Daily torpor and hibernation in birds and mammals

ABSTRACT Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states ass...

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Published inBiological reviews of the Cambridge Philosophical Society Vol. 90; no. 3; pp. 891 - 926
Main Authors Ruf, Thomas, Geiser, Fritz
Format Journal Article
LanguageEnglish
Published Oxford, UK Blackwell Publishing Ltd 01.08.2015
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Abstract ABSTRACT Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian‐mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (∼35°) than daily heterotherms (∼25°). Variables of torpor for an average 30 g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30‐fold longer, and mean torpor bout duration >25‐fold longer in hibernators. Mean minimum body temperature differed by ∼13°C, and the mean minimum torpor metabolic rate was ∼35% of the basal metabolic rate (BMR) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.
AbstractList Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian-mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (~35...) than daily heterotherms (~25...). Variables of torpor for an average 30 g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30-fold longer, and mean torpor bout duration >25-fold longer in hibernators. Mean minimum body temperature differed by ~13...C, and the mean minimum torpor metabolic rate was ~35% of the basal metabolic rate (BMR) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators. (ProQuest: ... denotes formulae/symbols omitted.)
Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian‐mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (∼35°) than daily heterotherms (∼25°). Variables of torpor for an average 30 g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30‐fold longer, and mean torpor bout duration >25‐fold longer in hibernators. Mean minimum body temperature differed by ∼13°C, and the mean minimum torpor metabolic rate was ∼35% of the basal metabolic rate ( BMR ) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.
Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e., the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e., hypometabolic states associated with low body temperatures (torpor), have been distinguished: Daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged however, suggesting that these phenotypes may merely represent the extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species, 43 birds and 171 mammals form a continuum or a bimodal distribution. We use Gaussian-mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms are small on average, but hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (~35°) than daily heterotherms (~25°). Variables of torpor for an average 30-g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30-fold longer, and mean torpor bout duration >25-fold longer in hibernators. Mean minimum body temperature differed by ~13°C, and the mean minimum torpor metabolic rate was ~35% of the BMR in daily heterotherms but only 6% of basal metabolic rate in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.
Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian-mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (∼35°) than daily heterotherms (∼25°). Variables of torpor for an average 30 g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30-fold longer, and mean torpor bout duration >25-fold longer in hibernators. Mean minimum body temperature differed by ∼13°C, and the mean minimum torpor metabolic rate was ∼35% of the basal metabolic rate (BMR) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.
Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian-mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (∼35°) than daily heterotherms (∼25°). Variables of torpor for an average 30 g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30-fold longer, and mean torpor bout duration >25-fold longer in hibernators. Mean minimum body temperature differed by ∼13°C, and the mean minimum torpor metabolic rate was ∼35% of the basal metabolic rate (BMR) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian-mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (∼35°) than daily heterotherms (∼25°). Variables of torpor for an average 30 g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30-fold longer, and mean torpor bout duration >25-fold longer in hibernators. Mean minimum body temperature differed by ∼13°C, and the mean minimum torpor metabolic rate was ∼35% of the basal metabolic rate (BMR) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.
ABSTRACT Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian‐mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (∼35°) than daily heterotherms (∼25°). Variables of torpor for an average 30 g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30‐fold longer, and mean torpor bout duration >25‐fold longer in hibernators. Mean minimum body temperature differed by ∼13°C, and the mean minimum torpor metabolic rate was ∼35% of the basal metabolic rate (BMR) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.
Author Geiser, Fritz
Ruf, Thomas
AuthorAffiliation 2 Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, NSW 2351, Australia
1 Department of Integrative Biology and Evolution, Research Institute of Wildlife Ecology, University of Veterinary Medicine, Vienna, Savoyenstrasse 1, A-1160 Vienna, Austria
AuthorAffiliation_xml – name: 1 Department of Integrative Biology and Evolution, Research Institute of Wildlife Ecology, University of Veterinary Medicine, Vienna, Savoyenstrasse 1, A-1160 Vienna, Austria
– name: 2 Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, NSW 2351, Australia
Author_xml – sequence: 1
  givenname: Thomas
  surname: Ruf
  fullname: Ruf, Thomas
  email: Thomas.Ruf@vetmeduni.ac.at
  organization: Department of Integrative Biology and Evolution, Research Institute of Wildlife Ecology, University of Veterinary Medicine, Vienna, Savoyenstraße 1, A-1160 Vienna, Austria
– sequence: 2
  givenname: Fritz
  surname: Geiser
  fullname: Geiser, Fritz
  organization: Centre for Behavioural and Physiological Ecology, Zoology, University of New England, New South Wales 2351, Armidale, Australia
BackLink https://www.ncbi.nlm.nih.gov/pubmed/25123049$$D View this record in MEDLINE/PubMed
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Issue 3
Keywords hypometabolism
hypothermia
over‐wintering
daily torpor
energy savings
heterothermy
hibernation
thermoregulation
endotherms
Language English
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1980; 137
2010; 97
2004; 20
1987; 32
2009; 87
2005; 175
1970; 168
2004; 29
2002; 97
2009; 82
1967; 23
1999; 49
1980; 45
1999; 47
1988; 76
1988; 77
2000a; 17
1939; 15
1972; 41
1985; 207
2010; 180
2001; 46
1974; 183
1994; 266
2000; 407
1993b; 66
2009; 96
1984; 154
1987; 43
2009; 98
2006; 209
2000; 14
2007; 177
2009; 90
1999; 54
1964; 37
2008; 22
1998; 168
2008; 110
2010; 5
2012; 21
2003; 284
2013; 87
1962; 6
1980; 65
2012; 182
2003; 173
2005; 86
2009; 179
2001; 26
1985; 85
2011; 6
2004; 429
1976; 54
1980; 58
1991; 168
1989; 244
1987; 60
1964; 18
1994; 19
1971; 38
1991; 161
2004; 59
1997; 200
1976; 53A
1977; 115
1977; 232
2004; 66
2007; 148
1965; 54
1992; 162
1984; 246
2013; 22
1984; 125
1969; 71
1963; 41
1984; 21
1965; 50
1985; 125
1985; 63
2008; 77
2002; 119
1999; 123
1964; 80
1975; 51
1951; 101
1957; 59
1974; 19
2012b; 87
2000; 170
2004; 77
1963; 36
1965; 65
1963; 33
1970; 70
1997; 99
1978; 23
2000
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1999; 13
1999; 12
2002; 104
2001; 16
1948; 109
1985; 50
2003; 83
2012; 335
1994; 107
2012; 215
1970; 69
1985; 58
1964; 71
1980; 28
2010; 75
1966; 211
1968; 49
2010; 79
2012
2000; 278
2000; 279
2011
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2010
1982; 73
1981; 69
1964; 66
2008
1978; 15
2004
1932; 229
2000; 156
2008; 320
1979; 52
1993; 267
2008; 95
1839
1957; 38
2007; 56
2010; 85
2011; 331
1956
1968; 41
2012c; 182
2010; 83
1974; 39
2010; 88
1980; 15
1965; 87
1950; 99
1986; 64
2005; 289
1986; 67
1980; 11
1997; 78
1996; 41
2000b; 123
1961
2013
1985; 33
1992; 65
2008; 81
1848
1981; 54
1969
1967
1845
2007; 104
2004; 286
2013; 3
1973; 180
1973; 11
1997; 273
1982; 52
2010; 466
1969; 30
1983; 7
1976
2010; 100
1970; 33
1970; 32
1999; 169
1970
2014; 28
2013; 8
1965; 16
2013; 5
1979
2013; 9
1978
1832; 122
2009; 12
2003; 206
1991; 223
2010; 25
1960; 124
1990
2004; 174
1948; 4
1987
1989; 193
1986
1977; 33
1982
1969; 217
2000; 123
2001b; 74
1989
1988; 214
1970; 24
2006; 52
2007; 446
2010; 35
2002; 131
1990; 37
1963; 61
1991; 72
2011; 84
1993; 41
2000; 73
1996
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1983; 74
1993
1978; 59
2007; 94
1992
2002a; 172
1965; 38
2005a; 83
1993a; 66
2011; 301
1965; 43
1990; 23
1986; 127
1965; 46
2006; 40
1973; 23
2010; 213
1984; 7
2011; 92
2003b; 76
1997; 167
1997; 34
2001a; 171
1985; 156
1931; 6
2000; 81
2007; 80
2007; 85
1979; 86
1958; 194
1998; 79
2006; 70
2012; 162
1966; 19
2011; 278
1997; 117
2012; 167
2006; 79
1988; 36
1995; 76
1980; 87
1978; 3
2003; 18
2012; 169
1990; 145
1961; 34
1998; 113
1999; 401
1990; 144
2003a; 76
1961; 39
1983; 56
2009; 52
1974; 89
1987; 157
2001; 171
1973; 46
1995; 68
2005; 30
1982; 7
2012a
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2011; 25
1961; 45
1955; 57
2008; 150
2006; 93
1987; 11
2002; 172
2009; 21
1986; 156
2011; 31
1998; 22
1998; 25
1990; 83
1990; 63
2012; 93
2001; 82
2002b; 172
2002; 160
2002; 282
1962; 136
2012; 1
2006; 87
1988; 69
1993; 11
1989; 92
2011; 51
2011; 42
1977; 50
2005; 208
1999; 76
2011; 181
1988; 61
1999; 74
1978; 125
1999; 72
1933; 19
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Snippet ABSTRACT Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning...
Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning...
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SubjectTerms Animals
Birds
Birds - physiology
Body Temperature
Circadian Clocks - physiology
Cluster Analysis
daily torpor
Drought
endotherms
Energy Metabolism
Energy reserves
energy savings
Foraging behavior
Genotype & phenotype
Geographical distribution
heterothermy
Hibernation
Hibernation - physiology
High temperature
hypometabolism
hypothermia
Low temperature
Mammals
Mammals - physiology
Metabolism
over-wintering
thermoregulation
Torpor - physiology
Title Daily torpor and hibernation in birds and mammals
URI https://api.istex.fr/ark:/67375/WNG-DJ7K4Z17-B/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fbrv.12137
https://www.ncbi.nlm.nih.gov/pubmed/25123049
https://www.proquest.com/docview/1697515726
https://www.proquest.com/docview/1812881651
https://pubmed.ncbi.nlm.nih.gov/PMC4351926
Volume 90
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