Hibernation and torpor in tropical and subtropical bats in relation to energetics, extinctions, and the evolution of endothermy

Integrative and Comparative Biology

Volumn 51, Issue 3, 2011, Pages 337-348

  Geiser, Fritz ^a   Stawski, Clare ^a  

^a UNIVERSITY OF NEW ENGLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BAT; CLASSIFICATION; CONFERENCE PAPER; ECOSYSTEM; ENERGY METABOLISM; EVOLUTION; HIBERNATION; PHYLOGENY; PHYSIOLOGY; SEASON; THERMOREGULATION; TROPIC CLIMATE;

ANIMALS; BIOLOGICAL EVOLUTION; BODY TEMPERATURE REGULATION; CHIROPTERA; ECOSYSTEM; ENERGY METABOLISM; HIBERNATION; PHYLOGENY; SEASONS; TROPICAL CLIMATE;

AVES; CHIROPTERA; MAMMALIA; MOLOSSIDAE; RHINOLOPHIDAE; VESPERTILIONIDAE;

EID: 80051711183     PISSN: 15407063     EISSN: 15577023     Source Type: Journal    
DOI: 10.1093/icb/icr042     Document Type: Conference Paper

References (91)

1. Arlettaz R, Ruchet C, Aeschimann J, Brun E, Genoud M, Vogel P. 2000. Physiological traits affecting the distribution and wintering strategy of the bat Tadarida teniotis. Ecology 81:1004-14. (Pubitemid 30442002)
2. Audet D, Thomas DW. 1997. Facultative hypothermia as a thermoregulatory strategy in the phyllostomid bats, Carollia perspicillata and Sturnira lilium. J Comp Physiol B 167:146-52. (Pubitemid 27147897)
3. Barnes BM. 1989. Freeze avoidance in a mammal: body temperatures below 08C in an Arctic hibernator. Science 244:1593-5.
4. Bartels W, Law BS, Geiser F. 1998. Daily torpor and energetics in a tropical mammal, the northern blossom-bat Macroglossus minimus (Megachiroptera). J Comp Physiol B 168:233-9. (Pubitemid 28213855)
5. Bartholomew GA, Dawson WR, Lasiewski RC. 1970. Thermoregulation and heterothermy in some of the smaller flying foxes (Megachiroptera) of New Guinea. Z Vergl Physiol 70:196-209.
6. Baudinette RV, Churchill SK, Christian KA, Nelson JE, Hudson PJ. 2000. Energy, water balance, and roost environment in three Australian cave-dwelling bats. J Comp Physiol B 170:439-46.
7. Boyer BB, Barnes BM. 1999. Molecular and metabolic aspects of mammalian hibernation. Bioscience 49:713-24. (Pubitemid 29405250)
8. Boyles JG, Dunbar MB, Storm JJ, Brack V. 2007. Energy availability influences microclimate selection of hibernating bats. J Exp Biol 210:4345-50.
9. Boyles JG, Willis C K R. 2010. Could localized warm areas inside cold caves reduce mortality of hibernating bats affected by white-nose syndrome? Front Ecol Environ 8:92-8.
10. Brigham RM. 1987. The significance of winter activity by the big brown bat (Eptesicus fuscus): the influence of energy reserves. Can J Zool 65:1240-2.
11. Buck CL, Barnes BM. 2000. Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator. Am J Physiol 279:R255-62. (Pubitemid 30625441)
12. Canale CI, Perret M, Théry M, Henry P-Y. 2011. Physiological flexibility and acclimation to food shortage in a heterothermic primate. J Exp Biol 214:551-60.
13. Chruszcz BJ, Barclay R M R. 2002. Thermoregulatory ecology of a solitary bat, Myotis evotis, roosting in rock crevices. Funct Ecol 16:18-26. (Pubitemid 34220023)
14. Coburn DK, Geiser F. 1998. Seasonal changes in energetics and torpor patterns in the sub-tropical blossom-bat Syconycteris australis (Megachiroptera). Oecologia 113:467-73. (Pubitemid 28126739)
15. Cory Toussaint D, McKechnie AE, van der Merwe M. 2010. Heterothermy in free-ranging male Egyptian Free-tailed bats (Tadarida aegyptiaca) in a subtropical climate. Mamm Biol 75:466-70.
16. Crompton AW, Taylor CR, Jagger JA. 1978. Evolution of homeothermy in mammals. Nature 272:333-6. (Pubitemid 8308077)
17. Dausmann KH. 2008. Hypometabolism in primates: torpor and hibernation. In: Lovegrove BG, McKechnie AE, editors. Hypometabolism in animals: torpor, hibernation and cryobiology. 13th International Hibernation Symposium. Pietermaritzburg: University of KwaZulu-Natal. p. 327-36.
18. Dunbar MB, Brigham RM. 2010. Thermoregulatory variation among populations of bats along a latitudinal gradient. J Comp Physiol B 180:885-93.
19. Eisentraut M. 1956. der Winterschlaf mit seinen ökologischen und physiologischen Begleiterscheinungen. Jena: Fischer.
20. Geiser F. 2004. Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239-74. (Pubitemid 40614445)
21. Geiser F, Baudinette RV, McMurchie EJ. 1986. Seasonal changes in the critical arousal temperature of the marsupial Sminthopsis crassicaudata correlate with the thermal transition in mitochondrial respiration. Experientia 42:543-7.
22. Geiser F, Brigham RM. 2000. Torpor, thermal biology, and energetics in Australian long-eared bats (Nyctophilus). J Comp Physiol B 170:153-62. (Pubitemid 30351660)
23. Geiser F, Coburn DK, Körtner G, Law BS. 1996. Thermoregulation, energy metabolism, and torpor in blossom-bats, Syconycteris australis (Megachiroptera). J Zool 239:583-90.
24. Geiser F, Goodship N, Pavey CR. 2002. Was basking important in the evolution of mammalian endothermy? Naturwissenschaften 89:412-14. (Pubitemid 35192095)
25. Geiser F, Holloway J, Körtner G, Maddocks TA, Turbill C, Brigham RM. 2000. Do patterns of torpor differ between free-ranging and captive mammals and birds? In: Heldmaier G, Klingenspor M, editors. Life in the cold. 11th International Hibernation Symposium. Berlin Heidelberg: Springer. p. 95-102.
26. Geiser F, Kenagy GJ. 1988. Torpor duration in relation to temperature and metabolism in hibernating ground squirrels. Physiol Zool 61:442-9.
27. Geiser F, Ruf T. 1995. Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68:935-66. (Pubitemid 3017960)
28. 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 98:447-52.
29. Geiser F, Turbill C. 2009. Hibernation and daily torpor minimize mammalian extinctions. Naturwissenschaften 96:1235-40.
30. Genoud M. 1993. Temperature regulation in subtropical tree bats. Comp Biochem Physiol A 104:321-31. (Pubitemid 23045633)
31. Genoud M, Bonaccorso FJ, Arends A. 1990. Rate of metabolism and temperature regulation in two small tropical insectivorous bats (Peropteryx macrotis and Natalus tumidirostris). Comp Biochem Physiol A 97:229-34. (Pubitemid 20336039)
32. Giroud S, Perret M, LeMaho Y, Momken I, Gilbert C, Blanc S. 2009. Gut hormones in relation to body mass and torpor pattern changes during food restriction and re-feeding in the gray mouse lemur. J Comp Physiol B 179:99-111.
33. Grigg GC, Beard LA, Augee ML. 2004. The evolution of endothermy and its diversity in mammals and birds. Physiol Biochem Zool 77:982-97. (Pubitemid 40241043)
34. Hall LS, Pettigrew J. 1995. The bat with the stereo nose. Aust Nat History 24:26-8.
35. Henshaw RE. 1970. Thermoregulation in bats. In: Slaugher BH, Walton DW, editors. About bats. Dallas: Southern Methodist University Press. p. 188-232.
36. Hock RJ. 1951. The metabolic rates and body temperatures of bats. Biol Bull 101:289-99.
37. Hosken DJ, Withers PC. 1997. Temperature regulation and metabolism of an Australian bat, Chalinolobus gouldii (Chiroptera: Vespertilionidae) when euthermic and torpid. J Comp Physiol B 167:71-80. (Pubitemid 27114550)
38. Humphries MM, Thomas DW, Speakman JR. 2002. Climatemediated energetic constraints on the distribution of hibernating mammals. Nature 418:313-6. (Pubitemid 34790679)
39. Jacobs DS, Kelly EJ, Mason M, Stoffberg S. 2007. Thermoregulation in two free-ranging subtropical insectivorous bat species: Scotophilus species (Vespertilionidae). Can J Zool 85:883-90. (Pubitemid 350145251)
40. Jefimow M, Glabska M, Wojciechowski MS. 2011. Social thermoregulation and torpor in the Siberian hamster. J Exp Biol 214:1100-8.
41. Johnson CN. 2006. Australia's mammal extinctions. Melbourne: Cambridge University Press.
42. Kelm DH, von Helversen O. 2007. How to budget metabolic energy: torpor in a small Neotropical mammal. J Comp Physiol B 177:667-77. (Pubitemid 47106432)
43. Kulzer E. 1965. Temperaturregulation bei Fledermäusen (Chiroptera) aus verschiedenen Klimazonen. Z Vergl Physiol 50:1-34.
44. Kulzer E, Nelson JE, McKean JL, Möhres PF. 1970. Untersuchungen über die Temperaturregulation australischer Fledermäuse. Z Vergl Physiol 69:426-51.
45. Kulzer E, Storf R. 1980. Schlaf-Lethargie bei dem afrikanischen Langzungenflughund Megaloglossus woermanni Pagenstecher, 1885. Z Säugetierkd 45:23-9.
46. Kunz TH, Fenton MB, editors. 2003. Bat ecology. Chicago: University of Chicago Press.
47. Leitner P, Nelson JE. 1967. Body temperature, oxygen consumption and heart rate in the Australian false vampire bat, Macroderma gigas. Comp Biochem Physiol 21:65-74.
48. Levin E, Ar A, Hefetz A., Yom-Tov Y, Kronfeld-Schor N. 2010. Some like it hot: hibernation patterns of the greater mouse-tailed bat (Rhinopoma microphyllum). 27th Annual Meeting, Australian and New Zealand Society for Comparative Physiology and Biochemistry, Australian National University, Canberra, 3-5 December, Abstracts p. 26.
49. Levy O, Dayan T, Kronfeld-Schor N. 2011. Adaptive thermoregulation in golden spiny mice: the influence of season and food availability on body temperature. Physiol Biochem Zool 84:175-84.
50. Liow LH, Fortelius M, Lintulaakso K, Mannila H, Stenseth NC. 2009. Lower extinction in sleep-or-hide mammals. Am Nat 173:264-72.
51. Liu J-N, Karasov WH. 2011. Hibernation in warm hibernacula by free-ranging Formosan leaf-nosed bats, Hipposideros terasensis, in subtropical Taiwan. J Comp Physiol B 181:125-35.
52. Lovegrove BG, Genin F. 2008. Torpor and hibernatioin in a basal placental mammals, the Lesser Hedgehog Tenrec Echinops telfairi. J Comp Physiol B: 691-8.
53. Lovegrove BG, Körtner G, Geiser F. 1999. The energetic cost of arousal from torpor in the marsupial Sminthopsis macroura: benefits of summer ambient temperature cycles. J Comp Physiol B 169:11-8. (Pubitemid 29153747)
54. Lumsden L. 2010. The probable extinction of the Christmas Island Pipistrelle: causal factors and rescue attempts. Aust Bat Soc Newsletter 35:29.
55. Lyman CP. 1970. Thermoregulation and metabolism in bats. In: Wimsatt WA, editor. Biology of bats. New York: Academic Press. p. 301-30.
56. Lyman CP, Willis JS, Malan A, Wang L C H. 1982. Hibernation and torpor in mammals and birds. New York: Academic Press.
57. Maloney SK, Bronner GN, Buffenstein R. 1999. Thermoregulation in the Angolan free-tailed bat Mops condylurus: a small mammal that uses hot roosts. Physiol Biochem Zool 72:385-96. (Pubitemid 29447212)
58. McNab BK. 1974. The behaviour of temperate cave bats in a subtropical environment. Ecology 55:943-58.
59. McNab BK, Bonaccorso FJ. 2001. The metabolism of New Guinean pteropodid bats. J Comp Physiol B 171:201-14. (Pubitemid 32663105)
60. Morrison P. 1959. Body temperatures in some Australian mammals. I. Chiroptera. Biol Bull 116:484-97.
61. Namekata S, Geiser F. 2009. Effects of nest use, huddling, and torpor on thermal energetics of eastern pygmy-possums. Aust Mammal 31:31-4.
62. Nowak RM. 1999. Walkers mammals of the world. Baltimore: The Johns Hopkins University Press.
63. Park KJ, Jones G, Ransome RD. 2000. Torpor, arousal and activity of hibernating Greater Horseshoe Bats (Rhinolophus ferrumequinum). Funct Ecol 14:580-8.
64. Pohl H. 1961. Temperaturregulation und Tagesperiodik des Stoffwechsels bei Winterschläfern. Z Vergl Physiol 45:109-53.
65. Ransome RD. 1990. The natural history of hibernating bats. London: Christopher Helm.
66. Rasweiler JJ. 1973. Care and management of the long-tongued bat, Glossophaga soricina (Chiroptera: Phyllostomatidae), in the laboratory, with observations on estivation induced by food deprivation. J Mammal 54:391-404.
67. Riek A, Körtner G, Geiser F. 2010. Thermobiology, energetics and activity patterns of the Eastern tube-nosed bat (Nyctimene robinsoni) in the Australian tropics: effect of temperature and lunar cycle. J Exp Biol 213:2557-68.
68. Ruben J. 1995. The evolution of endothermy in mammals and birds: from physiology to fossils. Annu Rev Physiol 57:69-95.
69. Schmid J, Speakman JR. 2009. Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus): a comparison of dry and wet forests. Naturwissenschaften 96:609-20.
70. Speakman JR, Thomas DW. 2003. Physiological ecology and energetics of bats. In: Kunz TH, Fenton MB, editors. Bat ecology. Chicago and London: The University of Chicago Press. p. 430-90.
71. Stawski C, Geiser F. 2010a. Fat and fed: frequent use of summer torpor in a subtropical bat. Naturwissenschaften 97:29-35.
72. Stawski C, Geiser F. 2010b. Seasonality of torpor patterns and physiological variables of a free-ranging subtropical bat. J Exp Biol 213:393-9.
73. Stawski C, Turbill C, Geiser F. 2009. Hibernation by a free-ranging subtropical bat (Nyctophilus bifax). J Comp Physiol B 179:433-41.
74. Thomas DW. 1995. The physiological ecology of hibernation in vespertilionid bats. Symp Zool Soc 67:233-44.
75. Thomas DW, Dorais M, Bergeron J-M. 1990. Winter energy budgets and cost of arousal for hibernating little brown bats, Myotis lucifugus. J Mammal 71:475-9.
76. Thomas DW, Geiser F. 1997. Periodic arousals in hibernating mammals: is evaporative water loss involved? Funct Ecol 11:585-91. (Pubitemid 27461912)
77. Turbill C, Bieber C, Ruf T. 2011. Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc Roy Soc B published online (doi: 10.1098/rspb.2011.0190).
78. Turbill C, Körtner G, Geiser F. 2008. Timing of the daily temperature cycle affects the critical arousal temperature and energy expenditure of the lesser long-eared bat. J Exp Biol 211:3871-8.
79. Turbill C, Law BS, Geiser F. 2003. Summer torpor in a free-ranging bat from sub-tropical Australia. J Therm Biol 28:223-6. (Pubitemid 36383353)
80. Twente JW, Twente JA. 1964. A hypothesis concerning the evolution of heterothermy in bats. Ann Acad Scientiarum Fennicae A IV. Biologica 71:435-42.
81. Vivier L, van der Merwe M. 2007. The incidence of torpor in winter and summer in the Angolan free-tailed bat, Mops condylurus (Microchiroptera: Molossidae), in a subtropical environment, Mpumulanga, South Africa. Afr Zool 42:50-8. (Pubitemid 46813714)
82. Webb PI, Speakman JR, Racey PA. 1996. How hot is a hibernaculum? A review of the temperatures at which bats hibernate. Can J Zool 74:761-5. (Pubitemid 126557921)
83. Williams CT, Goropashnaya AV, Buck LC, Fedorov VB, Kohl F, Lee TN, Barnes BM. 2011. Hibernation above the permafrost: effects of ambient temperature and season on expression of metabolic genes in liver and brown adipose tissue of arctic ground squirrels. J Exp Biol 214:1300-6.
84. Willig MR, Patterson BD, Stevens RD. 2003. Patterns of range size, richness, and body size in the Chiroptera. In: Kunz TH, Fenton MB, editors. Bat ecology. Chicago and London: The University of Chicago Press. p. 430-90.
85. Willis C K R, Brigham RM. 2003. Defining torpor in free-ranging bats: experimental evaluation of external temperature-sensitive radiotransmitters and the concept of active temperature. J Comp Physiol B 173:379-89. (Pubitemid 36990261)
86. Willis C K R, Brigham RM, Geiser F. 2006. Deep, prolonged torpor by pregnant, free-ranging bats. Naturwissenschaften 93:80-3. (Pubitemid 43260380)
87. Willis C K R, Turbill C, Geiser F. 2005. Torpor and thermal energetics in a tiny Australian vespertilionid, the little forest bat (Vespadelus vulturnus). J Comp Physiol B 175:479-86. (Pubitemid 41545609)
88. Wilson DE, Reeder DM. 2005. Mammal species of the world. Baltimore: Johns Hopkins University Press.
89. Winter Y. 1998. Energetic cost of hovering flight in a nectar-feeding bat measured with fast-response respirometry. J Comp Physiol B 168:434-44. (Pubitemid 28403887)
90. Withers PC. 1992. Comparative animal physiology. Fort Worth: Saunders. p. 949.
91. Wojciechowski MS, Jefimow M, Tegowska E. 2007. Environmental conditions, rather than season, determine torpor use and temperature selection in large mouseeared bats (Myotis myotis). Comp Biochem Physiol A 147:828-40. (Pubitemid 46843613)