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

  • QUINN M. R. WEBBER (a1), ZENON J. CZENZE (a1) (a2) and CRAIG K. R. WILLIS (a1)

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.

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Corresponding author

* Corresponding author. E-mail: webber.quinn@gmail.com

References

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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, 541547.
Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. and Pejman, R. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467484.
Buckner, C. H. (1964). Fleas (Siphonaptera) of Manitoba mammals. The Canadian Entomologist 96, 850856.
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, 11631169.
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, 207212.
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, 703710.
Côté, I. M. and Poulin, R. (1995). Parasitism and group size in social animals: a meta-analysis. Behavioral Ecology 6, 159165.
Creel, S. and Creel, N. M. (1995). Communal hunting and pack size in African wild dogs, Lycaon pictus . Animal Behaviour 50, 13251339.
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, 19.
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.
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.
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, 813819. http://dx.doi.org/10.1603/0022-2585-40.6.813
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, 153159.
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, 1117.
Ezenwa, V. O. (2004). Host social behavior and parasitic infection: a multifactorial approach. Behavioral Ecology 15, 446454.
Fenton, M. B. (1969). Summer activity of Myotis lucifugus (Chiroptera: Vespertilionidae) at hibernacula in Ontario and Quebec. Canadian Journal of Zoology 47, 597602.
Fenton, M. B. and Barclay, R. M. R. (1980). Myotis lucifugus . Mammalian Species 142, 18.
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, 679682.
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, 1020810213.
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, 20712075.
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, 99107.
Hart, B. L. (1992). Behavioral adaptations to parasites: an ethological approach. Journal of Parasitology 78, 256265.
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, 4860.
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, 528539.
Hawlena, H., Abramsky, Z. and Krasnov, B. R. (2006). Ectoparasites and age-dependent survival in a desert rodent. Oecologia 148, 3039.
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, 10061011.
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.
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, 349354.http://dx.doi.org/10.1017/S0952836902001498
Klein, S. L. (2000). The effects of hormones on sex differences in infection: from genes to behaviour. Neuroscience and Biobehavioral Reviews 24, 627638.
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, 649656.http://dx.doi.org/10.1644/06-MAMM-A-140R
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. 389. University Chicago Press, Chicago and London.
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.
Lewis, S. E. (1995). Roost fidelity of bats: a review. Journal of Mammalogy 76, 481496.
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, 811823.
Lingle, S. (2001). Anti-predator strategies and grouping patterns in white-tailed deer and mule deer. Ethology 107, 295314.
Lochmiller, R. L. and Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 8798.
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, 147152.
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, 19.
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, 321339.
Marshall, A. G. (1982). Ecology of insects ectoparasitic on bats. In Ecology of Bats (ed. Kunz, T. H.), pp. 369397. Plenum Press, New York and London.
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. 321362. Academic Press, San Diego, USA.
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, 515519.
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, 638649.
Møller, A. P. (1990). Parasites and sexual selection: current status of the Hamilton and Zuk hypothesis. Journal of Evolutionary Biology 3, 319328.
Møller, A. P. (1993). Ectoparasites increase the cost of reproduction in their hosts. Journal of Animal Ecology 62, 309322.
Møller, A. P. (2000). Survival and reproductive rate of mites in relation to resistance of their barn swallow hosts. Oecologia 124, 351357.
Moore, S. L. and Wilson, K. (2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 20152018.
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, 213215.
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, 506515. http://dx.doi.org/10.1644.12-MAMM-A-065.1
Norquay, K. J. O. and Willis, C. K. R. (2014). Hibernation phenology of Myotis lucifugus . Journal of Zoology 294, 8592.
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, 37033712.
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, 515522.http://dx.doi.org/10.1656/1092-6194-15.4.515
R Development Core Team (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. http://www.r-project.org
Radovsky, F. J. (1967). The Macronyssidae and Laelapidae (Acarina: Mesostgmata) Parasitic on Bats. University of California Press, Berkeley and Los Angeles, USA.
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. 186217. Chapman and Hall, New York, NY, USA.
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, 628635.http://www.jstor.org/stable/3279431
Rudnick, A. (1960). A revision of the mites of the family Spinturnicidae (Acarina). University of California Publications in Entomology 17, 157284.
Safi, K. (2008). Social bats: the males’ perspective. Journal of Mammalogy 89, 13421350.http://dx.doi.org/10.1644/08-MAMM-S-058.1
Schalk, G. and Forbes, M. R. (1997). Male biases of parasitism in mammals: effects of study type, host age, and parasite taxon. Oikos 78, 6774.
Schulte-Hostedde, A. I., Millar, J. S. and Hickling, G. J. (2001). Evaluating body condition in small mammals. Canadian Journal of Zoology 79, 10211029.
Senior, P., Butlin, R. K. and Altringham, J. D. (2005). Sex and segregation in temperate bats. Proceedings of the Royal Society B 272, 24672473.
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. 119140. Springer-Verlag, Tokyo, Japan.
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, 413424.http://dx.doi.org/10.1093/jmedent/25.5.413
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, 5468.
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, 129136.
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.
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, 83105.
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.
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, 97108.
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. 644. Oxford University Press, Oxford.
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, 57.
Zahn, A. and Rupp, D. (2004). Ectoparasite load in European vespertilionid bats. Journal of Zoology 262, 383391.
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, 136143. http://dx.doi.org/10.1644/08-MAMM-A-306R2.1
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal of Parasitology 26, 10091024.
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.

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

  • QUINN M. R. WEBBER (a1), ZENON J. CZENZE (a1) (a2) and CRAIG K. R. WILLIS (a1)

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