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Acanthocephalan size and sex affect the modification of intermediate host colouration

Published online by Cambridge University Press:  19 May 2009

D. P. BENESH*
Affiliation:
Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306Plön, Germany
O. SEPPÄLÄ
Affiliation:
EAWAG, Department of Aquatic Ecology, and ETH-Zürich, Institute of Integrative Biology, Überlandstrasse 133, 8600Dübendorf, Switzerland
E. T. VALTONEN
Affiliation:
Department of Biological and Environmental Science, POB 35, FI-40014University of Jyväskylä, Finland
*
*Corresponding author: Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306Plön, Germany. Tel: +494522763258; fax: +494522763310. E-mail: [email protected]

Summary

For trophically transmitted parasites, transitional larval size is often related to fitness. Larger parasites may have higher establishment success and/or adult fecundity, but prolonged growth in the intermediate host increases the risk of failed transmission via natural host mortality. We investigated the relationship between the larval size of an acanthocephalan (Acanthocephalus lucii) and a trait presumably related to transmission, i.e. altered colouration in the isopod intermediate host. In natural collections, big isopods harboured larger worms and had more modified (darker) abdominal colouration than small hosts. Small isopods infected with a male parasite tended to have darker abdominal pigmentation than those infected with a female, but this difference was absent in larger hosts. Female size increases rapidly with host size, so females may have more to gain than males by remaining in and growing mutually with small hosts. In experimental infections, a large total parasite volume was associated with darker host respiratory operculae, especially when it was distributed among fewer worms. Our results suggest that host pigment alteration increases with parasite size, albeit differently for male and female worms. This may be an adaptive strategy if, as parasites grow, the potential for additional growth decreases and the likelihood of host mortality increases.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Abrams, P. A., Leimar, O., Nylin, S. and Wiklund, C. (1996). The effect of flexible growth rates on optimal sizes and development times. American Naturalist 147, 381395.CrossRefGoogle Scholar
Amin, O. M., Burns, L. A. and Redlin, M. J. (1980). The ecology of Acanthocephalus parksidei (Acanthocephala: Echinorhynchidae) in its isopod intermediate host. Proceedings of the Helminthological Society of Washington 47, 3746.Google Scholar
Andryuk, L. V. (1979). Developmental cycle of the thorny-headed worm, Acanthocephalus lucii (Echinorhynchidae). Parazitologiia 13, 530539 (in Russian).Google Scholar
Benesh, D. P. and Valtonen, E. T. (2007 a). Effects of Acanthocephalus lucii (Acanthocephala) on intermediate host survival and growth: implications for exploitation strategies. Journal of Parasitology 93, 735741.CrossRefGoogle ScholarPubMed
Benesh, D. P. and Valtonen, E. T. (2007 b). Proximate factors affecting the larval life history of Acanthocephalus lucii (Acanthocephala). Journal of Parasitology 93, 742749.CrossRefGoogle ScholarPubMed
Benesh, D. P. and Valtonen, E. T. (2007 c). Sexual differences in larval life history traits of acanthocephalan cystacanths. International Journal for Parasitology 37, 191198.CrossRefGoogle ScholarPubMed
Benesh, D. P., Valtonen, E. T. and Seppälä, O. (2008). Multidimentionality and intra-individual variation in host manipulation by parasites. Parasitology 135, 617626.CrossRefGoogle Scholar
Benesh, D. P., Hasu, T., Seppälä, O. and Valtonen, E. T. (2009). Seasonal changes in host phenotype manipulation by an acanthocephalan: time to be transmitted? Parasitology 136, 219230.CrossRefGoogle ScholarPubMed
Berrigan, D. and Koella, J. C. (1994). The evolution of reaction norms: simple models for age and size at maturity. Journal of Evolutionary Biology 7, 549566.CrossRefGoogle Scholar
Bethel, W. M. and Holmes, J. C. (1974). Correlation of altered evasive behavior in Gammarus lacustris (Amphipoda) harboring cystacanths of Polymorphus paradoxus (Acanthocephala) with the infectivity to the definitive host. Journal of Parasitology 60, 272274.CrossRefGoogle Scholar
Brattey, J. (1983). The effects of larval Acanthocephalus lucii on the pigmentation, reproduction and susceptibility to predation of the isopod Asellus aquaticus. Journal of Parasitology 69, 11721173.CrossRefGoogle Scholar
Brattey, J. (1986). Life history and population biology of larval Acanthocephalus lucii (Acanthocephala: Echinorhynchidae) in the isopod Asellus aquaticus. Journal of Parasitology 72, 633645.CrossRefGoogle ScholarPubMed
Brown, S. P., Loot, G., Grenfell, B. T. and Guégan, J. F. (2001). Host manipulation by Ligula intestinalis: accident or adaptation? Parasitology 123, 519529.CrossRefGoogle ScholarPubMed
Day, T. and Rowe, L. (2002). Developmental thresholds and the evolution of reaction norms for age and size at life history transitions. American Naturalist 159, 338350.CrossRefGoogle ScholarPubMed
Duerr, H. P., Dietz, K. and Eichner, M. (2003). On the interpretation of age-intensity profiles and dispersion patterns in parasitological surveys. Parasitology 126, 87–101.CrossRefGoogle ScholarPubMed
Franceshi, N., Bauer, A., Bollache, L. and Rigaud, T. (2008). The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation. International Journal for Parasitology 38, 11611170.CrossRefGoogle Scholar
Fredensborg, B. L. and Poulin, R. (2005). Larval helminthes in intermediate hosts: does competition early in life determine the fitness of adult parasites? International Journal for Parasitology 35, 10611070.CrossRefGoogle ScholarPubMed
Hargeby, A., Johansson, J. and Ahnesjö, J. (2004). Habitat-specific pigmentation in a freshwater isopod: adaptive evolution over a small spatiotemporal scale. Evolution 58, 8194.Google Scholar
Hargeby, A., Stoltz, J. and Johansson, J. (2005). Locally differentiated cryptic pigmentation in the freshwater isopod Asellus aquaticus. Journal of Evolutionary Biology 18, 713721.CrossRefGoogle ScholarPubMed
Hasu, T., Holmes, J. C. and Valtonen, E. T. (2007). Isopod size (Asellus aquaticus) and acanthocephalan (Acanthocephalus lucii) infections. Journal of Parasitology 93, 450457.CrossRefGoogle ScholarPubMed
Iwasa, Y. and Wada, G. (2006). Complex life cycle and body sizes at life-history transitions for macroparasites. Evolutionary Ecology Research 8, 14271443.Google Scholar
Kaldonski, N., Perrot-Minnot, M.-J., Dodet, R., Martinaud, G. and Cézilly, F. (2009). Carotenoid-based colour of acanthocephalan cystacanths plays no role in host manipulation. Proceedings of the Royal Society of London, B 276, 169176.Google ScholarPubMed
Mason, C. H. and Perreault, W. D. (1991). Collinearity, power, and interpretation of multiple regression analysis. Journal of Marketing Research 28, 268280.CrossRefGoogle Scholar
Michaud, M., Milinski, M., Parker, G. A. and Chubb, J. C. (2006). Competitive growth strategies in intermediate hosts: experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus. Evolutionary Ecology 20, 3957.CrossRefGoogle Scholar
Moore, J. (2002). Parasites and the Behavior of Animals. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Ness, J. H. and Foster, S. A. (1999). Parasite-associated phenotype modifications in threespine stickleback. Oikos 85, 127134.CrossRefGoogle Scholar
Oetinger, D. F. and Nickol, B. B. (1981). Effects of acanthocephalans on pigmentation of freshwater isopods. Journal of Parasitology 67, 672684.CrossRefGoogle Scholar
Outreman, Y., Cézilly, F. and Bollache, L. (2007). Field evidence of host size-dependent parasitism in two manipulative parasites. Journal of Parasitology 93, 750754.CrossRefGoogle ScholarPubMed
Parker, G. A., Chubb, J. C., Roberts, G. N., Michaud, M. and Milinski, M. (2003). Optimal growth strategies of larval helminths in their intermediate hosts. Journal of Evolutionary Biology 16, 4754.CrossRefGoogle ScholarPubMed
Poulin, R., Curtis, M. A. and Rau, M. E. (1992). Effects of Eubothrium salvelini (Cestoda) on the behaviour of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105, 265271.CrossRefGoogle Scholar
Pulkkinen, K., Pasternak, A. F., Hasu, T. and Valtonen, E. T. (2000). Effect of Triaenophorus crassus (Cestoda) infection on behavior and susceptibility to predation of the first intermediate host Cyclops strenuous (Copepoda). Journal of Parasitology 86, 664670.CrossRefGoogle Scholar
Rosen, R. and Dick, T. A. (1983). Development and infectivity of the procercoid of Triaenophorus crassus Forel and mortality of the first intermediate host. Canadian Journal of Zoology 61, 21202128.CrossRefGoogle Scholar
Rousset, F., Thomas, F., de MeeÛs, T. and Renaud, F. (1996). Inference of parasite-induced host mortality from distributions of parasite loads. Ecology 77, 22032211.CrossRefGoogle Scholar
Rowe, L. and Ludwig, D. (1991). Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72, 413427.CrossRefGoogle Scholar
Seppälä, O., Karvonen, A. and Valtonen, E. T. (2005). Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Animal Behaviour 70, 889894.CrossRefGoogle Scholar
Seppälä, O., Valtonen, E. T. and Benesh, D. P. (2008). Host manipulation by parasites in the world of dead-end predators: adaptation to enhance transmission? Proceedings of the Royal Society of London, B 275, 16111615.Google ScholarPubMed
Shostak, A. W., Walsh, J. G. and Wong, Y. C. (2008). Manipulation of host food availability and use of multiple exposures to assess the crowding effect on Hymenolepis diminuta in Tribolium confusum. Parasitology 135, 10191033.CrossRefGoogle ScholarPubMed
Stearns, S. C. (1992). The Evolution of Life Histories. Oxford University Press, Oxford, UK.Google Scholar
Steinauer, M. L. and Nickol, B. B. (2003). Effect of cystacanth body size on adult success. Journal of Parasitology 89, 251254.CrossRefGoogle ScholarPubMed
Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185199.CrossRefGoogle ScholarPubMed
Thomas, F., Renaud, F., Rousset, F., Cézilly, F. and de MeeÛs, T. (1995). Differential mortality of two closely related host species induced by one parasite. Proceedings of the Royal Society of London, B 260, 349352.Google Scholar