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Torpor and Tinbergen: Integrating Physiological and Behavioral Traits with Ontogeny, Phylogenetic History, Survival and Fitness to Understand Heterothermy in Bats

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50 Years of Bat Research

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Abstract

The importance of connecting physiological, behavioral, and life-history traits with evolutionary outcomes has long been recognized by biologists and was perhaps most elegantly formalized in Tinbergen’s (Z Tierpsychol 20:410–433, 1963) four-question framework. What are the mechanisms associated with a trait? How does the trait develop over an individual’s lifetime? What is the phylogenetic context of the trait? And finally, often the most difficult to answer, what are the fitness implications of the trait? This framework was developed to understand behavior and rarely has been applied in other fields, despite its potential to inform our understanding of many biological phenomena. Niko Tinbergen and colleagues were awarded a Nobel Prize in 1973 just after the first North American Symposium on Bat Research (NASBR), and since then, Tinbergen’s framework has become second nature to researchers studying bat behavior. However, it is under-used for studying other aspects of bat biology. Thus, in honor of 50 years of NASBR, we use studies on heterothermy and hibernation in bats to highlight the value of Tinbergen’s four questions for research in physiology. We conclude by addressing the implications of an integrative Tinbergen-like approach for addressing conservation threats to bats, with emphasis on research concerning white-nose syndrome, much of which was first presented at NASBR meetings.

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References

  • Auteri GG, Knowles LL (2020) Decimated little brown bats show potential for adaptive change. Sci Rep 10(1):1–10

    CAS  Google Scholar 

  • Bateson P, Laland KN (2013) Tinbergen’s four questions: an appreciation and an update. Trends Ecol Evol 28(12):712–718

    Article  PubMed  Google Scholar 

  • Beer JR, Richards AG (1956) Hibernation of the big brown bat. J Mammal 37:31–41

    Article  Google Scholar 

  • Ben-Hamo M, Muñoz-Garcia A, Williams JB, Korine C, Pinshow B (2013) Waking to drink: rates of evaporative water loss determine arousal frequency in hibernating bats. J Exp Biol 216:573–577

    Article  PubMed  Google Scholar 

  • Bieber C, Juškaitis R, Turbill C, Ruf T (2012) High survival during hibernation affects onset and timing of reproduction. Oecologia 169:155–166

    Article  PubMed  Google Scholar 

  • Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JT, Darling SR, Gargas A, Niver R, Okoniewski JC (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science 323(5911):227–227

    Article  CAS  PubMed  Google Scholar 

  • Boratyński JS, Rusiński M, Kokurewicz T, Bereszyński A, Wojciechowski MS (2012) Clustering behavior in wintering greater mouse-eared bats Myotis myotis—the effect of micro-environmental conditions. Acta Chiropterol 14:417–424

    Google Scholar 

  • Boratyński JS, Willis CKR, Jefimow M, Wojciechowski MS (2015) Huddling reduces evaporative water loss in torpid Natterer’s bats, Myotis nattereri. Comp Biochem Physiol Part A Mol Integr Physiol 179:125–132

    Article  CAS  Google Scholar 

  • Boyles JG, Brack V Jr (2009) Modeling survival rates of hibernating mammals with individual-based models of energy expenditure. J Mammal 90:9–16

    Google Scholar 

  • Boyles JG, Dunbar MB, Storm JJ, Brack V Jr (2007) Energy availability influences microclimate selection of hibernating bats. J Exp Biol 210:4345–4350

    Article  PubMed  Google Scholar 

  • Boyles JG, Storm JJ, Brack V Jr (2008) Thermal benefits of clustering during hibernation: a field test of competing hypotheses on Myotis sodalis. Funct Ecol 22:632–636

    Article  Google Scholar 

  • Burton RS, Reichman OJ (1999) Does immune challenge affect torpor duration? Funct Ecol 13:232–237

    Google Scholar 

  • Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181

    Article  CAS  PubMed  Google Scholar 

  • Cheng TL, Gerson A, Moore MS, Reichard JD, DeSimone J, Willis CKR, Frick WF, Kilpatrick AM (2019) Higher fat stores contribute to persistence of little brown bat populations with white-nose syndrome. J Anim Ecol 88(4):591–600

    Article  PubMed  Google Scholar 

  • Cryan PM, Meteyer CU, Boyles JG, Blehert DS (2010) Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology. BMC Biol 8:135

    Article  PubMed  PubMed Central  Google Scholar 

  • Czenze ZJ, Willis CKR (2015) Warming up and shipping out: arousal and emergence timing in hibernating little brown bats (Myotis lucifugus). J Comp Physiol B 185:575–586

    Article  PubMed  Google Scholar 

  • Czenze ZJ, Park AD, Willis CKR (2013) Staying cold through dinner: cold-climate bats rewarm with conspecifics but not sunset during hibernation. J Comp Physiol B 183:859–866

    Article  PubMed  Google Scholar 

  • Czenze ZJ, Jonasson KA, Willis CKR (2017) Thrifty females, frisky males: winter energetics of hibernating bats from a cold climate. Physiol Biochem Zool 90:502–511

    Article  PubMed  Google Scholar 

  • Davies NB, Krebs JR, West SA (2012) An introduction to behavioural ecology. Wiley-Blackwell, West Sussex, UK, p 520

    Google Scholar 

  • Frick WF, Reynolds DS, Kunz TH (2010) Influence of climate and reproductive timing on demography of little brown myotis Myotis lucifugus. J Anim Ecol 79:128–136

    Google Scholar 

  • Frick WF, Puechmaille SJ, Hoyt JR, Nickel BA, Langwig KE, Foster JT, Barlow KE, Bartonička T, Feller D, Haarsma A-J, Herzog C, Horáček I, van der Kooij I, Mulkens B, Petrov B, Reynolds R, Rodrigues L, Stihler CW, Turner GG, Kilpatrick AM (2015) Disease alters macroecological patterns of North American bats. Glob Ecol Biogeogr 24:741–749

    Google Scholar 

  • Frick WF, Cheng TL, Langwig KE, Hoyt JR, Janicki AF, Parise KL, Foster JT, Kilpatrick AM (2017) Pathogen dynamics during invasion and establishment of white-nose syndrome explain mechanisms of host persistence. Ecology 98:624–631

    Google Scholar 

  • Gager Y, Gimenez O, O’Mara MT, Dechmann DK (2016) Group size, survival and surprisingly short lifespan in socially foraging bats. BMC Ecol 16(1):2

    Article  PubMed  PubMed Central  Google Scholar 

  • Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274

    Article  CAS  PubMed  Google Scholar 

  • Geiser F (2008) Ontogeny and phylogeny of endothermy and torpor in mammals and birds. Comp Biochem Physiol Part A Mol Integr Physiol 150:176–180

    Google Scholar 

  • Geiser F, Brigham RM (2012) The other functions of torpor. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world: thermoregulatory and metabolic adaptations. Springer, Berlin, Germany, pp 109–121

    Chapter  Google Scholar 

  • Geiser F, Stawski C (2011) Hibernation and torpor in tropical and subtropical bats in relation to energetics, extinctions, and the evolution of endothermy. Integra Comp Biol 51:337–348

    Article  Google Scholar 

  • Geiser F, Turbill C (2009) Hibernation and daily torpor minimize mammalian extinctions. Naturwissenschaften 96:1235–1240

    Google Scholar 

  • Geiser F, Hiebert S, Kenagy GJ (1990) Torpor bout duration during the hibernation season of two sciurid rodents: interrelations with temperature and metabolism. Physiol Zool 63:489–503

    Google Scholar 

  • Geiser F, Stawski C, Bondarenco A, Pavey CR (2011) Torpor and activity in a free-ranging tropical bat: implications for the distribution and conservation of mammals? Naturwissenschaften 98:447–452

    Article  PubMed  Google Scholar 

  • Geiser F, Wen J, Sukhchuluun G, Chi Q-S, Wang D-H (2019) Precocious torpor in an altricial mammal: the functional implications of heterothermy during development. Front Physiol 10:469

    Article  PubMed  PubMed Central  Google Scholar 

  • Giroud S, Turbill C, Ruf T (2012) Torpor use and body mass gain during pre-hibernation in late-born juvenile garden dormice exposed to food shortage. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world: thermoregulatory and metabolic adaptations. Springer, Heidelberg, Germany, pp 481–491

    Google Scholar 

  • Hollis LM (2004) Thermoregulation by big brown bats (Eptesicus fuscus): ontogeny, proximate mechanisms, and dietary influences. PhD dissertation, University of Calgary, Canada

    Google Scholar 

  • Hooper JHD, Hooper WM (1956) Habits and movements of cave-dwelling bats in Devonshire. Proc Zool Soc London 127:1–26

    Article  Google Scholar 

  • Humphries MM, Thomas DW, Speakman JR (2002) Climate-mediated energetic constraints on the distribution of hibernating mammals. Nature 418:313–316

    Article  CAS  PubMed  Google Scholar 

  • Humphries MM, Thomas DW, Kramer DL (2003) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76:165–179

    Google Scholar 

  • Humphries MM, Umbanhowar J, McCann KS (2004) Bioenergetic prediction of climate change impacts on northern mammals. Integr Comp Biol 44:452–462

    Article  Google Scholar 

  • Johnson JS, Blomberg AS, Boyles JG, Lilley TM (2021) The winter worries of bats: past and present perspectives on winter habitat and management of cave hibernating bats. In: Lim BK et al. (eds) 50 Years of Bat Research Foundations and New Frontiers. Fascinating Life Sciences. Springer, Cham, pp 209–222

    Google Scholar 

  • Jonasson KA, Willis CKR (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jonasson KA, Willis CKR (2012) Hibernation energetics of free-ranging little brown bats. J Exp Biol 215:2141–2149

    Article  PubMed  Google Scholar 

  • Keen R, Hitchcock HB (1980) Survival and longevity of the little brown bat (Myotis lucifugus) in southeastern Ontario. J Mammal 61:1–7

    Article  Google Scholar 

  • Kunz TH (1996) Methods of marking bats. In: Wilson DE, Cole FR, Nichols JD, Rudran R, Foster MS (eds) Measuring and monitoring biological diversity. Standard methods for mammals. Smithsonian Institution Press, Washington, DC, pp 304–310

    Google Scholar 

  • Kurta A (2014) The misuse of relative humidity in ecological studies of hibernating bats. Acta Chiropterol 16:249–254

    Google Scholar 

  • Langwig KE, Hoyt JR, Parise KL, Frick WF, Foster JT, Kilpatrick AM (2017) Resistance in persisting bat populations after white-nose syndrome invasion. Philos Trans R Soc London B Biol Sci 372(1712):20160044

    Article  PubMed  PubMed Central  Google Scholar 

  • Lentini PE, Bird TJ, Griffiths SR, Godinho LN, Wintle BA (2015) A global synthesis of survival estimates for microbats. Biol Lett 11(8):20150371

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Linton DM, Macdonald DW (2018) Spring weather conditions influence breeding phenology and reproductive success in sympatric bat populations. J Anim Ecol 87:1080–1090

    Google Scholar 

  • Lovegrove BG (2019) Fires of life: endothermy in birds and mammals. Yale University Press, New Haven, p 384

    Book  Google Scholar 

  • Lyman CP (1970) Thermoregulation and metabolism in bats. In: Wimsatt WA (ed) Biology of bats, vol 1. Academic, New York, pp 301–330

    Google Scholar 

  • Maslo B, Fefferman NH (2015) A case study of bats and white-nose syndrome demonstrating how to model population viability with evolutionary effects. Conserv Biol 29:1176–1185

    Google Scholar 

  • McNab BK (1982) Evolutionary alternatives in the physiological ecology of bats. In: Kunz TH (ed) Ecology of bats. Plenum Press, New York, pp 151–200

    Google Scholar 

  • Moyes CD, Schulte PM (2016) Principles of animal physiology. Pearson Education Inc., Toronto, Canada, p 784

    Google Scholar 

  • Norquay KJO, Willis CKR (2014) Hibernation phenology of Myotis lucifugus. J Zool 294(2):85–92

    Article  Google Scholar 

  • Norquay KJO, Martinez-Nunez F, Dubois JE, Monson K, Willis CKR (2013) Long-distance movements of little brown bats (Myotis lucifugus). J Mamm 94:506–515

    Article  Google Scholar 

  • Nowack J, Stawski C, Geiser F (2017) More functions of torpor and their roles in a changing world. J Comp Physiol B 187:889–897

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Farrell MJ, Studier EH (1973) Reproduction, growth and development in Myotis thysanodes and M. lucifugus (Chiroptera: Vespertilionidae). Ecology 54:18–30

    Article  Google Scholar 

  • O’Farrell MJ, Studier EH (1975) Population structure and emergence activity patterns in Myotis thysanodes and M. lucifugus (Chiroptera: Vespertilionidae) in northeastern New Mexico. Am Midl Nat 93:368–376

    Google Scholar 

  • O’Farrell MJ, Studier EH (1976) Cyclical changes in flight characters, body composition and organ weights in Myotis thysanodes and M. lucifugus (Chiroptera: Vespertilionidae). Bull S Calif Acad Sci 75:258–266

    Google Scholar 

  • O’Shea TJ, Ellison LE, Stanley TR (2004) Survival estimation in bats: historical overview critical appraisal, and suggestions for new approaches. In: Thompson W (ed) Sampling rare or elusive species: concepts, designs, and techniques for estimating population parameters. Island Press, Washington, DC, pp 297–336

    Google Scholar 

  • Pearl R (1928) The rate of living: being an account of some experimental studies on the biology of life duration. University of London Press Ltd., London, p 185

    Google Scholar 

  • Procter JW, Studier EH (1970) Effects of ambient temperature and water vapor pressure on evaporative water loss in Myotis lucifugus. J Mammal 51:799–804

    Article  Google Scholar 

  • Puechmaille SJ, Wibbelt G, Korn V, Fuller H, Forget F, Mühldorfer K, Kurth A, Bogdanowicz W, Borel C, Bosch T, Cherezy T (2011) Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS One 6(4):e19167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Racey PA (1973) Environmental factors affecting the length of gestation in heterothermic bats. J Reprod Fertil Suppl 19:175–189

    CAS  PubMed  Google Scholar 

  • Reeder DM, Frank CL, Turner GG, Meteyer CU, Kurta A, Britzke ER, Vodzak ME, Darling SR, Stihler CW, Hicks AC, Jacob R (2012) Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS One 7(6):e38920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Renninger M, Sprau L, Geiser F (2020) White mouse pups can use torpor for energy conservation. J Comp Physiol B 190:253–259

    Google Scholar 

  • Reynolds S, Kunz TH (2000) Changes in body composition during reproduction and postnatal growth in the little brown bat, Myotis lucifugus (Chiroptera: Vespertilionidae). Ecoscience 7:10–17

    Google Scholar 

  • Rubenstein DR, Alcock J (2019) Animal behavior. Sinauer Associates, Sunderland, MA, p 550

    Google Scholar 

  • Ruf T, Geiser F (2015) Daily torpor and hibernation in birds and mammals. Biol Rev 90:891–926

    Article  PubMed  Google Scholar 

  • Sherwood L, Klandorf H, Yancey PH (2012) Animal physiology: from genes to organisms. Brooks/Cole, Belmont, CA, p 896

    Google Scholar 

  • Speakman JR, Racey PA (1989) Hibernal ecology of the pipistrelle bat: energy expenditure, water requirements and mass loss, implications for survival and the function of winter emergence flights. J Animal Ecol 58:797–813

    Google Scholar 

  • Speakman JR, Thomas DW, Kunz TH, Fenton MB (2003) Physiological ecology and energetics of bats. In: Kunz TH, Fenton MB (eds) Bat ecology. University of Chicago Press, Chicago, pp 430–490

    Google Scholar 

  • Stawski C, Geiser F (2012) Will temperature effects or phenotypic plasticity determine the thermal response of a heterothermic tropical bat to climate change? PloS One 7:e40278

    Google Scholar 

  • Stawski C, Willis CKR, Geiser F (2014) The importance of temporal heterothermy in bats. J Zool 292:86–100

    Article  Google Scholar 

  • Studier EH (1970) Evaporative water loss in bats. Comp Biochem Physiol 35(4):935–943

    Article  Google Scholar 

  • Studier EH, O’Farrell MJ (1972) Biology of Myotis thysanodes and M. lucifugus (Chiroptera: Verspertilionidae)—I. thermoregulation. Comp Biochem Physiol 41:567–595

    Article  CAS  Google Scholar 

  • Studier EH, O’Farrell MJ (1976) Biology of Myotis thysanodes and M. lucifugus (Chiroptera: Verspertilionidae)—III. Metabolism, heart rate, breathing rate, evaporative water loss and general energetics. Comp Biochem Physiol 54:423–432

    Article  CAS  Google Scholar 

  • Studier EH, Lysengen VL, O’Farrell MJ (1973) Biology of Myotis thysanodes and M. lucifugus (Chiroptera: Verspertilionidae)—II. Bioenergetics of pregnancy and lactation. Comp Biochem Physiol 44:467–471

    Article  CAS  Google Scholar 

  • Teeling EC, Springer MS, Madsen O, Bates P, O'Brien SJ, Murphy WJ (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307(5709):580–584

    Article  CAS  PubMed  Google Scholar 

  • Thomas DW (1993) Lack of evidence for a biological alarm clock in bats (Myotis spp.) hibernating under natural conditions. Can J Zool 71:1–3

    Google Scholar 

  • Thomas DW, Cloutier D (1992) Evaporative water loss by hibernating little brown bats, Myotis lucifugus. Physiol Zool 65:443–456

    Google Scholar 

  • Thomas DW, Geiser F (1997) Periodic arousals in hibernating mammals: is evaporative water loss involved? Funct Ecol 11:585–591

    Article  Google Scholar 

  • Thomas DW, Fenton MB, Barclay RM (1979) Social behavior of the little brown bat, Myotis lucifugus: I. Mating behavior. Behav Ecol Sociobiol 6:129–136

    Google Scholar 

  • Thomas DW, Dorais M, Bergeron J-M (1990) Winter energy budgets and cost of arousals for hibernating little brown bats, Myotis lucifugus. J Mammal 71:475–479

    Google Scholar 

  • Tinbergen N (1963) On aims and methods of ethology. Z Tierpsychol 20:410–433

    Google Scholar 

  • Tomlinson S, Arnall SG, Munn A, Bradshaw SD, Maloney SK, Dixon KW, Didham RK (2014) Applications and implications of ecological energetics. Trends Ecol Evol 29:280–290

    Google Scholar 

  • Turbill C, Bieber C, Ruf T (2011) Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc R Soc B Biol Sci 278:3355–3363

    Article  Google Scholar 

  • Twente JW (1955) Some aspects of habitat selection and other behavior of cavern-dwelling bats. Ecology 36:706–732

    Article  Google Scholar 

  • Twente JW, Twente J, Brack V Jr (1985) The duration of the period of hibernation of three species of vespertilionid bats. II. Laboratory studies. Can J Zool 63:2955–2961

    Article  Google Scholar 

  • Verant ML, Meteyer CU, Speakman JR, Cryan PM, Lorch JM, Blehert DS (2014) White-nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host. BMC Physiol 14:10

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Verant ML, Bohuski EA, Richgels KL, Olival KJ, Epstein JH, Blehert DS (2018) Determinants of Pseudogymnoascus destructans within bat hibernacula: implications for surveillance and management of white-nose syndrome. J Appl Ecol 55:820–829

    Google Scholar 

  • Voigt CC, Kingston T (2016) Bats in the Anthropocene: conservation of bats in a changing world. SpringerOpen, Cham, p 606

    Google Scholar 

  • Warnecke L, Turner JM, Bollinger TK, Lorch JM, Misra V, Cryan PM, Wibbelt G, Blehert DS, Willis CKR (2012) Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc Natl Acad Sci U S A 109:6999–7003

    Google Scholar 

  • Warnecke L, Turner JM, Bollinger TK, Misra V, Cryan PM, Blehert DS, Wibbelt G, Willis CKR (2013) Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing damage to mortality. Biol Lett 9(4):20130177

    Article  PubMed  PubMed Central  Google Scholar 

  • Wikelski M, Cooke SJ (2006) Conservation physiology. Trends Ecol Evol 21:38–46

    Article  PubMed  Google Scholar 

  • Wilde CJ, Knight CR, Racey PA (1999) Influence of torpor on milk protein composition and secretion in lactating bats. J Exp Zool 284:35–41

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson GS, South JM (2002) Life history, ecology and longevity in bats. Aging Cell 1:124–131

    Article  CAS  PubMed  Google Scholar 

  • Willis CKR, Menzies AK, Boyles JG, Wojciechowski MS (2011) Evaporative water loss is a plausible explanation for mortality of bats from white-nose syndrome. Integr Comp Biol 51:364–373

    Google Scholar 

  • Yuan L, Zhao X, Lin B, Rossiter SJ, He L, Zuo X, He G, Jones G, Geiser F, Zhang S (2011) Adaptive evolution of leptin in heterothermic bats. PLoS One 6(11):e27189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Dzal, Y.A., Menzies, A.K., Webber, Q.M.R., Willis, C.K.R. (2021). Torpor and Tinbergen: Integrating Physiological and Behavioral Traits with Ontogeny, Phylogenetic History, Survival and Fitness to Understand Heterothermy in Bats. In: Lim, B.K., et al. 50 Years of Bat Research. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-030-54727-1_14

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