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Seasonal changes in host phenotype manipulation by an acanthocephalan: time to be transmitted?

Published online by Cambridge University Press:  18 December 2008

D. P. BENESH ,
T. HASU ,
O. SEPPÄLÄ  and
E. T. VALTONEN
D. P. BENESH*
Affiliation:
Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306Plön, Germany
T. HASU
Affiliation:
Department of Biological and Environmental Science, POB 35, FI-40014University of Jyväskylä, Finland
O. SEPPÄLÄ
Affiliation:
EAWAG, Swiss Federal Institute of Aquatic Science and Technology, and ETH-Zürich, Institute of Integrative Biology (IBZ), Überlandstrasse 133, PO Box 611, CH-8600, Dübendorf, 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: +49 4522763258. Fax: +49 4522763310. E-mail: benesh@evolbio.mpg.de
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Summary

Many complex life cycle parasites exhibit seasonal transmission between hosts. Expression of parasite traits related to transmission, such as the manipulation of host phenotype, may peak in seasons when transmission is optimal. The acanthocephalan Acanthocephalus lucii is primarily transmitted to its fish definitive host in spring. We assessed whether the parasitic alteration of 2 traits (hiding behaviour and coloration) in the isopod intermediate host was more pronounced at this time of year. Refuge use by infected isopods was lower, relative to uninfected isopods, in spring than in summer or fall. Infected isopods had darker abdomens than uninfected isopods, but this difference did not vary between seasons. The level of host alteration was unaffected by exposing isopods to different light and temperature regimes. In a group of infected isopods kept at 4°C, refuge use decreased from November to May, indicating that reduced hiding in spring develops during winter. Keeping isopods at 16°C instead of 4°C resulted in higher mortality but not accelerated changes in host behaviour. Our results suggest that changes in host and/or parasite age, not environmental conditions, underlie the seasonal alteration of host behaviour, but further work is necessary to determine if this is an adaptive parasite strategy to be transmitted in a particular season.

Keywords

AcanthocephalaAsellus aquaticushost manipulationhost-parasite interactionhost pigmentationintermediate hostplastic/flexible behaviourseasonalitytrophic transmission
Type
Research Article
Information
Parasitology , Volume 136 , Issue 2 , February 2009 , pp. 219 - 230
Copyright
Copyright © 2008 Cambridge University Press

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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, 381–395.CrossRefGoogle Scholar
Andryuk, L. V. (1979). Developmental cycle of the thorny-headed worm, Acanthocephalus lucii (Echinorhynchidae). Parazitologiia 13, 530–539 (in Russian).Google Scholar
Amundsen, P.-A., Knudsen, R., Kuris, A. M. and Kristoffersen, R. (2003). Seasonal and ontogenetic dynamics in trophic transmission of parasites. Oikos 102, 285–293.CrossRefGoogle Scholar
Atkinson, D. (1994). Temperature and organism size: a biological law for ectotherms? Advances in Ecological Research 25, 1–58.CrossRefGoogle Scholar
Bakker, T. C. M., Mazzi, D. and Zala, S. (1997). Parasite-induced changes in behaviour and color make Gammarus pulex more prone to fish predation. Ecology 78, 1098–1104.CrossRefGoogle 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, 735–741.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, 742–749.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, 191–198.CrossRefGoogle ScholarPubMed
Benesh, D. P., Valtonen, E. T. and Seppälä, O. (2008). Multidimentionality and intra-individual variation in host manipulation by an acanthocephalan. Parasitology 135, 617–626.CrossRefGoogle Scholar
Bethel, W. M. and Holmes, J. C. (1977). Increased vulnerability of amphipods to predation owing to altered behaviour induced by larval acanthocephalans. Canadian Journal of Zoology 55, 110–115.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, 1172–1173.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, 633–645.CrossRefGoogle ScholarPubMed
Brattey, J. (1988). Life history and population biology of adult Acanthocephalus lucii (Acanthocephala: Echinorhynchidae). Journal of Parasitology 74, 72–80.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, 519–529.CrossRefGoogle ScholarPubMed
Chubb, J. C. (1982). Seasonal occurrence of helminths in freshwater fishes. Part IV. Adult Cestoda, Nematoda, and Acanthocephala. Advances in Parasitology 20, 1–292.CrossRefGoogle ScholarPubMed
Cohen, J. (1988). Statistical Power Analyses for the Behavioural Sciences. 2nd Edn. Erlbaum Associates, Hillsdale, NJ, USA.Google Scholar
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, 1161–1170.CrossRefGoogle Scholar
Gotthard, K. (2001). Growth strategies of ectothermic animals in temperate environments. In Environment and Animal Development (ed. Atkinson, D. and Thorndyke, M.), pp. 287–304. BIOS Scientific Publishers, Oxford, UK.Google Scholar
Graca, M. A. S., Maltby, L. and Calow, P. (1993). Importance of fungi in the diet of Gammarus pulex and Asellus aquaticus I: feeding strategies. Oecologia 96, 139–144.CrossRefGoogle Scholar
Hasu, T., Holmes, J. C. and Valtonen, E. T. (2007). Isopod size (Asellus aquaticus) and acanthocephalan (Acanthocephalus lucii) infections. Journal of Parasitology 93, 450–457.CrossRefGoogle ScholarPubMed
Johansson, F. and Rowe, L. (1999). Life history and behavioural responses to time constraints in a damselfly. Ecology 80, 1242–1252.CrossRefGoogle Scholar
Lagrue, C., Kaldonski, N., Perrot-Minnot, M. J., Motreuil, S. and Bollache, L. (2007). Modification of hosts' behaviour by a parasite: field evidence for adaptive manipulation. Ecology 88, 2839–2847.CrossRefGoogle ScholarPubMed
Leimar, O. (1996). Life history plasticity: influence of photoperiod on growth and development in the common blue butterfly. Oikos 76, 228–234.CrossRefGoogle Scholar
Levri, E. P., Lunnen, S. J., Itle, C. T., Mosquea, L., Kinkade, B. V., Martin, T. G. and DeLisser, M. A. (2007). Parasite-induced alteration of diurnal rhythms in a freshwater snail. Journal of Parasitology 93, 231–237.CrossRefGoogle Scholar
Lyndon, A. R. (1996). The role of acanthocephalan parasites in the predation of freshwater isopods by fish. In Aquatic Predators and their Prey (ed. Greenstreet, S. P. R. and Tasker, M. L.), pp. 26–32. Blackwell Scientific, Oxford, UK.Google Scholar
Margraf, N., Gotthard, K. and Rahier, M. (2003). The growth strategy of an alpine beetle: maximization or individual growth adjustment in relation to seasonal time horizons? Functional Ecology 17, 605–610.CrossRefGoogle Scholar
Moore, J. (1983). Responses of an avian predator and its isopod prey to an acanthocephalan parasite. Ecology 64, 1000–1015.CrossRefGoogle Scholar
Moore, J. (2002). Parasites and the Behaviour of Animals. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Mouritsen, K. M. and Poulin, R. (2003). Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare. International Journal for Parasitology 33, 1043–1050.CrossRefGoogle ScholarPubMed
Nakagawa, S. (2004). A farewell to Bonferroni: the problems of low statistical power and publication bias. Behavioral Ecology 15, 1044–1045.CrossRefGoogle Scholar
Nickol, B. B. (1985). Epizootiology. In Biology of the Acanthocephala (ed. Nickol, B. B. and Crompton, D. W. T.), pp. 307–346. Cambridge University Press, Cambridge, UK.Google Scholar
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, 47–54.CrossRefGoogle ScholarPubMed
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, 645–651.CrossRefGoogle Scholar
Poulin, R. (1994). The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109, S109–S118.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Rask, M. and Hiisivuori, C. (1985). Predation on Asellus aquaticus (L.) by perch, Perca fluviatilis (L.), in a small forest lake. Hydrobiologia 121, 27–33.CrossRefGoogle Scholar
Rowe, L. and Ludwig, D. (1991). Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72, 413–427.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 Soceity of London, B 275, 1611–1615.Google ScholarPubMed
Skorping, A. (1980). Population biology of the nematode Camallanus lacustris in perch, Perca fluviatilis L., from an oligotrophic lake in Norway. Journal of Fish Biology 16, 483–492.CrossRefGoogle Scholar
Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185–199.CrossRefGoogle ScholarPubMed
Wahl, C. M., Mills, E. L., McFarland, W. N. and DeGisi, J. S. (1993). Ontogenetic changes in prey selection and visual acuity of the yellow perch, Perca flavescens. Canadian Journal of Fisheries and Aquatic Sciences 50, 743–749.CrossRefGoogle Scholar
Wilson, K. and Grenfell, B. T. (1997). Generalized linear modelling for parasitologists. Parasitology Today 13, 33–38.CrossRefGoogle ScholarPubMed