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Average longevity in free-living edible dormice (Glis glis) can reach 9 years, which is extremely high for a small rodent. This remarkable life span has been related to a peculiar life history strategy and the rarity of reproductive bouts in these seed eaters. Most females (96%) reproduce only once or twice in their lifetime, predominantly during years of mast seeding of, e.g., beech, but entire populations can skip reproduction in years of low seed availability. Surprisingly, in non-reproductive years, large fractions of populations apparently vanished and were never captured above ground. Therefore, we determined the duration of above-ground activity, and body temperature profiles in a subset of animals, of dormice under semi-natural conditions in outdoor enclosures. We found that non-reproductive dormice returned to dormancy in underground burrows throughout summer after active seasons as short as <2 weeks. Thus, animals spent up to >10 months per year in dormancy. This exceeds dormancy duration of any other mammal under natural conditions. Summer dormancy was not caused by energy constraints, as it occurred in animals in good condition, fed ad libitum and without climatic stress. We suggest that almost year-round torpor has evolved as a strategy to escape birds of prey, the major predators of this arboreal mammal. This unique predator-avoidance strategy clearly helps in explaining the unusually high longevity of dormice.
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SHORT COMMUNICATION
Summer dormancy in edible dormice (Glis glis)
without energetic constraints
Claudia Bieber &Thomas Ruf
Received: 20 June 2008 /Revised: 22 October 2008 / Accepted: 3 November 2008 / Published online: 26 November 2008
#Springer-Verlag 2008
Abstract Average longevity in free-living edible dormice
(Glis glis) can reach 9 years, which is extremely high for a
small rodent. This remarkable life span has been related to a
peculiar life history strategy and the rarity of reproductive
bouts in these seed eaters. Most females (96%) reproduce
only once or twice in their lifetime, predominantly during
years of mast seeding of, e.g., beech, but entire populations
can skip reproduction in years of low seed availability.
Surprisingly, in non-reproductive years, large fractions of
populations apparently vanished and were never captured
above ground. Therefore, we determined the duration of
above-ground activity, and body temperature profiles in a
subset of animals, of dormice under semi-natural conditions
in outdoor enclosures. We found that non-reproductive
dormice returned to dormancy in underground burrows
throughout summer after active seasons as short as
<2 weeks. Thus, animals spent up to >10 months per year
in dormancy. This exceeds dormancy duration of any other
mammal under natural conditions. Summer dormancy was
not caused by energy constraints, as it occurred in animals
in good condition, fed ad libitum and without climatic
stress. We suggest that almost year-round torpor has evolved
as a strategy to escape birds of prey, the major predators of
this arboreal mammal. This unique predator-avoidance
strategy clearly helps in explaining the unusually high
longevity of dormice.
Keywords Aestivation .Hibernation .Torpor .Predation .
Pulsed resources
Introduction
Dormancy occurs in more than half of the mammalian
orders in species that range from arctic ground squirrels to
tropical primates (Geiser and Ruf 1995; Dausmann et al.
2004). However, mammals are generally thought to restrict
torpid hypometabolic states such as hibernation [i.e.,
prolonged (>24 h) torpor in winter], aestivation or summer
dormancy (prolonged torpor in summer) and daily torpor
(<24 h) to times when environmental conditions are
unfavourable for proficient foraging (e.g., Geiser and Ruf
1995; Webb and Skinner 1996). Typically, states of
dormancy are restricted to cold or dry seasons and last,
even in extremely harsh climates such as the Arctic, not
more than approximately 8 months (Buck and Barnes
1999). Most previous reports on mammalian summer
dormancy indicate that torpor occurred in response to
adverse environmental conditions during periods of drought
(Bartholomew and Hudson 1961; Kenagy and Bartholomew
1985; Dausmann et al. 2004) or, sporadically, in animals
that fail to reproduce due to a poor body condition
(Nicol and Andersen 2002; Nicol et al. 2004). Indeed,
mammals are thought to minimise the duration of
hypometabolic states whenever possible because it may
be associated with costs such as reduced immunocompe-
tence (Prendergast et al. 2002; Luis and Hudson 2006),
neuronal damage (Arendt et al. 2003), cardiac dysfunction
(Ruf and Arnold 2008), or impairment of memory (Millesi
et al. 2001).
Edible (or fat) dormice (Glis glis) are hibernators closely
adapted to the temporally limited availability of beechnut
and acorn, their major food source in autumn in central and
northern Europe (Bieber 1998; Schlund et al. 2002; Pilastro
et al. 2003; Fietz et al. 2005; Ruf et al. 2006). In this
distribution range, females give birth to a single litter per
Naturwissenschaften (2009) 96:165171
DOI 10.1007/s00114-008-0471-z
C. Bieber (*):T. Ruf
Research Institute of Wildlife Ecology,
University of Veterinary Medicine Vienna,
Savoyenstrasse 1,
1160 Vienna, Austria
e-mail: claudia.bieber@vu-wien.ac.at
year only late in the summer season (July/August) and
nurse young in early autumn when these energy-rich seeds
are available (Bieber 1998; Schlund et al. 2002; Pilastro et
al. 2003). However, whilst beech and oak can swamp seed
eaters with overabundant food in mast seeding years,
beechnuts and acorn can be rare or completely absent in
years of seeding failure (Silvertown 1980; Ostfeld and
Keesing 2000). Dormice have responded to this pulsed
resource fluctuation by evolving a sit-and-waitstrategy of
reproduction (Pilastro et al. 2003; Ruf et al. 2006). In years
with low seed availability, large fractions or even entire
populations of dormice can skip reproduction. In those
years, dormice consume leaves, flowers and fruits (Fietz et
al. 2005), which allow them to gain weight during summer
but are insufficient to cover the additional costs of
reproduction (Bieber 1998). In addition, in the absence of
high-caloric seeds, the rapid fattening of juveniles within a
small time window in fall, and hence their survival over the
first hibernation season, seems impossible (Bieber and Ruf
2004).
Data from a long-term field study have demonstrated a
strong trade-off between reproduction and future survival in
dormice (Ruf et al. 2006). This at least partly explains why
frequent reproduction skipping can lead to a mean
longevity of up to 9 years in certain dormouse populations,
which is extremely high for a 150-g rodent (Pilastro et al.
2003). However, up to now, it remains unclear how
dormice increase survival probability in years with lower
food availability. Does the lack of investment in reproduc-
tion, and hence decreased metabolic stress, sufficiently
explain for this phenomenon? Capturerecapture field
studies revealed that dormice in mast failure years were
captured over a shortened active season (Bieber 1998).
Additionally, the probability to capture individuals at least
once during the summer season in the field was signifi-
cantly reduced (by 45%) in years of low mast seeding and
low reproduction (Ruf et al. 2006). Hence, parts of the
population seemed to vanish during years of reproduction
skipping, but were recaptured later in reproductive years.
Further, in free-living male dormice, the occurrence of daily
torpor (bouts <24 h) was found to significantly increase in
years with reproduction skipping (Fietz et al. 2004). The
aim of our study was to investigate whether reproduction
skipping affects the use and extension of hibernation or
other dormant states in dormice.
Materials and methods
All dormice (n=44, colony established in 1996) were held
in mixed groups (age and sex) year-round in three outdoor
enclosures (6×4×3.5 m each). The enclosures were located
at 370 m a.s.l. in Vienna, Austria (48°10N, 16°20E).
Mean air temperature at the enclosures during the study
period (20052007) was 11.1°C (range, 7.4 to 31.2°C).
The coldest month in our study site was January (mean
maximum, 2.9°C; mean minimum, 2.0°C), the warmest
July (mean maximum, 25.6°C; mean minimum, 15.4°C).
iButtons (DS1922L, Maxim/Dallas) were used to record
burrow temperature (15 cm below ground) and air
temperature (shaded, 2 m above ground).
The outdoor enclosures were shaded and provided with
branches. One nest box was available for each individual
(positioned at heights of 1.22 m). However, we frequently
observed two to six individuals sharing a single nest box.
Food (rodent chow, Altromin 1314 FORTI), vitamins and
water were available ad libitum. At the constantly good
food supply, we observed in both years females which
skipped reproduction whilst the others raised their litters
successfully.
Animals were captured in their nest boxes once a week
during their active season, and enclosures were searched
carefully to assure that all dormice were captured. How-
ever, we cannot completely rule out that some dormice
occasionally escaped our control. During weekly checks,
body mass was recorded to the nearest 1.0 g. Whilst the
animals occupied the offered nest boxes during the active
season, all dormice exclusively used underground burrows
dug by the animals for hibernation and summer dormancy.
Comparisons between records of subcutaneous body tem-
peratures and the nest box presence indicated that the
median time interval between termination of hibernation
and occurrence in the nest boxes above ground was 6 days
(range, 028 days; interquartile range, 411 days). Thus,
active animals were detected rapidly above ground.
Wax-coated iButtons (DS1922L, Maxim/Dallas) were
implanted for measurements of subcutaneous temperature
in the lateral area of the thorax, caudal of the scapula in 23
dormice (18 males, 15 females). Anesthesia for implanta-
tion was introduced with 4 mg ketamine + 0.8 mg xylazine
and maintained with inhalation anesthesia (isoflurane in
oxygen). At the date of implantation, animals weighed on
average 153±30 g. Implanted dormice were released 1 week
after implantation to their groups in the outdoor enclosures.
Subcutaneous temperature was recorded at approximately
hourly (3,650 s) intervals to cover 1 year. Implantation (and
start of iButtons) was carried out between June and August
2005, explantation and new implantation/replacement of
loggers between May and August 2006. Ten out of 23
dormice were implanted in the two subsequent years
(resulting in 33 datasets). Since our study was planned to
be terminated after hibernation 2006/2007, we explanted
most iButtons immediately after emergence from hiberna-
tion in MayJune 2007. However, three dormice of our
colony unexpectedly retreated again into their underground
burrows before we were able to retrieve the iButtons. In
166 Naturwissenschaften (2009) 96:165171
these three dormice, we explanted the iButtons later, in
August 2007.
Arousal and torpor duration were determined from the
times spent above and below a subcutaneous temperature of
25°C, respectively. We calculated body mass loss during
dormancy only for animals that were weighed within 6 days
after termination of hibernation.
Statistical analyses, i.e., linear models with subsequent
ANOVA, linear mixed models with a random factor
animalfor repeated measurements, and generalised linear
models (GLM), were carried out in R (R Development Core
Team 2007) partly using the package nlme(Pinheiro et
al. 2007). The tests used are specified in the text. Means are
given ±SEM.
Results
In fall of both years, all implanted animals (n= 23) retreated
to their burrows and entered hibernation for approximately
8 months (mean duration, 234.41± 4.58 days, n= 33) from
September/October to May/June. Whilst we found no
evidence for summer dormancy in 2006 (Fig. 1a), T
b
profiles of those three animals (two females, one male)
recorded until August 2007 revealed that 24 weeks after
hibernation, they reentered dormancy during summer for up
to 4 months (Fig. 1b). Another eight non-implanted
individuals of our colony showed long phases of absence
from above ground (i.e., from nest boxes or elsewhere in
the enclosures) in summer 2007 (for periods of 49 to
157 days between early April and late August; Fig. 2).
These animals lost body mass at rates (0.69 ± 0.12 g day
1
)
similar to those of the three animals in which summer
dormancy was directly recorded in the same year (0.83 ±
0.24 g day
1
; ANOVA, F
1,9
=0.305, P=0.594). In contrast,
active (not summer-dormant) dormice were captured
regularly (every 721 days) and showed a mean increase
in body mass of 0.87±0.11 g day
1
during the active
season. Together, these data suggest that 11 animals (five
females, six males, 25% of the colony) used prolonged
dormancy during summer 2007, and, as during hibernation
in this species (von Vietinghoff-Riesch 1960), solely relied
on body fat reserves to fuel energy demands during these
periods. This conclusion was further supported by the fact
that we never found any food or food remnants in the
hibernacula. Following phases of summer dormancy, eight
out of the 11 dormice (three animals were dug up from their
burrows) emerged again in autumn. All animals dug up
from their burrows, including one non-implanted individual,
felt cold to the touch and were clearly torpid. Subsequently,
some showed a brief period of pre-hibernation fattening
(Fig. 2) before they entered hibernation in September/
October 2008.
All of the five females among the 11 summer-dormant
animals did not reproduce in 2007. However, reproductive
activity was certainly not the only decisive factor for
summer dormancy, since 54% of those females that were
regularly encountered in nest boxes during summer 2007
also failed to reproduce. Further, in the previous year
(2006), only two out of 16 adult females had young, but
activity and T
b
records gave no evidence for summer
dormancy in either females or males.
Importantly, all animals that entered summer dormancy
did so in good body condition and in the presence of
energy-rich food. In spring of 2007, the mean body weight
of dormice after emergence was even significantly higher
than in the previous year (2005/2006, 131 ± 6 g; 2006/2007,
159±8 g, ANOVA, F
1,23
=6.83, P=0.015). Also, body mass
f 16EF
2006/2007
Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct
0
10
20
30
40
m 812C
0
10
20
30
40
f F086
Subcutaneous temperature (˚C)
0
10
20
30
40
m 65C6
2005/2006
Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct
0
10
20
30
40
f 16EF
0
10
20
30
40
Subcutaneous temperature (˚C)
a
b
18th April 5th May
27th May
27th June
29th May
26th June
22nd Sept.
22nd Sept.
13th Sept.
10th May
16th August
22nd August 3rd April
22nd Sept.
31st August
Fig. 1 Year-round records of subcutaneous body temperature in a
2005/2006 for two dormice with normal temperature pattern during
active season (animals were sexually active) and b2006/2007 for
three individuals with an extremely shortened active season after
hibernation (animals were sexually inactive). All three animals entered
a state of dormancy long before the expected onset of hibernation
under natural climatic conditions with food provided ad libitum.
Arrows indicate the date of emergence and immergence into natural
hibernacula, dug by the animals. ffemale, mmale. Red (grey)line =
body temperature, blue (black) line = ambient temperature recorded in
an artificial burrow. Please note that all three animals were recaptured
alive after the hibernation season in 2007/2008. Thus, they spent
approximately 19 out of the last 21 months in dormancy below ground
Naturwissenschaften (2009) 96:165171 167
after emergence was not a significant predictor of whether
or not an individual would enter summer dormancy (GLM,
family binomial,P=0.198) or of the total duration of the
time spent dormant (range, 49157 days, GLM on log-
transformed data, family Poisson,P=0.671).
As during hibernation, T
b
alternated during summer
dormancy between bouts of torpor lasting several hours to
6.8 days and intermittent brief periods of arousal to
normothermia (Fig. 3). Dormice displayed torpor at burrow
temperatures ranging between 4.6°C in winter and 20.2°C
in summer and with minimum T
b
s varying between 0.6°C
and 21.2°C (arousal temperatures not considered). Pooling
torpor bouts from summer dormancy and hibernation, we
found that arousal duration increased and torpor bout
duration decreased as burrow temperature increased
(Fig. 3). However, adding a factor seasonto a repeated
measurements regression (linear mixed effects) did not
improve the model, but caused slight increases in AICs in
both cases (from 577.9 to 579.6 for arousal duration and
from 1634.7 to 1635.9 for torpor bout duration). Body mass
loss during summer dormancy was significantly higher
(0.73±0.10 g day
1
,n=11) than during the two preceding
hibernation seasons (0.29 ± 0.03 g day
1
,n=14; ANOVA,
F
1,23
=20.07, P<0.001).
Burrow temperature (˚C)
246810121416182022
Torpor bout duration (h)
0
100
200
300
400
500
246810121416182022
Arousal duration (h)
0
4
8
12
16
20
24
f F086 Hibernation
f F086 Summer-dormancy
f 16EF Hibernation
f 16EF Summer-dormancy
m 812C Hibernation
m 812C Summer-dormancy
a
b
Fig. 3 Relation between dormancy pattern and burrow temperatures. a
Relation between arousal duration and burrow temperature (duration =
1.32+ 0.374 × T
a
,R
2
=0.60). bRelation between torpor bout duration
and burrow temperature (duration= 336.2015.94 × T
a
,R
2
=0.66).
Arousal and torpor duration were determined from the times spent
above and below a subcutaneous temperature of 25°C, respectively.
There was no evidence for a difference in these relations between
hibernation (closed symbols) and summer dormancy (open symbols)
m 061B
160
240
f 16EF
160
240
f 084F
80
160
m 812C
240
320
f F086
80
160
m 26D5
80
160
f 3294
160
240
m 5BAE
160
240
f C211
2007
Apr May Jun Jul Aug Sep Oct
160
240
157 days
126 days
114 days
91 days
70 days
67 days
67 days
126 days
m 618F
200
280 49 days
49 days
m 6CC3
Body mass (g)
160
240 53 days
Fig. 2 Body mass change in edible dormice showing summer
dormancy in 2007. Prolonged periods of summer dormancy (i.e.,
absence from above ground for at least 7 weeks accompanied by body
mass loss) were observed in 11 animals. Whilst the animals occupied
offered nest boxes during the active season, all dormice used
exclusively earth holes dug by the animals for hibernation and
summer dormancy. Coloured (grey)areas show periods of presumed
dormancy; animals with T
b
records available (Fig. 1) are shown in
yellow (light grey). White areas indicate periods of activity above
ground. Vertical black lines indicate cases in which we dug up torpid
animals from their burrows
168 Naturwissenschaften (2009) 96:165171
Discussion
There are two characteristics of our observations that differ
from previous reports on summer dormancy in other
mammals: First, dormice entered summer dormancy in
good body condition and in the presence of abundant food
with an energy content that would have allowed them to
rapidly gain weight. Second, summer dormancy in dormice
showed a temporal pattern that differs from typical summer
dormancy, i.e., aestivation. In desert rodents, aestivation
appears to actually represent an early onset of hibernation
after much longer periods of activity (Kenagy and
Bartholomew 1985) than in the summer-dormant animals
observed here. In contrast, dormice showing summer
dormancy emerged again in autumn, and most of them
showed a brief period of pre-hibernation fattening. Also,
periods of continuous summer dormancy in dormice were
much longer (up to 45 months, Figs. 1and 2) and more
regular than occasional episodes of prolonged torpor during
summer in echidnas (a few days, Nicol et al. 2004)orof
brief bouts of torpor in other mammals, e.g., bats (45h,
Turbill et al. 2003).
However, whilst the pattern and characteristics of
summer dormancy in dormice seems highly unusual, our
data support the view that hypometabolic states during
summer and winter dormancy are regulated by the same
physiological mechanisms (i.e., cooling rates and rates of
metabolic depression during entrance into the torpid state are
identical, Wilz and Heldmaier 2000; see also Bartholomew
and Hudson 1961). As in other hibernators (French 1982,
1985), arousal duration increased and torpor bout duration
decreased as burrow temperatures increased. Importantly,
there was no indication for different slopes or elevations
of the relation between torpor and arousal duration to ambient
temperature between summer and winter. The relation
between burrow temperature and frequency of arousals, the
most energy-consuming processes during hibernation,
explains why dormice lost body mass at significantly higher
rates during summer dormancy than during hibernation. Also,
summer dormancy was performed at a level of body temper-
atures which incurs higher energetic costs (e.g., Wilz and
Heldmaier 2000).
Our current data give reason to suggest that previous
observations of the disappearance of free-living non-
reproductive dormice during summer (Ruf et al. 2006)
may indicate their return to dormancy in underground
burrows. Summer dormancy in dormice is clearly linked to
their adaptation to strongly pulsed resources with the
associated skipping of reproduction in years with low tree
seeding (Ruf et al. 2006). Apparently, dormice employ a
unique sit-and-waittactic with long phases of dormancy
below ground, which may have evolved as a strategy to
maximise survival. However, our observation of a number
of reproductively quiescent animals that did not use
summer dormancy but remained active above ground in
both study years indicates that reproduction skipping alone,
whilst it may be a prerequisite, does not directly trigger
summer dormancy. Therefore, it remains to be clarified
which other factors elicit this strategy in certain years and
individuals.
We suggest that the main function of summer dormancy
in dormice is predator avoidance. Retreating to under-
ground burrows entirely protects arboreal and nocturnal
dormice from their main predators, i.e., nocturnal birds of
prey such as owls (von Vietinghoff-Riesch 1960), which
should significantly contribute to the extremely high
longevity of free-living dormice (Ruf et al. 2006). We can
only speculate that dormice may asses the density of
predators, e.g., by perceiving an increased number of owl
calls (possibly leading to increased stress levels), which
could act as a proximate factor causing dormice to retreat
and employ summer dormancy. Extrinsic mortality (e.g.,
predation) is thought to be one of the main factors
influencing the evolution of senescence and longevity
(Williams 1957; Kirkwood 2002; Wilkinson and South
2002; Williams et al. 2006). The extremely high longevity
in many bats, for example, has been related to two factors
that lower the risk of predation: (1) the ability to fly and (2)
hibernation (e.g., Brunet-Rossini and Austad 2004). In
years of reproduction skipping, which typically follow
years of full mast seeding (Ruf et al. 2006), predation
pressure is particularly high in dormice. This is because the
density of predators (e.g., birds of prey) increases following
the resource pulse of increased prey abundance such as
seed-eating mice (Schmidt and Ostfeld 2008). In dormice,
this pattern of pulsed resource cascades should further
enhance the benefits of predator avoidance by remaining
below ground in years of low food abundance, which
typically follow a full masting event. Decreased predation
risk was also thought to explain previous findings of a
higher survival probability over the hibernation season than
over the active season in the closely related garden
dormouse (Schaub and Vaterlaus-Schlegel 2001). Future
studies focusing on the influence of predator density on the
performance of summer dormancy and hibernation duration
are needed to clarify this hypothesis. However, survival
may be additionally enhanced by prolonged hypometabo-
lism as such, as there is evidence for an association between
the use of hibernation and increased longevity (e.g., Lyman
et al. 1981; Wilkinson and South 2002).
At least in some individuals, the combination of
hibernation and summer dormancy in dormice can sum up
to a total time of hypometabolism of >10 months per year
(see Fig. 1animal f F086) during which no food is
consumed. Similar (or even slightly longer) yearly times
spent in prolonged torpor have been observed only in
Naturwissenschaften (2009) 96:165171 169
hibernators placed in cold rooms (Mrosovsky 1977) in the
laboratory and/or following the complete removal of food
(French 1985; Geiser 2007). Irrespective of whether or not
summer dormancy in dormice indeed primarily serves to
avoid predators, in our experiments, it was clearly not
caused by poor body condition or climatic stress. Thus, its
adaptive value seems unrelated to energetic constraints.
Therefore, our findings question the common view of
torpor as a last resortstrategy that should be employed only
under conditions of negative energy balance (Humphries
et al. 2003).
Acknowledgments We thank P. Steiger, K. Außerlechner, C.
Skerget for their help with data collection and W. Zenker, F. Balfanz,
C. Beiglböck, C. Walzer for implantation of iButtons. We thank the
province of lower Austria and the city of Vienna for financial support.
We declare that all experiments in this study comply with the current
laws of Austria in which they were performed.
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... Dormice show fast increased fattening prior hibernation (e.g. [20,57]), therefore collars are not feasible for this species, and we opted for surgical bio-logger implantation. The biggest drawback of this procedure is that is invasive and carries a small risk of chronic inflammation or even device rejection [58]. ...
... Handraising and keeping conditions of edible dormice. Animals were taken from our breeding colony at the Research Institute of Wildlife Ecology, University of Veterinary Medicine Vienna (for details see [57]). For our experiment it was mandatory that the dormice were not afraid of humans. ...
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The effect of hibernation on cognitive capacities of individuals is not fully understood, as studies provide conflicting results. Most studies focus on behavioural observations without taking the physiological state of individuals to account. To mechanistically understand the effect of hibernation on the brain, physiological parameters need to be included. The implantation of bio-loggers can provide insights on i.e. body temperature without further manipulation of the animals. Surgeries and anaesthesia, however, can harm animals’ health and cause cognitive dysfunction, potentially biasing data collected through bio-loggers. We investigated the effects of bio-logger implantation surgery on cognitive performance and learning, controlling for animal and study design characteristics. First, juvenile dormice successfully learned to solve a spatial cognition task using a vertical maze. Distance, transitions, velocity, and duration were measured as indicators for performance. After training, bio-loggers were implanted intra-abdominally under general anaesthesia. Animals were re-tested in the maze two weeks after. We found no effect of bio-logger implantation and surgery on performance. This study is the first to show spatial cognition learning in edible dormice and provides a full description of the peri-anaesthetic management and a protocol for bio-logger implantation surgery in dormice. Importantly, measures were taken to mitigate common anaesthetic complications that could lead to post-operative cognitive dysfunction and influence animal behaviour. By pairing physiological measurements through bio-logger implantation with behaviour and cognition measurements, future research will significantly advance the understanding on mechanisms of learning and behaviour.
... It is worth noting that some species also use torpor for other purposes besides energy or water conservation, such as for predator avoidance or for coexistence with competitors (e.g. see Bieber & Ruf, 2009;Levy et al., 2011;Powers, 2004). Other forms of heterothermy, such as non-torpid heterothermy or facultative hyperthermia (sensu Gerson et al., 2019) have recently been recognized, but there has yet to be a systematic evaluation of both how common these are and if they correlate with the capacity to use daily torpor or hibernation. ...
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Many endotherms from diverse taxonomic groups can respond to environmental changes through torpor, that is, by greatly reducing their energy expenditure for up to 24 hours (daily torpor) or longer (hibernation). We currently have a poor understanding of how torpor evolved across endotherms and its associations with physiological traits and ecological factors. To fill this gap, we thoroughly examine the evolutionary patterns of torpor and its links with 21 key physiological and ecological variables across 1338 extant endotherms. We find that daily torpor and hibernation are parts of an evolutionary torpor continuum, and that there are several, albeit weak, associations between torpor and species' physiological or environmental characteristics. Furthermore, we show that early endotherm ancestors likely did not hibernate and that this trait evolved multiple times in independent lineages. Overall, our results suggest that the remarkable variation in torpor patterns across extant endotherms cannot solely be attributed to environmental niches, but partly arises from independent gains of daily torpor and hibernation in various clades. Read the free Plain Language Summary for this article on the Journal blog.
... When moonlight was available, the birds showed activity and foraging behaviour, but during periods of increased darkness or complete absence of moonlight, they became inactive and heterothermic, which could be due to a reduced ability to detect prey as well as predators (Smit et al. 2011). Similarly, Bieber & Ruf (2009) argue that the use of torpor itself might function as a predator avoidance strategy, since it also occurs in animals that are in good condition, fed ad libitum (ad lib) and not exposed to climatic stress. They hypothesise that torpor enables animals to reduce time spent foraging and thereby minimise exposure to predation risk. ...
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In many endotherms, i.e. birds and mammals, torpor is a common physiological response to changes food quantity and quality, environmental temperatures and water availability. Torpor is characterised by controlled reduction in metabolic rate and body temperature, as well as a reduced responsiveness to external stimuli, and inactivity of an animal. Traditionally, torpor (or controlled heterothermy) is associated with the high latitudes of the Northern Hemisphere, but also occurs in many endotherms in the tropical and subtropical latitudes of the Southern Hemisphere and at high ambient temperatures, possibly not only to reduce energy expenditure, but to conserve water. However, the inactivity and unresponsiveness to external stimuli of a torpid animal possibly leads to an animal’s loss of ability to avoid predation. Therefore, torpor might increase an animal’s vulnerability to predation and thus have high costs in terms of an animal’s fitness. In this study, African woodland dormice (Graphiurus murinus) were exposed to high temperatures in order to find out whether they employ torpor (by means of hypometabolism) not only at low ambient temperature, but also when exposed to increased ambient temperature. Moreover, the dormice were exposed to food reduction at different ambient temperatures in their environmental room to detect employment of torpor. Furthermore, we intended to determine whether metabolic rates of resting and torpid woodland dormice will change when the animals are exposed to olfactory predator cues. The animals’ metabolic rate and evaporative water loss were measured through open-flow respirometry, and recorded the skin temperatures of the dormice with external datalogger collars. The animals did not show signs of metabolic depression at high ambient temperatures. However, the dormice in this study showed remarkable tolerance to high ambient temperatures up to 42 °C, as well as to hyperthermia. The dormice employed torpor at moderate temperatures with free food availability. Under different ambient temperatures and food reduction, torpor employment changed by means of more, longer, and deeper torpor bouts at colder temperatures and under food restriction. Metabolic responses of both resting as well as torpid dormice to different olfactory cues were significant. The responses were strongest to cues from a predator, intermediate to herbivore cues, and lowest to odours from conspecifics of the same sex. This suggests that torpid dormice are responsive to predation risk. Moreover, our results suggest that woodland dormice are able to distinguish between different olfactory cues, and therefore possibly between predators and non-predators.
... We studied OS and IF as manifestations of the costs of reproduction in free-ranging female edible dormice Glis glis that can live up to 14 years under natural conditions [27]. Dormice are hibernators with very short activity season (2-4 months) [28], which must suffice to restore depleted reserves after the winter season, reproduce and prepare for the next several months without feeding opportunities. Moreover, hibernation-related metabolic adjustments are associated with OS [29] and severely decreased immunocompetence [30]. ...
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Oxidative stress (OS) and impaired immune function (IF) have been proposed as key physiological costs of reproduction. The relationship between OS and IF remains unresolved, particularly in long-living iteroparous species. We studied physiological markers of maintenance (OS, IF markers) in lactating, post-lactating and non-lactating females of edible dormice—a long-living rodent. We predicted the OS balance and IF to be compromised by lactation, especially in older females expected to face stronger trade-offs between life functions. We found that the age predictor (body size) correlated negatively with white blood cell level (WBC), positively with neutrophils to lymphocytes ratio and had no effect on OS markers. Oxidative damage markers (reactive oxygen metabolites (ROMs); but not antioxidant capacity) and body size-adjusted WBC were the lowest in lactating, higher in post-lactating and the highest in non-lactating females. Body size/age did not affect this correlation suggesting a similar age-independent allocation strategy during reproduction in this species. The path analysis testing the causal relationship between ROMs and WBC revealed that IF is more likely to affect OS than vice versa. Our study indicates the trade-off between crucial life functions during reproduction and suggests that immunosuppression reduces the risk of OS; therefore, mitigating oxidative costs of reproduction.
... However, some animals immerge into dormancy while environmental conditions would allow (from a physiological point of view) a continuation of activity, suggesting other survival benefits than coping with a short growing season (Jameson and Allison, 1976;Wiklund et al., 1996;Humphries et al., 2002). A reduction in the risk of predation or competition during animal dormancy has been suggested based on increased survival during hibernation, compared to the active season (Turbill et al., 2011;Ruf, 2012;Constant et al., 2020), in particular from studies of the hibernating edible dormouse (Glis glis) (Bieber and Ruf, 2009;Bieber et al., 2014;Hoelzl et al., 2015;Ruf and Bieber, 2023). To date, however, the generality of an influence of these factors on the evolution of prolonged dormancy lacks attention. ...
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Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the ‘life-history’ hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.
... However, some animals immerge into dormancy while environmental conditions would allow (from a physiological point of view) a continuation of activity, suggesting other survival benefits than coping with a short growing season (Jameson and Allison, 1976;Wiklund et al., 1996;Humphries et al., 2002). A reduction in the risk of predation or competition during animal dormancy has been suggested based on increased survival during hibernation, compared to the active season (Turbill et al., 2011;Ruf, 2012;Constant et al., 2020), in particular from studies of the hibernating edible dormouse (Glis glis) (Bieber and Ruf, 2009;Bieber et al., 2014;Hoelzl et al., 2015;Ruf and Bieber, 2023). To date, however, the generality of an influence of these factors on the evolution of prolonged dormancy lacks attention. ...
Preprint
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Seasonal animal dormancy, hibernation or diapause, is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Other survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the “life-history” hypothesis), but comparative tests across animal species are not yet available. Under this hypothesis, dormancy phenology is influenced by a trade-off between reproductive advantages of being active and survival benefits of dormancy. Within a species, males and females differ in the amount of time and energy they invest in reproduction. Thus, the trade-off between reproduction and survival may be reflected by within-species sex differences in the phenology of dormancy. To examine this hypothesis, we used two complementary approaches: (i) a set of phylogenetic comparative analyses on mammals (mainly holarctic rodents), and (ii) a comparison between endotherm and ectotherm dormancy, via analyses of endotherms (including mainly holoarctic rodents) and the existing literature on ectotherms. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life history hypotheses, sex differences in emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that, low temperature and precipitation as well as smaller body mass influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy (invertebrates and reptiles) may be 1) less temperature dependent than previously thought and 2) associated with trade-offs consistent with the life history hypothesis. Dormancy in some endotherms and ectotherms show staggered phenology with respect to the growing season (earlier emergence and immergence than expected) which illustrates the selection pressure exerted by the trade-off between reproduction (earlier emergence than expected) and adult survival (earlier immergence than expected). Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously appreciated.
... Hibernation is an adaptive, physiological, and behavioural, life-history strategy used by many mammals. It is used as a survival tactic to save energy during long periods of food limitations and unfavorable climatic conditions (Humphries et al. 2003;Ruf and Geiser 2015;Wang and Wolowyk 1988), and sometimes used to avoid predation (Bieber and Ruf 2009;Ruf and Bieber 2023). While hibernation is known as a period of dormancy, it is punctuated by periodic arousals which occur for several potential reasons. ...
Article
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Winter energy stores are finite and factors influencing patterns of activity are important for overwintering energetics and survival. Hibernation patterns (e.g., torpor bout duration and arousal frequency) often depend on microclimate, with more stable hibernacula associated with greater energy savings than less stable hibernacula. We monitored hibernation patterns of individual big brown bats (Eptesicus fuscus; Palisot de Beauvois, 1796) overwintering in rock-crevices that are smaller, drier, and less thermally stable than most known cave hibernacula. While such conditions would be predicted to increase arousal frequency in many hibernators, we did not find support for this. We found that bats were insensitive to changes in hibernacula microclimate (temperature and humidity) while torpid. We also found that the probability of arousal from torpor remained under circadian influence, likely because throughout the winter during arousals, bats commonly exit their hibernacula. We calculated that individuals spend most of their energy on maintaining a torpid body temperature a few degrees above the range of ambient temperatures during steady-state torpor, rather than during arousals as is typical of other small mammalian hibernators. Flight appears to be an important winter activity that may expedite the benefits of euthermic periods and allow for short, physiologically effective arousals. Overall, we found that big brown bats in rock crevices exhibit different hibernation patterns than conspecifics hibernating in buildings and caves.
... However, some animals immerge in dormancy while energy availability would allow them to continue their activity, suggesting improved survival and perhaps fitness benefits of being dormant (Jameson and Allison 1976, Wiklund et al. 1996, Humphries et al. 2002. A reduction in the risk of predation or competition during animal dormancy has been suggested mainly based on increased survival during hibernation compared to the active season (Turbill et al. 2011, Ruf et al. 2012, Constant et al. 2020, in particular from studies of the hibernating edible dormouse (Glis glis) (Bieber and Ruf 2009, Bieber et al. 2014, Hoelzl et al. 2015, Ruf and Bieber 2022. To date, however, the generality of an influence of these factors on the evolution of prolonged dormancy lacks attention. ...
Preprint
Full-text available
Seasonal animal dormancy, hibernation or diapause, is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year. However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy over time, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Other survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the “life-history” hypothesis), but comparative tests across animal species are not yet available. Under this hypothesis, dormancy phenology is influenced by a trade-off between the reproductive advantages of being active and the survival benefits of being in dormancy. Thus, species may emerge from dormancy when reproductive benefits occur, regardless of the environmental conditions for obtaining energy. Species may go into dormancy when these environmental conditions would allow continued activity, if there were benefits from reduced predation or competition. Within a species, males and females differ in the amount of time and energy they invest in reproduction. Thus, the trade-off between reproduction and survival may be reflected in sex differences in phenology of dormancy. Using a phylogenetic comparative method applied to more than 20 hibernating mammalian species, we predicted that differences between the sexes in hibernation phenology should be associated with differences in reproductive investment, regardless of energetic status. Consistent with the life-history hypothesis, the sex that spent the less time in activities directly associated with reproduction (e.g. testicular maturation, gestation) or indirectly (e.g. recovery from reproductive stress) spent more time in hibernation. This was not expected if hibernation phenology were solely influenced by energetic constraints. Moreover, hibernation sometimes took place at times when the environment would allow the maintenance of a positive energy balance. We also compiled, initial evidence consistent with the life history hypothesis to explain the dormancy phenology of ectotherms (invertebrates and reptiles). Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously appreciated.
... However, the various costs of daily torpor have only very rarely been tested experimentally. From a few studies in mammals (mostly hibernators), we know that some potential costs include immune impairment and predation vulnerability (Bouma et al. 2010), although it may also be used for predator avoidance (Bieber and Ruf 2009). A daily heterotherm (the Djungarian hamster Phodopus sungorus) emerges from torpor and sleeps and shows many signs of recovering from sleep deprivation in this period, suggesting this as a physiological cost to the use of torpor (Palchykova et al. 2002(Palchykova et al. , 2006. ...
Article
Synopsis Torpor is an incredibly efficient energy-saving strategy that many endothermic birds and mammals use to save energy by lowering their metabolic rates, heart rates, and typically body temperatures. Over the last few decades, the study of daily torpor—in which torpor is used for <24 h per bout—has advanced rapidly. The papers in this issue cover the ecological and evolutionary drivers of torpor, as well as some of the mechanisms governing torpor use. We identified broad focus areas that need special attention: clearly defining the various parameters that indicate torpor use and identifying the genetic and neurological mechanisms regulating torpor. Recent studies on daily torpor and heterothermy, including the ones in this issue, have furthered the field immensely. We look forward to a period of immense growth in this field.
Preprint
Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the ‘life-history’ hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.
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For 3 yr we studied the reproductive responses of desert rodents in the Owens Valley of eastern California (average annual precipitation 14 cm): four nocturnal heteromyids--the kangaroo rats Dipodomys microps and D. merriami and the pocket mice Perognathus formosus and P. longimembris--and one diurnal sciurid, the antelope ground squirrel, Ammospermophilus leucurus. Reproductive status was assessed by autopsies of adults trapped at approximately monthly intervals. Reproduction differed conspicuously among the five species. Our analysis illustrates effects of body size, phylogenetic association, and adaptation to the desert environment upon reproductive performances and associated life-history parameters. Most breeding occurs in late winter and early spring. Winter rains cause a series of pulses in vegetation growth and an attendant increase in availability of water in food plants, which contribute to rodent reproduction. Among the four heteromyids, onset of breeding is sequential according to body size, with the largest first. Pocket mice hibernate (P. formosus typically 3@2 mo, P. longimembris 6@2 mo), which restricts their breeding season compared to that of Dipodomys, but breeding normally begins following hibernation. The males of all species precede females in reproductive readiness; sperm production begins 1@2 to 2 mo before mating begins. Some male D. merriami remain spermatogenic throughout the year, and the mating season of this species is the longest (typically 2@2 mo) and most variable of any of the species. D. merriami typically produces only two young, which are weaned in just less than 3 wk. It can breed repeatedly under favorable conditions and is the only species in which we observed reproductive maturity of both male and female juveniles in the season of birth. D. merriami has the highest annual reproductive potential of any of the five species studied. D. microps, although larger than D. merriami and sharing similar traits of small litter size and rapid growth, has a more restricted mating season (typically 1@2 mo), but its breeding success generally exceeds that of D. merriami. The diet of saltbush leaves consumed by D. microps is atypical within this generally granivorous rodent family. Saltbush is a perennial shrub with highly predictable spring growth of leaves that are used by lactating mothers and developing young. Consequently the breeding season of D. microps is less variable and shorter than that of D. merriami. D. microps typically produces one litter per year and the juveniles typically do not mature sexually in the season of their birth. Due to their small size, seasonal dormancy, and restricted reproductive season, pocket mice are more prone to reproductive failure than are Dipodomys. We observed a complete reproductive failure in both species of Perognathus in a year when winter-spring temperature was below average and precipitation only 47% normal. Perognathus have larger litter size (@?5 young) than Dipodomys. Consequently, the total annual reproductive potential of Perognathus is close to that of Dipodomys. The relative energy investment and attendant risks for production of a given litter are considerably greater in Perognathus than in Dipodomys, particularly in P. longimembris, which is at the lower limit of body size in rodents. Nonetheless both species of Perognathus have the potential for breeding twice inan unusually favorable year. The pattern of reproduction of the marmotine sciurid A. leucurus contrasts sharply with that of heteromyids. It breeds only once a year, at a fixed time and with a mating season that lasts only 2 wk. Litter size is larger (average 8 or 9) and more variable (range 5-14) than that of any of the heteromyids. Growth and development are slow: 8 wk to weaningin contrast to
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The Madagascan fat-tailed dwarf lemur, Cheirogaleus medius, hibernates in tree holes for seven months of the year, even though winter temperatures rise to over 30 degrees C. Here we show that this tropical primate relies on a flexible thermal response that depends on the properties of its tree hole: if the hole is poorly insulated, body temperature fluctuates widely, passively following the ambient temperature; if well insulated, body temperature stays fairly constant and the animal undergoes regular spells of arousal. Our findings indicate that arousals are determined by maximum body temperatures and that hypometabolism in hibernating animals is not necessarily coupled to a low body temperature.
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We monitored a natural population of arctic ground squirrels (Spermophilus parryii kennicottii) on the North Slope of Alaska for seasonal changes in body mass and composition and dates of immergence into and emergence from hibernation. Yearlings and adult females were at the lowest body mass of their active season at emergence in spring. Their mean body mass did not increase for 1 month after emergence and peaked in July (adult females) and August (yearlings). Body mass of adult males was near the highest of the active season when they emerged from hibernation and decreased by 21% over the subsequent 10-day mating season. Juveniles gained body mass during their active season, except for significant losses associated with dispersal. During hibernation, females lost >30% of their body mass, but adult males emerged in spring without significant decreases in body mass, fat, or lean. Yearling and nonreproductive males were significantly lower in fat but not lean mass at emergence than immergence, and females were significantly lower in fat and lean mass. Arctic ground squirrels entered hibernation over a >1-month interval beginning in early August; females entered before males, and adults of each sex immerged before juveniles. Reproductive males emerged before females, and fatter females emerged significantly earlier than leaner females. Vaginal estrus was maximal at 3 days post-emergence. Nonreproductive males emerged last from hibernation. Mean +/- SE days in hibernation was 240.1 +/- 12.1 for adult females (69% of the year), 235.8 +/- 10.3 for juvenile females, 230.3 +/- 4.2 for nonreproductive males, 220.3 +/- 12.5 for adult males, and 214.7 +/- 6.5 for juvenile males. Timing of immergence into and emergence from hibernation for arctic ground squirrels did not differ significantly from sciurid populations in temperate latitudes.
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Hibernation and daily torpor are usually considered to be two distinct patterns of heterothermia. In the present comparison we evaluated (1) whether physiologi- cal variables of torporfrom 104 avian and mammalian species warrant the dis- tinction betweenzhibernation and daily torpor as two different states of torpor and (2), if so, whether this distinction is best based on maximum torpor bout du- ration, minimum hody3temperature (Tb), minimum metabolic rate during tor- por, or the reductionz of metabolic rate expressed aspercentage of basal metabo- lism Initially, animals grouped into species displaying either daily (HBMR). uwere torpor or prolonged torpor (bibernation) according to observations from original sources. Both cluster and discriminant analyses supported this division, and fur- ther analyses uwerethere/forebased on these tuwogroups. Frequency distributions for all tvariables tested difiered significantly (P < 0.001i) between daily torpor and hibernation. The average maximum torpor bout duration was 355.3 h in hiber- nators and 11.2 h inzdaily heterotherms. Mean minimum Tb'swere lower in hi- bernators than inl daily heterotherms (5.80 C zs. 17.4 C) as were minimum meta- bolic rates measured as rate of oxygen consumption (Vo2; 0.037 vs. 0.535 mL 02 g~'h'), and the metabolic rate reduction expressed aspercentage ofBMR (5.1% vs. 29. 5%). Furthermore, mean body uweightswere significantly higher in hbiberna- tors (2384 g) than inzdaily heterotherms (253 g; P < 0.001). Thus, the compari- sons of sei eral phy3siological ,ariables appear to justify a distinction between the tu'o torporpatterns. Houweier, of all iariables tested, only thefrequency distribu- tions of maximum torpor bout duration (1. 5-22 hfor daily torpor; 96-1,080 hfor hibernationz) shouweda clear gap between daily heterotherms and hibernators.
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Edible Dormice (Glis glis1) hibernate for extremely long periods (up to > 8 months), although they inhabit temperate zone areas with moderate climatic conditions. Juveniles are born late in the active season (August) and have little time for growth and prehibernation fattening. Compared to other hibernators with single litters per year, this seasonal onset of reproduction is extremely late. However, we found no evidence for exceptionally high growth rates in juvenile dormice. Our field ob - servations indicate that juveniles instead respond to the limited time for fattening in fall by a significantly shorter hibernation period than adults. Evidence from this and previous studies indicates that this peculiar tem- poral pattern of hibernation and reproduction is due to a specialization of dormice on tree-seeds, namely beechnuts, which reach highest mass and energy content only late in the vegetation season. We found that dormice after emergence in spring anticipate future food availability and may, in years without beechnuts, entirely skip gonadal growth and reproduction. Skipping of reproduction results in increased probabilities to survive until the next year and thus maximizes lifetime reproductive success.
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Hibernation is widely regarded as an adaptation to seasonal energy shortage, but the actual influence of energy availability on hibernation patterns is rarely considered. Here we review literature on the costs and benefits of torpor expression to examine the influence that energy may have on hibernation patterns. We first establish that the dichotomy between food- and fat-storing hibernators coincides with differences in diet rather than body size and show that small or large species pursuing either strategy have considerable potential scope in the amount of torpor needed to survive winter. Torpor expression provides substantial energy savings, which increase the chance of surviving a period of food shortage and emerging with residual energy for early spring reproduction. However, all hibernating mammals periodically arouse to normal body temperatures during hibernation. The function of these arousals has long been speculated to involve recovery from physiological costs accumulated during metabolic depression, and recent physiological studies indicate these costs may include oxidative stress, reduced immunocompetence, and perhaps neuronal tissue damage. Using an optimality approach, we suggest that trade-offs between the benefits of energy conservation and the physiological costs of metabolic depression can explain both why hibernators periodically arouse from torpor and why they should use available energy to minimize the depth and duration of their torpor bouts. On the basis of these trade-offs, we derive a series of testable predictions concerning the relationship between energy availability and torpor expression. We conclude by reviewing the empirical support for these predictions and suggesting new avenues for research on the role of energy availability in mammalian hibernation.
Article
The hypothesis that masting by trees is a defensive strategy which satiates seed predators in mast years and starves them in the intervening periods is tested in 59 sets of data on the seed production and pre-dispersal seed-predation of 25 tree species. Twenty-lour of the 59 data-sets support the hypothesis and show a statistically significant positive relationship between the proportion of seeds surviving the pre-dispersal stage and the log10 of the crop size for the same year. Evidence that pre-dispersal seed survival increases with the length of the mast interval is poor. A positive relationship between the strength of the masting habit and the maxintum observed pre-dispersal seed mortality in a sample of 15 tree species suggests that the masting habit is best developed in predator-prone species. A survey of seed crop frequencies in the woody plant flora of Nortli America shows masting species to be under-represented amongst shrubs and amongst trees which disperse their seeds in fleshy dispersal units. The selection pressures and evolutionary constraints which operate on the evolution of masting plants and their seed predators are discussed.