Many animals change behaviour in response to pathogenic infections. White-nose syndrome (WNS) is a fungal skin disease causing rapid declines of North American bats. Infection with Pseudogymnoascus destructans causes hibernating bats to arouse from torpor too often, potentially causing starvation. Mechanisms underlying increased arousals are not understood but fungal invasion of the wings could trigger thirst to relieve fluid loss or grooming to relieve skin irritation. Alternatively, bats might exhibit ‘sickness behaviour’, a suite of responses to infection that save energy. We quantified behaviours of healthy and experimentally inoculated little brown bats (Myotis lucifugus) that could reflect active (i.e., drinking, grooming) or inactive (i.e., sickness behaviour) responses to infection. Infected bats groomed less and were less likely to visit their water dish compared to controls. These results are consistent with research suggesting that P. destructans causes sickness behaviour which could help bats compensate for energetic costs associated with infection.
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Adamo S.A., Kovalko I., Easy R.H., Stoltz D. (2014). A viral aphrodisiac in the cricket Gryllus texensis. — J. Exp. Biol. 217: 1970-1976.
Adelman J.S., Martin L.B. (2009). Vertebrate sickness behaviours: adaptive and integrated neuroendocrine immune responses. — Integr. Comp. Biol. 49: 202-214.
Bos N., Lefèvre T., Jensen A.B., d’Ettorre P. (2012). Sick ants become unsocial. — J. Evol. Biol. 25: 342-351.
Brownlee-Bouboulis S.A., Reeder D.M. (2013). White-nose syndrome-affected little brown myotis (Myotis lucifugus) increase grooming and other active behaviours during arousals from hibernation. — J. Wildlife Dis. 49: 850-859.
Canadian Wildlife Service (2014). Order amending Schedule 1 to the Species at Risk Act. — Available online at http://www.registrelep-sararegistry.gc.ca/document/default_e.cfm?documentID=2315.
Cryan P.M., Meteyer C.U., Boyles J.G., Blehert D.S. (2010). Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology. — BMC Biol. 8: 135.
Cryan P.M., Meteyer C.U., Blehert D.S., Lorch J.M., Reeder D.M., Turner G.G., Webb J., Behr M., Verant M., Russell R.E., Castle K.T. (2013). Electrolyte depletion in white-nose syndrome bats. — J. Wildlife Dis. 49: 398-402.
Dantzer R., Bluthé R., Gheusi G., Cremona S., Laye S., Parnet P., Kelley K.W. (1998). Molecular basis of sickness behavior. — Ann. NY Acad. Sci. 856: 132-138.
Davis W.H. (1970). Hibernation: ecology and physiological ecology. — In: Biology of bats, Vol. III ( Wimsatt W.A., ed.). Academic Press, New York, NY, p. 265-300.
Davy C.M., Martinez-Nunez F., Willis C.K.R., Good S.V. (2015). Implications of spatial genetic structure among winter aggregations of bats along the leading edge of a rapidly spreading pathogen. — Conserv. Genet. 16: 1013-1024.
Dingemanse N.J., Both C., Drent P.J., Van Oers K., Van Noordwijk A.J. (2002). Repeatability and heritability of exploratory behaviour in great tits from the wild. — Anim. Behav. 64: 929-938.
Elliot S.L., Blanford S., Thomas M.B. (2002). Host–pathogen interactions in a varying environment: temperature, behavioural fever and fitness. — Proc. R. Soc. Lond. B Biol. 269: 1599-1607.
Frick W.F., Puechmaille S., Willis C.K.R. (2015). White-nose syndrome in bats. — In: Bats in the anthropocene ( Voigt C.C., Kingston T., eds). Springer, Berlin, p. 245-262.
Gargas A., Trest M.T., Christensen M., Volk T.J., Blehert D.S. (2009). Geomyces destructans sp. nov. associated with bat white-nose syndrome. — Mycotaxon 108: 147-154.
Giorgi M.S., Arlettaz R., Christe P., Vogel P. (2001). The energetic grooming costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host (Myotis myotis). — Proc. Roy. Soc. Lond. B: Biol. Sci. 268: 2071-2075.
Grossberg A.J., Zhu X.X., Leinninger G.M., Levasseur P.R., Braun T.P., Myers M.G. Jr., Marks D.L. (2011). Inflammation-induced lethargy is mediated by suppression of orexin neuron activity. — J. Neurosci. 31: 11376-11386.
Hart B.L. (1988). Biological basis of the behaviour of sick animals. — Neurosci. Biobehav. Rev. 12: 123-137.
Jonasson K.A., Willis C.K.R. (2012). Hibernation energetics of little brown bats. — J. Exp. Biol. 215: 2141-2149.
Katz R.J., Roth K.A. (1979). Stress induced grooming in the rat — an endorphin mediated syndrome. — Neurosci. Lett. 13: 209-212.
Langwig K.E., Frick W.F., Bried J.T., Hicks A.C., Kunz T.H., Kilpatrick A.M. (2012). Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. — Ecol. Lett. 15: 1050-1057.
Léonard N.J., Forbes M.R., Baker R.L. (1999). Effects of a mite, Limnochares americana (Hydrachnida: Limnocharidae), on the life-history traits and grooming behaviour of its damselfly host, Enallalgma ebrium (Odonata: Coenagrionidae). — Can. J. Zool. 77: 1615-1622.
Lorch J.M., Meteyer C.U., Behr M.J., Boyles J.G., Cryan P.M., Hicks A.C., Ballmann A.E., Coleman J.T.H., Redell D.N., Reeder D.M., Blehert D.S. (2011). Experimental infection of bats with Geomyces destructans causes white-nose syndrome. — Nature 480: 376-378.
Lotz C.M., Martínez del Rio E.C., Nicholson E.S.W. (2003). Hummingbirds pay a high cost for a warm drink. — J. Comp. Physiol. B 173: 455-462.
Lovegrove B.G. (2009). Modification and miniaturization of Thermochron iButtons for surgical implantation to small animals. — J. Comp. Physiol. 179: 451-458.
Martin J.G.A., Réale D. (2008). Temperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus. — Anim. Behav. 75: 309-318.
Maslo B., Fefferman N.H. (2015). A case study of bats and white-nose syndrome demonstrating how to model population viability with evolutionary effects. — Conserv. Biol. 29: 1176-1185.
McGuire L.P., Turner J.M., Warnecke L., McGregor G., Bollinger T.K., Misra V., Foster J.T., Frick W.F., Kilpatrick A.M., Willis C.K.R. (2016). White-nose syndrome disease severity and a comparison of diagnostic methods. — Ecohealth 13: 60-71.
Menzies A.K., Timonin M.E., McGuire L.P., Willis C.K.R. (2013). Personality variation in little brown bats. — PLOS One 8: e80230.
Meteyer C.U., Buckles E.L., Blehert D.S., Hicks A.C., Green D.E., Shearn-Bochsler V., Thomas N.J., Gargas A., Behr M.J. (2009). Histopathologic criteria to confirm white-nose syndrome in bats. — J. Vet. Diagn. Invest. 21: 411-414.
Mooring M.S., Mckenzie A.A., Hart B.J. (1996). Grooming in impala: role of oral grooming in removal of ticks and effects of ticks in increasing grooming rate. — Physiol. Behav. 59: 965-971.
Ochoa-Acuña H., Kunz T.H. (1999). Thermoregulatory behaviour in the small island flying fox, Pteropus melanopus (Chirportera: Pteropodidae). — J. Therm. Biol. 24: 15-20.
Owen-Ashley N.T., Wingfield J.C. (2006). Seasonal modulation of sickness behaviour in free-living northwestern song sparrows (Melospiza melodia morphna). — J. Exp. Biol. 209: 3062-3070.
Poulin R. (1995). “Adaptive” changes in behaviour of parasitized animals: a critical review. — Int. J. Parasitol. 25: 1371-1383.
R Core Team (2014). R: a language and environment for statistical computing. — R Foundation for Statistical Computing, Vienna, available online at http://www.R-project.org/.
Rapin N., Johns K., Martin L., Warnecke L., Turner J.M., Bollinger T.K., Willis C.K.R., Voyles J., Misra V. (2014). Activation of innate-response genes in little brown bats (Myotis lucifugus) infected with the fungus Pseudogymnoascus destructans. — PLOS One 9: e112285.
Reeder D.M., Frank C.L., Turner G.G., Meteyer C.U., Kurta A., Britzke E.R., Vodzak M.E., Darling S.R., Stihler C.W., Hicks A.C., Jacob R., Grieneisen L.E., Brownlee S.A., Muller L.K., Blehert D.S. (2012). Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. — PLOS One 7: e38920.
Thomas D.W., Geiser F. (1997). Periodic arousals in hibernating mammals: is evaporative water loss involved? — Funct. Ecol. 11: 585-591.
Toelch U., Stich K.P., Gass C.L., Winter Y. (2008). Effect of local spatial cues in small-scale orientation of flower bats. — Anim. Behav. 75: 913-920.
Toscano B.J., Newsome B., Griffen B.D. (2014). Parasite modification of predator functional response. — Oecologia 175: 345-352.
Turner J.M., Warnecke L., Wilcox A., Baloun D., Bollinger T.K., Misra V., Willis C.K.R. (2015). Conspecific disturbance contributes to altered hibernation patterns in bats with white-nose syndrome. — Physiol. Behav. 140: 71-78.
U.S. Fish and Wildlife Service (2015). U.S. Fish and Wildlife Service protects northern long-eared bat as threatened under Endangered Species Act (Press release, 1 April). — Available online at http://www.fws.gov/midwest/news/778.html.
Verant M.L., Meteyer C.U., Speakman J.R., Cryan P.M., Lorch J.M., Blehert D.S. (2014). White-nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host. — BMC Physiol. 14: 10.
Verboom B., Huitema H. (1997). The importance of linear landscape elements for the pipistrelle Pipistrellus pipistrellus and the serotine bat Eptesicus serotinus. — Landscape Ecol. 12: 117-125.
Warnecke L., Turner J.M., Bollinger T.K., Lorch J.M., Misra V., Cryan P.M., Wibbelt G., Blehert D.S., Willis C.K.R. (2012). Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. — Proc. Natl. Acad. Sci. USA 109: 6999-7003.
Warnecke L., Turner J.M., Bollinger T.K., Misra V., Cryan P.M., Blehert D.S., Wibbelt G., Willis C.K.R. (2013). Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing damage to mortality. — Biol. Lett. 9: 20130177.
Weary D.M., Huzzey J.M., von Keyerslingk M.A.G. (2009). Using behaviour to predict and identify ill health in animals. — J. Anim. Sci. 87: 770-777.
Wilcox A., Warnecke L., Turner J.M., McGuire L.P., Jameson J.W., Misra V., Bollinger T.C., Willis C.K.R. (2014). Behaviour of hibernating little brown bats experimentally inoculated with the pathogen that causes white-nose syndrome. — Anim. Behav. 88: 157-164.
Wilder A.P., Frick W.F., Langwig K.E., Kunz T.H. (2011). Risk factors associated with mortality from white-nose syndrome among hibernating bat colonies. — Biol. Lett. 7: 950-953.
Willis C.K.R. (2015). Conservation physiology for conservation pathogens: white-nose syndrome and integrative biology for host–pathogen systems. — Integr. Comp. Biol. 55: 631-641.
Willis C.K.R., Wilcox A. (2014). Hormones and hibernation: possible links between hormone systems, winter energy balance and white-nose syndrome in bats. — Horm. Behav. 66: 66-73.
Willis C.K.R., Menzies A.K., Boyles J.G., Wojciechowski M.S. (2011). Evaporative water loss is a plausible explanation for mortality of bats from white-nose syndrome. — Integr. Comp. Biol. 51: 364-373.
Zuur A., Ieno E.N., Walker N., Saveliev A.A., Smith G.M. (2009). GLM and GAM for count data. — In: Mixed effects models and extensions in ecology with R. Springer, New York, NY, p. 209-239.
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Many animals change behaviour in response to pathogenic infections. White-nose syndrome (WNS) is a fungal skin disease causing rapid declines of North American bats. Infection with Pseudogymnoascus destructans causes hibernating bats to arouse from torpor too often, potentially causing starvation. Mechanisms underlying increased arousals are not understood but fungal invasion of the wings could trigger thirst to relieve fluid loss or grooming to relieve skin irritation. Alternatively, bats might exhibit ‘sickness behaviour’, a suite of responses to infection that save energy. We quantified behaviours of healthy and experimentally inoculated little brown bats (Myotis lucifugus) that could reflect active (i.e., drinking, grooming) or inactive (i.e., sickness behaviour) responses to infection. Infected bats groomed less and were less likely to visit their water dish compared to controls. These results are consistent with research suggesting that P. destructans causes sickness behaviour which could help bats compensate for energetic costs associated with infection.
All Time | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 611 | 131 | 9 |
Full Text Views | 163 | 19 | 0 |
PDF Views & Downloads | 74 | 35 | 0 |