Abstract
The energy and nutrient demands of parasites on their hosts are frequently invoked as an explanation for negative impacts of parasitism on host survival and reproductive success. Although cuterebrid bot flies are among the physically largest and most-studied insect parasites of mammals, the only study conducted on metabolic consequences of bot fly parasitism revealed a surprisingly small effect of bot flies on host metabolism. Here we test the prediction that bot fly parasitism increases the resting metabolic rate (RMR) of free-ranging eastern chipmunks (Tamias striatus), particularly in juveniles who have not previously encountered parasites and have to allocate energy to growth. We found no effect of bot fly parasitism on adults. In juveniles, however, we found that RMR strongly increased with the number of bot fly larvae hosted. For a subset of 12 juveniles during a year where parasite prevalence was particularly high, we also compared the RMR before versus during the peak of bot fly prevalence, allowing each individual to act as its own control. Each bot fly larva resulted in a ~7.6% increase in the RMR of its host while reducing juvenile growth rates. Finally, bot fly parasitism at the juvenile stage was positively correlated with adult stage RMR, suggesting persistent effects of bot flies on RMR. This study is the first to show an important effect of bot fly parasitism on the metabolism and growth of a wild mammal. Our work highlights the importance of studying cost of parasitism over multiple years in natural settings, as negative effects on hosts are more likely to emerge in periods of high energetic demand (e.g. growing juveniles) and/or in harsh environmental conditions (e.g. low food availability).
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Acknowledgments
We thank J. P. Boyer, M. Descôteaux, R. Morin, and all field assistants who have helped to collect the data presented in this paper and to P. Bourgault for help with data management. We are grateful to M. Odiere, M. Scott, three anonymous reviewers, and especially P. Koteja for helpful comments on earlier drafts of this manuscript. This research was supported by a Québec FQRNT team grant, NSERC discovery grants to D. T. and M. M. H., and a NSERC doctoral scholarship to V. C. Animals were captured and handled with compliance to the Canadian Council on Animal Care (no. 2007-DT01-Université de Sherbrooke) and the Ministère des Ressources Naturelles et de la Faune du Québec (no. 2008-04-15-101-05-S-F). We are grateful to the Ruiter Valley Land Trust for allowing us to conduct this research within their boundaries.
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Communicated by Pawel Koteja.
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Careau, V., Thomas, D.W. & Humphries, M.M. Energetic cost of bot fly parasitism in free-ranging eastern chipmunks. Oecologia 162, 303–312 (2010). https://doi.org/10.1007/s00442-009-1466-y
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DOI: https://doi.org/10.1007/s00442-009-1466-y