Daily torpor and hibernation in birds and mammals

THOMAS RUF; FRITZ GEISER

doi:10.1111/brv.12137

. Author manuscript; available in PMC: 2016 Feb 15.

Published in final edited form as: Biol Rev Camb Philos Soc. 2014 Aug 15;90(3):891–926. doi: 10.1111/brv.12137

Daily torpor and hibernation in birds and mammals

THOMAS RUF ^1,², FRITZ GEISER ²

PMCID: PMC4351926 EMSID: EMS61344 PMID: 25123049

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 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.

Keywords: daily torpor, hibernation, heterothermy, energy savings, hypothermia, hypometabolism, endotherms, thermoregulation, over-wintering

I. INTRODUCTION

Birds and mammals spend a large proportion of their energy expenditure on maintaining high euthermic¹ body temperatures (T_b). This optimises many physiological functions, such as mobility, digestion, and brain function, but becomes costly during periods of cold exposure, which require substantial heat production that is impossible to sustain during food shortages. The only ‘logical solution’ (Schmidt-Nielsen, 1979) for animals that cannot escape harsh environmental conditions by migration is to suspend the maintenance of high body temperatures (T_b) and employ a mode of living that saves energy. This is the strategy used by many birds and mammals that employ hypometabolism, i.e., periods of profoundly reduced metabolic rate (MR) and T_b, which typically occur on a seasonal basis (Lyman et al., 1982). States of profound but controlled reductions of MR and T_b in endotherms are called torpor (cold-lethargy). Birds and mammals that use torpor are traditionally classified as either hibernators or species using daily torpor (i.e., daily heterotherms). The main distinguishing trait that is often invoked, is that species regarded as hibernators are capable of consecutive multiday torpor bouts, lasting on average for more than a week, whereas torpor in animals traditionally viewed as daily heterotherms usually lasts only between ~3 and 12 hours (Geiser & Ruf, 1995). Other traits that point to functional differences are the minimum metabolic rate (MR) during torpor (TMR_min), which in in animals categorized as hibernators appears to be much lower, as well as the minimum body temperature (T_{b min}) that is defended during torpor, which seems higher in species regarded as daily heterotherms, although the variation among species in T_{b min} is large. It appears that body mass also differs between the two categories with species conventionally viewed as hibernators being significantly bigger than species classified as daily heterotherms (Geiser & Ruf, 1995).

In recent years, the development of miniature temperature data loggers and transmitters has resulted in a large number of new data on torpor expression in free-living animals. Obviously, these species are subject to natural ambient conditions, especially to short-term fluctuations in ambient temperature (T_a) which may hamper the detection of the actual capabilities of species: (1) Variables usually measured in the field, such as T_b and torpor bout duration (TBD), are strongly affected by T_a (e.g., Twente & Twente, 1965; Geiser & Kenagy, 1988; Bieber & Ruf, 2009; Stawski & Geiser, 2010). During torpor, T_b decreases with T_a over a wide range of T_a until T_{b min} is reached (e.g., Buck & Barnes, 2000; Arnold et al., 2011). (2) Whereas species conventionally categorized as hibernators may remain torpid for more than a month at low T_a and thus T_b, the duration of torpor bouts shortens with increasing T_a. At high T_a between 20° and 30°C, where some of these species still express torpor, torpor bouts often last only for hours and superficially appear to be indistinguishable from the traditional category daily torpor (e.g., Song et al., 1997; Bieber & Ruf, 2009). (3) Many species are sensitive to fluctuating T_a as usually experienced in the wild and will not remain torpid if T_a is not stable (Henshaw, 1970). Thus, patterns of torpor observed in free-ranging animals are often not an indication of the animals’ physiological capability, but rather reflect its response to current ambient conditions. Consequently, these data may not be suitable for meaningful inter-specific comparisons of physiological capabilities. With regard to laboratory measurements, a commonly overlooked problem with quantitatively characterising torpor patterns is that species capable of very long torpor episodes often require a number of short torpor bouts before they express multiday bouts (Strumwasser et al., 1967; Geiser, 2007). Laboratory measurements of torpor, especially when respirometry is involved, typically last for around 1 day or less and even species traditionally classified as hibernators under these conditions usually express torpor that lasts only for hours rather than days (Song et al., 1997).

Despite these shortcomings, data from the field under varying thermal conditions and short-term measurements in the laboratory have been used to question whether “hibernators” and “daily heterotherms” are two distinct functional groups or simply a single group of heterotherms characterized by a continuum of variables (Wilz & Heldmaier, 2000; Lovegrove et al., 2001; Canale et al., 2012; Boyles et al., 2013). For instance, using indices of heterothermy in a recent comprehensive study, Boyles et al. (2013) found that, with the exception of permanent homoeotherms, T_b variation was otherwise largely continuously distributed, and concluded that the traditional classification of mammals as hibernators versus daily heterotherms is “clouded or possibly misleading”. Here, we re-address this controversy by analysing physiological variables characterising torpor in both birds and mammals. In contrast to Boyles et al. (2013), however, we focused on extremes of characteristics such as minimum T_b (T_{b min}) or maximum TBD (TBD_max) in order to assess species-specific physiological capabilities, rather than short-term responses to environmental conditions. Compared with previous studies on these variables (e.g., Geiser & Ruf, 1995) we investigated a much larger dataset now available for 214 heterothermic bird and mammal species.

We hypothesized that, variables characterizing each species’ capacity for torpor would support the classical distinction between daily torpor and hibernation. Specifically we hypothesized (1) That frequency distributions of TBD_max (and possibly also mean torpor bout duration; TBD_mean) absolute TMR (TMR_min), as well as TMR_rel, i.e., the relative reduction of TMR below basal metabolic rate (BMR) and T_{b min} would all show clearly bimodal patterns. (2) That statistical cluster analysis based on the above variables would support the existence of two distinct subgroups among heterotherms and show a high degree of coherence with the traditional classification. (3) That phylogenetically informed regression analysis within hibernators and daily heterotherms, if maintaining these categories was in fact justified by results of the above analyses, would support earlier findings (e.g., Geiser and Ruf 1995, Geiser 2004) suggesting that (a) Mean body mass of hibernators is higher than in daily heterotherms (b) TBD_max (and probably also TBD_mean) is different between the two subgroups (c) Both TMR and T_{b min} show allometric relationships to body mass with distinctly different elevations in the two categories. 4) That similar to results for general heterothermy indices (Boyles et al., 2013), the maximum depth or duration of torpor may increase with latitude of the species’ geographical range.

II. METHODS

Data were collected using primary literature on 43 birds and 171 mammals. As a “working hypothesis” all species were initially classified according to the maximum torpor bout duration (TBD_max) as reported by the respective authors or determined by us (see below; TBD_max <1day, or TBD_max >1 day; Table 1) and preliminarily labelled “daily heterotherms” (42 birds, 78 mammals) or “hibernators” (1 bird, 93 mammals). The only exception to this rule was classifying Sminthopsis macroura as a daily heterotherm, despite a reported TBD_max of 25.9 h, which was observed only once (see Discussion). Our initial classification was identical to that of the original authors of the studies evaluated, except for Elephantulus myurus, as it showed a TBD_max of 39 h, but has been classified as a daily heterotherm previously (see sources in Table 1). If data for a species were available in more than one publication, the season in which torpor was most pronounced, or the reference with the most extensive data set was used. For TBD the maximum values and mean values as reported were used. However, TBD_mean was often not reported. In these cases we either calculated TBD_mean from raw data obtained during ‘mid-hibernation’ presented in figures, or, if only a range of torpor bout durations was provided, we estimated the mean from the average minimum and maximum given. TBD_max was difficult to define in a few species (e.g., Cheirogaleus medius) that maintained T_b slightly above fluctuating T_a for up to several weeks with no indications for active warm-ups (e.g., Dausmann et al., 2004). In these species we used two alternative methods to determine TBD_max: 1) We used the maximum time of passively fluctuating T_b observed and 2) we used TBD_max from conventional torpor bout patterns (with clear arousals) determined in the same species at lower and more constant mean T_a. Because using type 1 or type 2 TBD_max did not affect any of the conclusions, we maintained only type 2 TBD_max, because using maximum observation periods (as in type 1) seemed somewhat arbitrary. TBD_max was also difficult to assign in 3 carnivores (Ursus americanus, Ursus arctos and Meles meles), which - based on records of T_b, MR and behaviour - were initially classified as “hibernators” as they are capable of consecutive multiday torpor episodes (e.g., Tøien et al., 2011). Whereas these species show multiday T_b cycles, the peaks in these cycles are not considered homologous to arousal episodes in small hibernators (Tøien et al., 2011). Therefore, we assigned no values for TBD in these three species. For minimum TMR only values that were below the basal metabolic rate (BMR) of a species were included in our analyses. TMR_min that were not steady-state, according to visual inspection of graphs, usually because animals were not measured long enough (or if torpor was induced for brief periods at inappropriate times of day), were excluded. If only T_b measurements were available, we considered animals with a T_b reduction of >5°C below euthermic resting values to be torpid.

Table 1.

Torpor characteristics in birds and mammals. T: type - daily torpor (DT) or hibernation (HIB); BM: body mass (kg); T_bmin: minimum body temperature in torpor (°C); TMR_min: Minimum torpor metabolic rate (mL O₂ g⁻¹ h⁻¹); TMR_rei: Relative metabolic rate in torpor (TMR_min as % of BMR); TBD_max: Maximum torpor bout duration(h); TBD Ø: Mean torpor bout duration(h); IBE: Duration of inter-bout euthermia (h)¹; LAT: Latitude of mid species range (>0: °N, <0: °S).

Taxon	T	BM	Tb min	TMR min	TMR rel	TBD max	TBD ø	IBE	LAT	Source
AVES
Coraciiformes
Dacelo novaeguineae	DT	0.35	28.6			11.1	9.3		−25	Cooper et al. (2008)
Todus mexicanus	DT	0.0062	22.4	2	62				18	Merola-Zwartjes and Ligon (2000)
Coliiformes
Colius castanotus	DT	0.058	18	0.49	21	11			−10	Prinzinger et al. (1981); Hoffmann and Prinzinger (1984)
Colius colius	DT	0.035	26						−27	McKechnie and Lovegrove (2001b)
Colius striatus	DT	0.051	18.2	0.11	13	10			−4	Hoffmann and Prinzinger (1984); McKechnie and Lovegrove (2001a)
Urocolius indicus	DT	0.053		0.68	28	10			−23	Hoffmann and Prinzinger (1984)
Urocolius macrourus	DT	0.049	22	0.65	24	11			3	Hoffmann and Prinzinger (1984); Schaub et al. (1999)
Apodiformes
Aeronautes saxatalis	DT	0.0305	20			10			23	Bartholomew et al. (1957)
Apus apus	DT	0.042	28	0.4		5			50	Koskimies (1948)
Hirundapus caudacutus	DT	0.085	28			10			−25	Pettigrew and Wilson (1985)
Trochiliformes
Amazilia versicolor	DT	0.0039	21.8			10.4	6.3		−8	Bech et al. (1997)
Archilochus alexandri	DT	0.0032	13.5	0.2	5.7				35	Lasiewski (1963); Lasiewski (1964)
Calypte anna	DT	0.0034	16	0.17	4.4				39	Lasiewski (1963)
Calypte costae	DT	0.0032	9	0.38	12.7				37	Lasiewski (1963); Lasiewski (1964)
Chrysuronia oenone	DT	0.005	18	2.05					−4	Krüger et al. (1982)
Clytolaema rubricauda	DT	0.0077	18	0.5	16				−22	Bech et al. (2006)
Eugenes fulgens	DT	0.008	10	0.5					27	Wolf and Hainsworth (1972)
Eulampis jugularis	DT	0.008	18	1	33				15	Hainsworth and Wolf (1970)
Eupetomena macroura	DT	0.0085	22			9	5.8		−15	Bech et al. (1997)
Lampornis clemenciae	DT	0.008	19.6	0.45	17				25	Krüger et al. (1982)
Melanotrochilus fuscus	DT	0.0069	22			11.2	9.6		−26	Bech et al. (1997)
Oreotrochilus estella	DT	0.0085	6.5	0.75			10		−17	Carpenter (1974); Krüger et al. (1982)
Orthorhynchus cristatus	DT	0.0029	20.8	1.25	20				16	Krüger et al. (1982)
Panterpe insignis	DT	0.005	10	0.5					9	Wolf and Hainsworth (1972)
Selasphorus platycercus	DT	0.0035	6.5	0.54					37	Calder and Booser (1973); Bucher and Chappell (1992)
Selasphorus rufus	DT	0.0033	13	0.43	12.8	10	5		48	Lasiewski (1963); Hiebert (1990); Hiebert (1993)
Selasphorus sasin	DT	0.003	23	1.24	32.6				38	Lasiewski (1963)
Strigiformes
Otus senegalensis	DT	0.061	29			5	2.8		−2	Smit and McKechnie (2010)
Caprimulgiformes
Aegotheles cristatus	DT	0.05	22.4			10.7	3		−25	Brigham et al. (2000); Doucette et al. (2012)
Caprimulgus europaeus	DT	0.07	14			16	3		−7	Peiponen (1965); Schlegel (1969)
Caprimulgus guttatus (argus)	DT	0.075	29.6	0.4	48				−28	Dawson and Fisher (1969)
Caprimulgus tristigma	DT	0.073	10.5			15	6.4		−11	Smit et al. (2011); McKechnie and Mzilikazi (2011)
Caprimulgus vociferus	DT	0.055	18.5						34	Lane et al. (2004)
Chordeiles acutipennis	DT	0.05	15.7						33	Marshall (1955)
Chordeiles minor	DT	0.073	18						43	Lasiewski and Dawson (1964)
Phalaenoptilus nuttallii	HIB	0.035	3	0.05	6	120			35	Withers (1977); Brigham (1992); Woods and Brigham (2004)
Podargus strigoides	DT	0.5	29.1			11	7		−25	Körtner et al. (2000); Körtner et al. (2001)
Columbiformes
Drepanoptila holosericea	DT	0.2	24.8	0.27	38	10	7		21	Schleucher (2001)
Scardafella inca	DT	0.044	29	1	66	10			23	MacMillen and Trost (1967)
Passeriformes
Artamus cyanopterus	DT	0.035	29			12			−30	Maddocks and Geiser (2007)
Delichon urbicum	DT	0.022	26	0.75	59	12			50	Prinzinger and Siedle (1986); Prinzinger and Siedle (1988)
Nectarinia famosa	DT	0.017	25.4			10			−12	Downs and Brown (2002)
Manacus vitellinus	DT	0.0155	26.8	1.8	66	3.5			5	Bartholomew et al. (1983)
MAMMALIA
Monotremata
Tachyglossus aculeatus	HIB	2.8	4	0.03	20	648	271	25	−22.26	Augee and Ealey (1968); Grigg et al. (1989); Nicol and Andersen (2002)
Placentalia Rodentia
Acomys russatus	DT	0.064	25	0.25	38	10	7.5		22.84	Ehrhardt et al. (2005); Levy et al. (2011)
Aethomys namaquenesis	DT	0.046	18.9						−23.16	Withers et al. (1980)
Allactaga euphratica	HIB	0.09				336	96		33	Çolak and Yiğit (1998)
Allactaga williamsi	HIB	0.15				144	96		39	Çolak and Yiğit (1998)
Apodemus peninsulae	DT	0.026	20			6.5	2.1		48.26	Masaki et al. (2005)
Baiomys taylori	DT	0.0064	22	0.5	26	20	10		26.19	Hudson (1965)
Calomys musculinus	DT	0.017		0.52	32	16	13		−31.61	Bozinovic and Rosenmann (1988)
Calomys venustus	DT	0.05	16.4	0.96	67	8	7		−37	Caviedes-Vidal et al. (1990)
Cricetus cricetus	HIB	0.4	3.6	0.032	4	160	87		51.6	Eisentraut (1933); Kayser (1964); Waßmer and Wollnik (1997); Siutz et al. (2012); Siutz C. pers. comm.
Cynomys leucurus	HIB	1.5	8			199	121		41.59	Bakko and Nahornia (1986)
Cynomys ludovicianus	HIB	1	15			214	141		39.25	Lehmer et al. (2001)
Cynomys parvidens	HIB	0.8	6			418	252		38.49	Lehmer and Biggins (2005)
Eliomys quercinus	HIB	0.07	1	0.034	3	480	336	12	42.91	Kayser (1964); Pajunen (1984)
Fukomys damarensis	DT	0.145	28.5						−18.37	Streicher (2010)
Gerbillus pusillus	DT	0.0126	16.7	0.38	43	20	9		0.57	Buffenstein (1985)
Glirulus japonicus	HIB	0.025				380	254		34.25	Otsu and Kimura (1993)
Glis glis	HIB	0.2	1	0.026	3	977	222	6.7	45.93	Wyss (1932); Kayser (1939); Kayser (1961); Pengelley and Fisher (1961); Bieber and Ruf (2009); Bieber & Ruf unpublished
Graphiurus murinus	HIB	0.028	1.5			192	33		−10.12	Mzilikazi et al. (2012)
Graphiurus ocularis	HIB	0.068				312	176	16	−30.24	Perrin and Ridgard (1999)
Ictidomys tridecemlineatus	HIB	0.14	1.5			456	336	14.4	41.11	Kisser and Goodwin (2012)
Jaculus orientalis	HIB	0.17	10			158	77	24	29.53	El Ouezzani et al. (2011)
Marmota broweri	HIB	3.094				480	334	18.4	68.5	Lee et al. (2009)
Marmota flaviventris	HIB	2.5	7.5	0.022	9	360	206	15	42.67	Florant and Heller (1977); Florant et al. (2000); French (1985)
Marmota marmota	HIB	3.1	2.4	0.013	4	353	280	27.8	46.15	Arnold (1993); Ortmann and Heldmaier (2000); Ruf and Arnold (2000); Arnold et al. (2011); Ruf & Arnold unpublished.
Marmota monax	HIB	3.4	5	0.014	5	185	364	28.3	48.68	Lyman (1958); Armitage et al. (2000); Zervanos et al. (2010)
Mesocricetus auratus	HIB	0.09	4	0.07	6	264	90		36.76	Lyman (1948); Pohl (1961)
Mesocricetus brandti	HIB	0.15				144	108		38.08	Goldman (1989)
Microdipodops pallidus	HIB	0.012	6	0.1	4.8	84	48	8.2	38.57	Brown and Bartholomew (1969) Bartholomew and MacMillen (1961)
Mus musculus	DT	0.037	16	0.7	47	11	5.9		50	Hudson and Scott (1979)
Muscardinus avellanarius	HIB	0.0235	0	0.04	2	624	218	6	47.96	Kayser (1939); Kayser (1964); Eisentraut (1956); Prezlaff and Dausmann (2012)
Perognathus californicus	DT	0.021	15	0.15	15	15.4	11.1		31.11	Tucker (1962); Tucker (1965)
Perognathus fasciatus	DT	0.04	11	0.15	12	17	9.7		44.7	Wang and Hudson (1970)
Perognathus longimembris	HIB	0.008	4			112			35.77	Bartholomew and Cade (1957); French (1977)
Perognathus parvus	HIB	0.024	2	0.05	3	192	120		43.39	MacMillen (1983)
Peromyscus boylii	DT	0.033	18			8.8	4.3		32.94	Morhardt (1970)
Peromyscus crinitus	DT	0.02	17			9.5	4.6		36.88	Morhardt (1970)
Peromyscus eremicus	DT	0.017	16	0.3	19	11.2	6.3		29	Macmillen (1965); Morhardt (1970)
Peromyscus gossypinus	DT	0.022	14				4.9		31.36	Tannenbaum and Pivorun (1984)
Peromyscus leucopus	DT	0.02	16.8	0.47	28	13	4.6		33.49	Hill (1975); Deavers and Hudson (1981); Tannenbaum and Pivorun (1988)
Peromyscus maniculatus	DT	0.018	13.4	0.55	28	10.8	7.3		40.92	McNab and Morrison (1963); Morhardt (1970); Geiser (1991)
Petromyscus collinus	DT	0.019	18						−24.17	Withers et al. (1980)
Phodopus sungorus	DT	0.025	12.3	0.88	46	13.8	6.3		50.89	Ruf et al. (1993); T. Ruf unpublished data
Phyllotis darwini	DT	0.036	17.5	0.19	15	12			−30.74	Bozinovic and Marquet (1991)
Reithrodontomys megalotis	DT	0.008	13	0.3	12	10	4		33.28	Thompson (1985)
Saccostomus campestris	DT	0.071	25	0.35	56	2.7	6.8		−19.68	Mzilikazi and Lovegrove (2002)
Spermophilus armatus	HIB	0.5				576	302	9.5	42.02	Cranford (1986)
Spermophilus beecheyi	HIB	0.6	6.1			72	48		38.32	Strumwasser (1960); Pengelley and Kelley (1966)
Spermophilus beldingi	HIB	0.4				400		9	41.29	French (1985)
Spermophilus citellus	HIB	0.25	−0.7			415	192	14	45.52	Németh et al. (2009)
Spermophilus columbianus	HIB	0.5	0			424	600	12	49.15	Young (1990)
Spermophilus dauricus	HIB	0.35	−2.4			377	260	12.75	43.33	Yang et al. (2011)
Spermophilus elegans	HIB	0.3				450	338	24	43.96	Harlow and Menkens (1986)
Spermophilus lateralis	HIB	0.2	−1	0.028	4	504	408	13.5	44.51	Hammel et al. (1968); Healy et al. (2012)
Spermophilus mexicanus	HIB	0.2	7	0.06	7	60	36		26.39	Neumann and Cade (1965)
Spermophilus parryii	HIB	0.65	−2.9	0.012	2	550	420	14.8	63.39	Hock (1960); Barnes (1989); Barnes and Ritter (1993); Buck and Barnes (2000); Karpovich et al. (2009)
Spermophilus richardsonii	HIB	0.4	2	0.02	4	456		10.3	49.39	Hudson and Deavers (1973); Wang (1978)
Spermophilus saturatus	HIB	0.23	0.3	0.017	4	360	254		47.94	Geiser et al. (1990)
Spermophilus tereticaudus	HIB	0.125		0.048	7	120			32.04	Pengelley and Kelley (1966); Bickler (1984)
Spermophilus variegatus	HIB	0.7	8			172	110		29.99	Pengelley (1964); Pengelley and Kelley (1966)
Spermophilus xanthoprymnus	HIB	0.3	4			468	199		38.76	Kart Gür et al. (2009)
Steatomys pratensis	DT	0.028	16.4	0.3	22	16.9	21.5		−20	Ellison (1995)
Tamias amoenus	HIB	0.054	−0.2	0.026	2	312	211		45.07	Kenagy and Vleck (1982); Geiser et al. (1990)
Tamias striatus	HIB	0.087	4.9	0.06	6	150	120	18	40.78	Wang and Hudson (1971); Pivorun (1976); Levesque and Tattersall (2010)
Zapus hudsonius	HIB	0.0226		0.043	3	451			48.34	Muchlinski and Rybak (1978)
Zapus princeps	HIB	0.0336	5.5	0.024	2	650	480	5	47.4	Cranford (1983); French (1985)
Primates
Cheirogaleus crossleyi	HIB	0.5	9			168	111	10.2	−18.72	Blanco and Rahalinarivo (2010)
Cheirogaleus medius	HIB	0.25	9.3	0.044	8.3	1680	160	6	−19.03	Dausmann et al. (2000); Dausmann et al. (2004); Dausmann et al. (2005); Dausmann et al. (2009)
Galago moholi	DT	0.18	21.8	0.09	10	6.5	5		−13.46	Nowack et al. (2010)
Microcebus griseorufus	HIB	0.05	6.5			1848	43.1		−22.94	Dausmann et al. (2012); Kobbe et al. (2011)
Microcebus murinus	DT	0.06	7.8	0.16	19	17.6	9.3		−18.95	Perret (1998); Schmid (2000)
Microcebus myoxinus	DT	0.033	6.8	0.09	4.5	19.2	4.6		−20.08	Schmid et al. (2000)
Microcebus ravelobensis	DT	0.063	25			7	5		−19.32	Lovegrove et al. (2013)
Carnivora
Meles meles	HIB	13	28						51	Fowler and Racey (1988)
Mephitis mephitis	DT	2.88	26			20	7.8		43.15	Hwang et al. (2007)
Proteles cristata	DT	9	31						−5.74	Anderson (2004)
Taxidea taxus	DT	9	28	0.13	43	22	14		38.45	Harlow (1981)
Ursus americanus	HIB	80	29.4	0.042	19				47.57	Watts et al. (1981); Tøien et al. (2011)
Ursus arctos	HIB	100	32.5						50.76	Hissa (1997)
Chiroptera
Barbastella barbastellus	HIB	0.007		0.04	2				44.28	Pohl (1961)
Carollia perspicillata	DT	0.018	22	1	53				−4.14	Audet and Thomas (1997)
Chalinolobus gouldii	HIB	0.018	5	0.05	3				−27.37	Hosken and Withers (1997)
Corynorhinus rafinesquii	HIB	0.01	13.9				58		32.8	Johnson (2012)
Eptesicus fuscus	HIB	0.0147	1	0.03	3	600	488	2	31.15	Kulzer (1965) French (1985); Willis et al. (2005a)
Glossophaga soricina	DT	0.01	21	0.23	9	17.5	11.4		−2.61	Kelm and von Helversen (2007)
Hipposideros terasensis	HIB	0.057	13.8	0.046	7	456	185	1.8	17.13	Liu and Karasov (2011); Liu and Karasov (2012)
Lasiurus borealis	HIB	0.011	3	0.035	2	260	190	2.83	36.39	Dunbar and Tomasi (2006)
Lasiurus cinereus	HIB	0.033	2			135	105		12.6	Cryan and Wolf (2003); Willis et al. (2006)
Macroglossus minimus	DT	0.016	21.6	0.52	40	9.5	6.7		−1.28	Bartels et al. (1998)
Megaloglossus woermanni	DT	0.012	26.2	0.8	50				−1.12	Kulzer and Storf (1980)
Miniopterus schreibersii	HIB	0.015	5			288			5.87	Hall (1982); Brown and Bernard (1994)
Mops condylurus	HIB	0.029	13						−5.77	Vivier and van der Merwe (2011)
Myotis adversus	HIB	0.0078	9			192			4.84	Kulzer et al. (1970)
Myotis lucifugus	HIB	0.0052	1.3	0.022	1	1152	314	2.4	43	Hock (1951) Jonasson and Willis (2012)
Myotis myotis	HIB	0.025	2	0.04	3	2352	989		47.44	Pohl (1961); Harmata (1987); Koteja et al. (2001)
Myotis nattereri	HIB	0.009	7			490	160		46.05	Hope and Jones (2012)
Myotis velifer	HIB	0.012	0.6	0.04	3				27.11	Tinkle and Patterson (1965); Riedesel and Williams (1976)
Nyctalus noctula	HIB	0.029	3	0.036	2		192		39.16	Ransome (1990); Arlettaz et al. (2000)
Nycteris thebaica	DT	0.011	27						1.28	Cory Toussaint and McKechnie (2012)
Nyctimene albiventer	DT	0.028	25.5	0.67	47				−4.02	Bartholomew et al. (1970)
Nyctophilus bifax	HIB	0.01	7.3	0.046	3	129	27	3	−16.48	Stawski et al. (2009); Stawski and Geiser (2010); Stawski and Geiser (2011)
Nyctophilus geoffroyi	HIB	0.007	1.4	0.037	3	362	106	3	−27.37	Geiser and Brigham (2000); Turbill and Geiser (2008)
Nyctophilus gouldi	HIB	0.01	2.3	0.052	4	259	106	3	−33.54	Geiser and Brigham (2000); Turbill and Geiser (2008)
Pipistrellus pipistrellus	HIB	0.0074	3	0.024	1				43.44	Kayser (1964); Kulzer (1965)
Pipistrellus subflavus	HIB	0.005				1800	607	1.5	31.01	Brack and Twente (1985); French (1985)
Plecotus auritus	HIB	0.01	−2						44.65	Eisentraut (1956)
Rhinolophus ferrumequinum	HIB	0.023	9			432	104	4.3	38.48	Kulzer (1965); Park et al. (2000)
Rhinolophus hipposideros	HIB	0.006				2064	427		31.68	Harmata (1987)
Rhinopoma microphyllum	HIB	0.01	23						18.84	Kulzer (1965); Levin et al. (2010)
Scotophilus dinganii	DT	0.029	18.5			19	15		−8.02	Jacobs et al. (2007)
Scotophilus mhlanganii	DT	0.028	17.2			18.5	17.2		−6	Jacobs et al. (2007)
Sturnira lilium	DT	0.016	22	0.5	25				−2.47	Audet and Thomas (1997)
Syconycteris australis	DT	0.018	17.2	0.47	36	8.2	7.3		−16.55	Coburn and Geiser (1998)
Tadarida aegyptiaca	HIB	0.017	6			228			1.12	Cory Toussaint et al. (2010)
Tadarida brasiliensis	HIB	0.01	9	0.06	3				1.23	Herreid (1963); Herreid and Schmidt-Nielsen (1966)
Tadarida teniotis	HIB	0.035	6.7	0.04	4	192	528	4.5	35.4	Arlettaz et al. (2000); Marom et al. (2006)
Vespadelus vulturnus	HIB	0.004	5	0.014	1.3				−34.21	Willis et al. (2005b)
Eulipotyphla
Atelerix algirus	HIB	0.63	9.7			168	84	16	33.74	Mouhoub-Sayah et al. (2008)
Atelerix frontalis	HIB	0.4	1			116	22	12	−23.03	Hallam and Mzilikazi (2011)
Crocidura flavescens	DT	0.032	19						−30.94	Baxter (1996)
Crocidura leucodon	DT	0.012	18.6						42.54	Nagel (1985)
Crocidura russula	DT	0.01	17.9	0.9	38	3			40.48	Nagel (1977); Nagel (1985)
Crocidura suaveolens	DT	0.008	21.6						45	Nagel (1985)
Erinaceus europaeus	HIB	0.7	5.4	0.01	2.5	288	213	22.1	53.78	Kristoffersson and Soivio (1964); Thati (1978)
Notiosorex crawfordi	DT	0.004	27.4	1.42	43				31	Lindstedt (1980)
Sorex sinuosus	DT	0.0078		1.3	28	1			31.46	Newman and Rudd (1978)
Suncus etruscus	DT	0.002	12	0.6	10	7.6	2		28.2	Vogel (1974); Frey (1979); Frey (1980)
Xenarthra
Zaedyus pichiy	HIB	1.1	12.5			112	75		−40.89	Superina and Boily (2007)
Afrosoricida
Amblysomus hottentotus	HIB	0.075	8.6			96	78		−29.74	Scantlebury et al. (2008)
Echinops telfairi	HIB	0.085	11	0.026	2	264	162		−22.58	Dryden et al. (1974); Scholl (1974)
Geogale aurita	DT	0.006	16	0.15	13				−22.55	Stephenson and Racey (1993a)
Microgale dobsoni	DT	0.045	20	0.22	24				−18.56	Stephenson and Racey (1993b)
Setifer setosus	HIB	0.32	13	0.014	4	3600			−18.96	Kayser (1964); Hildwein (1970); Lovegrove et al. (2013)
Tenrec ecaudatus	HIB	0.65	15	0.027	9	6480			−18.96	F. Lachiver cited in Kayser (1961); Kayser (1964); Hildwein (1970); Lobban and Lovegrove (2012)
Macroscelidea
Elephantulus edwardii	HIB	0.045	9.3			44	17.3		−31.59	Geiser and Mzilikazi (2011)
Elephantulus myurus	HIB	0.057	5.5	0.078	7	39	8.8		−23.07	Lovegrove et al. (2001); Mzilikazi and Lovegrove (2004); McKechnie and Mzilikazi (2011)
Elephantulus rozeti	DT	0.045	5.1	0.023	2	20.1	13.6		32.6	Lovegrove et al. (2001)
Elephantulus rupestris	DT	0.06	12			12	5		−25.59	Oelkrug et al. (2012)
Macroscelides proboscideus	DT	0.046	9.4			18	10.7		−26.24	Lovegrove et al. (1999)
Marsupialia Diprodontia
Acrobates pygmaeus	HIB	0.011	1.6	0.056	5	192	85		−24.91	Fleming (1985); Geiser and Ferguson (2001)
Burramys parvus	HIB	0.063	1.8	0.025	2	480	342		−36.29	Geiser and Broome (1991)
Cercartetus concinnus	HIB	0.018	4.7	0.046	4	264	102		−33.82	Geiser (1987)
Cercartetus lepidus	HIB	0.012	5.9	0.052	3	144			−38.97	Geiser (1987)
Cercartetus nanus	HIB	0.02	1.3	0.018	2.7	840	101		−35.06	Geiser (1993); Song et al. (1997); Turner et al. (2012)
Petaurus breviceps	DT	0.13	10.4	0.07	9.5	23	13		−20.7	Fleming (1980); Körtner and Geiser (2000b)
Tarsipes rostratus	DT	0.01	5.4	0.15	5	14.4	10.5		−31.3	Collins et al. (1987); Withers et al. (1990)
Microbiotheria
Dromiciops gliroides	HIB	0.0402	7.1	0.03	3.8	144	120		−39.86	Grant and Temple-Smith (1987); Bozinovic et al. (2004); Franco et al. (2012)
Dasyuromorphia
Antechinomys laniger	DT	0.027	11	0.14	13	16	11.5		−27.09	Geiser (1986)
Antechinus flavipes	DT	0.026	24.5	0.48	46	5.5	2		−26.92	Geiser (1988)
Antechinus stuartii	DT	0.026	19.9	0.66	62	9	4		−26.74	Geiser (1988)
Dasycercus cristica uda/blythi	DT	0.1	10.8	0.12	23	20.8	5.8		−25.02	MacMillen and Nelson (1969); Geiser and Masters (1994); Kortner et al. (2008)
Dasykaluta rosamondae	DT	0.027	21			16.4	12.3		−22.58	Kortner et al. (2010)
Dasyuroides byrnei	DT	0.12	20.4	0.4	54	7.5	2.7		−26.08	Geiser and Baudinette (1987)
Dasyurus geoffroii	DT	1	23.1						−33.17	Arnold (1976)
Dasyurus hallucatus	DT	0.516	28.4						−18	Cooper and Withers (2010)
Dasyurus viverrinus	DT	1	25						−41.61	Moyle in Reardon (1999)
Myrmecobius fasciatus	DT	0.5	19.1			15.3	9.7		−33.82	Cooper and Withers (2004)
Ningaui yvonnae	DT	0.011	15.3	0.3	23	12.3	7.5		−31.98	Geiser and Baudinette (1988)
Planigale gilesi	DT	0.008	14.3	0.36	25	15.3	8.8		−29.48	Geiser and Baudinette (1988)
Planigale ingrami	DT	0.0076		0.48	30	4			−18.58	Dawson and Wolfers (1978)
Planigale maculata	DT	0.013	19.6	0.4	40	1.8			−21.9	Morton and Lee (1978)
Planigale tenuirostris	DT	0.007		0.48	30	4			−28.53	Dawson and Wolfers (1978)
Pseudantechinus macdonnellensis	DT	0.031	15.9			14.3	5.8		−22.83	Geiser and Pavey (2007)
Sminthopsis crassicaudata	DT	0.017	10.8	0.27	22	19.5	15		−28.79	Geiser and Baudinette (1987); Warnecke et al. (2008)
Sminthopsis douglasi	DT	0.06	16.9	0.43	40	8.8	3.2		−20.1	Muller (1996)
Sminthopsis macroura	DT	0.024	11.3	0.3	29	25.9	11		−24.29	Geiser and Baudinette (1987); Kortner and Geiser (2009)
Sminthopsis murina	DT	0.019	15	0.25	22	8			−27.47	Geiser et al. (1984)
Sminthopsis ooldea	DT	0.0111		0.77	48				−24.7	Tomlinson et al. (2012)
Didelpimorphia
Gracilinanus agilis	DT	0.0291	20	0.3	30				−18.71	Cooper et al. (2009)
Marmosa microtarsus	DT	0.013	16	0.25	18	9			15.53	Morrison and McNab (1962)
Thylamys elegans	DT	0.032	14	0.4	47	20	14		−30	Opazo et al. (1999); Silva-Duran and Bozinovic (1999)

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The duration of euthermic intervals between torpor episodes (inter-bout euthermia, IBE) was taken from the literature for species traditionally classified as hibernators, but limited data on IBE were available for species traditionally considered daily heterotherms. To obtain at least a rough estimate of IBE in for this subgroup, we computed IBE from 24 hours – TBD.

Both euthermic and torpor MR were analysed as mass-specific MR. We are aware that this is a potential source of error and that computing allometric relationships based on absolute MR would be much preferable (e.g., Packard & Boardman, 1988; Hayes, 2001). However, the vast majority of MRs in the literature we cite were given as mass-specific MR and – also in the majority of cases – body masses were provided for the species or experimental animals in general, but not the actual individuals in which MR was measured (and typically, only mean body masses were given). Thus, estimating total MRs from these different sources (i.e., multiplying mass-specific MR from one sample of individuals by mean body mass from another set) would lead to the same potential error pointed out by Packard and Boardman (1988): assuming a linear isometric relationship when this assumption may not be valid. Balancing the possible error in using mass-specific MR versus omitting most MR data altogether, we decided to analyse MR as given, especially as there is no apparent source of bias that could lead to larger errors in any subgroup of species investigated.

To test if either single variables (e.g., TMR_min) or combinations of torpor characteristics would point to the existence of a grouping structure within heterotherms we used cluster analysis based on Gaussian mixture models as implemented in R-package “mclust” (Fraley & Raftery, 2002). This procedure determines the number of clusters (one, two or more) of normally distributed variables that minimize the variance in the dataset based on the Bayesian Information Criterion (BIC), which adds a penalty term on the number of parameters to the log-likelihood of each model. To obtain approximately equal variances between potential groups, all variables (except T_{b min}) were log-transformed. We did not attempt to include IBE duration into these cluster analyses, as this variable may be affected by prior torpor episodes, but is not a characteristic of torpor episodes as such. As a measure of the strength of clustering, we used χ² and P-values from likelihood-ratio tests comparing the best model for each variable with the null-model (i.e., a model assuming no subgroups). To minimize multiplicity of P-values, we limited testing of combinations of variables to those unrelated to TBD (i.e., TMR_min, TMR_rel and Tb_min). We did not discriminate between birds and mammals in these cluster analyses. For models resulting in more than one cluster, each data point can be assigned to one of the groups determined. We compared these independent, model-generated classifications to our initial categories that were based on TBD_max being greater or less than 24 h.

To investigate the relationship of variables characterizing torpor (e.g., TBD_max or T_{b min}) to body mass or latitude of the species’ geographical range we fitted phylogenetically-informed generalized least squares (PGLS) models. Models were computed using function “gls” from package “nlme” (Pinheiro et al., 2013) in R 3.0.2 (R Development Core Team, 2013). In these models, phylogenetic correlation between taxonomically related species is used for sample-weighting, as data-points obtained from closely related species cannot be considered entirely independent.

The bird phylogeny used was based on Sibley and Ahlquist (1990). Two families (the Artamidae and the Pipridae) were added to this tree using information on their phylogenetic position given by (Norman et al., 2009) and (Ericson et al., 2006) (Fig. 1). As no sufficient information on branch lengths was available for birds, all initial branch lengths in this tree were set to 1. We are aware that more recent, albeit controversial, phylogenies of birds are available (e.g., Hackett et al., 2008). However, we decided to use the phylogeny proposed by Sibley & Ahlquist (1990), mainly to allow for comparisons with McKechnie & Lovegrove (2002) who used the same phylogeny. For mammals we used an updated version (Fritz et al., 2009) of the mammalian supertree (Bininda-Edmonds et al., 2007). For each data set analysed, tips for unavailable data were trimmed from this tree. The mammalian tree (which includes different branch lengths) for all species investigated here is shown in Fig. 2.

Fig. 1 — Phylogenetic tree of the bird species investigated. Different colours indicate the following families (from top to bottom): Nectariniidae, Hirundinidae, Artamidae, Pipridae, Columbidae, Podargidae, Aegothelidae, Strigidae, Trochilidae, Apodidae, Coliidae, Alcedinidae, Todidae. * The single hibernating species among birds was the Common Poorwill, *Phalaenoptilus nuttallii*.

Fig. 2 — Phylogenetic tree of the mammal species investigated. Species names in different colours indicate different orders. The coloured blocks next to species names indicate the use of hibernation (blue) or daily torpor (red), according to the traditional definition of heterothermy types.

To compute phylogenetically informed regressions we used the evolutionary models and branch length transformation algorithms implemented in the R-library “ape” (Paradis et al., 2004). These included the Ornstein-Uhlenbeck model, the Brownian model, the ACDC model, Grafen’s method and Pagel’s algorithm. Initial trials showed that for all response variables investigated, using Pagel’s method (Pagel, 1999; Freckelton et al., 2002) led to much lower estimates of model AIC (Akaike’s information criterion) than any other algorihm. Hence, all PGLS models were computed using Pagel’s method. Pagels’ λ is expected to vary between 0 and 1 and can be determined by maximum likelihood fits. A λ of 0 indicates the absence of a phylogenetic signal, i.e., the trait under consideration is not more similar among closely related species. If λ equals 1 the trait distribution matches a Brownian model of evolution (i.e., “random walk” evolution). To determine 95% confidence limits for λ we used function “pgls” from the R-package “caper” (Orme et al., 2013), which also provides their probabilities of differing from 0 and 1 (which we give as P_lower>0 and P_upper<1, respectively).

Parameter estimates (i.e., intercepts and slopes) were obtained from function “gls”, because this function allows the use of restricted maximum likelihood (REML), which returns unbiased estimates, and in this regard is preferable to full maximum likelihood (ML) as used by function “pgls” (e.g., Ives et al., 2007). Since the subset of species completely differed between the classical categories (i.e., avian and mammalian daily heterotherms and mammalian hibernators) separate statistical models were computed for each subgroup (please note that there was only a single bird species preliminarily classified as a hibernator). This separation of subgroups was justified by the results from cluster analysis, which confirmed the initial categories based on TBD_max.

The primary predictor variable to explain variation in torpor characteristics was body mass (c.f., Geiser & Ruf, 1995). Initially, we also included the absolute values of the latitude of the centre of species ranges as a predictor variable for all response variables. Species range latitudes (as a proxy for environmental harshness) were obtained from the PanTHERIA database (Jones et al., 2009) for 159 mammal species. For 12 additional mammals the latitude was estimated from visually locating the approximate centre of the species range in maps provided by the International Union for Conservation of Nature (www.iucn.org) and determining its latitude. This procedure was also used for all bird species. For migratory species with two ranges, we used the geographic range in which torpid animals had been observed. The latitude of the species range was indeed the best predictor of avian torpor bout duration (see Results). In all other cases, including latitude complicated the models without substantially decreasing the residual variance, as indicated by unchanged or strongly increased AIC values. At least partly, this was probably caused by multicollinearity, i.e., a correlation between body mass and latitude among hibernators (see Results). Therefore, latitude was omitted from these models. In models with TMR as the response variable and body mass as the predictor, we did not use T_{b min} as an additional covariate, because for many species T_{b min} and TMR_min were determined in different individuals and/or times.

To obtain approximately linear relationships and normally distributed residuals, body mass was log₁₀ transformed, and in several cases, so was the response and other predictor variables (see Results). For significant linear PGLS regressions, we report R² values as well as intercept, slope and the t- and corresponding P-values for the difference between the slope and 0. To compare slopes from separate regressions, we computed their 95% confidence intervals. It should be noted that regression lines in PGLS, due to sample weighting as derived from the phylogeny may substantially differ from “eye-fitted” lines, i.e. the relationship expected from the data scatterplot. Therefore, we show regression lines from PGLS models even if their slope was not significantly different from zero. As several torpor variables were affected by body mass, and mean masses considerably differed between subgroups, simple group means of variables investigated may reflect the combined effects of both torpor-type and body mass differences. Therefore, we additionally give variable values predicted from the regression equations for a 30 g animal of each subgroup (i.e., very close to the overall median body mass of 32 g for all species included in our analysis), which we also call “adjusted means”. Adjusted means, which arguably are better suited to assess the pure effects of torpor-type, are given together with 95% confidence intervals (95% CI) computed from the standard errors of model coefficients. Further 95% CI are also given for the arithmetic mean of all variables. These 95% CI were computed by bootstrapping the data (i.e., generating distributions of 1000 means by random sampling with replacement and determining their 0.025 an 0.975 quantiles; (for details see Efron & Tibshirani, 1993)). For body masses, which were skewed to the right, we also give geometric means. To allow for a comparison of body masses of heterothermic mammals with terrestrial mammals in general (both heterothermic and homeothermic species), we also computed mean and median, as well as their 95% CI, from adult body masses of 2636 terrestrial mammal species provided in the PanTHERIA database (Jones et al., 2009). All statistical analyses were all carried out using R 3.0.2 (R Development Core Team, 2013).

III. RESULTS

(1) Classification of torpid states

TBD_max was the variable that showed the clearest bimodal distribution (Fig. 3). All other variables, except for IBE, also showed distinctly bimodal distributions, with some overlap, however, between species previously classified as daily heterotherms and hibernators.

Results from Gaussian-mixture cluster analyses unambiguously pointed to the existence of two groups within the species investigated. A two-cluster structure was the best model for all single variables and variable combinations tested (P<0.0001 in all cases). The separation of clusters was strongest when based on TBD_max (χ²=91.3), followed by TBD_mean (χ²=74.1), a combination of TMR_min and T_{b min} (Fig. 4; χ²=51.0), TMR_rel (χ²=36.3), a combination of TMR_rel and T_{b min} (χ²=32.9), and T_{b min} alone (χ²=22.5). The clusters suggested based on TBD_max were virtually identical to our initial classification (99% of species, with only two exceptions, i.e., Elephantulus edwardii and Elephantulus myurus). However, the agreement was also very high when based on other variables, i.e., 97% for TMR_min + T_{b min}, 96% for TBD_mean, 95% for TMR_min, 93% for TMR_rel, 92% for TMR_rel + T_{b min}, and 84% for T_{b min}. Given that classifying species as daily heterotherms was confirmed by bimodal variable distributions (Fig. 3) as well as cluster analyses, and could be based largely on variables beyond TBD_max, such as TMR_min and T_{b min} alone (Fig. 4), we henceforth simply refer to these groups as “daily heterotherms” and “hibernators”, and maintain our preliminary classification of species.

Fig. 4 — Results from a cluster analysis based on the traits TMR_min and T_{b min} indicating the existence of two clusters within heterotherms. Circles represent 95% confidence ellipses for the estimated cluster centres (indicated by asterisks). All species on left of the dashed line were classified as belonging to cluster 1, which was identical to our initial category “hibernators” except for three species (*Elephantulus rozeti, Microcebus myoxinus, Petaurus breviceps*). Species on the right of the dashed line assigned to cluster 2, which was identical to the traditonal category “daily heterotherms” except for 1 species (*Ursus americanus*). Overall there was a high degree of agreement (117 of 121 species) between this cluster analysis and classical categories. The inset graph shows the density surface computed from the parameters of the Gaussian mixture model.

(2) Geographical and phylogenetic distribution of species

Centres of species geographic ranges were located in the northern hemisphere in 93 cases (mean latitude: 36.9 ± 1.3°N) and in the southern hemisphere in 78 cases (23.1 ± 1.1°S). The absolute mean latitude of species ranges was very similar for mammalian and avian daily heterotherms (Table 2; overall mean: 24.5 ± 1.1°). The mean latitude was significantly higher, i.e., 35.0 ± 1.4°, for mammalian hibernators (Table 2, and 35° for the single avian hibernator). Moreover, these mean latitudes of geographical ranges in heterothermic species were considerably higher than in mammals in general (17.5 ± 0.2°; no estimates were available for all birds). Among daily heterotherms, body mass was unaffected by the species range latitude among both mammals (log₁₀BM=)1.66+0.003 Latitude, t=0.82, P=0.411) and birds (log₁₀BM=−1.48+0.005 Latitude, t=0.18, P=0.858). However, body mass increased slightly with latitude in mammalian hibernators (log₁₀BM=−0.901+0.007 Latitude, t=2.18, P=0.0031). Body mass contained a strong phylogenetic signal in all three subgroups. Pagel’s λ was 1.0 (95% CI: 0.93-1; P_lower>0=<0.0001, P_upper<1=1) among avian daily heterotherms, 1.00 (95% CI: 00.86-1; P_lower>0=<0.0001, P_upper<1=1) among mammalian daily heterotherms, and 0.99 (; 95% CI: 0.95-1; P_lower>0=<0.0001, P_upper<1=0.39) among mammalian hibernators.

Table 2.

Central tendencies of variables of torpor as well as of body mass and the absolute value of latitude of species geographic ranges in mammals and birds. Adjusted means are values for a 30 g animal (the overall median body mass in the data set) predicted from the regression of variables against body mass. TBD_max: maximum torpor bout duration; TBD_mean: mean torpor bout duration; IBE: inter-bout euthermia duration; TMR_min: minimum MR in torpor; TMR_rei: metabolic reduction below BMR.

	Avian daily heterotherms	Mammalian daily heterotherms	Mammalian hibernators
Body mass (kg)
Mean	0.052	0.336	2.410
95% CI	0.028-0.083	0.069 – 0.706	0.350 – 5.413
Geometric Mean	0.020	0.033	0.093
95% CI	0.013 – 0.030	0.024 – 0.049	0.061-0.147
Median	0.026	0.026	0.068
N	42	78	93
Latitude (°)
Mean	23.1	25.3	35.0
95% CI	19.1 – 27.1	22.5 – 27.8	32.3 – 37.4
Median	24.0	26.2	38.1
N	42	78	93
TBD_max (h)
Adjusted mean	10.1	11.2	266.6
95% CI	9.7 – 10.6	10.6 – 11.8	111.7-636.6
Mean	10.1	12.9	391.9
95% CI	9.0 – 11.2	11.4 – 14.5	303.9-479.9
Median	10	12.3	288
N	23	57	82
TBD_mean (h)
Adjusted mean	6.1	6.0	123.9
95% CI	3.0 – 12.4	3.0-12.4	51.7 – 297.2
Mean	6.3	8.2	198.0
95% CI	4.9 – 7.6	7.0 – 9.3	158.2-233.8
Median	6.3	7.4	161
N	12	50	70
Tb_min (°C)
Adjusted mean	21.8	16.9	3.9
95% CI	17.5 – 26.1	11.4 – 22.5	--2.9 - 10.7
Mean	20.2	18.1	6.2
95% CI	18.0 – 22.1	16.6 – 19.4	4.8 – 7.7
Median	20.8	17.9	5.0
N	41	73	79
TMR_min (mL O₂ g⁻¹ h⁻¹)
Adjusted mean	0.585	0.237	0.039
95% CI	0.302 – 1.134	0.100 – 0.600	0.036 – 0.040
Mean	0.740	0.430	0.037
95% CI	0.557 – 0.951	0.352 – 0.509	0.032 – 0.043
Median	0.500	0.370	0.035
N	25	54	50
TMR_rel (% of BMR)
Adjusted mean	35.3	18.8	4.3
95% CI	16.0-78.0	7.5-47.2	2.1 – 8.7
Mean	30.5	29.9	4.4
95% CI	22.0 – 39.8	26.1 – 34.4	3.5 – 5.6
Median	24.0	28.0	3.0
N	19	54	50
IBE (h)
Adjusted mean	17.2	14.1	6.9
95% CI	13.9-21.4	10.1-19.7	3.5-13.4
Mean	17.7	15.8	12.0
95% CI	16.4-19.0	14.6-16.8	9.8-14.4
Median	17.7	16.6	10.3
N	12	50	49

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1) Note that inter-bout euthermia (IBE) in daily heterotherms was estimated from 24 h - TBD_mean.

The mean body mass was significantly higher in mammalian hibernators than in both mammalian and avian daily heterotherms (Table 2). This was also true when geometric means were compared, to adjust for the skewness in the body mass data (Table 2). Body mass of the single avian hibernator was 0.035 kg. The mean and median body masses of mammalian heterotherms were significantly lower than those of terrestrial mammals in general (n=2636; mean: 24.4 kg, 95%CI: 17.3-32.4 kg; median: 0.134 kg, 95%CI: 0.111-0.165 kg).

Among mammals most orders represented here contained both daily heterotherms and hibernators (Fig. 2), with two exceptions: the carnivorous/omnivorous marsupial orders Dasyuromorphia and Didelphimorphia, for which daily torpor but not hibernation has been reported. In all other orders, the proportion of hibernators (overall 57%) and daily heterotherms (43%) was approximately the same (Chi²=11.4, df=10, P=0.325).

(3) Maximum torpor bout duration

TBD_max slightly increased with body mass among mammalian daily heterotherms, but was independent of body mass among both avian daily heterotherms and mammalian hibernators (Fig. 5A); regression slopes did not differ between the three groups. Pagel’s λ was 0 (95% CI: 0-0.58; P_lower>0=1, P_upper<1=<0.001) among mammalian daily heterotherms, indicating that a phylogenetic signal in this response variable was absent among mammals using daily torpor. This was also the case for avian daily heterotherms (λ=0, 95% CI: 0-0.67; P_lower>0=1, P_upper<1=<0.0001). TBD_max did contain a significant phylogenetic signal, however, among hibernating mammals (λ=0.56, 95% CI: 0.13-0.82; P_lower>0=0.018, P_upper<1=<0.0001). TBD_max significantly increased with latitude of the species’ distribution centre among hibernating mammals, but not among daily heterotherms (Fig. 5 B).

Fig. 5 — A) Maximum torpor bout duration in relation to body mass. In mammalian daily heterotherms TBD slightly increased with body mass (log₁₀duration=1.28+0.152 log₁₀BM, t=2.56, P=0.013, R²=0.10). In mammalian hibernators maximum TBD was independent of body mass (P=0.968) and this was also the case for avian daily heterotherms (P=0.55). B) Maximum torpor bout duration in relation to absolute latitude of the species distribution centre. For mammalian daily heterotherms the regression was not significant (t=−0.49, P=0.621). Among mammalian hibernators maximum torpor bout duration increased with latitude (log₁₀duration=1.985+0.0144 Latitude, t=5.05, P<0.0001, R²=0.12). There was no significant relationship in avian daily heterotherms (t=−0.73, P=0.471).

Adjusted means of TBD_max (calculated for a body mass of 30 g) were ~10-11 h in both mammalian and avian daily heterotherms, and >200 h in hibernating mammals (Table 2). TBD_max was 120 h in the common poorwill.

(4) Mean torpor bout duration

Mean torpor bout duration (TBD_mean) was independent of body mass in all subgroups of birds and mammals (t<=1.04, P>=0302). TBD_mean contained no significant phylogenetic signal among mammalian (λ=0, 95% CI: 0-1; P_lower>0=1, P_upper<1=<0.0001) or avian (λ=0.53; 95% CI: 0-1; P_lower>0=0.49, P_upper<1=0.21) daily heterotherms. TBD_mean did, however, contain a slight phylogenetic signal in mammalian hibernators (λ=0.47, 95% CI: 0-0.79; P_lower>0=0.070, P_upper<1=<0.0001). TBD_mean increased with increasing latitude of the distribution range among hibernating mammals, but not for daily heterotherms (Fig. 6). The slope for this relationship in hibernators was steeper than that for TBD_max.

Fig. 6 — Mean torpor bout duration in relation to absolute latitude of the species distribution centre. There were no significant relationships in avian (t=0.73, P=0.487) or mammalian daily heterotherms (t=−1.49, P=0.140). Mean torpor bout duration increased with latitude in mammalian hibernators (log₁₀duration=1.503+0.019 × Latitude, t=5.36, P<0.0001, R²=0.26).

Adjusted means (to 30 g body mass) of TBD_mean were ~6-7 h in both avian and mammalian daily heterotherms, and >120 h (i.e., >17 times longer) in mammalian hibernators (Table 2). No mean torpor bout length was available for the single avian hibernator. Among mammals traditionally classified as hibernators the shortest TBD_mean were recorded for Elephantulus myurus (8.8 h), Elephantulus edwardii (17.3 h) and Atelerix frontalis (22 h).

(5) Minimum body temperature

T_{b min} in daily heterotherms increased with increasing body mass among both mammals and birds (Fig. 7). The slopes of the regression lines did not differ significantly between avian daily heterotherms, mammalian daily heterotherms, and mammalian hibernators. Among hibernators, the regression was heavily influenced by data from 3 carnivores (Ursus americanus, Ursus arctos, Meles meles, all with T_{b min} >28°C). After removing these data points (as well as a T_{b min} of 23°C reported for the arid-zone bat Rhinopoma microphyllum) the regression slope was still significantly greater than zero, however. T_{b min} contained a strong significant phylogenetic signal among mammals, both among daily heterotherms (λ=0.68; 95% CI: 0.31-0.88; P_lower>0=<0.001, P_upper<1=<0.0001) and among hibernators (λ=0.78; 95% CI: 0.55-0.91; P_lower>0=<0.0001, P_upper<1=<0.0001). Among avian daily heterotherms however, the signal was weak (λ=0.35; 95% CI: 0-0.87; P_lower>0=0.271, P_upper<1=0.004).

The predicted T_{b min} for a 30 g avian daily heterotherm was ~22°C, which was only slightly higher than in a mammalian daily heterotherm of the same body mass (17°C; Table 2). Adjusted mean T_{b min} in mammalian hibernators was ~4°C, i.e., significantly lower than in the other subgroups (Table 2). Interestingly, 8 mammalian hibernators had T_{b min} ≤ 0°C, and 3 of these had T_{b min} ≤−2°C.

(6) Minimum metabolic rate

Mass-specific TMR_min decreased with increasing body mass in both daily heterotherms and hibernators (Fig. 8A). Among daily heterotherms the slopes of the regression lines for these relationships in both mammals and birds were not statistically different from that for BMR within the same group. In hibernating mammals, however, the slope of TMR_min as a function of body mass was significantly lower (P<0.05) than that for mammalian or avian BMR. Notably though, the decrease in TMR_min of hibernators with increasing body mass was statistically significant both with and without the largest hibernator (Ursus americanus; Fig. 8A). After excluding the black bear, the regression equation was TMR=−1.651-0.156 log₁₀BM (t=−3.43, P=0.0012, R²=0.17).

BMR contained a significant phylogenetic signal among mammals (λ=0.61; 95% CI: 0.18-0.87; P_lower>0=<0.001, P_upper<1=<0.0001), but not among birds (λ=0; 95% CI: 0-1; P_lower>0=1, P_upper<1=0.117). TMR_min during daily torpor in mammals was affected by phylogeny (λ=0.81; 95% CI: 0.44-0.96; P_lower>0=0.003, P_upper<1=0.004). There was no evidence for a phylogenetic signal in TMR_min among hibernating mammals (λ=0; 95% CI: 0-0.48; P_lower>0=1, P_upper<1=<0.0001) or birds using daily torpor (λ=52; 95% CI: 0-1; P_lower>0=0.312, P_upper<1=<0.134).

The predicted, mass-specific BMR for 30-g animals was 1.060 mL O₂ g⁻¹ h⁻¹ (95% CI: 0.757-1.48 mL O₂ g⁻¹ h⁻¹) for mammals and 1.628 mL O₂g⁻¹ Fi. 10h⁻¹ (95%CI 0.993-2.671 mL O₂ g⁻¹ h⁻¹) for birds. In mammalian daily heterotherms the predicted TMR_min at a body mass of 30 g was 60% lower than in avian daily heterotherms, but the 95% CI of the estimates overlapped (Table 2). The adjusted mean of TMR_min in mammalian hibernators (~0.04 mL O₂ g⁻¹ h⁻¹) was only 17% of that in mammalian daily heterotherms (~0.24 mL O₂ g⁻¹ h⁻¹), and this difference was significant (Table 2).

There was a significant relationship between TMR_min and TBD_max among hibernators with short TBD_max being associated with high mass-specific torpor metabolic rate (Fig. 8B). A similar, but much weaker relationship between these traits was also detectable in mammalian, but not in avian daily heterotherms (Fig. 8B). At the median TMR_min across all subgroups (0.09 mL O₂ g⁻¹ h⁻¹), the predicted TBD_max was significantly higher (133.2 h; 95%CI: 52.4-338.2 h) than among mammalian (13.2; 95% CI: 10.2-16.8 h) and avian daily heterotherms (13.0; 95% Ci: 7.0-23.9 h).

(7) Relative torpor metabolic rate

TMR_rel, i.e., the TMR_min as % of BMR was variable among daily heterotherms and showed a tendency to increase with body mass, but not significantly so (Fig. 9). In mammalian hibernators the increase of TMR_rel with body mass was statistically significant.

Fig. 9 — Metabolic reduction (TMR_rel) as a function of body mass. Slight increases of TMR_rel among daily heterothems were non-significant (birds: t= 1.12, P=0.275; mammals: t=1.59, P=0.117). Among hibernating mammals there was a significant relationship between TMR_rel and body mass (log₁₀TMR_rel=0.81+0.20 log₁₀BM, t=5.40, P<0.0001, R²=0.42).

There was evidence for a phylogenetic signal in TMR_rel among mammalian daily heterotherms (λ=0.86; 95% CI: 0.49-0.99; P_lower>0=0.002, P_upper<1=0.035) but only a tendency for a signal among avian daily heterotherms (λ=0.70; 95% CI: 0-1; P_lower>0=0.104, P_upper<1=0.171). No phylogenetic signal was detectable among hibernating mammals (λ=0; 95% CI: 0-0.52; P_lower>0=1, P_upper<1=<0.0001).

Adjusted means to 30 g body mass for TMR_rel were ~40% and 30% for avian and mammalian daily heterotherms, respectively, but with overlapping 95% CI (Table 2). Among birds, the lowest TMR_rel during daily torpor were observed in Calypte anna (4.4%) and Archilochus alexandri (5.5%); among mammals the lowest values for daily torpor were reported for Elephantulus rozeti (2.0%), Microcebus myoxinus (4.5%) and Tarsipes rostratus (5.0%). Among hibernators, the adjusted mean TMR_rel was ~6% for all species (Table 2) and 4.0% (95%CI: 1.4-6.6) when the two largest values were excluded. The lowest TMR_rel was found in a bat, Vespadelus vulturnus (1.3%). Relative TMR in the single avian hibernator, Phalaenoptilus nuttallii, was 6%.

(8) Inter-Bout Euthermia

IBE was more variable in hibernators (range 1.5-44 h) than in daily heterotherms (6.8-22 h; Fig. 3, Table 2). IBE was not affected by body mass in either avian or daily heterotherms, but significantly increased with body mass in mammalian hibernators (Fig. 10A). IBE significantly decreased as mass-specific BMR increased among mammalian hibernators (Fig. 10B), but such a relationship was absent in daily heterotherms (not shown on graph). IBE contained a phylogenetic signal in mammalian hibernators (λ=0.77; 95% CI: 0.19-0.95; P_lower>0=0.028, P_upper<1=<0.0001), but the signal was non-significant among mammalian (λ=0.63; 95% CI: 0-0.94; P_lower>0=0.310, P_upper<1=<0.0001) and avian daily heterotherms (λ=0.53; 95% CI: 0-1; P_lower>0=0.394, P_upper<1=0.182). There was no significant relationship between IBE and the latitude of the species’ geographical range (all t≤1.1, P≥0.275).

Fig. 10 — A) Duration of inter-bout euthermia as a function of body mass. There was no significant relationship to body mass in avian (t=−0.59, P=0.562) or mammalian (t=0.01, P=0.987) daily heterotherms, but the duration of euthermia episodes increased with body mass among mammalian hibernators (log₁₀IBE=1.22+0.255 log₁₀BM, t=4.59, P<0.0001, R²=0.66). B) The relationship between basal metabolic rate (BMR) and the duration of interbout euthermia in mammalian hibernators (IBE=8.92-15.39 log₁₀BMR, t=−3.80, P<0.001, R²=0.50). There was no such relationship in daily heterotherms (data not shown for clarity).

IV. DISCUSSION

(1) The classification of types of heterothermy

Our results show that the classical distinction between hibernation and daily torpor is supported by clear differences in most torpor traits. Even traits that showed considerable overlap between the two groups (e.g. T_{b min}, Fig. 3), when combined with other characteristics such as TMR_min, can be used to predict whether a species uses daily torpor or hibernation to a reasonable degree of certainty (Fig. 4). Our results also show that allometric relationships of daily torpor and hibernation characteristics show distinct elevations and slopes if phylogeny is taken into account. Thus, previous analyses that pointed to the validity of this distinction of heterothermy types (e.g., Geiser & Ruf, 1995) were not caused by a lack of accounting for similar characteristics of closely-related species. The fact that T_{b min} was the variable least suited (using cluster analysis) to differentiate between daily torpor and hibernation may also explain why a recent comprehensive study (Boyles et al., 2013), using T_b-based indices of heterothermy, found only very weak evidence to support this classical division. In view of our current analysis, it seems clear that this outcome of the study by Boyles et al. (2013) does not indicate the absence of distinct types of torpor but merely underlines the problems inherent in focusing on T_b, or T_b-based indices, which -more than other variables- are affected by confounding factors such as body mass. Another reason why Boyles et al. (2013) found no clear subgroups among heterotherms was probably due to the fact that in that study, data were not restricted to extreme values, i.e., estimates of a species maximum physiological capability. Further, one of the indices used by Boyles et al. (2013), the Heterothermy Index, is intrinsically unable to distinguish between deep/short and long/shallow torpor bouts, which, given the high predictive value of torpor bout duration indicated by our analyses, questions is usefulness for the purpose of testing for the existence of physiologically distinct subgroups. This also applies to another recently suggested measure, the Thermoregulatory Index (Muñoz-Garcia et al., 2013) that requires simultaneous measurements of T_b, T_a, and MR, which currently limits its use largely to laboratory measurements. While this index may be a sensible measure of the degree of heterothermy at any point in time, it does not include the duration of torpor bouts, which, according to our analysis, was the most prominent distinctive characteristic of torpor types. For these reasons, the avoidance of arbitrary thresholds, which was the recommendable major rationale behind the development of the above indices of heterothermy, may also limit their usefulness, at least for classification purposes.

(2) Torpor bout duration and Interbout Euthermia

Our results show that classifying endotherms as daily heterotherms or hibernators based on their TBD_max (<>24 h) is highly reliable. The average TBD_max for a 30-g hibernator was >30 times greater than in a 30-g daily heterotherm. In our data set comprising 214 species, there was only one ambiguous species, Sminthopsis macroura, which had been classified as a daily heterotherm despite a TBD_max of 25.9 h. However, as pointed out by the authors (Körtner & Geiser, 2009) this maximum duration was taken from a highly unusual torpor bout for this species, and the species usually had TBDs of 11 h.

As mentioned before, hibernators may express bouts of torpor that last less than one day. Nevertheless, there are several reasons why hibernation and daily torpor should be considered as two distinct physiological states. Firstly, only one species previously classified as a daily heterotherm (Elephantulus myurus) has the capability to exhibit multiday torpor bouts (Fig. 3). Secondly, as demonstrated above, it is possible to separate the vast majority of hibernators from daily heterotherms based on a combination of T_{b min} and TMR_min alone. It remains to be seen whether those species with both low T_{b min} and low TMR_min (e.g., Elephantulus rozeti) were simply misclassified (based on TBD_max alone) and will display multiday torpor in future studies. On the other hand, reliance on extreme characteristics bears the danger of artefacts from unusual laboratory conditions, such as too low T_a (Tomlinson et al., 2007; Lovegrove, 2012a), which may have been the case in E. rozeti. However, only very few species were difficult to classify via cluster analysis, namely Elephantulus edwardii and E. myurus, both traditionally viewed as hibernators. At least in the latter species even free-ranging animals occasionally show torpor bouts lasting more than 24 hours (Mzilikazi & Lovegrove, 2004). Thus, these exptional cases seem insufficient to question the dichotomy between daily torpor and hibernation, or to postulate a third type of heterothermy (for which there was no evidence in our statistical analyses).

A third, and very important argument for differentiating between the two types of torpor is supported by studies showing that daily torpor is an extension of the circadian rhythm of T_b, and free-runs, i.e., continues with an endogenous period that slightly deviates from 24 h, under constant lighting conditions (Lynch et al., 1980; Ruf et al., 1989; Kirsch et al., 1991; Körtner & Geiser, 2000b). This is not the case, however, in hibernators, in which the circadian clock seems at least strongly suppressed, although it may still exert some influence on torpor/arousal cycles (e.g., Daan, 1973; Pohl, 1987; Grahn et al., 1994). Some studies suggest that the circadian clock actually is arrested and is restarted only after the hibernation season, at least when hibernators experience naturally low T_a (Hut et al., 2002a; Hut et al., 2002b; Ruby, 2003; Malan, 2010). Also, there is evidence that genes involved in the molecular mechanism of the circadian clock, such as Per1, Per2 and Bmal1, are expressed constantly, rather than rhythmically, during hibernation (Revel et al., 2007). Hence, although mechanisms of hypothalamic control of T_b or metabolic reduction may be similar in daily heterotherms and hibernators (while T_b set-points and the degrees of metabolic reduction differ), at least those physiological mechanisms that govern the temporal structure of heterothermy are clearly different between daily torpor and hibernation. Therefore, we concur with Sheriff et al. (2012) who suggested that short, shallow torpor bouts (<24 h), which hibernators often exhibit just prior to the hibernation season, physiologically resemble consecutive multiday torpor and should be called “short torpor”, but not “daily torpor”.

An early attempt to explain variation in TBD was a metabolism-dependent, so called “hourglass mechanism” that may control torpor/euthermia cycles. This hypothesis assumes the development of a metabolic imbalance during torpor (e.g., the accumulation or depletion of metabolites or the accretion of cellular damage) that can be eliminated only in the euthermic state (Fisher, 1964; French, 1985). This idea seemed to be supported by a decrease of TBD with body mass (and, by inference, MR), albeit in a very limited sample of mammals (French, 1985). Subsequent, more comprehensive comparisons showed no evidence for such a relationship between TBD and body mass (e.g., Geiser & Ruf, 1995; Malan, 2010), which was confirmed by the present study (Fig. 5A). The absence of an effect of body mass on TBD has been used to argue that torpor-arousal cycles are not governed by metabolism, and to dismiss the hypothesis that arousal from hibernation is driven by an hourglass mechanism (Malan, 2010). A problem with this argument is, however, that in torpid hibernators, the dependency of MR on body mass is drastically reduced (Fig. 8A), which renders body mass a very poor proxy for metabolic processes during deep torpor. Therefore, a more direct test of the hourglass hypothesis is evaluating the relationship between MR in torpor (rather than body mass) and the duration of torpor episodes. Our finding of a significant decrease of TBD with increasing TMR among hibernators (Fig. 8B), as well as a decrease of IBE with metabolic rate (Fig. 10), is fully compatible with the idea of an hourglass mechanism. If arousal is due to a metabolic imbalance, this imbalance will progress faster at high TMR, and can be eliminated more rapidly at high euthermic MR. Such a mechanism seems a more parsimonious explanation than the assumption of a specialized, non-temperature-compensated circadian torpor-arousal clock, as suggested by Malan (2010). However, the two mechanisms may not be entirely mutually exclusive, because any metabolism-driven hourglass may still be modulated by an endogeneous clock that influences the probability of actual arousal, once a certain metabolic imbalance is reached during torpor. In any case, it should be noted that such an endogenous clock modulating TBD in hibernators, if it exists, must differ anatomically and functionally from the central circadian clock controlling daily torpor (Ruby, 2003; Malan, 2010).

Arguably, the differences between clock mechanisms and respective temporal structures constitute the fundamental difference between daily torpor and hibernation, which has subsequently led to distinct levels of minimum T_b and degree metabolic reduction. They may explain the fact that most traits showed little overlap between daily heterotherms and hibernators (Fig. 3). As outlined in more detail before (Geiser & Ruf, 1995), the advantages of keeping entrained with the light-dark cycle should select against multiday torpor bouts in animals that continue to remain active and forage above ground, i.e., daily heterotherms. Species that opt to employ multiday torpor, on the other hand, should benefit from larger body mass facilitating higher body energy stores, and from reaching lower TMR_min to maximise energy savings. These differences may well have led to disruptive selection and hence to the absence of intermediate types of torpor.

Obviously, further research is necessary to clarify if it is indeed the clock mechanism governing the temporal control of torpor that separate hibernators from daily heterotherms. For instance, it would be would be interesting to see whether the constant, arrhythmic expression of clock genes in the central circadian pacemaker, which to our knowledge was demonstrated only in one mammal (Revel et al., 2007), is a general feature of hibernating mammals. We would predict that the massive suppression of clock genes in the SCN is a prerequisite of the capability for consecutive multiday torpor. However, a group of species that may be particularly important to study in this context, because some residual circadian clock activity may be adaptive for them, are those hibernators that occasionally show above ground activity during winter, such as hedgehogs (Morris, 1973) which may be exposed to light/dark cycles. Since our present analysis supports the hypothesis of an hourglass mechanism driving the torpor arousal cycles in hibernators, it points to a need for a renewed search for the nature of the “metabolic imbalance” that seems to accumulate during torpor (e.g., Fisher, 1964; French, 1985). It may be promising to concentrate this search on physiological functions that are paramount for survival at low T_b, and that have been previously suggested to play a role in the induction of arousals, namely brain and heart function (Daan et al., 1984; Carey et al., 2003; Ruf & Arnold, 2008; Giroud et al., 2013).

Advanced methods of genomics, transcriptomics and proteomics could help to identify molecular targets whose accumulation or depletion rates correlate with the durations of torpor bouts and inter-bout euthermia. Finally, another possible (albeit time-consuming) approach to better clarify the physiological differences between daily torpor and hibernation are artificial selection regimes designed to select either for or against long/deep torpor (again, along with genomics/transcriptomics or proteomics studies to identify molecular factors that may differ between selection lines). The most promising models for such a project may be those species with torpor characteristics that seem to be borderline between daily torpor and hibernation, such as Elephantulus spec.

There are further differences, apart from the circadian system functionality in winter, mainly concerning the seasonal control of torpor that appear to generally differ between hibernators and daily heterotherms. For instance, several hibernators make use of an endogenous circannual clock that drives the onset and termination of the hibernation season (Pengelley & Fisher, 1963; Pengelley & Asmundson, 1969; review in Körtner & Geiser, 2000a), whereas the seasonal occurrence of daily torpor is often triggered by short photoperiods (e.g., Lynch et al., 1978; Ruf et al., 1993), shortage of food or low ambient temperatures (e.g., Hainsworth et al., 1977; Hudson & Scott, 1979; Ruf et al., 1993; Silva-Duran & Bozinovic, 1999). Hibernation and daily torpor also differ in that the former typically relies on the availability of substantial energy reserves, either body fat or food stores, whereas daily torpor is accompanied by continued foraging. This factor likely contributed to our finding of a significant difference in body mass between daily heterotherms and hibernators. Although this variable showed the largest overlap between the two types of torpor, mean and median body mass was several times larger in hibernators. As pointed out earlier (Lindstedt & Boyce, 1985; Calder, 1996), small body mass constrains the size of body fat stores, not just absolute storage amounts but also in terms of the proportion of body fat. Hence hibernators, which seem to mostly rely on endogenous energy stores, i.e., body fat (Humphries et al., 2003b), will benefit from increased body size. Daily heterotherms, on the other hand, which continue to forage, should benefit from a functional circadian system that keeps them entrained with the light-dark cycle and serves to optimize times of daily activity and rest. The need to continue foraging also explains why both TBD_mean and TBD_max among daily heterotherms peaked well below 24 h (Fig. 3; means: ~7 h for TBD_mean and ~10 h for TBD_max; Table 2) as this average duration of daily torpor leaves sufficient time for foraging within the daily cycle.

Continued foraging versus reliance on energy stores would also help to explain why, on average, species using daily torpor have distribution ranges at lower latitudes, whereas hibernators extend geographic ranges closer to the poles. This result – which, to our knowledge, has not been reported previously – almost certainly reflects adaptations to increasing seasonality of habitats at higher latitudes and the absence of food resources in the environment during winter, favouring physiological responses that rely on energy reserves. The fact that among hibernators, and only in this subgroup, body mass increased with latitude can also be understood in terms of increased capacity for body fat stores in larger animals. However, this effect may also be explained in terms of Bergmann’s rule (Bergmann, 1848), i.e., the concept that colder climates select for increased body sizes because the associated decrease of relative body surface reduces heat loss. For a more detailed discussion of the effects of environmental conditions on body mass in hibernators see Gür (2010) and Ozgul et al. (2010).

The absolute latitude of the species’ geographic range was also a significant predictor of TBD_max, and even more so of TBD_mean, among hibernators (Figs 5, 6). To our knowledge this is also a novel finding, as the effects of latitude on hibernation characteristics have not been investigated before (but see Boyles et al., 2013 for effects of latitude on the general degree of heterothermy). TBD was not associated with latitude, however, among daily heterotherms (Figs 5, 6). The absence of this effect among daily heterotherms, as outlined above, is most likely due to the fact that TBD_max is constrained to <24 h in order to maintain entrainment with the light-dark cycle. Mean and maximum TBD in hibernators increased towards higher latitudes, which indicates that most hibernating mammals prolong torpor (even if it does increase energy savings) only if environmental conditions dictate such a behaviour. In some cases, species that hibernate for several months at higher latitudes may remain euthermic and even reproduce during winter in warmer parts of their geographical distribution range (e.g., the Garden dormouse, Gil-Delgado et al., 2006). Striking differences in the use of torpor and hibernation, likely due to local climatic conditions, may even occur on a small geographical scale (Lehmer et al., 2006). Incidentally, this degree of flexibility in the use of prolonged torpor also questions the validity of the terms “obligate” versus “facultative” hibernator.

It is evident that the coldest winter habitats at extreme latitudes require the most profound energy savings. This would explain why hibernators lengthen TBD with decreasing T_a and T_b in torpor (e.g., French, 1982; Hut et al., 2002a; Bieber & Ruf, 2009). This seems the most straightforward proximate physiological mechanism that links low hibernaculum temperatures – via T_{b min} – to decreased energy expenditure. On the other hand, high-latitude geographical ranges are also characterized by long periods of low food availability, which also should facilitate the use of energy stores and hibernation, independent of cold load. It has long been recognized that factors other than low T_a can be a major selective force favouring hibernation, such as seasonal droughts, which often occur even in subtropical and tropical environments (Darwin, 1845).

Even when adjusted for the effect of latitude, there was still a large residual variation in both maximum and mean TBD in our analyses, likely caused by species-specific factors we could not account for here. It appears that TBD_max and other characteristics of hibernation (or torpor in general) result from both the benefits and costs of hypometabolic states (Humphries et al., 2003a; Humphries et al., 2003b). The costs of prolonged torpor are evident from the fact that within a species, animals overwintering in mild winter apparently avoid its use (e.g., Gil-Delgado et al., 2006; Lehmer et al., 2006). Further, supplemental feeding of food-hoarding hibernators can significantly reduce their use of torpor (Humphries et al., 2003a) and individuals with high body energy reserves among fat-storing hibernators reduce torpor use and increase euthermic episodes during winter (Zervanos et al., 2013; Bieber et al., 2014). While these observations indicate that torpor use is minimized whenever possible, the physiological mechanisms generating costs are not as easy to pinpoint. One physiological function that may be impaired is memory (Millesi et al., 2001), but this effect may be species specific (Clemens et al., 2009). It has also been hypothesized that torpor may represent a state of sleep deprivation, but there was little experimental support for this hypothesis (review in Kräuchi & Deboer, 2011). Further, torpor at low T_b is associated with extreme immune-suppression that is reversed during periodic arousals (Burton & Reichman, 1999; Prendergast et al., 2002; Bouma et al., 2010). Generally, immune-suppression during torpor is probably beneficial as it saves energy, protects from inflammatory processes, and typically has little risks since most microbes proliferate very slowly at low temperatures (Ma et al., 2005; Bouma et al., 2010). However, impaired immune function during hibernation may increase the risk of contracting certain viral or fungal diseases that can be lethal (Prendergast et al., 2002; Bouma et al., 2010). Torpor also seems associated with increased oxidative stress and the potentially costly up-regulation of antioxidant defences (Buzadžić et al., 1997; Carey et al., 2000; Ni & Storey, 2010). Recent evidence from edible dormice suggests that despite up-regulated antioxidant defences, arousals from deep hibernation are associated with cellular damage in terms of shortening of telomeres, i.e., the repeated sections of DNA that ensure the integrity of the ends of chromosomes (Turbill et al., 2013). This effect may be directly related to rewarming from low T_b as the use of daily torpor in Djungarian hamsters (with much higher T_{b min}), was found to have a positive effect on relative telomere-lengths (Turbill et al., 2012).

The benefits of torpor are easier to characterize, because they were the focus of research in this field in the past. In particular, it has been known for some time that hibernation and daily torpor result in significant energy savings (Hall, 1832; Darwin, 1839; Wyss, 1932; Kayser, 1939). However, recent data identify several other beneficial functions of torpor. Torpor facilitates migration in certain birds, it is an integral part of reproductive strategies that involve sperm storage in certain bats and other mammals, it can primarily serve as a water conservation mechanism, and it was found to lower the risk of extinction (review in Geiser & Brigham, 2012). The latter finding is due to the fact that hibernation, which typically is associated with retreat into underground burrows and other secluded areas, decreases predation risk and, although often assumed otherwise, leads to much higher survival rates than during the active season in the same species (review in Turbill et al., 2011). The fact that torpor indirectly facilitates predator avoidance may help to explain why both hibernators and daily heterotherms have relatively low body masses, compared to terrestrial mammals on average: Large mammals have fewer predators and extrinsic mortality decreases as body mass increases (Owen-Smith & Mills, 2008; Ricklefs, 2008). Further, large animals seem unable to dig underground burrows, which prohibits this avenue of predator avoidance, but maintain high alertness and fast flight, which are incompatible with deep torpor. Obviously, further important energetic reasons, related to T_b and TMR_min (see below) may account for the finding that hibernation and daily torpor become exceedingly rare as body size increases.

(3) Minimum body temperature in torpor

The T_{b min} of a typical 30-g mammal was 13°C lower in hibernators than in mammalian daily heterotherms (and 18°C lower than in birds showing daily torpor). However, there was also considerable overlap between these subgroups (Figs 3, 7) confirming the earlier conclusion that T_{b min} alone is not well suited to discriminate between hibernation and daily torpor (Geiser & Ruf, 1995).

T_{b min} increased significantly with body mass in all groups, whether apparent outliers (i.e., large carnivores with T_{b min} >28°C) were included or not. This differs from euthermic mammals, in which resting T_b shows no allometric relationship to body mass (Lovegrove, 2012b). Our present result also differs from previous analyses of smaller samples that had not shown any body mass effect on T_{b min} among hibernators (Geiser & Ruf, 1995). One might be tempted to attribute this increase of T_{b min} to effects of thermal conductance decreasing as body mass increases. However, based on the allometric equation for conductance in mammals (Bradley & Deavers, 1980) the increase of T_{b min} (in animals at steady state with identical TMR_min) would only be of 2.5°C, for an increase in body mass from 10 g to 10 kg. The observed effect was much larger (+6°C) over the same body mass range, among mammalian hibernators even after removal of outliers, and even larger (+ 11 to 17°C) in daily heterotherms (Fig. 7). Moreover, whereas large body size and the ensuing large heat capacity may create time-constraints for entrance into and rewarming from daily torpor, this factor should be negligible in hibernators that may stay torpid for several weeks. Therefore, we suggest that small animals, with higher mass-specific metabolic rates, select a low T_{b min} in order to reach TMR_min similar to those reached by larger animals. Lower T_{b min} will always be associated with lower TMR_min irrespective of whether metabolic reduction results from active metabolic depression (with decreasing T_{b min} as a side effect) or from temperature effects (cf. Carey et al., 2003). The finding that many large animals maintain relatively high T_{b min} provides further support for the view that the torpid state appears to be also associated with risks or physiologically adverse effects, making the regulated depth of torpor the evolved result of a trade-off between its costs and benefits. Since the use of energy reserves, namely body fat stores, to cover energy expenditure will be inevitably lower in small animals (Calder, 1996), it is not surprising that they are apparently forced to undergo extremely deep torpor bouts, and to risk adverse consequences such as cellular damage during arousals (Turbill et al., 2013).

Another factor associated with very low T_{b min} during hibernation are very low ambient temperatures, down to ~ −20°C in hibernacula of the Arctic ground squirrel (Barnes, 1989). Whereas several species may reach T_{b min} below 0°C at low T_a, supercooling seems limited to T_{b min} above −3°C (Table 1). This is probably because in the supercooled state, animals are vulnerable to ice nucleation and freezing (Boyer & Barnes, 1999), and ice-formation is much slower at high subzero temperatures (Storey & Storey, 2013), which also may allow hibernators to escape freezing by arousal.

The highest T_{b min} during torpor, on the other hand, are maintained by large carnivores (Meles meles, Ursus americanus, Ursus arctos). This trait differentiates them from other hibernators more than the TMR (although data on TMR_min are currently available only for Ursus americanus). This suggests that adverse effects of torpor may be due to, in particular, low T_{b min}. Black bears, and other large carnivores, seem to avoid adverse effects of low T_b, by maintaining body temperatures >28°C (Fowler & Racey, 1988; Tøien et al., 2011). Notably, in Ursus americanus, even at this high T_b, TMR_min reached a level (0.042 mLO₂ g⁻¹ h⁻¹) that was within the 95% confidence interval of a typical 30-g hibernator (0.036-0.043 mLO₂ g⁻¹ h⁻¹). Arguably then, the most efficient type of torpor that combines metabolic reduction typical for hibernation with an almost euthermic T_b, has evolved in these large carnivores. It remains to be clarified, however, whether torpor in these “denning” species is a separate type of heterothermy or simply represents the extreme in a continuum of hypometabolic states, and resultant body mass related T_b reductions among hibernators. In any case, the fact that high T_b apparently does not constrain the TMR_min argues against the usefulness of the term “deep hibernator” sometimes used in the literature to characterize species. Neither our analysis of T_{b min} nor that of TMR_min or TMR_rel point to the existence of distinct subgroups within hibernators.

Adverse effects of a reduction in T_b, even if decreases in T_b are small, as in bears, may also explain the conspicuous absence of torpor and hibernation, in its typical form, in certain taxonomical groups such as the ungulates. Even under extremely harsh environmental conditions, as experiences for instance by the Svalbard reindeer, these animals not use torpor but remain euthermic throughout winter (Blix, 1989). In the past, drastic reductions of food intake during winter were thought to be primarily due to a marked reduction in locomotor activity, a behaviour called “Arctic resignation” (Blix, 1989). There is, however, increasing evidence that both Cetartiodactyla and Perissodactyla are also capable of profound hypometabolism in winter (Arnold et al., 2004; Kuntz et al., 2006; Signer et al., 2011). Importantly however, such reductions in winter metabolic rate in red deer, horses, or ibex were associated with reduced peripheral tissue temperatures, rather than core temperatures (e.g., Arnold et al., 2011). It remains to be seen how many endothermic species (perhaps including marine mammals) use this type of hypometabolism, which is much less conspicuous than hibernation or daily torpor, as an alternative over-wintering strategy. As suggested by Lovegrove (2012b) one reason for the maintenance of high euthermic T_b and the avoidance of torpor may be a cursorial lifestyle, e.g., in several Lagomorpha, Artiodactyla, Perrisodactyla and Carnivora, which requires high T_b for maximum muscle function and high running speed (Clarke & Pörtner, 2010; Rojas et al., 2012). An interesting open question in this context is however, whether even cursors when using peripheral cooling may sacrifice some flight or hunting capability for energy savings under harsh winter conditions.

(4) Metabolic reduction

TMR, both in terms of absolute and relative MR, was another trait that clearly separated daily heterotherms from hibernators. For a 30-g mammal, TMR_min in hibernators was only 16.7% of that in daily heterotherms, and there was little overlap in TMR_min between these subgroups (Fig. 8). The degree of reduction of TMR_min below BMR was similar in avian and mammalian daily heterotherms (Fig. 8), resulting in statistically equivalent relative TMR_rel in these groups (Fig. 9).

TMR_min decreased with increasing body mass in both daily heterotherms and hibernators (Fig. 8). Among hibernators, the slope of this relationship was only −0.116, but significantly different from 0. In a smaller subsample of hibernators TMR_min previously appeared to be body mass independent (Geiser & Ruf, 1995), but a slope (−0.128) very similar to our present findings has been reported before (Geiser, 2004), suggesting that TMR_min in hibernators does indeed decrease slightly with body mass.

This observation raises the question why small mammalian hibernators do not reduce TMR_min further? We hypothesize there may be at least two reasons: 1) High thermal conductance forces small mammals to spend more energy to maintain a certain T_b-T_a gradient in torpor than larger animals. 2) Small species, which have to reduce MR when entering torpor from a high mass-specific BMR, may be limited by the extent of possible TMR reductions. For instance, one component of the “metabolic machinery” that generates higher BMR in small animals is mitochondrial basal proton leak, which is associated with increased membrane polyunsaturated fatty acid content (reviews in Hulbert & Else, 2005; Polymeropoulos et al., 2012). Although proton leak decreases with T_b (Polymeropoulos et al., 2012), and seems to be actively suppressed during hibernation (Barger et al., 2003), it is most likely never entirely absent. Hence, differences in membrane composition and proton leak that affect BMR may well still be present in the torpid state and could at least partly explain the mass-dependency of TMR_min.

The relative reduction of metabolic rate, i.e., TMR_rel as % of BMR was highly variable among both avian and mammalian daily heterotherms (Fig. 9). Partly, this can be attributed to measurement error in both BMR and TMR_min, used to compute TMR_rel. In very small mammals and birds, it may be almost impossible to obtain “true” values of BMR, because these animals are rarely in a genuinely post-absorptive, euthermic state at rest. Among mammalian hibernators, however, there was little variation in TMR_rel, and after the removal of two apparent outliers it was best described by a constant, i.e., 4% of BMR. Some of the larger variability in species displaying daily torpor may also be due to the maintenance of large T_b-T_a gradients in some daily heterotherms, while, at least in most hibernators, T_b typically is very close to T_a (e.g., Heldmaier & Ruf, 1992; Arnold, 1993; Bieber & Ruf, 2009).

Interestingly, the degree of metabolic reduction during mammalian hibernation is similar to the extent of metabolic depression in many other animals (e.g., molluscs, crustaceans, or reptiles; Guppy & Withers, 1999). However, much lower metabolic rates and degrees of depression can be reached by invertebrates under conditions such as desiccation, freezing, supercooling, and oxygen deficiency, down to a virtually complete absence of metabolism in diapaused eggs of brine-shrimps (Clegg, 1997). In mammals, the lowest MR_min reported was 0.01 mL O₂ g⁻¹ h⁻¹ in the hedgehog (Thäti, 1978). Conceivably, this may be close to the absolute minimum metabolic rate attainable by mammals, or even endothermic vertebrates in general. If this is the case, it would have interesting consequences, because this minimum metabolic rate will be identical to BMR once an animal reaches a body mass of 115 tonnes, which is intriguingly close to the mass of the largest known animal, the blue whale (Balaenoptera musculus; weighing up to 170 tonnes; Fig. 11). Even if mammals could further decrease their cellular metabolism, as predicted by the regression through TMR_min, minimum metabolism would be equal to BMR at a body mass of 750 tonnes, which is still within the same order of magnitude (Fig. 11). Thus, an absolute lower limit of MR around or slightly below 0.01 mL O₂ g⁻¹ h⁻¹ may well constrain the upper limit of body mass that can be reached by a mammal. This is because BMR generates just sufficient heat at thermoneutrality to keep T_b at euthermic levels. It seems that blue whales indeed always live at temperatures within or above their thermoneutral zone (Lavigne et al., 1990), and arguably will face additional thermoregulatory problems when heat production is elevated due to locomotion or lactation (Hokkanen, 1990). Of course, specialized heat-dissipation mechanisms, such as increased blood flow to body appendages may have co-evolved with larger body sizes. Still, even with such adaptations, there may be a maximum body mass at which endotherms are unable to dissipate the excess heat generated by their BMR plus other processes, and overheat with detrimental consequences (Speakman & Król, 2010).

Fig. 11 — Basal and hibernation metabolic rates among mammals intersect at a body mass close to that of the largest animal known to have ever existed, the blue whale. Body mass of endotherms may in fact reach an upper limit due to excess heat production if BMR cannot be reduced below minimum MR as reached during hibernation.

(5) Phylogeny, torpor use, and its apparent absence in certain taxa

Many of the variables investigated here contained a significant phylogenetic signal. This underlines the need for phylogenetically informed statistics in this context, although it seems that using these methods has only confirmed the classical view that daily torpor and hibernation are distinct adaptations (e.g., Geiser & Ruf, 1995). Differences in the strength of a phylogenetic signal between traits and subgroups can be partly explained by differences in the variation of torpor variables. For instance, coefficients of variation (i.e., SD/mean) were very low for TBD_max in avian (0.27) and mammalian (0.47) daily heterotherms, in which the timing of bouts is controlled by the circadian system. Not surprisingly then, there was no significant phylogenetic signal in this variable. In mammalian hibernators, on the other hand, TBD_max varied considerably (CV=1.58), which allowed for a strong phylogenetic signal. Overall there was a significant correlation between the coefficient of variation of a variable and Pagel’s λ (Spearman’s rho=0.68, P<0.002, n=18), indicating that phylogenetically close species had similar characteristics whenever variation was not constrained. Notably, several variables, such as T_{b min} in mammals, contained a strong phylogenetic signal even when the effect of body mass on these variables was statistically eliminated. Thus, phylogenetic signals in torpor variables were not just due to the fact that closely related species typically have similar body weights.

The finding that closely-related species showed similar torpor characteristics is fully compatible with a plesiomorphic origin of heterothermy. The view that torpor is an ancestral trait dates back at least to the 19^th century (reviewed in Johnson, 1931) and was subsequently reinforced by several authors, based on different lines of arguments (e.g., Eisentraut, 1956; Kayser, 1961; Grigg et al., 1990; Augee & Gooden, 1992; Malan, 1996; Grigg et al., 2004; Lovegrove, 2012a). There also seems to be a prevailing view that daily torpor, i.e., “circadian heterothermy” (Malan, 1996), represents the ancient trait, whereas prolonged hibernation, especially in cold environments, appears to be viewed as an advanced, secondary adaptation (Malan, 1996; Grigg et al., 2004; Lovegrove, 2012a). However, our present phylogenetic analysis does not rule out, of course, that heterothermy may have evolved independently in birds and mammals (c.f., Geiser, 1998). Also, significant phylogenetic signals in torpor characteristics could also be detectable if heterothermy evolved more than once in separate mammalian clades, e.g., in marsupials and placentals (discussed in Geiser, 2008). It seems entirely unlikely, however, that heterothermy involved independently in at least 11 mammalian orders (Fig. 1). Thus, a single origin of heterothermy, with subsequent adaptive adjustments depending on the biology of each species, seems the most parsimonious view, and this explanation has recently gained some evidence from a phylogenetic statistical analysis (Lovegrove, 2012c).

If heterothermy indeed is a plesiomorphic trait, this raises the question why it is absent in many extant endotherms. As pointed out before, there may well be physiological specializations and ecological conditions of certain taxa that preclude modes of energy conservation involving large drops in core T_b (c.f., Lovegrove, 2012a; Ruf et al., 2012). Adverse effects of torpor, such as memory loss (Millesi et al., 2001) or impaired muscle function (Clarke & Pörtner, 2010; Rojas et al., 2012) may have selected against torpor whenever environmental conditions in terms of climate and food availability permit continued euthermia. This view is supported by the observation that certain species may make extensive use of heterothermy under harsh, but to a much lesser extent or not at all under mild winter conditions (e.g., Lehmer & Biggins, 2005; Gil-Delgado et al., 2006; Dunbar & Brigham, 2010). Even in cold climates, costs associated with torpor may have favoured the evolution of alternatives such as increased body size (e.g., Secord et al., 2012), which lowers heat-loss due to a reduced relative body surface and additionally facilitates the development of a long, well-insulating fur (Scholander et al., 1950). Surprisingly then, at least at first glance, many small mammals alternatively save energy by a reduction of body mass towards winter. Because such a reduction of body size is typically accompanied by moult to winter fur with improved insulation, the net effect is a decrease of total energy expenditure (review in Heldmaier, 1989). Small endotherms also show various other adaptations that allow overwintering under harsh conditions without torpor. In several species of shrews, tree squirrels or moles, for instance, these adaptations include the use of elaborate nests, thermally buffered burrow systems, reliance on abundant, energy-rich prey, and food hoarding (e.g., Thompson & Thompson, 1980; Genoud, 1985; Merritt, 1986; Larsen et al., 1997). In tree squirrels, the hoarding strategy is further augmented by specialized cognitive functions that allow for very high rates of recovery of cached food (Jacobs & Liman, 1991). Another adaptation of both small and large endotherms that significantly decreases energy expenditure is reduced activity during the coldest winter periods (e.g., Merritt, 1986; Blix, 1989). There are of course further avenues by which endotherms, depending on their ecology, may avoid torpor even under severe climatic conditions.

However, even considering adverse effects of torpor and alternative adaptations, the number of heterotherms (171 mammalian, 43 avian species) examined here appears to represent only a stunningly small minority of all mammals (>5,000 species) and birds (>10,000 species). As already noted by McKechnie and Lovegrove (2002) for birds, the limited number of orders and families with species known to use heterothermy is surprising. There are of course a number of species for which some indication for heterothermy was observed (for examples of such cases, see Lovegrove, 2012a), but not enough quantitative information was provided to be included in our present analysis. Even so, the number of known heterotherms remains very limited. One might be tempted to conclude that this is simply related to the fact that the vast majority of species live in the tropics. Indeed, the mean geographical distribution range of all terrestrial mammals, for instance, is located at an absolute latitude of approximately 17.5°, which is considerably lower than that of daily heterotherms (25°) or hibernators (35°) alone. The same holds for birds for which species richness peaks in the tropical band (0-5°, Kissling et al., 2012), while heterothermic birds had geographical ranges at a mean latitude of 23°. However, heterothermic species – at least in certain taxa – commonly occur even in the tropics (e.g., McKechnie & Lovegrove, 2002; Dausmann et al., 2009; Geiser & Stawski, 2011). Relatively low numbers of known tropical heterotherms – as in the dataset examined here – are, to a certain degree, likely caused by a bias in the distribution of researchers and their preferred study species (Lovegrove, 2000). To some degree, this may have also biased our results on the latitudinal distribution of heterotherms. Another reason for the limited overall number of known heterothermic species may be the fact that only relative small fraction of species and families have been systematically investigated in regard to torpor use (Geiser & Körtner, 2010; Lovegrove, 2012a).

An additional cause for the apparent absence of heterothermy in some species can be the study of captive individuals, which does not necessarily reflect the biology of free-ranging individuals. Animals in captivity are often stressed and may not behave like their free-ranging con-specifics in regard to torpor use. This seems to be especially pronounced in birds. For instance, in captivity, frogmouths (Podargus strigoides) and kookaburras (Dacelo novaeguinea) maintain stable euthermic T_b even at low T_a (McNab & Bonaccorso, 1995; Bech & Nicol, 1999; Buttemer et al., 2003), whereas free-ranging individuals regularly reduce T_b by up to 10°C on cold winter nights (Körtner et al., 2000; Cooper et al., 2008). Moreover, under laboratory conditions, substantial decreases in T_b have been recorded only in small birds and often only after severe starvation (Marshall, 1955; Lasiewski & Dawson, 1964; Peiponen, 1965; Dawson & Fisher, 1969). In the field, some of the same species frequently enter torpor even under apparently favourable environmental conditions (Brigham, 1992; McKechnie & Lovegrove, 2002; Doucette et al., 2012). Therefore, we expect that even among birds, which typically can avoid periods of unfavourable conditions by migration, future studies will uncover many more heterothermic species that express not only daily torpor but perhaps also hibernation.

Mammals also may resist entering torpor in captivity. Free-ranging echidnas (Tachyglossus aculeatus) hibernate in many areas of Australia, including warm habitats (Grigg et al., 1989; Nicol & Andersen, 1996). In contrast, they are reluctant to do so in captivity. In sugar gliders (Petaurus breviceps), daily torpor is shallow and rare in captivity, whereas deep and frequent torpor bouts occur in the wild under similar environmental conditions (Geiser et al., 2007). Moreover, edible dormice (Glis glis) are extremely reluctant to hibernate in captivity unless they are allowed to dig their own hibernacula or are provided with elaborate artificial burrows (Wilz & Heldmaier, 2000; Bieber & Ruf, 2009). Finally, species or entire groups may be misclassified as homoeothermic based on non-systematic, short-term investigations of torpor use. This was the case, for example, for shrews and pteropodid bats, which were regularly described as being entirely homeothermic (Stoddart, 1979; Ransome, 1990), although experimental evidence clearly shows otherwise (Table 1). Especially among bats, there are probably a much larger number of heterothermic species than currently known (Geiser & Stawski, 2011; Lovegrove, 2012c; Lovegrove, 2012a). Similar incorrect conclusions were drawn from early evolutionary examinations on murid rodents including the house mouse (Mus musculus; Cade (1964)) or studies on the rock elephant shrew (Elephantulus edwardii; Leon et al. (1983)). Thus, it is likely that with an increasing number of studies on free-living animals and more systematic work on thermal biology of mammals and birds, the number of known heterotherms will increase enormoususly.

V. CONCLUSIONS

Daily torpor and hibernation are distinct physiological adaptations, and species employing these two types of metabolic reduction differ particularly in their maximum (and mean) torpor bout duration, as well as their capacity for absolute and relative reduction of metabolic rate. Moreover, hibernators, on average, reach lower T_{b min} than daily heterotherms, have higher body masses, and live at geographical ranges closer to the poles.
Arguably, a fundamental difference between daily heterotherms and hibernators is the temporal structure of torpor patterns. Daily heterotherms employ the circadian system to control torpor timing in order to stay entrained with the light-dark cycle, which facilitates continued foraging. In contrast, hibernators appear to have uncoupled their temporal control of torpor from the circadian system to allow prolonged bouts of hypometabolism and reliance on energy stores.
Within each functional group, most torpor traits (i.e., T_{b min}, TMR_min, TMR_rel) are significantly affected by body mass, suggesting a dependence on metabolic processes. Even though torpor bout duration is independent of body mass, it decreases with an increase in mass specific TMR among hibernators. Moreover, the duration of euthermic intervals between hibernation torpor bouts decreases as euthermic metabolic rate (BMR) increases. These observations support the classical hypothesis that torpor-arousal cycles in hibernators (but not in daily heterotherms) are driven by a metabolism-dependent imbalance that accumulates during torpor and is eliminated during inter-bout euthermic phases.
The degree of metabolic reduction during mammalian hibernation is similar to the extent of metabolic depression in many other animal groups (e.g., molluscs, crustaceans, or reptiles). We suggest that the absolute minimum MR observed in hibernators (~0.01 mL O₂ g⁻¹ h⁻¹) may constrain the maximum body mass of mammals – or even of endotherms in general – because this MR will generate excessive heat load under thermoneutrality at body masses > ~100 tonnes.
Most torpor traits (if they are not constrained for ecological (i.e., TBD_max in daily heterotherms) or physiological reasons (i.e., TMR_min in hibernators) contain a significant phylogenetic signal, that is, closely-related species often show similar characteristics. This supports the view of a plesiomorphic origin of torpor, with adaptive adjustments to the environmental conditions and ecology of each species.
Species-specific adaptations to certain habitats or resources may, on the other hand, also lead to the avoidance of torpid states that are associated with low core T_b. This is because decreased T_b also has adverse effects, such as an impairment of muscle function and maximum running speed. These costs of torpor may explain why many endotherms even in harsh environments employ alternative avenues of overwintering, such as food hoarding, building of elaborate nests, reducing activity or, particularly in large endotherms, regional heterothermy.
Possible adverse effects of torpor alone do not sufficiently explain however, why the occurrence of torpid states has been demonstrated only in several hundred out of >15,000 bird and mammal species. We largely attribute this fact to a scarcity of studies on undisturbed, free-ranging animals. Given the availability of new devices to measure T_b and/or MR in the field, we expect that the number of species known to exhibit torpor will increase substantially.

Supplementary Material

Appendix

NIHMS61344-supplement-Appendix.pdf^{(93.7KB, pdf)}

ACKNOWLEDGEMENTS

This study was financially supported by the Austrian Science Fund (FWF grant no. P25023), the DVCR of UNE and the Australian Research Council. We thank Renate Hengsberger for her help with the formatting of the manuscript.

Footnotes

For a definition of key terms used see Appendix 1

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PERMALINK

Daily torpor and hibernation in birds and mammals

THOMAS RUF

FRITZ GEISER

Abstract

I. INTRODUCTION

II. METHODS

Table 1.

Fig. 1.

Fig. 2.

III. RESULTS

(1) Classification of torpid states

Fig. 3.

Fig. 4.

(2) Geographical and phylogenetic distribution of species

Table 2.

(3) Maximum torpor bout duration

Fig. 5.

(4) Mean torpor bout duration

Fig. 6.

(5) Minimum body temperature

Fig. 7.

(6) Minimum metabolic rate

Fig. 8.

(7) Relative torpor metabolic rate

Fig. 9.

(8) Inter-Bout Euthermia

Fig. 10.

IV. DISCUSSION

(1) The classification of types of heterothermy

(2) Torpor bout duration and Interbout Euthermia

(3) Minimum body temperature in torpor

(4) Metabolic reduction

Fig. 11.

(5) Phylogeny, torpor use, and its apparent absence in certain taxa

V. CONCLUSIONS

Supplementary Material

ACKNOWLEDGEMENTS

Footnotes

REFERENCES

Associated Data

Supplementary Materials

ACTIONS

PERMALINK

RESOURCES

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