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The Hibernation Continuum: Physiological and Molecular Aspects of Metabolic Plasticity in Mammals


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Mammals are often considered to be masters of homeostasis, with the ability to maintain a constant internal milieu, despite marked changes in the environment; however, many species exhibit striking physiological and biochemical plasticity in the face of environmental fluctuations. Here, we review metabolic depression and body temperature fluctuation in mammals, with a focus on the extreme example of hibernation in small-bodied eutherian species. Careful exploitation of the phenotypic plasticity of mammals with metabolic flexibility may provide the key to unlocking the molecular secrets of orchestrating and surviving reversible metabolic depression in less plastic species, including humans. ©2015 Int. Union Physiol. Sci./Am. Physiol. Soc.
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The Hibernation Continuum:
Physiological and Molecular Aspects of
Metabolic Plasticity in Mammals
Mammals are often considered to be masters of homeostasis, with the ability
to maintain a constant internal milieu, despite marked changes in the envi-
ronment; however, many species exhibit striking physiological and biochem-
ical plasticity in the face of environmental fluctuations. Here, we review
metabolic depression and body temperature fluctuation in mammals, with a
focus on the extreme example of hibernation in small-bodied eutherian spe-
cies. Careful exploitation of the phenotypic plasticity of mammals with met-
abolic flexibility may provide the key to unlocking the molecular secrets of
orchestrating and surviving reversible metabolic depression in less plastic
species, including humans.
Frank van Breukelen,
Sandra L. Martin
School of Life Sciences, University of Nevada, Las Vegas,
Nevada; and
Department of Cell and Developmental Biology,
University of Colorado School of Medicine, Aurora, Colorado
Patterns of Heterothermy in
In birds and mammals, endothermy is defined as
an increase of resting or routine oxygen consump-
tion that is 5- to 15-fold higher than that ob-
served in similar sized ectotherms (89). The result
of this increased metabolism is an increased body
temperature (T
). Conversely, decreased metabo-
lism is accompanied by reduced T
. Modification
of the thermoregulatory setpoint in mammals al-
lows for control of both T
and metabolism (29);
when the setpoint is lowered to approach an am-
bient temperature that is below T
, both metabo-
lism and T
decrease. Hibernation lies at the
extreme end of a broad spectrum of phenotypes in
endotherms that conserve energy by lowering me-
tabolism and hence T
Slow-wave sleep is considered the most shallow
form of metabolic depression and is common to all
mammals (4). T
is only slightly depressed
(FIGURE 2A), and oxygen consumption is reduced
just 10-15% in this state (95). Torpor is a deeper
form of metabolic depression that can be ex-
pressed in a variety of patterns. In daily torpor,
core T
is usually moderately depressed below
33°C for relatively short periods of time, e.g., 24 h
(FIGURE 2B). In the white-footed mouse, Peromys-
cus leucurus, effective daily torpor use can result in
an energetic savings of 74% (85). The most extreme
form of metabolic depression in mammals occurs
during deep hibernation (FIGURE 2C), as exempli-
fied by small-bodied, temperate-zone species from
a wide range of taxa (reviewed in Refs. 7, 70). In
some hibernators, oxygen consumption decreases
to as low as 1% of active rates and T
to as low as
2.9°C (2), leading to a seasonal energy savings of
as much as 90% (88). Historically, some authors
have used the term estivation to describe torpor
bouts that are longer than 1 day (characteristic of
hibernation) but occur in warm dry periods rather
than in the cold (93). As our knowledge of the
thermoregulatory and activity patterns of different
mammalian species increases (reviewed in Refs.
21, 22), so does our appreciation of the extent of
their metabolic flexibility.
At this point, it is important to attempt to dispel
some of the confusion surrounding the nomencla-
ture of hibernation and torpor. Some of this con-
fusion may be the result of the diversity of
metabolic strategies underlying torpor use and of
hibernation patterns. Most authors refer to torpor
as a physiologically controlled depression of met-
abolic rate and activity. Torpor initiates with a
regulated lowering of heart, respiratory, and met-
abolic rates as well as T
setpoint, which allows T
to approach ambient temperature (FIGURE 2, B
AND C). After a period of low metabolic activity
and stable, but lowered T
, the animal elevates
heart, respiratory, and metabolic rates to initiate
rewarming and restoration of active T
, recovering
from torpor (FIGURE 2B). Many species use torpor
to conserve energy during their daily periods of
inactivity; this pattern of torpor utilization is daily
torpor or daily heterothermy (FIGURE 2B). Here,
we will use the terms “daily torpor” and “daily
heterothermy” interchangeably. In contrast to the
pattern in daily heterotherms, torpor bouts in deep
hibernators have classically been defined as ex-
tending to longer than 1 day; these are typically
confined to the cold or dry season when food re-
sources become limiting. Given that hibernation
PHYSIOLOGY 30: 273–281, 2015; doi:10.1152/physiol.00010.2015
1548-9213/15 ©2015 Int. Union Physiol. Sci./Am. Physiol. Soc. 273
was first described as “winterschlaf,” a widely use-
ful and historically correct definition of hiberna-
tion is “multiday bouts of torpor during winter.”
During deep hibernation, the multiday periods of
torpor are punctuated periodically by arousals to
euthermia, also known as interbout arousals, giv-
ing rise to a pattern of heterothermy (FIGURE 2C).
Unfortunately, the hibernation literature is often
confused by indiscriminate use of the word “hiber-
nation” to mean the period of low T
(e.g., torpor),
the entire season of heterothermy, or both. Here,
we define hibernation to be the season of torpor
utilization (FIGURE 2C) and will further specify the
physiologically distinct stages of hibernation,
which are minimally 1) entering; 2) maintaining, or
3) arousing from torpor; and 4) interbout euther-
mia (IBE; FIGURE 2D).
The physiological mechanisms controlling tem-
perature and metabolism during entry into and
exit from torpor, whether they occur in the pattern
context of daily torpor or hibernation, appear to be
identical (Ref. 93; compare FIGURE 2, B AND D). It
is important to note that, despite the shared fea-
ture of lowered T
between mammalian torpor and
hypothermia, the controlled lowering of T
point and metabolism during torpor is unique to
torpor; in hypothermia, metabolic rate is elevated
as T
drops, such that a great deal of energy is
expended attempting to fight the decline in T
This is the exact opposite of what happens during
entrance into torpor. Additionally, the hypother-
mic mammal is unable to orchestrate a spontane-
ous recovery from low T
using endogenous
mechanisms (9), whereas the ability to rewarm
spontaneously is a key feature of natural torpor.
Much of our knowledge about the physiology of
torpor and patterns of torpor utilization in mam-
mals originates from work on rodents. Mice and
other murid rodents have been excellent models
for studies of daily torpor, whereas ground squir-
rels and other sciurid rodents have been widely
used for hibernation studies (12). As we will see,
many mammals deviate in various ways from the
classical patterns of hibernation seen in these
models and illustrated in FIGURE 2. For instance,
black bear hibernation (“denning”) consists of a
continuous torpor for months despite cyclical
warming (Ref. 76; FIGURE 3A). Oxygen consump-
tion during denning may be reduced to 25% of
basal values. These data suggest a metabolic
suppression independent of T
. However, other
indicators imply a more shallow torpor status than
that of ground squirrels. In bears, there is only a
moderate depression of T
to 30°C, and females
give birth and nurse their neonate(s) during the
denning period. Although often cited otherwise,
there are data to suggest depressed but sustained
kidney function and urine production in denning
bears, which is absent under normal conditions in
ground squirrels (e.g., Refs. 8, 31, 38, 60). In other
words, hibernation can be accompanied by mark-
edly varying physiological attributes depending on
In attempting to designate hibernation vs. daily
torpor sensu stricto, it is important to consider the
evolutionary origins of torpor and endothermy.
The predominant view in the earlier literature as-
sumes torpor use evolved as a derived phenotypic
response to survive the hardships of a boreal win-
ter (50). These assumptions include consideration
of basal mammals as maintaining high and stable
. However, many mammals, including marsupi-
als, monotremes, and even some placental species
such as tenrecs, are considered protoendothermic
and demonstrate highly variable T
, even during
their active season (FIGURE 3B).
Tenrecs are Afrotherians and are related to ele-
phants, manatees, elephant shrews, and hyraxes.
Tenrecidae consists of some 10 genera encompass-
ing 35 species, with all but three of these being en-
demic to Madagascar (1, 20). There is tremendous
diversity among the tenrecs in niche, morphology,
and use of torpor. These protoendotherms may be
the closest extant representatives to a very early
mammalian ancestor (61). Genetic and morphologi-
cal studies of the evolution of placental mammals
have been unable to establish a robust phylogeny.
Significant support exists for at least three different
origins of placental mammals; in at least one of
these scenarios, Afrotherians are basal to the
other placental mammals (e.g., Exafroplacentalia
rooting; Ref. 68).
Several features of metabolic flexibility in mam-
mals blur the distinctions between daily torpor and
hibernation. Tenrecs highlight the difficulties in
strictly delineating daily torpor vs. hibernation. Al-
though much remains to be discovered regarding
tenrec hibernation and torpor use, the available
data suggest marked inter- and intra-species dif-
ferences in the extent and duration of torpor use.
In one study, investigators implanted temperature
loggers in penned lesser hedgehog tenrecs, Echi-
nops telfairi (49), and found the winter season con-
sists primarily of daily torpor bouts. However, one
individual experienced bouts of torpor that lasted
up to 4 days–a period most would consider char-
acteristic of hibernation. The data suggest these
extended torpor bouts are due to large fluctuations
FIGURE 1. A continuum of metabolic depression in
Energy consumption from least (dark blue, hibernation) to most
(no color, actively foraging). SWS, slow-wave sleep.
PHYSIOLOGY • Volume 30 • July 2015 • www.physiologyonline.org274
in ambient temperature and that E. telfairi may be
changing its normal active period to exploit the
energetic advantages of passive rewarming. In
greater hedgehog tenrecs, Setifer setosus, hiberna-
tion consists of conforming largely to fluctuations
in ambient temperature that include temperatures
that exceed those experienced by the thermoregu-
lating animal in the active season (47, 51). In con-
trast to the rather modest hibernation pattern of E.
telfairi or S. setosus, the common or tailless tenrec,
Tenrec ecaudatus, undergoes deep hibernation.
Rather than choosing tree holes or shallow bur-
rows like E. telfairi or S. setosus,T. ecaudatus
hibernates underground (52). These animals expe-
rience low T
throughout their extended hiberna-
tion season, with no interbout arousal that
characterizes every other known deep hibernator
(52). We very recently acquired a colony of T. ecau-
datus and found that animals are consistently le-
thargic during the Austral winter even when
housed at 28°C or handled, although the depth of
this lethargy is variable (van Breukelen F, personal
observations). This contrasts to the end of the hi-
bernation season in ground squirrels, when ani-
mals spontaneously cease to orchestrate torpor
bouts and return to homeothermy, i.e., they main-
tain a narrowly regulated and stable T
(12, 80). On
the other hand, it is similar to what is seen in bears,
who, along with T. ecaudatus, end their hiberna-
tion season by gradual resumption of feeding and
increased activity over the course of a few weeks in
a state of “walking torpor.” More surprisingly is
that preliminary observations (van Breukelen F,
unpublished observations) suggest sporadic facul-
tative torpor or hibernation at ambient tempera-
tures from 11 to 28°C in individual tenrecs during
the active season, when their conspecifics are re-
producing, eating, and generally active.
As indicated earlier, daily torpor is generally
characterized by a modest depression of T
, i.e,
below 32°C (93). However, in another Afrotherian,
the rock elephant shrew, Elephantulus myurus,T
may become quite low (5–10°C) despite short tor-
por bout lengths that are 27 h (57). It would be
very easy and perhaps appropriate to ascribe the
Afrotherians as being atypical. However, patterns
of torpor use that defy ready assignment as either
daily torpor or hibernation can also be found in
phylogenetically distinct species such as lemurs.
Fat-tailed dwarf lemurs, Cheirogaleus medius, hi-
bernate in tree holes for extended periods (as
much as 7 mo) despite ambient temperatures
that may be over 30°C during the day (13, 14).
These lemurs experience an apparent poikilo-
thermy that is quite distinct from the more usual
poikilothermic behavior of ectotherms, because
the torpid dwarf lemur may periodically increase
its T
to above ambient temperature. Remarkably,
the dwarf lemur’s T
pattern depends on its tree
hole, i.e., the ambient temperature fluctations. If
the tree hole is poorly insulated and its tempera-
ture regularly exceeds 30°C, the animal appears to
be strictly poikilothermic, that is, T
closely tracks
the temperature of the tree hole (FIGURE 3C). If the
dwarf lemur spends too many consecutive days
below 30°C in a better-insulated tree hole, how-
ever, it periodically adds a boost of metabolic heat
production during the rewarming phase of the
daily ambient temperature cycle to drive T
above 30°C and above the temperature in the tree
hole (FIGURE 3D). Finally, if that same animal
moves to a very well insulated tree hole where the
ambient temperature remains more constant and
close to 20°C, the lemur’s T
rhythm looks much
more like hibernation in a temperate-zone mam-
mal, with continuous torpor at low T
FIGURE 2. Schematics illustrating rhythms of sleep, daily tor-
por, and deep hibernation
A: 8 days in summer, golden-mantled ground squirrel (Martin SL, un-
published observations). B: daily torpor in Glis glis showing body tem-
perature (T
), ambient temperature, and metabolic rate (data adapted
from Ref. 93). C: ground squirrel hibernation: T
across 8 mo illustrates
the homeothermic and heterothermic (blue shadow) periods (T
trace is
adapted from Ref. 3). D: metabolic rate and T
during various hiberna-
tion phases in Glis glis. IBE, interbout euthermia. Data are adapted from
Ref. 93. In all panels, blue lines represent body temperature, red lines
represent metabolic rate, and dashed black lines represent ambient
PHYSIOLOGY • Volume 30 • July 2015 • 275
by short arousals to euthermia (FIGURE 3E) that
are driven by a large increase in metabolic rate
(15). During the dry season in mouse lemurs, Mi-
crocebus griseorufus, there are marked inter-indi-
vidual variations in torpor use that may extend
from daily torpor to hibernation over the course of
weeks (43, 44). Other mammals, including the mar-
supial Smithopsis macroura, also avail themselves
of passive solar warming in their torpor ecology
It has been argued that daily torpor and hiber-
nation are discrete adaptations (70) rather than
belong to a continuum (7) of metabolic plasticity,
as illustrated in FIGURE 1. We note that the plas-
ticity within individuals to orchestrate diverse pat-
terns of metabolic activity and T
, as seen with
dwarf lemurs moving among different tree holes
with different insulating properties (FIGURE 3,
C–E; Ref. 14); dormice engaging in daily torpor,
hibernation, and estivation (93); highly variable T
patterns of ground squirrels preparing for hiberna-
tion during fall (71); seasonal changes in torpor
bout duration and frequency of arousal that leads
to reproducibly longer periods of torpor mid-hi-
bernation season (23); and variable patterns of
woodchuck hibernation depending on environ-
mental conditions (97); taken together with the
intermediate torpor utilization patterns of the
Patagonian opossum (24) and tenrecs described
above are consistent with the view that the meta-
bolic plasticity observed among mammals repre-
sents a continuum of possible phenotypes rather
than fixed discrete patterns. It is reasonable to
infer that the apparent clustering of features, such
as minimum T
and metabolic rate during torpor
or maximum torpor bout length, into apparently
distinct pattern groups for daily torpor and hiber-
nation (70) may reflect optimal conditions for en-
ergy conservation given specific conditions of
ambient temperature and body size taken together
with strategies for avoiding predation and enhanc-
ing reproduction (79, 96).
The Mysterious Periodic Arousals
from Torpor That Give Rise to
Heterothermy in Hibernators: Or,
Why Arouse?
With the exception of the common tenrec de-
scribed above, all deep hibernators, e.g., animals
spending multiple days with low T
, experience
periodic arousals to euthermia between bouts of
torpor (IBE; FIGURE 2; Refs. 12, 52). These periodic
arousals are paradoxical because hibernation is
reasonably presumed to be an energy-saving ad-
aptation, yet at least 70% of the energy consumed
over a ground squirrel’s hibernation season is used
to drive the periodic arousals from torpor (88).
Given that so much more energy could be saved by
remaining torpid continuously, why would an
animal apparently waste it to repeatedly restore
high T
numerous times over a period of many
months? The answer to this question remains one
Temperature (C˚) Temperature (C˚)
Time (days)
Time (days)
1 16 31 15 30 1 16 31 15 30
Temperature (C˚)
FIGURE 3. Variation in patterns of heterothermy in mammals
A: hibernation in black bear over 5 mo. Figure is modified from Ref. 76 and used with permission. B: Tenrec body temperature flexibility and
ambient temperature over 5 days (van Breukelen F, unpublished observations). C–E: dwarf lemurs in different tree holes, from least (C) to most
(E) insulated, based on ambient temperature difference from outside to tree-hole, as described in Ref. 14. All panels, blue represents T
, and
dashed black represents T
.InA, red tics show movement; in C-E, red lines show outside T
vs. treehole T
in black.
PHYSIOLOGY • Volume 30 • July 2015 • www.physiologyonline.org276
of hibernation’s biggest mysteries, despite sub-
stantial speculation and research effort.
There is no question that, as a hibernator recov-
ers from the near-freezing temperatures of torpor,
the activities of cell and molecular processes that
slowed at low T
(the so-called Q
effect) are rap-
idly elevated throughout the body, along with the
more apparent physiological processes. But is this
biochemical activation effectively equivalent to
halting a reaction on ice and restarting it by mov-
ing it to 37°C (temperature explains both cause and
effect), or is arousal actually triggered by the need
to restore one or more of those processes, and, if
so, which process is key? In most cases where a
given process has been claimed as the reason un-
derlying the periodic arousals, it is more likely that
the process simply resumed because T
was re-
stored; among these are DNA, RNA and protein
synthesis, cell division, various aspects of immune
function, and sleep (reviewed in Refs. 12, 80). More
recent findings of alterations that occur during tor-
por and are restored during the interbout euther-
mic periods include dendritic retraction (69, 86,
87), leukocyte sequestration in secondary lym-
phoid organs (6), receptor-mediated endocytosis
(39), protein degradation in the proteasome (83),
and IRES-dependent initiation of translation (63).
It has been argued for decades that the hiberna-
tor’s periodic arousals from torpor are needed to
rectify some imbalance that accrues at low T
(FIGURE 4; reviewed in Ref. 54). This view is sup-
ported by the strong association of torpor bout
length with total metabolism. Specifically, elevated
oxygen consumption rates during torpor occur ei-
ther when T
is elevated due to higher ambient
temperature or when hibernators increase meta-
bolic heat production to maintain a near (but
above) freezing T
against ambient temperatures
that are well below freezing (10). In both cases,
torpor bout lengths are shortened, thereby tying
torpor bout duration to overall metabolism. These
data are consistent with at least two possible
mechanisms: 1) depletion or accrual of a metabolic
product that causes arousal from torpor
(FIGURE 4)or2) a lengthening of the normal cir-
cadian clock leads to a more extreme version of the
standard mammalian daily activity cycle (54). In-
terestingly, these two seemingly disparate views
may actually not be separable, since there is grow-
ing appreciation for the impact of metabolites and
metabolism on the transcription/translation feed-
back loops that orchestrate the mammalian circa-
dian system (16, 46, 64, 66).
If the circadian system is merely extended to
specify a torpor-arousal cycle, it predicts that tor-
por bout length is related to a central nervous
system-based timer. As depicted in FIGURE 1, daily
torpor and hibernation can be considered elabo-
rations of mechanisms evoked for slow-wave sleep
(30), a view supported by the marked similarities
FIGURE 4. Kinetic model of biochemical alterations determining torpor-arousal cycles
A: a hypothetical critical inducer/enabler of torpor (blue) increases during the euthermic period and then slowly depletes over the
torpor bout. B: conversely, an inhibitor of torpor (or activator of arousal, red) accumulates at low T
during torpor and is eliminated
during the euthermic arousal (IBE). Although definitive evidence for either an inducer or an inhibitor of torpor is lacking, there are
circulating metabolites that have been shown to cycle as predicted in both Aand B. Several amino acids, modified amino acids, ace-
toacetate, and degradation products of branched-chain amino acids deplete during torpor but are restored during each IBE (A)in
hibernating ground squirrels. Conversely, other modified and unmodified amino acids, vitamin B metabolites, myo-inositol, and allan-
toin accumulate across the torpor bout and are restored to lower levels (B) before entrance into the next bout of torpor (17). Clearly
frequent, precisely timed samples are needed to capture these types of abundance changes over the torpor-arousal cycle; metabolite
and gene product dynamics will be obscured by averaging among randomly collected torpor vs. IBE samples.
PHYSIOLOGY • Volume 30 • July 2015 • 277
between sleep and torpor physiology, e.g., reduced
setpoint, lowered electroencephalographic ac-
tivity, and behavioral quiescence. Sleep timing and
duration are greatly influenced by circadian
rhythm function (11); thus it is plausible that the
simplest path to evolving a timer for hibernation
cycles is via adaptation of the circadian timer. The
view that periodic arousals during hibernation are
the result of a lengthened circadian activity-inac-
tivity cycle was proposed long ago (54) and has
since been elaborated (55). In effect, given an os-
cillator that is not temperature compensated, tor-
por bouts of hibernation can be considered 1 long
circadian day (or night) at the molecular level. This
view has significant merit. The canonical view of
the mammalian molecular clock consists of tran-
scription factors CLOCK and BMAL1 driving the
transcription of cryptochrome and period (per)
genes, which then feedback to inhibit clock and
bmal1 gene expression (42). Oscillations are de-
pendent on transcription, translation, and mRNA
and protein degradation; processes we know are
markedly depressed during torpor in hibernating
ground squirrels (81–83) and hamsters (62), and
less, but nevertheless significantly, depressed in
Djungarian hamsters torpid at 25°C during daily
heterothermy (5).
In hibernating European hamsters, in situ hy-
bridization of the superchiasmatic nucleus shows
that per1,per2, and Bmal1 cease to cycle in a
circadian manner across torpor bouts (65). Fur-
thermore, the mRNA hybridization intensity for
arylalkylamine N-acetyltransferase, the clock-re-
sponsive gene that controls melatonin synthesis
in the pineal gland, as well as that of arginine
vasopressin are consistent with torpor being a
prolonged, continuous night phase. Unfortunately,
the sampling frequency in this study was insuffi-
cient to determine whether the clock is simply
slowed in torpor-arousal cycles or whether it is
completely abandoned. However, gene expression
changes measured by quantitative methods on
RNA extracts from hibernating ground squirrels
indicate that a peak of circadian gene expression
occurs in the hypothalamus and in peripheral tis-
sues during the euthermic arousals (73, 94), con-
sistent with a possible role for this system in the
timing of torpor-arousal cycles during hibernation.
In contrast to these limited molecular data, how-
ever, results from careful field studies on male
arctic ground squirrels seem to favor the view that
the circadian system ceases to function during hi-
bernation. Body temperature was continuously el-
evated but was arrhythmic for as many as 10–27
days while the animals remained sequestered in
their hibernacula before spring emergence and ex-
posure to light. Interestingly, these same males
retained a free-running circadian rhythm in similar
conditions after immergence into their hibernacula
in the fall but before the onset of heterothermy (90
92). A more inclusive and precisely timed sampling
strategy for assessment of the molecular circuitry of
the circadian system during torpor-arousal cycles is
needed to determine conclusively whether the clock
simply stops ticking during hibernation or whether it
continues with normal, albeit slowed, rhythm.
Just as deciphering the molecular components of
the circadian system requires precisely timed, fre-
quent sampling (37, 45, 48, 67), so will deciphering
the molecular components of hibernation. And,
like the circadian circuitry (42), hibernation cir-
cuitry is no doubt complex, with multiple levels of
regulation; it clearly involves distinct gene expres-
sion responses in different organ systems through-
out the body (18, 19, 25–28, 32–35, 39, 56, 73, 84,
94), which may be controlled by underlying meta-
bolic status (17, 40, 64, 66, 72, 75, 77, 78). It is
reasonable to hypothesize that interactions be-
tween changing metabolite concentrations and the
core clock components lead to torpor-arousal cy-
cles. Arousal could be caused by either depletion of
a factor (or factors) critical for torpor (FIGURE 4A)
or accumulation of a factor(s) inhibitory for torpor
(FIGURE 4B). There is growing evidence for accu-
mulation or depletion of certain plasma (17, 58) or
liver (59, 74) metabolites during torpor. However,
studies of hibernators to date have lacked the sam-
pling precision, intensity, or depth to elucidate the
key players. From FIGURE 4, it is clear that impre-
cise sampling will erase all chance of finding mol-
ecules with the expected kinetics of key molecular
components of the cycle. The complexity of hiber-
nation is further increased by the fact that more
than one cycle may be involved, with a seasonal
FIGURE 5. Torpor-arousal cycles
in ground squirrels are embed-
ded in a seasonal cycle
The circannual rhythm of hibernation
is represented by the outer circle (ho-
meothermic period in red; hetero-
thermic, i.e., hibernation in blue), and
the torpor-arousal cycle is repre-
sented by the inner circle (IBE, green;
torpor, dark blue).
PHYSIOLOGY • Volume 30 • July 2015 • www.physiologyonline.org278
cycle superimposed on the torpor-arousal cycle
(FIGURE 5); key factors, e.g., the nutritional and
reproductive status of the animal, vary tremen-
dously across the season (12). Therefore, the tim-
ing of sample collection across the year is also
crucial for molecular studies involving hibernators.
The importance of the seasonal framework is high-
lighted by results of a recent study showing that
muscle atrophy precedes rebuilding in hibernating
13-lined ground squirrels (36) and the finding that
a seasonal change in purinergic signaling confers
sensitivity to induction of torpor by an adenosine
receptor agonist in Arctic ground squirrels in
winter (41).
The use of a multi-species comparative ap-
proach may also facilitate elucidation of torpor
timing mechanisms. In ground squirrels, there are
pronounced cycles of torpor and arousal that im-
ply a robust timing system. In common tenrecs
and bears, animals remain torpid for the entire
season. In dwarf lemurs, the animals must appar-
ently reach a T
of 30°C to maintain torpor, oth-
erwise, they arouse. When married to an
elucidated molecular model of timing, the diversity
represented in these species could provide the
means to resolve one of hibernation’s greatest
mysteries: Why arouse? Despite much speculation
to the contrary, biochemical mechanisms that de-
termine the torpor-arousal cycle are not well un-
derstood. We believe that revealing these
mechanisms will be the key to engineering safe,
reversible metabolic depression in humans for a
wide range of applications, and hence such under-
standing deserves vigorous pursuit.
No conflicts of interest, financial or otherwise, are de-
clared by the author(s).
Author contributions: F.v.B. and S.L.M. analyzed data;
F.v.B. and S.L.M. interpreted results of experiments; F.v.B.
and S.L.M. prepared figures; F.v.B. and S.L.M. drafted
manuscript; F.v.B. and S.L.M. edited and revised manu-
script; F.v.B. and S.L.M. approved final version of
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... It has been argued, on the other hand, that the simplest path to evolving a timer for hibernation cycles is via adaptation of an existing timing mechanism, the circadian system (van Breukelen and Martin, 2015). This led to the view mentioned above that a torpor/arousal cycle is considered a single non-temperature compensated circadian day (Malan 2010;(van Breukelen and Martin, 2015). ...
... It has been argued, on the other hand, that the simplest path to evolving a timer for hibernation cycles is via adaptation of an existing timing mechanism, the circadian system (van Breukelen and Martin, 2015). This led to the view mentioned above that a torpor/arousal cycle is considered a single non-temperature compensated circadian day (Malan 2010;(van Breukelen and Martin, 2015). ...
Hibernating mammals drastically lower their rate of oxygen consumption and body temperature (Tb) for up to several weeks, but regularly rewarm and stay euthermic for brief periods (< 30 h). It has been hypothesized that these periodic arousals are driven by the development of a metabolic imbalance during torpor, that is, the accumulation or the depletion of metabolites or the accrual of cellular damage that can be eliminated only in the euthermic state. We obtained oxygen consumption (as a proxy of metabolic rate) and Tb at 7-minute intervals over entire torpor-arousal cycles in the garden dormouse (Eliomys quercinus). Torpor bout duration was highly dependent on mean oxygen consumption during the torpor bout. Oxygen consumption during torpor, in turn, was elevated by Tb, which fluctuated only slightly in dormice kept at∼3-8°C. This corresponds to a well-known effect of higher Tb on shortening torpor bout lengths in hibernators. Arousal duration was independent from prior torpor length, but arousal mean oxygen consumption increased with prior torpor Tb. These results, particularly the effect of torpor oxygen consumption on torpor bout length, point to an hourglass mechanism of torpor control, i.e., the correction of a metabolic imbalance during arousal. This conclusion is in line with previous comparative studies providing evidence for significant interspecific inverse relationships between the duration of torpor bouts and metabolism in torpor. Thus, a simple hourglass mechanism is sufficient to explain torpor/arousal cycles, without the need to involve non-temperature-compensated circadian rhythms.
... However, subsequent, comprehensive comparisons showed only an extremely weak dependency of torpor metabolic rate on body mass among hibernating mammals (Ruf and Geiser, 2015). Also, if each torpor episode represented a single circadian cycle (Malan, 2010;van Breukelen and Martin, 2015), this would require a nontemperature compensated clock, which contradicts the empirical evidence (Rawson, 1960;Zimmerman et al., 1968). Moreover, in free-living dormice, for example, a single circadian day would have to be lengthened from 24 h to >800 h during midwinter (Hoelzl et al., 2015). ...
Full-text available
Hibernating mammals drastically lower their metabolic rate (MR) and body temperature (Tb) for up to several weeks, but regularly rewarm and stay euthermic for brief periods. It has been hypothesized that the necessity for rewarming is due to the accumulation or depletion of metabolites, or the accrual of cellular damage that can be eliminated only in the euthermic state. Recent evidence for significant inverse relationships between the duration of torpor bouts (TBD) and MR in torpor strongly supports this hypothesis. We developed a new mathematical model that simulates hibernation patterns. The model involves an hourglass process H (Hibernation) representing the depletion/accumulation of a crucial enzyme/metabolite, and a threshold process Hthr. Arousal, modelled as a logistic process, is initiated once the exponentially declining process H reaches Hthr. We show that this model can predict several phenomena observed in hibernating mammals, namely the linear relationship between TMR and TBD, effects of ambient temperature on TBD, the modulation of torpor depth and duration within the hibernation season, (if process Hthr undergoes seasonal changes). The model does not need but allows for circadian cycles in the threshold T, which lead to arousals occurring predominantly at certain circadian phases, another phenomenon that has been observed in certain hibernators. It does not however, require circadian rhythms in Tb or MR during torpor. We argue that a two-process regulation of torpor-arousal cycles has several adaptive advantages, such as an easy adjustment of TBD to environmental conditions as well as to energy reserves and, for species that continue to forage, entrainment to the light-dark cycle.
... Nonetheless, it is important to note that many hibernators exhibit beneficial redox-related adaptations and have been found to be very tolerant to hypoxia and reoxygenation. However, this may be due to exceptional metabolic plasticity rather than due to specific adaptations to environmental hypoxic exposure (Staples, 2014;van Breukelen and Martin, 2015). ...
Reactive oxygen species (ROS) are important cellular signalling molecules but sudden changes in redox balance can be deleterious to cells and lethal to the whole organism. ROS production is inherently linked to environmental oxygen availability and many species live in variable oxygen environments that can range in both severity and duration of hypoxic exposure. Given the importance of redox homeostasis to cell and animal viability, it is not surprising that early studies in species adapted to various hypoxic niches have revealed diverse strategies to limit or mitigate deleterious ROS changes. Although research in this area is in its infancy, patterns are beginning to emerge in the suites of adaptations to different hypoxic environments. This review focuses on redox adaptations (i.e., modifications of ROS production and scavenging, and mitigation of oxidative damage) in hypoxia-tolerant vertebrates across a range of hypoxic environments. In general, evidence suggests that animals adapted to chronic lifelong hypoxia are in homeostasis, and do not encounter major oxidative challenges in their homeostatic environment, whereas animals exposed to seasonal chronic anoxia or hypoxia rapidly downregulate redox balance to match a hypometabolic state and employ robust scavenging pathways during seasonal reoxygenation. Conversely, animals adapted to intermittent hypoxia exposure face the greatest degree of ROS imbalance and likely exhibit enhanced ROS-mitigation strategies. Although some progress has been made, research in this field is patchy and further elucidation of mechanisms that are protective against environmental redox challenges is imperative for a more holistic understanding of how animals survive hypoxic environments.
... The drop in T b may be considerable in hibernators, which often allow T b to reach values close to 0°C, but it can also be much shallower, as is often the case in species entering daily torpor (Ruf and Geiser, 2015). It has been suggested that a continuum may exist between these types of torpor as well as between torpor and euthermic rest (Boyles et al., 2013;McKechnie and Lovegrove, 2002;van Breukelen and Martin, 2015). Torpor use has profound implications on energy expenditure and allocation and affects many biological functions (Geiser and Brigham, 2012;Nowack et al., 2017). ...
Full-text available
Torpor is a state of controlled reduction of metabolic rate (M) in endotherms. Assigning measurements of M to torpor or euthermy can be challenging, especially when the difference between euthermic M and torpid M is small, in species defending a high minimal body temperature in torpor, in thermolabile species, and slightly below the thermoneutral zone (TNZ). Here, we propose a novel method for distinguishing torpor from euthermy. We use the variation in M measured during euthermic rest and torpor at varying ambient temperatures (Ta) to objectively estimate the lower critical temperature (Tlc) of the TNZ and to assign measurements to torpor, euthermic rest or rest within TNZ. In addition, this method allows the prediction of M during euthermic rest and torpor at varying Ta, including resting M within the TNZ. The present method has shown highly satisfactory results using 28 published sets of metabolic data obtained by respirometry on 26 species of mammals. Ultimately, this novel method aims to facilitate analysis of respirometry data in heterothermic endotherms. Finally, the development of the associated R-package (torpor) will enable widespread use of the method amongst biologists.
... Much of the relatively recent work on the metabolic torpor spectrum has focused on mammals (Boyles et al., 2020;Kräuchi and Deboer, 2011;Reher and Dausmann, 2021;Ruf and Geiser, 2015;van Breukelen and Martin, 2015). Energetic, neurological (electroencephalogram, EEG), transcriptomic and ecological evidence exists for a physiological continuum from shallow to deep torpor in mammals, as found in several ground squirrel species, marmots and kangaroo rats (Berger, 1984;Canale et al., 2012;Florant and Heller, 1977;Glotzbach and Heller, 1976;Heller, 1979Heller, , 1978Walker et al., 1977Walker et al., , 1979. ...
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Many endotherms use torpor, saving energy by a controlled reduction of their body temperature and metabolic rate. Some species (e.g., arctic ground squirrels, hummingbirds) enter deep torpor, dropping their body temperatures by 23-37°C, while others can only enter shallow torpor (e.g., pigeons, 3-10°C reductions). However, deep torpor in mammals can increase predation risk (unless animals are in burrows or caves), inhibit immune function, and result in sleep deprivation, so even for species that can enter deep torpor, facultative shallow torpor might help balance energy savings with these potential costs. Deep torpor occurs in three avian orders, but the trade-offs of deep torpor in birds are unknown. Although the literature hints that some bird species (mousebirds and perhaps hummingbirds) can use both shallow and deep torpor, little empirical evidence of such an avian heterothermy spectrum within species exists. We infrared imaged three hummingbird species that are known to use deep torpor, under natural temperature and light cycles, to test if they were also capable of shallow torpor. All three species used both deep and shallow torpor, often on the same night. Depending on the species, they used shallow torpor for 5-35% of the night. The presence of a heterothermic spectrum in these bird species indicates a capacity for fine-scale physiological and genetic regulation of avian torpid metabolism.
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Bats are often associated with zoonotic diseases risks, a trend that has been magnified by the global COVID-19 pandemic, although no direct infection from bat to human has been documented. Rapid deforestation seems to be a major contributing factor to new viral emergencies. Education is a good tool to minimize prejudice against bats and a key step to creating a harmonious coexistence between humans and bats. This book address such topics as bats in folklore and culture, bat dispersal patterns, bats in ecosystem management, pesticide exposure risks, roost-tier preference, diversity and conservation, and ecology of white-nose syndrome.
Torpor, a state of lowered body temperature due to active reduction of the metabolic rate, has potential medical benefits. The aim of this study was to establish a novel laboratory animal that enter torpor without imposing complex conditions. When house musk shrews (Suncus murinus) were kept at an ambient temperature of 24°C, most of the animals did not enter daily torpor. However, when the ambient temperature was lowered to below 20°C, all of the shrews showed torpor in the absence of fasting and short-day photoperiod. The shrews that were exposed to a stepwise decrease in ambient temperature from 24°C to 8°C entered torpor even after returning them to a room kept at 24°C. In conclusion, this study indicates that Suncus murinus may be a suitable model animal for elucidating the mechanism of daily torpor. Elucidation of the mechanisms of torpor by using this model may be useful for inducing a state of artificial hibernation in various species including humans.
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Mammals entering hibernation undergo drastic reductions in metabolic rate and body temperature (Tb; to as low as ∼2% of euthermic metabolic rate and 1°C to -2°C). Although ventilation (V˙E) is also greatly reduced in hibernating ground squirrels, their relative ventilatory response (%ΔV˙E) to increases in inspired CO2 (∼400% increase to 7% CO2) dwarfs that of euthermic squirrels (∼60% increase). On the basis of data from earlier studies on hypothermic animals, we hypothesized that this switch in apparent ventilatory sensitivity was the result of the change in state (from euthermic to hibernating) and not due to the change in core Tb. Thus, we used whole-body plethysmography to assess the hypercapnic ventilatory response (HCVR) in thirteen-lined ground squirrels in steady-state hibernation at 20°C, 15°C, 10°C, 7°C, and 5°C. With the transition into hibernation as Tb fell, the breathing pattern became irregular and then episodic. Total V˙E and the oxygen consumption rate (V˙O2) decreased progressively as Tb fell. Hibernating squirrels with a core Tb of 20°C increased V˙E by 150% from normocapnic levels when given 7% CO2 to breathe, while squirrels with a Tb of 7°C increased V˙E by 650% when exposed to the same inspired CO2. When Tb was cooled from 7°C to 5°C, however, the increase in the HCVR fell to 450% and was associated with a rise in V˙O2 and total V˙E. These results reveal progressive changes in breathing pattern and the HCVR with decreasing Tb and suggest that the effects of hibernation state may be Tb dependent. V˙E did not fall in proportion to metabolic rate, and the HCVR increased progressively in both absolute terms and relative terms until a Tb of 7°C, both of which potentially constrain the extent of the metabolic suppression.
A variety of responses to climate seasonality have evolved by small mammals, including adjustments of the basal rate of metabolism (BMR) and the use of daily or seasonal torpor (here referred to as short-bout and long-bout torpor). The seasonal variation of their BMR is known to depend mainly on the concurrent variation of body mass, but it should also be affected by structural and functional changes occurring within the body that could depend on the expression of torpor. Thus it was hypothesized that BMR seasonality is related to the expression of torpor at an interspecific level. Seasonal BMR and body mass data were gathered from the literature and phylogenetic comparative analyses were done to test this hypothesis among mammals of less than 1 kg. BMR seasonality (dBMR) was quantified as the log-transformed ratio of the mean whole-animal BMR reported for the period P2 (autumn-winter) over that for the period P1 (spring-summer). Predictors were the seasonal body mass adjustment (dm), mean body mass (m) and torpor expression (TO, a three-level factor: no torpor, short-bout torpor, long-bout torpor). The seasonal variation of BMR was significantly related to dm but also to. Accounting for dm, species expressing long-bout torpor, but not those entering short-bout torpor, collectively exhibited a lower dBMR than species not entering torpor. Fat storage and use by species entering long-bout torpor, alone, could not explain their lower dBMR, as the TO:dm interaction was not significant. The low dBMR of species entering long-bout torpor may result from their collective tendency to down-regulate more strongly costly visceral organs during P2. The dBMR of the different TO categories overlapped appreciably, which highlights our still limited knowledge of the BMR seasonality among small mammals.
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Polar organisms must cope with an environment that periodically lacks the strongest time-giver, or zeitgeber, of circadian organization-robust, cyclical oscillations between light and darkness. We review the factors influencing the persistence of circadian rhythms in polar vertebrates when the light-dark cycle is absent, the likely mechanisms of entrainment that allow some polar vertebrates to remain synchronized with geophysical time, and the adaptive function of maintaining circadian rhythms in such environments. ©2015 Int. Union Physiol. Sci./Am. Physiol. Soc.
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Throughout the hibernation season, the thirteen-lined ground squirrel (Ictidomys tridecemlineatus) experiences extreme fluctuations in heart rate, metabolism, oxygen consumption, and body temperature, along with prolonged fasting and immobility. These conditions necessitate different functional requirements for the heart, which maintains contractile function throughout hibernation, and the skeletal muscle, which remains largely inactive. The adaptations used to maintain these contractile organs under such variable conditions serves as a natural model to study a variety of medically relevant conditions including heart failure and disuse atrophy. To better understand how two different muscle tissues maintain function throughout the extreme fluctuations of hibernation we performed Illumina HiSeq 2000 sequencing of cDNAs to compare the transcriptome of heart and skeletal muscle across the circannual cycle. This analysis resulted in the identification of 1,076 and 1,466 differentially expressed genes in heart, and skeletal muscle respectively. In both heart and skeletal we identified a distinct cold-tolerant mechanism utilizing peroxisomal metabolism to make use of elevated levels of unsaturated depot fats. The skeletal muscle transcriptome also shows an early increase in oxidative capacity necessary for the altered fuel utilization and increased oxygen demand of shivering. Expression of the fetal gene expression profile is used to maintain cardiac tissue, either through increasing myocyte size, or proliferation of resident cardiomyocytes, while skeletal muscle function and mass are protected through transcriptional regulation of pathways involved in protein turnover. This study provides insight into how two functionally distinct muscles maintain function under the extreme conditions of mammalian hibernation. Copyright © 2014, Physiological Genomics.
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Mammalian hibernators provide an extreme example of naturally occurring challenges to muscle homeostasis. The annual hibernation cycle is characterized by shifts between summer euthermy with tissue anabolism and accumulation of body fat reserves, and winter heterothermy with fasting and tissue catabolism. The circannual patterns of skeletal muscle remodeling must accommodate extended inactivity during winter torpor, the motor requirements of transient winter active periods, and sustained activity following spring emergence. Muscle volume in 13- lined ground squirrels (Ictidomys tridecemlineatus) calculated from MRI upper hindlimb images (n=6 squirrels, n=10 serial scans) declined from hibernation onset, reaching a nadir in early February. Paradoxically, mean muscle volume rose sharply after February despite ongoing hibernation, and continued total body mass decline until April. Correspondingly, the ratio of muscle volume to body mass was steady during winter atrophy (October–February) but increased (+70%) from February–May, which significantly outpaced changes in liver or kidney examined by the same method. Generally stable myocyte cross-sectional area and density indicated that muscle remodeling is well regulated in this hibernator despite vastly altered seasonal fuel and activity levels. Body composition analysis by ECHO MRI showed lean tissue preservation throughout hibernation amid declining fat mass by end of winter. Muscle protein synthesis was 66% depressed in early but not late winter compared to a summer fasted baseline, while no significant changes were observed in the heart, liver or intestine, providing evidence that could support a transition in skeletal muscle regulation between early and late winter, prior to spring emergence and re-feeding.
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Free-ranging common tenrecs, Tenrec ecaudatus, from sub-tropical Madagascar, displayed long-term (nine months) hibernation which lacked any evidence of periodic interbout arousals (IBAs). IBAs are the dominant feature of the mammalian hibernation phenotype and are thought to periodically restore long-term ischaemia damage and/or metabolic imbalances (depletions and accumulations). However, the lack of IBAs in tenrecs suggests no such pathology at hibernation Tbs > 22°C. The long period of tropical hibernation that we report might explain how the ancestral placental mammal survived the global devastation that drove the dinosaurs and many other vertebrates to extinction at the Cretaceous–Palaeogene boundary following a meteorite impact. The genetics and biochemistry of IBAs are of immense interest to biomedical researchers and space exploration scientists, in the latter case, those envisioning a hibernating state in astronauts for deep space travel. Unravelling the physiological thresholds and temperature dependence of IBAs will provide new impetus to these research quests.
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Torpor bouts of mammalian hibernators are generally shorter at the beginning and end and are consistently longer during the main part of the hibernation season. Because it is not known why the duration of torpor bouts changes at the beginning and end of the hibernation season, we studied this phenomenon in two sciurid rodents: Spermophilus saturatus (200-300g) and Eutamias amoenus (45-60g). We examined the seasonal change in torpor bout duration during hibernation at a constant air temperature ( $T_{a}$ ) of 2° C in relation to (1) the minimum body temperature (minimum $T_{b}$ ) to which the animals could be experimentally cooled before they maintained a constant $T_{b}$ or began to arouse, (2) $T_{a}$ at the time of minimum $T_{b}$ (minimum $T_{a}$ ), and (3) oxygen consumption ( $\dot{V}O_{2}$ ) of torpid individuals at $T_{a}$ 2° C. Average duration of torpor bouts during the main part of the hibernation season was about 11 d in S. saturatus and 8-9 d in E. amoenus; in response to experimental cooling, minimum $T_{b}$ of both species declined as low as -0.2° C. In early and late hibernation, when torpor bouts were short, minimum $T_{b}$ , minimum $T_{a}$ , and $\dot{V}O_{2}$ during torpor were higher than in the main part of the hibernation season. Regression analyses suggest that minimum $T_{b}$ and minimum $T_{a}$ are more strongly correlated with torpor bout duration than $\dot{V}O_{2}$ in both species.
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Small-bodied hibernators partition the year between active homeothermy and hibernating heterothermy accompanied by fasting. To define molecular events underlying hibernation that are both dependent and independent of fasting, we analyzed the liver proteome among two active and four hibernation states in 13-lined ground squirrels. We also examined fall animals transitioning between fed homeothermy and fasting heterothermy. Significantly enriched pathways differing between activity and hibernation were biased towards metabolic enzymes, concordant with the fuel shifts accompanying fasting physiology. Although metabolic reprogramming to support fasting dominated these data, arousing (rewarming) animals had the most distinct proteome among the hibernation states. Instead of a dominant metabolic enzyme signature, torpor-arousal cycles featured differences in plasma proteins and intracellular membrane traffic and its regulation. Phosphorylated NSFL1C, a membrane regulator, exhibited this torpor-arousal cycle pattern; its role in autophagosome formation may promote utilization of local substrates upon metabolic reactivation in arousal. Fall animals transitioning to hibernation lagged in their proteomic adjustment, indicating that the liver is more responsive than preparatory to the metabolic reprogramming of hibernation. Specifically, torpor use had little impact on the fall liver proteome, consistent with a dominant role of nutritional status. In contrast to our prediction of reprogramming the transition between activity and hibernation by gene expression, and then within-hibernation transitions by posttranslational modification (PTM), we found extremely limited evidence of reversible PTMs within torpor-arousal cycles. Rather, acetylation contributed to seasonal differences, being highest in winter (specifically in torpor), consistent with fasting physiology and decreased abundance of the mitochondrial deacetylase, SIRT3.
Hibernation in the Ursidae has been extensively researched over the past 30 years. This paper reviews findings of that research in the areas of general physiology and energetics; protein, fat, and bone metabolism; metabolic endocrinology; reproductive physiology and lactation; serum chemistry and hematology; and the ureaxreatinine ratio. Bears in hibernation exhibit several characteristics distinct from the deep hibernation of rodents, such as a lesser reduction in body temperature, protein conservation, lack of defecation and urination, and normal bone activity. The physiological constraints of hibernation are coupled to adaptations in reproductive physiology, such as delayed implantation and lactation. I argue that ureaxreatinine is not a reliable indicator of hibernation, although ongoing research is searching for an opioid-like hibernation trigger. Study of hibernation physiology will continue to bear fruit, especially in the areas of evolution, physiology, and medicine.
Short-day (9 light:15 dark), cold-acclimated Peromyscus leucopus known to enter torpor (no. = 24) and P. leucopus never observed in torpor (no. = 12) were compared with and without a 5-g nest at 13, 7, and 1 C over 9 wk. Oxygen consumption and body temperature were monitored approximately hourly for 2-3 days under each treatment. A second group of short-day, cold-acclimated mice (13 torpid and 14 nontorpid) were monitored for oxygen consumption with and without a 5-g nest at 13 C, first individually and 10 days later as huddles of three. For individual mice, the time required to enter torpor (3.0-4.5 h), duration of torpor (4-5 h), and minimum body temperature during torpor (21-23 C) remained fairly constant at different ambient temperatures. The metabolic rate [cm³O₂/(g · h)] necessary to maintain minimum body temperature during torpor without a nest was 2.1 at 13, 3.0 at 7, and 3.7 at 1 C, while metabolic rates during the normothermic period at these temperatures were 4.8, 5.5, and 6.7, respectively. A similar trend, but with lower values, occurred with a nest. Without a nest, torpid mice had a mean daily metabolic rate which was 20% less at 13, 21% at 7, and 9% at 1 C than the corresponding value of nontorpid animals. Torpid mice with a 5-g nest reduced metabolic rate at those temperatures by 43%, 44%, and 34%, respectively, relative to nontorpid mice without a nest. Daily torpor and huddling together provided a 58% energetic saving at 13 C relative to individually housed, nontorpid mice. The addition of a nest fostered a 74% daily energy savings versus nontorpid, individual mice without a nest.
Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian-mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (∼35◦) than daily heterotherms (∼25◦). Variables of torpor for an average 30g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30-fold longer, and mean torpor bout duration >25-fold longer in hibernators. Mean minimum body temperature differed by ∼13◦C, and the mean minimum torpor metabolic rate was ∼35% of the basal metabolic rate (BMR) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.
AimThe ability of endotherms to physiologically regulate body temperature (Tb) is presumed to be important in the adaptive radiation of birds and mammals. Recently, attention has shifted towards determining the extent and energetic significance of Tb variation documented in an ever-expanding list of species. Thus, we provide the first global synthesis of ecological and evolutionary correlates of variation in mammalian Tb. LocationWorld-wide Methods We conducted a phylogenetically informed analysis of Tb variation using two complementary metrics, namely Thermoregulatory Scope (TS) and Heterothermy Index (HI), that treat Tb variation as a continuous variable. We included morphological (e.g. body mass), ecological (e.g. food habits) and environmental (e.g. latitude) correlates in the analysis. ResultsAmong 560 mammal species included in the TS analysis, Tb relates most strongly to body mass (included in all models), season (relative parameter weight: 0.95), absolute latitude (0.80) and hoarding behavior (0.72), with small-bodied, high latitude and non-hoarding species expressing the most Tb variation. Small-bodied and high latitude species also express a greater range of thermoregulatory patterns than large-bodied and low latitude species. Results were generally similar in HI analysis, but in summer the extent of heterothermy decreases with latitude. Main conclusionsMammalian heterothermy is related to evolutionary history, climate conditions constraining minimum Tb, resource conditions mediating energy supply for maintaining high Tb, and latitudinal variation in the nature of seasonality. Our analysis further shows that traditional classification of mammals as hibernators, daily heterotherms or homeotherms is clouded or possibly misleading.