Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-23T03:30:10.211Z Has data issue: false hasContentIssue false
  • English
  • Français

Host demographic predicts ectoparasite dynamics for a colonial host during pre-hibernation mating

Published online by Cambridge University Press:  10 June 2015

QUINN M. R. WEBBER ,
ZENON J. CZENZE  and
CRAIG K. R. WILLIS
QUINN M. R. WEBBER*
Affiliation:
Department of Biology and Centre for Forest Interdisciplinary Research (C-FIR), University of Winnipeg, Manitoba, Canada
ZENON J. CZENZE
Affiliation:
Department of Biology and Centre for Forest Interdisciplinary Research (C-FIR), University of Winnipeg, Manitoba, Canada Current Address: School of Biological Sciences, University of Auckland, Auckland, New Zealand
CRAIG K. R. WILLIS
Affiliation:
Department of Biology and Centre for Forest Interdisciplinary Research (C-FIR), University of Winnipeg, Manitoba, Canada
*
*Corresponding author. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Parasite dynamics can be mediated by host behaviours such as sociality, and seasonal changes in aggregation may influence risk of parasite exposure. We used little brown bats (Myotis lucifugus) captured during the autumn mating/swarming period to test the hypothesis that seasonal and demographic-based variation in sociality affect ectoparasitism. We predicted that ectoparasitism would: (1) be higher for adult females and young of the year (YOY) than adult males because of female coloniality; (2) increase for adult males throughout swarming because of increasing contact with females; (3) decrease for adult females and YOY throughout swarming because of reduced coloniality and transmission of individual ectoparasites to males; (4) be similar for male and female YOY because vertical transmission from adult females should be similar. Ectoparasitism was lowest for adult males and increased for males during swarming, but some effects of demographic were unexpected. Contrary to our prediction, ectoparasitism increased for adult females throughout swarming and YOY males also hosted fewer ectoparasites compared with adult and YOY females. Interestingly, females in the best body condition had the highest parasite loads. Our results suggest that host energetic constraints associated with future reproduction affect pre-hibernation parasite dynamics in bats.

Keywords

Body condition indexdemographylittle brown batsMyotis lucifugusparasitologyseasonal aggregationsocialitysocial phenology
Type
Research Article
Information
Parasitology , Volume 142 , Issue 10 , September 2015 , pp. 1260 - 1269
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Altizer, S., Nunn, C. L., Thrall, P. H., Gittleman, J. L., Antonovics, J., Cunningham, A. A., Dobson, A. P., Ezenwa, V., Jones, K. E., Pederson, A. B., Poss, M. and Pulliam, J. R. C. (2003). Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology Evolution and Systematics 34, 541–547.Google Scholar
Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. and Pejman, R. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467–484.Google Scholar
Buckner, C. H. (1964). Fleas (Siphonaptera) of Manitoba mammals. The Canadian Entomologist 96, 850–856.Google Scholar
Cattadori, I. M., Boag, B., Bjørnstad, O. N., Cornell, S. J. and Hudson, P. J. (2005). Peak shift and epidemiology in a seasonal host-nematode system. Proceedings of the Royal Society B 272, 1163–1169.CrossRefGoogle Scholar
Christe, P., Arlettaz, R. and Vogel, P. (2000). Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecology Letters 3, 207–212.CrossRefGoogle Scholar
Christe, P., Glaizot, O., Evanno, G., Bruyndonckx, N., Devevey, G., Yannic, G., Patthey, P., Maeder, A., Vogel, P. and Arlettaz, R. (2007). Host sex and ectoparasite choice: preference for, and higher survival on female hosts. Journal of Animal Ecology 76, 703–710.Google Scholar
Côté, I. M. and Poulin, R. (1995). Parasitism and group size in social animals: a meta-analysis. Behavioral Ecology 6, 159–165.CrossRefGoogle Scholar
Creel, S. and Creel, N. M. (1995). Communal hunting and pack size in African wild dogs, Lycaon pictus . Animal Behaviour 50, 1325–1339.CrossRefGoogle Scholar
Czenze, Z. J. and Broders, H. G. (2011). Ectoparasite community structure of two bats (Myotis lucifugus and M. septentrionalis) from the Maritimes of Canada. Journal of Parasitology Research 2011, 1–9.Google Scholar
Czenze, Z. J. and Willis, C. K. R. (2015). Warming up and shipping out: cues for arousal and emergence in hibernating bats. Journal of Comparative Physiology B In Press. doi: 10.1007/s00360-015-0900-1.Google Scholar
Davy, C. M., Martinez-Nuñez, F., Willis, C. K. R. and Good, S. V. (2015). Implications of spatial genetic structure among winter aggregations of bats along the leading edge of a rapidly spreading pathogen. Conservation Genetics In Press. doi: 10.1007/s10592-015-0719-z.Google Scholar
Dick, C. W., Gannon, M. R., Little, W. E. and Patrick, M. J. (2003). Ectoparasite associations of bats from central Pennsylvania. Journal of Medical Entomology 40, 813–819. http://dx.doi.org/10.1603/0022-2585-40.6.813 Google Scholar
Encarnaçąo, J. A., Baulechner, D. and Becker, N. I. (2012). Seasonal variations of wing mite infestations in male Daubenton's bats (Myotis daubentonii) in comparison to female and juvenile bats. Acta Chiropterologica 14, 153–159.Google Scholar
Entwistle, A. C., Racey, P. A. and Speakman, J. R. (2000). Social and population structure of a gleaning bat, Plecotus auritus . Journal of Zoology 252, 11–17.Google Scholar
Ezenwa, V. O. (2004). Host social behavior and parasitic infection: a multifactorial approach. Behavioral Ecology 15, 446–454.Google Scholar
Fenton, M. B. (1969). Summer activity of Myotis lucifugus (Chiroptera: Vespertilionidae) at hibernacula in Ontario and Quebec. Canadian Journal of Zoology 47, 597–602.Google Scholar
Fenton, M. B. and Barclay, R. M. R. (1980). Myotis lucifugus . Mammalian Species 142, 1–8.Google Scholar
Frick, W. F., Pollock, J. F., Hicks, A. C., Langwig, K. E., Reynolds, D. S., Turner, G. G., Butchkoski, C. M. and Kunz, T. H. (2010). An emerging disease causes regional population collapse of a common North American bat species. Science 329, 679–682.CrossRefGoogle ScholarPubMed
George, D. B., Webb, C. T., Farnsworth, M. L., O'Shea, T. J., Bowen, R. A., Smith, D. L., Stanley, T. R., Ellison, L. E. and Rupprecht, C. E. (2011). Host and viral ecology determine bat rabies seasonality and maintenance. Proceedings of the National Academy of Sciences of the United States of America 108, 10208–10213.CrossRefGoogle ScholarPubMed
Giorgi, M. S., Arlettaz, R., Christe, P. and Vogel, P. (2001). The energetic grooming costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host (Myotis myotis). Proceedings of the Royal Society B 268, 2071–2075.Google Scholar
Gorrell, J. C. and Schulte-Hostedde, A. I. (2008). Patterns of parasitism and body size in red squirrels (Tamiasciurus hudsonicus). Canadian Journal of Zoology 86, 99–107.Google Scholar
Hart, B. L. (1992). Behavioral adaptations to parasites: an ethological approach. Journal of Parasitology 78, 256–265.Google Scholar
Hawley, D. M. and Altizer, S. M. (2011). Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Functional Ecology 25, 48–60.Google Scholar
Hawley, D. M., Etienne, R. S., Ezenwa, V. O. and Jolles, A. E. (2011). Does animal behaviour underlie covariation between hosts’ exposure to infectious agents and susceptibility to infection? Implications for disease dynamics. Integrative and Comparative Biology 51, 528–539.Google Scholar
Hawlena, H., Abramsky, Z. and Krasnov, B. R. (2006). Ectoparasites and age-dependent survival in a desert rodent. Oecologia 148, 30–39.Google Scholar
Hillegass, M. A., Waterman, J. M. and Roth, J. D. (2008). The influence of sex and sociality on parasite loads in an African ground squirrel. Behavioral Ecology 19, 1006–1011.CrossRefGoogle Scholar
Jonasson, K. A. and Willis, C. K. R. (2011). Changes in body condition of hibernating bats support the thrifty female hypothesis and predict consequences for populations with white-nose syndrome. PLoS ONE 6, e21061.Google Scholar
Khoklova, I. S., Krasnov, B. R., Kam, M., Burdelova, N. I. and Degen, A. A. (2002). Energy cost of ectoparasitism: the flea Xenopsylla ramesis on the desert gerbil Gerbillus dasyurus . Journal of Zoology 258, 349–354.http://dx.doi.org/10.1017/S0952836902001498 CrossRefGoogle Scholar
Klein, S. L. (2000). The effects of hormones on sex differences in infection: from genes to behaviour. Neuroscience and Biobehavioral Reviews 24, 627–638.Google Scholar
Krochmal, A. R. and Sparks, D. W. (2007). Timing of birth and estimation of age of juvenile Myotis septentrionalis and Myotis lucifugus in West-Central Indiana. Journal of Mammalogy 88, 649–656.http://dx.doi.org/10.1644/06-MAMM-A-140R Google Scholar
Kunz, T. H. and Lumsden, L. F. (2003). Ecology of cavity and foliage roosting bats. In Bat Ecology (ed. Kunz, T. H. and Fenton, M. B.), pp. 3–89. University Chicago Press, Chicago and London.Google Scholar
Langwig, K. E., Frick, W. F., Reynolds, R., Parise, K. L., Drees, K. P., Hoyt, J. R., Cheng, T. L., Kunz, T. H., Foster, J. T. and Kilpatrick, A. M. (2015). Host and pathogen ecology drive the seasonal dynamics of a fungal disease white-nose syndrome. Proceedings of the Royal Society B 282, 20142335.Google Scholar
Lewis, S. E. (1995). Roost fidelity of bats: a review. Journal of Mammalogy 76, 481–496.Google Scholar
Lilley, T. M., Stauffer, J., Kanerva, M. and Eeva, T. (2014). Interspecific variation in redox status regulation and immune defence in five bat species: the role of ectoparasites. Oecologia 175, 811–823.CrossRefGoogle ScholarPubMed
Lingle, S. (2001). Anti-predator strategies and grouping patterns in white-tailed deer and mule deer. Ethology 107, 295–314.Google Scholar
Lochmiller, R. L. and Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87–98.Google Scholar
Luçan, R. K. (2006). Relationships between the parasitic mite Spinturnix andegavinus (Acari: Spinturnicidae) and its bat host, Myotis daubentonii (Chiroptera: Vespertilionidae): seasonal, sex- and age-related variation in infestation and possible impact of the parasite on host condition and roosting behaviour. Folia Parasitologica 53, 147–152.Google Scholar
Luis, A. D., Hayman, D. T. S., O'Shea, T. J., Cryan, P. M., Gilbert, A. T., Pulliam, J. R. C., Mills, J. N., Timonin, M. E., Willis, C. K. R., Cunningham, A. A., Fooks, A. R., Rupprecht, C. E., Wood, J. L. N. and Webb, C. T. (2013). A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proceedings of the Royal Society B 280, 1–9.Google Scholar
Martin, L. B., Weil, Z. M. and Nelson, R. J. (2008). Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philosophical Transactions of the Royal Society B: Biological Sciences 363, 321–339.Google Scholar
Marshall, A. G. (1982). Ecology of insects ectoparasitic on bats. In Ecology of Bats (ed. Kunz, T. H.), pp. 369–397. Plenum Press, New York and London.Google Scholar
McCracken, G. F. and Wilkinson, G. S. (2000). Bat mating systems. In Reproductive biology of bats. (ed. Crichton, E. G. and Krutzsch, P. H.), pp. 321–362. Academic Press, San Diego, USA.CrossRefGoogle Scholar
McGuire, L. P., Fenton, M. B. and Guglielmo, C. G. (2009). Effect of age on energy storage during prehibernation swarming in little brown bats (Myotis lucifugus). Canadian Journal of Zoology 87, 515–519.Google Scholar
Minnis, A. M. and Lindner, D. L. (2013). Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biology 117, 638–649.Google Scholar
Møller, A. P. (1990). Parasites and sexual selection: current status of the Hamilton and Zuk hypothesis. Journal of Evolutionary Biology 3, 319–328.Google Scholar
Møller, A. P. (1993). Ectoparasites increase the cost of reproduction in their hosts. Journal of Animal Ecology 62, 309–322.Google Scholar
Møller, A. P. (2000). Survival and reproductive rate of mites in relation to resistance of their barn swallow hosts. Oecologia 124, 351–357.Google Scholar
Moore, S. L. and Wilson, K. (2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 2015–2018.Google Scholar
Neuhaus, P. (2003). Parasite removal and its impact on litter size and body condition in Columbian ground squirrels (Spermophilus columbianus). Proceedings of the Royal Society B 270, 213–215.CrossRefGoogle ScholarPubMed
Norquay, K. J. O., Martinez-Nuñez, F., Dubois, J. E., Monson, K. M. and Willis, C. K. R. (2013). Long-distance movements of little brown bats (Myotis lucifugus). Journal of Mammalogy 94, 506–515. http://dx.doi.org/10.1644.12-MAMM-A-065.1 Google Scholar
Norquay, K. J. O. and Willis, C. K. R. (2014). Hibernation phenology of Myotis lucifugus . Journal of Zoology 294, 85–92.Google Scholar
Plowright, R. K., Foley, P., Field, H. E., Dobson, A. P., Foley, J. E., Eby, P. and Daszak, P. (2011). Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.). Proceedings of the Royal Society B 278, 3703–3712.Google Scholar
Poissant, J. A. and Broders, H. G. (2008). Ectoparasite prevalence in Myotis lucifugus and M. septentrionalis (Chiroptera: Vespertilionidae) during fall migration at Hayes Cave, Nova Scotia. Northeastern Naturalist 15, 515–522.http://dx.doi.org/10.1656/1092-6194-15.4.515 CrossRefGoogle Scholar
R Development Core Team (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. http://www.r-project.org Google Scholar
Radovsky, F. J. (1967). The Macronyssidae and Laelapidae (Acarina: Mesostgmata) Parasitic on Bats. University of California Press, Berkeley and Los Angeles, USA.Google Scholar
Radovsky, F. J. (1994). The evolution of parasitism and distribution of some dermanyssoid mites (Mesostigmata) on vertebrate hosts. In Mites (ed. Houck, M. A.), pp. 186–217. Chapman and Hall, New York, NY, USA.Google Scholar
Reisen, W. K., Kennedy, M. L. and Reisen, N. T. (1976). Winter ecology of ectoparasites collected from hibernating Myotis velifer (Allen) in Southwestern Oklahoma (Chiroptera: Vespertilionidae). Journal of Parasitology 62, 628–635.http://www.jstor.org/stable/3279431 Google Scholar
Rudnick, A. (1960). A revision of the mites of the family Spinturnicidae (Acarina). University of California Publications in Entomology 17, 157–284.Google Scholar
Safi, K. (2008). Social bats: the males’ perspective. Journal of Mammalogy 89, 1342–1350.http://dx.doi.org/10.1644/08-MAMM-S-058.1 Google Scholar
Schalk, G. and Forbes, M. R. (1997). Male biases of parasitism in mammals: effects of study type, host age, and parasite taxon. Oikos 78, 67–74.Google Scholar
Schulte-Hostedde, A. I., Millar, J. S. and Hickling, G. J. (2001). Evaluating body condition in small mammals. Canadian Journal of Zoology 79, 1021–1029.Google Scholar
Senior, P., Butlin, R. K. and Altringham, J. D. (2005). Sex and segregation in temperate bats. Proceedings of the Royal Society B 272, 2467–2473.Google Scholar
Shatrov, A. and Kudryashova, N. (2006). Taxonomy, life cycles and the origin of parasitism in trombiculid mites. In Micromammals and Macroparasites (ed. Morand, S. and Poulin, R.), pp. 119–140. Springer-Verlag, Tokyo, Japan.Google Scholar
Smith, S. A. and Clay, M. E. (1988). Biological and morphological studies on the bat flea Myodopsylla insignis (Siphonaptera: Ischnopsyllidae). Journal of Medical Entomology 25, 413–424.http://dx.doi.org/10.1093/jmedent/25.5.413 Google Scholar
Swinton, J., Harwood, J., Grenfell, B. T. and Gilligan, C. A. (1998). Persistence thresholds for phocine distemper virus infection in harbour seal Phoca vitulina metapopulations. Journal of Animal Ecology 67, 54–68.Google Scholar
Thomas, D. W., Fenton, M. B. and Barclay, R. M. R. (1979). Social behaviour of the little brown bat, Myotis lucifugus, I. Mating behaviour. Behavioral Ecology and Sociobiology 6, 129–136.Google Scholar
United States Fish and Wildlife Service (2012). National White-Nose Syndrome Decontamination Protocol. http://static.whitenosesyndrome.org/sites/default/files/resource/national_wns_revise_final_6.25.12.pdf.Google Scholar
Webber, Q. M. R., McGuire, L. P., Smith, S. B. and Willis, C. K. R. (2015). Host behaviour, age and sex correlate with ectoparasite prevalence and intensity in a colonial mammal, the little brown bat. Behaviour 152, 83–105.Google Scholar
Whitaker, J. O. Jr., Walters, B. L., Castor, L. K. and Ritzi, C. M. (2007). Host and Sistribution Lists of Mites (Acari), Parasitic and Phoretic, in the Hair or on the Skin of North American Wild Mammals North of Mexico: Records Since 1974. Faculty Publications from the Harold W. Manter Laboratory of Parasitology, University of Nebraska, Lincoln.Google Scholar
Willis, C. K. R. and Brigham, R. M. (2007). Social thermoregulation exerts more influence than microclimate on forest roost preferences by a cavity-dwelling bat. Behavioral Ecology and Sociobiology 62, 97–108.Google Scholar
Wilson, K., Bjørnstad, O. N., Dobson, A. P., Merler, S., Poglayen, G., Randolph, S. E., Read, A. F. and Skorping, A. (2002). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeck, H. and Dobson, A. P.), pp. 6–44. Oxford University Press, Oxford.Google Scholar
Wilson, N. A. and Galloway, T. D. (2002). The occurrence of the bat bug, Cimex pilosellus (Horvath) (Hemiptera: Cimicidae), in Manitoba, Canada. Proceedings of the Entomological Society of Manitoba 58, 5–7.Google Scholar
Zahn, A. and Rupp, D. (2004). Ectoparasite load in European vespertilionid bats. Journal of Zoology 262, 383–391.Google Scholar
Zhang, L., Parsons, S., Daszak, P., Wei, L., Zhu, G. and Zhang, S. (2010). Variation in the abundance of ectoparasitic mites of flat-headed bats. Journal of Mammalogy 91, 136–143. http://dx.doi.org/10.1644/08-MAMM-A-306R2.1 Google Scholar
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal of Parasitology 26, 1009–1024.Google Scholar
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. and Smith, G. M. (2009). Mixed Effects Models and Extensions in Ecology with R. Springer, New York, USA.Google Scholar
Supplementary material: File

Webber supplementary material

Tables S1-S3

Download Webber supplementary material(File)
File 67.6 KB