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Bot fly parasitism of the red-backed vole: host survival, infection risk, and population growth

  • Population Ecology - Original Paper
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Abstract

Parasites can play an important role in the dynamics of host populations, but empirical evidence remains sparse. We investigated the role of bot fly (Cuterebra spp.) parasitism in red-backed voles (Myodes gapperi) by first assessing the impacts of the parasite on the probability of vole survival under stressful conditions as well as on the reproductive activity of females. We then identified the main factors driving both the individual risk of infection and the abundance of bot flies inside red-backed voles. Finally, we evaluated the impacts of bot fly prevalence on the growth rate of vole populations between mid-July and mid-August. Thirty-six populations of red-backed voles were sampled in the boreal forest of Québec, Canada. The presence and the abundance of parasites in voles, two host life history traits (sex and body condition), three indices of habitat complexity (tree basal area, sapling basal area, coarse woody debris volume), and vole abundance were considered in models evaluating the effects of bot flies on host populations. We found that the probability of survival of red-backed voles in live traps decreased with bot fly infection. Both the individual risk of infection and the abundance of bot flies in red-backed voles were driven mainly by vole abundance rather than by the two host life history traits or the three variables of habitat complexity. Parasitism had population consequences: bot fly prevalence was linked to a decrease in short-term growth rate of vole populations over the summer. We found that bot flies have the potential to reduce survival of red-backed voles, an effect that may apply to large portions of populations.

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References

  • Abramsky Z, Rosenzweig ML, Subach A (2000) The energetic cost of competition: Gerbils as moneychangers. Evol Ecol Res 2:279–292

    Google Scholar 

  • Albon SD, Stien A, Irvine RJ, Langvatn R, Ropstad E, Halvorsen O (2002) The role of parasites in the dynamics of a reindeer population. Proc R Soc Lond B Biol Sci 269:1625–1632

    Article  CAS  Google Scholar 

  • Anderson RM, May RM (1978) Regulation and stability of host-parasite population interactions. I. Regulatory processes. J Anim Ecol 47:219–247

    Article  Google Scholar 

  • Bates D, Sarkar D (2006) lme4: linear mixed-effects models using S4 classes. R package version 0.9975–7

  • Beauvais GP, Buskirk SW (1999) Modifying estimates of sampling effort to account for sprung traps. Wildl Soc Bull 27:32–38

    Google Scholar 

  • Boonstra R, Krebs CJ (2006) Population limitation of the northern red-backed vole in the boreal forests of northern Canada. J Anim Ecol 75:1269–1284

    Article  PubMed  Google Scholar 

  • Boonstra R, Krebs CJ, Beacham TD (1980) Impact of botfly parasitism on Microtus townsendii populations. Can J Zool 58:1683–1692

    Article  Google Scholar 

  • Boucher D, De Granpré L, Gauthier S (2003) Développement d’un outil de classification de la structure des peuplements et comparaison de deux territoires de la pessière à mousses du Québec. For Chron 79:318–328

    Google Scholar 

  • Bowman J (2000) Forest components associated with parasitism of small mammals by botflies (Cuterebra). Mammalia 64:243–247

    Google Scholar 

  • Brown LN (1965) Botfly parasitism in the brush mouse and white-footed mouse in the Ozarks. J Parasitol 51:302–304

    Article  PubMed  CAS  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information—theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Burns CE, Goodwin BJ, Ostfeld RS (2005) A prescription for longer life? Bot fly parasitism of the white-footed mouse. Ecology 86:753–761

    Article  Google Scholar 

  • Catts EP (1982) Biology of New World bot flies: Cuterebridae. Annu Rev Entomol 27:313–338

    Article  Google Scholar 

  • Chappell MA, Garland T, Rezende EL, Gomes FR (2004) Voluntary running in deer mice: speed, distance, energy costs and temperature effects. J Exp Biol 207:3839–3854

    Article  PubMed  Google Scholar 

  • Clark BK, Kaufman DW (1990) Prevalence of botfly (Cuterebra spp.) parasitism in populations of small mammals in eastern Kansas. Am Midl Nat 124:22–30

    Article  Google Scholar 

  • Cockle KL, Richardson JS (2003) Do riparian buffer strips mitigate the impacts of clearcutting on small mammals? Biol Conserv 113:133–140

    Article  Google Scholar 

  • Cramer MJ, Cameron GN (2006) Effects of bot fly (Cuterebra fontinella) parasitism on a population of white-footed mice (Peromyscus leucopus). J Mammal 87:1103–1111

    Article  Google Scholar 

  • Dobson AP, Hudson PJ (1992) Regulation and stability of a free-living host-parasite system—Trichostrongylus tenuis in red grouse. 2. Population-models. J Anim Ecol 61:487–498

    Article  Google Scholar 

  • Dunaway PB, Payne JA, Lewis LL, Story JD (1967) Incidence and effects of Cuterebra in Peromyscus. J Mammal 48:38–51

    Article  PubMed  CAS  Google Scholar 

  • Eccard JA, Ylonen H (2002) Direct interference or indirect exploitation? An experimental study of fitness costs of interspecific competition in voles. Oikos 99:580–590

    Article  Google Scholar 

  • Eccard JA, Ylonen H (2003) Interspecific competition in small rodents: from populations to individuals. Evol Ecol 17:423–440

    Article  Google Scholar 

  • Falls JB, Falls EA, Fryxell JM (2007) Fluctuations of deer mice in Ontario in relation to seed crops. Ecol Monogr 77:19–32

    Article  Google Scholar 

  • Fielding AH, Bell JF (1997) A review for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24:38–49

    Article  Google Scholar 

  • Fletcher QE, Boonstra R (2006) Impact of live trapping on the stress response of the meadow vole (Microtus pennsylvanicus). J Zool 270:473–478

    Article  Google Scholar 

  • Galindo-Leal C (1997) Infestation of rock mice (Peromyscus difficilis) by botflies: ecological consequences of differences between sexes. J Mammal 78:900–907

    Article  Google Scholar 

  • Gilg O, Sittler B, Sabard B, Hurstel A, Sane R, Delattre P, Hanski L (2006) Functional and numerical responses of four lemming predators in high arctic Greenland. Oikos 113:193–216

    Article  Google Scholar 

  • Gingrich RE (1981) Migratory kinetics of Cuterebra fontinella (Diptera: Cuterebridae) in the white-footed mouse, Peromyscus leucopus. J Parasitol 67:398–402

    Article  PubMed  CAS  Google Scholar 

  • Guenette JS, Villard MA (2005) Thresholds in forest bird response to habitat alteration as quantitative targets for conservation. Conserv Biol 19:1168–1180

    Article  Google Scholar 

  • Hanski I, Henttonen H, Korpimaki E, Oksanen L, Turchin P (2001) Small-rodent dynamics and predation. Ecology 82:1505–1520

    Article  Google Scholar 

  • Harper JM, Austad SN (2001) Effect of capture and season on fecal glucocorticoid levels in deer mice (Peromyscus Maniculatus) and red-backed voles (Clethrionomys Gapperi). Gen Comp Endocrinol 123:337–344

    Article  PubMed  CAS  Google Scholar 

  • Hart BL (1994) Behavioral defense against parasites—interaction with parasite invasiveness. Parasitology 109:S139–S151

    Article  PubMed  Google Scholar 

  • Hart BL, Hart LA, Mooring MS, Olubayo R (1992) Biological basis of grooming behavior in antelope—the body-size, vigilance and habitat principles. Anim Behav 44:615–631

    Article  Google Scholar 

  • Hensley M (1976) Prevalence of cuterebrid parasitism among woodmice in Virginia. J Wildl Dis 12:172–179

    PubMed  CAS  Google Scholar 

  • Hosmer DW, Lemeshow S (2000) Applied logistic regression, 2nd edn. Wiley, New York

    Google Scholar 

  • Hunter DM, Sadleir RMFS, Webster JM (1972) Studies on the ecology of cuterebrid parasitism in deermice. Can J Zool 50:25–29

    Article  Google Scholar 

  • Hunter DM, Webster JM (1973) Determination of the migratory route of botfly larvae, Cuterebra grisea (Diptera:Cuterebridae) in deermice. Int J Parasitol 3:311–316

    Article  PubMed  CAS  Google Scholar 

  • Jackson DM, Trayhurn P, Speakman JR (2001) Associations between energetics and over-winter survival in the short-tailed field vole Microtus agrestis. J Anim Ecol 70:633–640

    Article  Google Scholar 

  • Jaffe G, Zegers DA, Steele MA, Merritt JF (2005) Long-term patterns of botfly parasitism in Peromyscus maniculatus, P. leucopus, and Tamias striatus. J Mammal 86:39–45

    Article  Google Scholar 

  • Kinahan AA, Pillay N (2008) Dominance status influences female reproductive strategy in a territorial African rodent Rhabdomys pumilio. Behav Ecol Sociobiol 62:579–587

    Article  Google Scholar 

  • Kollars TM (1995) Factors affecting the distribution of bot flies (Diptera, Oestridae) on Islands in Lake Barkley, Kentucky and Tennessee. J Entomol Sci 30:513–518

    Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elsevier, Amsterdam

    Google Scholar 

  • Lively CM (2006) The ecology of virulence. Ecol Lett 9:1089–1095

    Article  PubMed  Google Scholar 

  • Macdonald SE, Eaton B, Machtans CS, Paszkowski C, Hannon S, Boutin S (2006) Is forest close to lakes ecologically unique? Analysis of vegetation, small mammals, amphibians, and songbirds. For Ecol Manage 223:1–17

    Article  Google Scholar 

  • Manel S, Ceri Willians H, Ormerod SJ (2001) Evaluating presence-absence models in ecology: the need to account for prevalence. J Appl Ecol 38:921–931

    Article  Google Scholar 

  • May RM, Anderson RM (1978) Regulation and stability of host-parasite population interactions: II Destabilizing processes. J Anim Ecol 47:249–267

    Article  Google Scholar 

  • Millar JS, Hickling GJ (1990) Fasting endurance and the evolution of mammalian body size. Funct Ecol 4:5–12

    Article  Google Scholar 

  • Møller AP (2005) Parasitism and the regulation of host populations. In: Thomas F, Renaud F, Guéguan J-F (eds) Parasitism and ecosystems. Oxford University Press, New York, pp 43–53

    Chapter  Google Scholar 

  • Munger JC, Karasov WH (1991) Sublethal parasites in white-footed mice: impact on survival and reproduction. Can J Zool 69:398–404

    Article  Google Scholar 

  • Pearce J, Venier L (2005a) The incidence of botfly parasitism in small mammals near White River, Ontario, Canada. Mammalia 69:97–101

    Article  Google Scholar 

  • Pearce J, Venier L (2005b) Small mammals as bioindicators of sustainable boreal forest management. For Ecol Manage 208:153–175

    Article  Google Scholar 

  • R Development Core Team (2006) R: A language and environment for statistical computing. R Fundation for Statistical Computing, Vienna

    Google Scholar 

  • Ramos-Jiliberto R, Gonzalez-Olivares E, Bozinovic F (2002) Population-level consequences of antipredator behavior: a metaphysiological model based on the functional ecology of the leaf-eared mouse. Theor Popul Biol 62:63–80

    Article  PubMed  Google Scholar 

  • Sabrosky CW (1986) North American species of Cuterebra, the rabbit and rodent bot flies (Diptera : Cuterebridae). Entomological Society of America, College Park

    Google Scholar 

  • Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163

    Article  Google Scholar 

  • Slansky F (2007) Insect/mammal associations: effects of cuterebrid bot fly parasites on their hosts. Annu Rev Entomol 52:17–36

    Article  PubMed  CAS  Google Scholar 

  • Smith DH (1977) Natural-history and development of Cuterebra approximata (Diptera: Cuterebridae) in its natural host, Peromyscus maniculatus (Rodentia: Cricetidae), in Western Montana. J Med Entomol 14:137–145

    PubMed  CAS  Google Scholar 

  • Sorci G, deFraipont M, Clobert J (1997) Host density and ectoparasite avoidance in the common lizard (Lacerta vivipara). Oecologia 111:183–188

    Article  Google Scholar 

  • Stanko M, Krasnov BR, Morand S (2006) Relationship between host abundance and parasite distribution: inferring regulating mechanisms from census data. J Anim Ecol 75:575–583

    Article  PubMed  Google Scholar 

  • Sutherland GD, Harestad AS, Price K, Lertzman KP (2000) Scaling of natal dispersal distances in terrestrial birds and mammals. Conserv Ecol 4

  • Timm RM, Cook EF (1979) Effect of bot fly larvae on reproduction in white-footed mice, Peromyscus leucopus. Am Midl Nat 101:211–217

    Article  Google Scholar 

  • Turchin P, Hanski I (2001) Contrasting alternative hypotheses about rodent cycles by translating them into parameterized models. Ecology Lett 4:267–276

    Article  Google Scholar 

  • Wecker SC (1962) The effects of bot fly parasitism on a local population of the white-footed mouse. Ecology 43:561–565

    Article  Google Scholar 

  • Witting L (2000) Population cycles caused by selection by density dependent competitive interactions. Bull Math Biol 62:1109–1136

    Article  PubMed  CAS  Google Scholar 

  • Wolf M, Batzli GO (2001) Increased prevalence of bot flies (Cuterebra fontinella) on white-footed mice (Peromyscus leucopus) near forest edges. Can J Zool 79:106–109

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle River

    Google Scholar 

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Acknowledgements

We thank our field and laboratory assistants: E. Bilodeau, A. Bourke, M. Bouthillette, S. Brugerolle, G. Côté, C. Laberge-Pelletier, F. Lavoie, and I. Plante. G. Pelletier from the Canadian Forest Service helped with the identification of bot flies. L. Marschall, M. Wolf, C. A. Johnson, K. Poitras, P. Etcheverry, N. Courbin, J. Hodson, M. Houle and two anonymous reviewers provided useful comments on earlier versions of this manuscript. This research was founded by the NSERC–Université Laval industrial research chair in silviculture and wildlife, the Canada Foundation for Innovation, and the Fond Québécois de la Recherche sur la Nature et les Technologies. We thank our numerous industrial partners who facilitated field work and provided access to management areas: M. St-Onge (Kruger), C. Warren, C. Gauthier, and J.-F. Gauthier (Abitibi Consolidated), and D. Gagnon (Bowater). Animals were captured and handled following the protocol approved by the Animal Welfare Committee of Université Laval and the Ministère des Ressources Naturelles et de la Faune du Québec.

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Authors and Affiliations

  1. NSERC-Industrial Research Chair in Silviculture and Wildlife, Département de Biologie, Université Laval, Sainte-Foy, QC, G1V 0A6, Canada

    Jérôme Lemaître, Daniel Fortin & Pierre-Olivier Montiglio

  2. Ducks Unlimited Canada, 710 rue Bouvier, Bureau 260, Quebec, QC, G2J 1C2, Canada

    Marcel Darveau

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  1. Jérôme Lemaître
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  2. Daniel Fortin
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  3. Pierre-Olivier Montiglio
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  4. Marcel Darveau
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Correspondence to Jérôme Lemaître.

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Communicated by Libby Marschall.

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Lemaître, J., Fortin, D., Montiglio, PO. et al. Bot fly parasitism of the red-backed vole: host survival, infection risk, and population growth. Oecologia 159, 283–294 (2009). https://doi.org/10.1007/s00442-008-1219-3

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