. Parasitology Today 16, 333–339.Google Scholar
Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M. D. and Allen, J. E. (2004). Helminth parasites – masters of regulation. Immunological Reviews 201, 89–116.Google Scholar
Moret, Y., Bollache, L., Wattier, R. and Rigaud, T. (2007). Is the host or the parasite the most locally adapted in an amphipod-acanthocephalan relationship? A case study in a biological invasion context. International Journal for Parasitology 37, 637–644.CrossRefGoogle ScholarPubMed
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, 346–351.Google Scholar
Prenter, J., Macneil, C., Dick, J. T. A. and Dunn, A. M. (2004). Roles of parasites in animal invasions. Trends in Ecology & Evolution 19, 385–390.Google Scholar
Rigaud, T. and Moret, Y. (2003). Differential phenoloxidase activity between native and invasive gammarids infected by local acanthocephalans: differential immunosuppression? Parasitology 127, 571–577.CrossRefGoogle ScholarPubMed
Rivero, A., Agnew, P., Bedhomme, S., Sidobre, C. and Michalakis, Y. (2007). Resource depletion in Aedes aegypti mosquitoes infected by the microsporidia Vavraia culicis. Parasitology 134, 1355–1362.Google Scholar
Rivero, A. and Ferguson, H. M. (2003). The energtic budget of Anopheles stephensi infected with Plasmodium chabaudi: is energy depletion a mechanism for virulence? Proceedings of the Royal Society of London, B 270, 1365–1371.CrossRefGoogle Scholar
Sakai, A. K., Allendorf, F. W., Holt, J. S., Lodge, D. M., Molofsky, J., With, K. A., Baughman, S., Cabin, R. J., Cohen, J. E., Ellstrand, N. C., McCauley, D. E., O'Neil, P., Parker, I. M., Thompson, J. N. and Weller, S. G. (2001). The population biology of invasive species. Annual Review of Ecology and Systematics 32, 305–332.Google Scholar
Schmid-Hempel, P. (2003). Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London, B 270, 357–366.Google Scholar
Shelby, K. S., Adeyeye, O. A., Okot-Kotber, B. M. and Webb, B. A. (2000). Parasitism-linked block of host plasma melanization. Journal of Invertebrate Pathology 75, 218–225.Google Scholar
Tain, L., Perrot-Minnot, M.-J. and Cézilly, F. (2007). Differential influence of Pomphorhynchus laevis (Acanthocepahala) on brain serotonergic activity in two congeneric host species. Biology Letters 3, 68–71.CrossRefGoogle ScholarPubMed
Taraschewski, H. (2000). Host-parasite interactions in Acanthocephala: a morphological approach. Advances in Parasitology 46, 1–179.Google Scholar
Theodoropoulos, G., Hicks, S. J., Corfield, A. P., Miller, B. G. and Carrington, S. (2001). The role of mucins in host-parasite interactions: Part II – helminth parasites. Trends in Parasitology 17, 130–135.CrossRefGoogle ScholarPubMed
Torchin, M. E., Lafferty, K. D., Dobson, A. P., Mckenzie, V. J. and Kuris, A. M. (2003). Introduced species and their missing parasites. Nature, London 421, 628–630.Google Scholar
Torchin, M. E., Lafferty, K. D. and Kuris, A. M. (2002). Parasites and marine invasions. Parasitology 124 (Suppl), S137–S151.CrossRefGoogle Scholar
Volkmann, A. (1991). Localization of phenoloxidase in the midgut of Periplaneta americana parasitized by larvae of Moniliformis moniliformis (Acanthocephala). Parasitology Research 77, 616–621.CrossRefGoogle ScholarPubMed