Abstract
Seasonal changes in weather and food availability differentially impact energy budgets of small mammals such as bats. While most thermal physiological research has focused on species that experience extreme seasonal temperature variations, knowledge is lacking from less variable temperate to subtropical climates. We quantified ambient temperature (T a) and skin temperature (T sk) responses by individuals from a population of New Zealand lesser short-tailed bats (Mystacina tuberculata) during summer and winter using temperature telemetry. During summer, communal roosts were more thermally stable than T a. During winter, solitary roosts were warmer than T a indicating significant thermal buffering. Communal roost trees were used on 83 % of observation days during summer, and individuals occupying them rarely entered torpor. Solitary roosts were occupied on 93 % of observation days during winter, and 100 % of individuals occupying them used torpor. During summer and winter, bats employed torpor on 11 and 95 % of observation days, respectively. Maximum torpor bout duration was 120.8 h and winter torpor bout duration correlated negatively with mean T a. Torpor bout duration did not differ between sexes, although female minimum T sk was significantly lower than males. The summer Heterothermy Index varied, and was also significantly affected by T a. Mean arousal time was correlated with sunset time and arousals occurred most frequently on significantly warmer evenings, which are likely associated with an increased probability of foraging success. We provide the first evidence that torpor is used flexibly throughout the year by M. tuberculata, demonstrating that roost choice and season impact torpor patterns. Our results add to the growing knowledge that even small changes in seasonal climate can have large effects on the energy balance of small mammals.
Similar content being viewed by others
References
Arkins AM, Winnington AP, Anderson S, Clout MN (1999) Diet and nectarivorous foraging behaviour of the short-tailed bat (Mystacina tuberculata). J Zool (Lond) 247:183–187
Audet D, Thomas DW (1996) Evaluation of the accuracy of body temperature measurement using external radio transmitters. Can J Zool 74:1778–1781
Barclay RMR, Kalcounis MC, Crampton LH, Stefan C, Vonhof MJ, Wilkinson L, Brigham RM (1996) Can external radiotransmitters be used to assess body temperature and torpor in bats? J Mammal 77:1102–1106
Boyles JG, Brack JV (2009) Modeling survival rates of hibernating mammals with individual-based models of energy expenditure. J Mammal 90:9–16
Boyles JG, Smit B, McKechnie AE (2011) A new comparative metric for estimating heterothermy in endotherms. Physiol Biochem Zool 84:115–123
Buck CL, Barnes BM (1999) Temperatures of hibernacula and changes in body composition of arctic ground squirrels over winter. J Mammal 80:1264–1276
Casey TM (1981) Nest insulation: energy savings to brown lemmings using a winter nest. Oecologia 50:199–204
Christie JE (2003) Spatial and temporal activity patterns of lesser short-tailed bats (Mystacina tuberculata) in Fiordland. Unpublished MSc thesis, University of Otago, Dunedin, New Zealand
Christie JE (2006) Nocturnal activity patterns of the lesser short-tailed bats (Mystacina tuberculata) in temperate rainforest, Fiordland, New Zealand. N Z J Zool 33:125–132
Christie JE, Simpson W (2006) Influence of winter weather conditions on lesser short-tailed bat (Mystacina tuberculata) activity in Nothofagus forest, Fiordland. N Z J Zool 33:133–140
Csada RD, Brigham RM (1994) Reproduction constrains the use of daily torpor by free-ranging common poorwills (Phalaenoptilus nuttallii) (Aves, Caprimulgidae). J Zool 234:209–216
Daniel MJ (1979) The New Zealand short-tailed bat, Mystacina tuberculata; a review of present knowledge. N Z J Zool 6:357–370
Daniel MJ (1990) Order Chiroptera. In: King CM (ed) The handbook of New Zealand mammals. Oxford University Press, Auckland, pp 114–137
Dausmann KH, Glos J (2014) No energetic benefits from sociality in tropical hibernation. Funct Ecol 29:498–505
Davis WH, Hitchcock HB (1965) Biology and migration of the bat, Myotis lucifugus, in New England. J Mammal 46:296–313
Doucette LI, Brigham RM, Pavey CR, Geiser F (2012) Prey availability affects daily torpor by free-ranging Australian owlet-nightjars (Aegotheles cristatus). Oecologia 169:361–372
Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274
Geiser F (2007) Yearlong hibernation in a marsupial mammal. Naturwissenschaften 94:941–944
Grigg GC, Beard LA, Augee ML (2004) The evolution of endothermy and its diversity in mammals and birds. Physiol Biochem Zool 77:982–998
Heller HC, Hammel HT (1972) CNS control of body temperature during hibernation. Comp Biochem Physiol A 41:349–359
Hope PR, Jones G (2012) Warming up for dinner: torpor and arousal in hibernating Natterer’s bats (Myotis nattereri) studied by radio telemetry. J Comp Physiol B 182:569–578
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
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
Jones G, Duvergé PL, Ransome RD (1995) Conservation biology of an endangered species: field studies of greater horseshoe bats. Symp Zool Soc Lond 67:309–324
Körtner G, Geiser F (2000a) The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol Int 17:103–128
Körtner G, Geiser F (2000b) Weather patterns and daily torpor in free-ranging animals. In: Heldmaier G, Klingenspor M (eds) Life in the cold: 11th international hibernation symposium. Springer, Berlin, pp 103–110
Lyman CP (1982) Who is who among the hibernators. In: Lyman CP, Willis JS, Malan A, Wang LCH (eds) Hibernation and torpor in mammals and birds. Academic Press, New York, pp 2–36
McNab BK (2002) The physiological ecology of the vertebrates: a view from energetics. Cornell University Press, Ithaca, pp 459–466
Michener GR (1992) Sexual differences in over-winter torpor patterns of Richardson’s ground squirrels in natural hibernacula. Oecologia 89:397–406
Paige KN (1995) Bats and barometric pressure: conserving limited energy and tracking insects from the roost. Funct Ecol 9:463–467
Park KJ, Jones G, Ransome RD (2000) Torpor, arousal and activity of hibernating Greater Horseshoe Bats (Rhinolophus ferrumequinum). Funct Ecol 14:580–588
Racey PA, Swift SM (1985) Feeding ecology of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) during pregnancy and lactation. I. Foraging behaviour. J Anim Ecol 54:205–215
R Development Core Team (2009) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org
Ruf T, Geiser F (2015) Daily torpor and hibernation in birds and mammals. Biol Rev 90:891–926
Schmid J (1998) Tree holes used for resting by Gray Mouse Lemurs (Microcebus murinus) in Madagascar: insulation capacities and energetic consequences. Int J Primatol 19:797–809
Sedgeley JA (2003) Roost site selection and roosting behaviour in lesser short-tailed bats (Mystacina tuberculata) in comparison with long-tailed bats (Chalinolobus tuberculatus) in Nothofagus forest, Fiordland. N Z J Zool 30:227–241
Sedgeley JA (2006) Roost site selection by lesser short-tailed bats (Mystacina tuberculata) in mixed podocarp–hardwood forest, Whenua Hou/Codfish Island, New Zealand. N Z J Zool 33:97–111
Song X, Geiser F (1997) Daily torpor and energy expenditure in Sminthopsis macroura: interactions between food and water availability and temperature. Physiol Zool 70:331–337
Speakman JR, Webb PI, Racey PA (1991) Effects of disturbance on the energy expenditure of hibernating bats. J Appl Ecol 28:1087–1104
Stawski C, Geiser F (2010) Seasonality of torpor patterns and physiological variables of a free-ranging subtropical bat. J Exp Biol 213:393–399
Thomas DW, Dorais M, Bergeron JM (1990) Winter energy budgets and cost of arousals for hibernating little brown bats, Myotis lucifugus. J Mammal 71:475–479
Turner JM, Warnecke L, Wilcox A, Baloun D, Bollinger TK, Misra V, Willis CKR (2015) Conspecific disturbance contributes to altered hibernation patterns in bats with white-nose syndrome. Physiol Behav 140:71–78
Wallace J (2006) Short-tailed bats in Pikiariki Ecological Area, Pureora Forest Park. Unpublished Report. Pureora Field Centre, Department of Conservation
Wang LCH (1989) Ecological, physiological, and biochemical aspects of torpor in mammals and birds. In: Wang LCH (ed) Advances in comparative and environmental physiology. Springer, Berlin, pp 361–401
Willis CKR, Brigham RM (2003) Defining torpor in free-ranging bats: experimental evaluation of external temperature-sensitive radio transmitters and the concept of active temperature. J Comp Physiol B 173:379–389
Willis CKR, Voss CM, Brigham RM (2006) Roost selection by forest-living female big brown bats (Eptesicus fuscus). J Mammal 87:345–350
Acknowledgments
We thank C. Craig and J. Wilkins-Baigent for help with field work. New Zealand Department of Conservation for housing, the Pureora Field Base, specifically T. Thurley for essential logistical support. We also thank two anonymous reviewers whose comments on an earlier version greatly improved the quality of this manuscript. This study was funded by the University of Auckland and a Commonwealth Scholarship awarded to Z.C.
Author contribution statement
ZJC, RMB and SP conceived and designed the study. ZJC conducted fieldwork, analysed the data, and wrote the manuscript; RMB, SP and AJRH provided editorial advice.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Christian Voigt.
We show exciting flexibility in seasonal behaviour of a warm temperate mammal. New Zealand bats used a heterothermic continuum, like cold temperate bats, despite mild changes in ambient temperature.
Rights and permissions
About this article
Cite this article
Czenze, Z.J., Brigham, R.M., Hickey, A.J.R. et al. Cold and alone? Roost choice and season affect torpor patterns in lesser short-tailed bats. Oecologia 183, 1–8 (2017). https://doi.org/10.1007/s00442-016-3707-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-016-3707-1