Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-26T21:43:24.408Z Has data issue: false hasContentIssue false

Differential phenoloxidase activity between native and invasive gammarids infected by local acanthocephalans: differential immunosuppression?

Published online by Cambridge University Press:  05 December 2003

T. RIGAUD
Affiliation:
Equipe Ecologie-Evolutive, UMR CNRS 5561 Biogéosciences, Université de Bourgogne, 6 Boulevard Gabriel, 21000 Dijon, France
Y. MORET
Affiliation:
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK

Abstract

Manipulative endoparasites can alter the behaviour and the physiology of their intermediate hosts in ways that increase the probability of successful transmission to the final host. This requires that the parasite is able to circumvent its host's immune defence. Successful immune evasion may depend on host–parasite coevolutionary history and the appearance of new hosts invading the local host population may promote local parasite maladaptation. To test this hypothesis, we examined the effect of 2 acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus minutus, on the immunity of their local and new invasive gammarid intermediate hosts, respectively Gammarus pulex and Gammarus roeseli. We found that infection by each parasite was correlated with a decrease, at different degrees, of the standing level of immune defence in local hosts – measured as the phenoloxidase (PO) enzyme activity – whereas invasive hosts infected by P. laevis had their PO-enzyme activity enhanced. These results suggest that these acanthocephalans evade their local host immune response through immunosuppression but cannot evade the immune response of their new invasive host. The potential role of this maladaptation on the success of invasive species is discussed.

Type
Research Article
Copyright
2003 Cambridge University Press

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

REFERENCES

BAKKER, T. C. M., MAZZI, D. & ZALA, S. ( 1997). Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78, 10981104.CrossRefGoogle Scholar
BARNES, A. I. & SIVA-JOTHY, M. T. ( 2000). Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proceedings of the Royal Society of London, B 267, 177182.Google Scholar
BAUER, A., TROUVÉ, S., GRÉGOIRE, A., BOLLACHE, L. & CÉZILLY, F. ( 2000). Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native and invader gammarid species. International Journal for Parasitology 30, 14531457.CrossRefGoogle Scholar
BETHEL, W. M. & HOLMES, J. C. ( 1973). Altered evasive behavior and responses to light in amphipods harboring acanthocephalan cystacanths. Journal of Parasitology 59, 945956.CrossRefGoogle Scholar
BOËTE, C., PAUL, R. E. L. & KOELLA, J. C. ( 2002). Reduced efficacy of the immune melanization response in mosquitoes infected by malaria parasites. Parasitology 125, 9398.CrossRefGoogle Scholar
BOLLACHE, L., GAMBADE, G. & CÉZILLY, F. ( 2000). The influence of microhabitat segregation on size assortative pairing in Gammarus pulex (L.) (Crustacea, Amphipoda). Archive of Hydrobiology 147, 547558.Google Scholar
BOLLACHE, L., GAMBADE, G. & CÉZILLY, F. ( 2001). The effects of two acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus minutus, on pairing success in male Gammarus pulex (Crustacea: Amphipoda). Behavioural Ecology and Sociobiology 49, 296303.CrossRefGoogle Scholar
CÉZILLY, F., GRÉGOIRE, A. & BERTIN, A. ( 2000). Conflict between co-occurring manipulate parasites. An experimental study of joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology 120, 625630.Google Scholar
CHRISTENSEN, B. M. & LaFOND, M. M. ( 1986). Parasite-induced suppression of the immune response in Aedes aegypti by Brugia pahangi. Journal of Parasitology 72, 216219.CrossRefGoogle Scholar
CROMPTON, D. W. T. & NICKOL, B. B. ( 1985). Biology of the Acanthocephala. Cambridge University Press, Cambridge.
DAMIAN, R. T. ( 1997). Parasite immune evasion and exploitation: reflections and projections. Parasitology 115 (Suppl.), S169S175.CrossRefGoogle Scholar
DUNN, A. M. & DICK, J. T. A. ( 1998). Parasitism and epibiosis in native and non-native gammarids in freshwater in Ireland. Ecography 21, 593598.CrossRefGoogle Scholar
GANDON, S., CAPOWIEZ, Y., BUBOIS, Y., MICHALAKIS, Y. & OLIVIERI, I. ( 1996). Local adaptation and gene-for-gene coevolution in a metapopulation model. Proceedings of the Royal Society of London, B 263, 10031009.CrossRefGoogle Scholar
GILLESPIE, J., KANOST, M. R. & TRENCZECK, T. ( 1997). Biological mediators of insect immunity. Annual Review of Entomology 42, 611643.CrossRefGoogle Scholar
HOFFMANN, J. A., REICHHART, J. M. & HETRU, C. ( 1996). Innate immunity in higher insects. Current Opinion in Immunology 8, 813.CrossRefGoogle Scholar
HYNES, H. B. N. ( 1954). The ecology of Gammarus duebeni Lilljeborg and its occurence in freswater in western Britain. Journal of Animal Ecology 23, 3884.CrossRefGoogle Scholar
HYNES, H. B. N. & NICHOLAS, W. L. ( 1958). The resistance of Gammarus spp. to infection by Polymorphus minutus (Goeze, 1782) (Acanthocephala). Annals of Tropical Medicine and Parasitology 52, 376383.Google Scholar
JAZDZEWSKI, K. ( 1980). Range extension of some gammaridean species in European inland waters caused by human activity. Crustaceana S6, 84107.Google Scholar
KARAMAN, G. S. & PINKSTER, S. ( 1977). Freshwater Gammarus species from Europe, North Africa and adjacent region of Asia (Crustacea Amphipodea). II. Gammarus roeseli-group and related species. Bijdr Dierk 47, 148159.Google Scholar
LOKER, E. S. ( 1994). On being a parasite in an invertebrate host: a short survival course. Journal of Parasitology 80, 728747.CrossRefGoogle Scholar
MORAVEC, F. & SCHOLZ, T. ( 1991). Observation of the biology of Pomphorhynchus laevis (Zoega in Müller, 1776) (Acanthocephala) in the Rokytna River, Czech and Slovak Federative Republic. Helmintologia 28, 2329.Google Scholar
OUTREMAN, Y., BOLLACHE, L., PLAISTOW, S. & CÉZILLY, F. ( 2002). Patterns of intermediate host use and levels of association between two conflicting manipulative parasites. International Journal for Parasitology 32, 1520.CrossRefGoogle Scholar
PLAISTOW, S. J., TROUSSARD, J. P. & 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.CrossRefGoogle Scholar
RATCLIFFE, N. A., ROWLEY, A. F., FITZGERALD, S. W. & RHODES, C. P. ( 1985). Invertebrate immunity: basic concepts and recent advances. International Review of Cytology 97, 183350.CrossRefGoogle Scholar
ROLFF, J. ( 2002). Bateman's principle and immunity. Proceedings of the Royal Society of London, B 269, 867872.CrossRefGoogle Scholar
ROLFF, J. & SIVA-JOTHY, M. T. ( 2002). Copulation corrupts immunity: A mechanism for a cost of mating in insects. Proceedings of the National Academy of Sciences, USA 99, 99169918.CrossRefGoogle Scholar
ROUX, A. L., ROUX, C. & OPDAM, Y. ( 1980). Répartition écologique et métabolisme respiratoire de Gammarus roeseli Gervais 1835. Crustaceana S6, 11651196.Google Scholar
SAS INSTITUTE ( 1997). JMP Statistics and Graphic Guide. Cary, USA.
SÖDERHÄLL, K., CERENIUS, L. & JOHANSSON, M. W. (1996). New direction in invertebrate immunology. In The Prophenoloxidase Activating System in Invertebrates ( ed. Söderhäll, K., Iwanaga, S. & Vasta, G.), pp. 229253. SOS Publications, Fair Haven.
SÖDERHÄLL, K. & CERENIUS, L. ( 1998). Role of the prophenoloxidase-activating system in invertebrate immunity. Current Opinion in Immunology 10, 2328.CrossRefGoogle Scholar
STRAND, M. R. & PECH, L. ( 1995). Immunological basis for compatibility in parasitoid–host relationships. Annual Review of Entomology 40, 3156.CrossRefGoogle Scholar
TORCHIN, M. E., LAFFERTY, K. D. & KURIS, A. M. ( 2002). Parasites and marine invasions. Parasitology 124 ( Suppl.), S137S151.CrossRefGoogle Scholar
TORCHIN, M. E., LAFFERTY, K. D., DOBSON, A. P., MCKENZIE, V. J. & KURIS, A. M. ( 2003). Introduced species and their missing parasites. Nature, London 421, 628630.CrossRefGoogle Scholar
ZAMBRA-VILLA, S., ROSALES-BORJAS, D., CARRERO, J. C. & ORTIZ-ORTIZ, L. ( 2002). How protozoan parasites evade the immune response. Trends in Parasitology 18, 272278.CrossRefGoogle Scholar