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Behavioural fever in infected honeybees: parasitic manipulation or coincidental benefit?

Published online by Cambridge University Press:  26 May 2010

JENNIFER CAMPBELL
Affiliation:
Department of Biology, Colorado State University, Fort Collins, CO80523, USA
BETH KESSLER
Affiliation:
Department of Biology, Colorado State University, Fort Collins, CO80523, USA
CHRISTOPHER MAYACK
Affiliation:
Department of Biology, Colorado State University, Fort Collins, CO80523, USA
DHRUBA NAUG*
Affiliation:
Department of Biology, Colorado State University, Fort Collins, CO80523, USA
*
*Corresponding author: Tel: +1 970 491 2651. Fax: +1 970 491 0649. E-mail: [email protected]

Summary

Infection by a parasite often induces behavioural changes in the host and these changes may benefit either the host or the parasite. However, whether these changes are active host defence mechanisms or parasitic manipulations or simply incidental byproducts of the infection is not always clear. It has been suggested that understanding the proximate mechanisms of these changes as well as comparative studies could help distinguish these alternatives better. Behavioural fever is a common response to an infection in many animals and we investigated the phenomenon in the novel host-parasite relationship between the honeybee and the temperature-sensitive microsporidian Nosema ceranae. Our results show that infected bees prefer higher temperatures and even though this seems to benefit the pathogen, the proximate mechanism underlying this change is the pathological stress underlying the infection. Especially because it is a new host-parasite relationship, it is best to label the observed behavioural change as a case of incidental benefit although this does not rule out selection acting on it. We discuss the importance of looking at the behavioural outcomes of host-parasite relationships and the importance of studying them at multiple levels for understanding their origin and maintenance.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Bailey, L. (1981). Honey Bee Pathology. Academic Press, London, UK.Google Scholar
Dawkins, R. (1990). Parasites, desiderata lists and the paradox of the organism. Parasitology 100, S63S73.CrossRefGoogle ScholarPubMed
Fialho, R. F. and Schall, J. J. (1995). Thermal ecology of a malarial parasite and its insect vector: Consequences for the parasite's transmission success. Journal of Animal Ecology 64, 553562.CrossRefGoogle Scholar
Gould, S. J. and Lewontin, R. C. (1979). The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London, B 205, 581598.Google Scholar
Klee, J., Besana, A. M., Genersch, E., Gisder, S., Nanetti, A., Tam, D. Q., Chinh, T. X., Puerta, F., Ruz, J. M., Kryger, P., Message, D., Hatjina, F., Korpela, S., Fries, I. and Paxton, R. J. (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology 96, 110.CrossRefGoogle ScholarPubMed
Kluger, M. J. (1979). Fever in ectotherms: evolutionary implications. American Zoologist 19, 295304.CrossRefGoogle Scholar
Martín-Hernández, R., Meana, A., García-Palencia, P., Marín, P., Botías, C., Garrido-Bailón, E., Barrios, L. and Higes, M. (2009). Effect of temperature on the biotic potential of honeybee microsporidia. Applied and Environmental Microbiology 75, 25542557.CrossRefGoogle ScholarPubMed
Martín-Hernández, R., Meana, A., Prieto, L., Martínez Salvador, A., Garrido-Bailón, E. and Higes, M. (2007). Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology 73, 63316338.CrossRefGoogle ScholarPubMed
Mayack, C. and Naug, D. (2009). Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. Journal of Invertebrate Pathology 100, 185188.CrossRefGoogle ScholarPubMed
Moore, J. (2002). Parasites and the Behavior of Animals. Oxford University Press, New York, USA.CrossRefGoogle Scholar
Moore, J. and Freehling, M. (2002). Cockroach hosts in thermal gradients suppress parasite development. Oecologia 133, 261266.CrossRefGoogle ScholarPubMed
Müller, C. B. and Schmid-Hempel, P. (1993). Exploitation of cold temperature as defence against parasitoids in bumblebees. Nature, London 363, 6567.CrossRefGoogle Scholar
Poulin, R. (1994). The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109, S109S118.CrossRefGoogle ScholarPubMed
Poulin, R. (1995). “Adaptive” changes in the behaviour of parasitized animals: a critical review. International Journal for Parasitology 25, 13711383.CrossRefGoogle ScholarPubMed
Reeve, H. K. and Sherman, P. W. (1993). Adaptation and the goals of evolutionary research. Quarterly Review of Biology 68, 132.CrossRefGoogle Scholar
Robb, T. and Reid, M. L. (1996). Parasite-induced changes in the behaviour of cestode-infected beetles: adaptation or simple pathology? Canadian Journal of Zoology 74, 12681274.CrossRefGoogle Scholar
Starks, P. T., Blackie, C. A. and Seeley, T. D. (2000). Fever in honeybee colonies. Naturwissenschaften 87, 229231.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
Thompson, S. N. and Kavaliers, M. (1994). Physiological bases for parasite-induced alterations of host behaviour. Parasitology 109, S119S138.CrossRefGoogle ScholarPubMed
Watson, D. W., Mullens, B. A. and Petersen, J. J. (1993). Behavioral Fever response of Musca domestica (Diptera: Muscidae) to infections by Entomophthora muscae (Zygomycetes: Entomophthorales). Journal of Invertebrate Pathology 61, 1016.CrossRefGoogle Scholar