ArticlePDF Available

Abstract and Figures

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.
Content may be subject to copyright.
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.
References
Arendt T, Stieler J, Strijkstra AM, Hut RA, Rüdiger J, Van der Zee
EA, Harkany T, Holzer M, Härtig W (2003) Reversible paired
helical filament-like phosphorylation of tau is an adaptive
process associated with neuronal plasticity in hibernating
animals. J Neurosci 23:69726981
Bartholomew GA, Hudson JW (1961) Aestivation in the Mohave
ground squirrel (Citellus mohavensis). Bull Mus Comp Zool
124:193208
Bieber C (1998) Population dynamics, sexual activity, and reproduction
failure in the fat dormouse (Myoxus glis). J Zool (Lond) 244:223
229
Bieber C, Ruf T (2004) Seasonal timing of reproduction and
hibernation in the edible dormouse (Glis glis). In: Barnes BM,
Carey HV (eds) Life in the cold: evolution, mechanism,
adaptation, and application. Biological Papers of the University
of Alaska 27, Institute of Arctic Biology, University of Alaska,
Fairbanks, Alaska, USA, pp 113125
Brunet-Rossini AK, Austad SN (2004) Aging studies on bats: a
review. Biogerontology 5:211222
Buck CL, Barnes BM (1999) Annual cycle of body composition and
hibernation in free-living arctic ground squirrels. J Mammal
80:430442
Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation
in a tropical primate. Nature 429:825826
Fietz J, Schlund W, Dausmann KH, Regelmann M, Heldmaier G
(2004) Energetic constraints on sexual activity in the male edible
dormouse (Glis glis). Oecologia 138:202209
Fietz J, Pflug M, Schlund W, Tataruch F (2005) Influences of the
feeding ecology on body mass and possible implications for
reproduction in the edible dormouse (Glis glis). J Comp Physiol
B 175:4555
French AR (1982) Effects of temperature on the duration of arousal
episodes during hibernation. J Appl Physiol 52:216220
French AR (1985) Allometries of the durations of torpid and
euthermic intervals during mammalian hibernation: a test of the
theory of metabolic control of the timing of changes in body
temperatures. J Comp Physiol B 156:1319
Geiser F (2007) Yearlong hibernation in a marsupial mammal.
Naturwissenschaften 94:941944 doi:10.1007/s00114-007-0274-7
Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals
and birds: physiological variables and classification of torpor
patterns. Physiol Zool 68:935966
Humphries MM, Thomas DW, Kramer DL (2003) The role of energy
availability in mammalian hibernation: a costbenefit approach.
Physiol Biochem Zool 76:165179
Kenagy GJ, Bartholomew GA (1985) Seasonal reproductive patterns
in five coexisting California desert rodent species. Ecol Monogr
55:371397
Kirkwood TBL (2002) Evolution of ageing. Mech Ageing Dev
123:737745
Luis AD, Hudson PJ (2006) Hibernation patterns in mammals: a role
for bacterial growth? Funct Ecol 20:471477
Lyman CP, OBrien RC, Greene GC, Papafrangos ED (1981)
Hibernation and longevity in the Turkish hamster Mesocricetus
brandti. Science 212:668670
Millesi E, Prossinger H, Dittami JP, Fieder M (2001) Hibernation
effects on memory in European ground squirrels (Spermophilus
citellus). J Biol Rhythm 16:264271
Mrosovsky N (1977) Hibernation and body weight in dormice: a new
type of endogenous cycle. Science 196:902903
Nicol S, Andersen NA (2002) The timing of hibernation in Tasmanian
echidnas: why do they do it when they do? Comp Biochem
Physiol, Part B 131:603611
Nicol S, Vedel-Smith C, Andersen NA (2004) Behaviour, body
temperature, and hibernation in Tasmanian Echidnas (Tachyglos-
sus aculeatus). In: Barnes BM, Carey HV (eds) Life in the cold:
evolution, mechanism, adaptation, and application. Biological
Papers of the University of Alaska 27, Institute of Arctic Biology,
University of Alaska, Fairbanks, Alaska, USA, pp 149159
Ostfeld RS, Keesing F (2000) Pulsed resources and community
dynamics of consumers in terrestrial ecosystems. TREE 15:232
237
Pilastro A, Tavecchia G, Marin G (2003) Long living and reproduc-
tion skipping in the fat dormouse. Ecology 84:17841792
Pinheiro J, Bates D, DebRoy S, Sarkar D; the R Core Team (2007)
nlme: linear and nonlinear mixed effects models. R Package
Version 3, pp 186
Prendergast BJ, Freeman DA, Zucker I, Nelson RJ (2002) Periodic
arousal from hibernation is necessary for initiation of immune
responses in ground squirrels. Am J Physiol Regul Integr Comp
Physiol 282:R1054R1082
R development Core Team (2007) R: a language and environment for
statistical computing. R Foundation for Statistical Computing,
Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-
project.org
Ruf T, Arnold W (2008) Effects of polyunsaturated fatty acids
(PUFAs) on hibernation and torpor: a review and hypothesis.
Am J Physiol Regul Integr Comp Physiol 294:R1044R1052
doi:10.1152/ajpregu.00688.2007
Ruf T, Fietz J, Schlund W, Bieber C (2006) High survival in poor
years: life history tactics adapted to mast seeding in the edible
dormouse. Ecology 87:372381
Schaub M, Vaterlaus-Schlegel C (2001) Annual and seasonal variation
of survival rates in the garden dormouse (Eliomys quercinus).
J Zool (Lond) 255:8996
Schlund W, Scharfe F, Ganzhorn JU (2002) Long-term comparison
of food availability and reproduction in the edible dormouse
(Glis glis). Mamm Biol 67:219232
Schmidt KA, Ostfeld RS (2008) Numerical and behavioral effects
within a pulse-driven system: consequences for shared prey.
Ecology 89:635646
Silvertown JW (1980) The evolutionary ecology of mast seeding in
trees. Biol J Linn Soc 14:235250
Turbill C, Law BS, Geiser F (2003) Summer torpor in a free-ranging
bat from subtropical Australia. J Therm Biol 28:223226
170 Naturwissenschaften (2009) 96:165171
von Vietinghoff-Riesch AF (1960) Der Siebenschläfer (Glis glis L.).
Monographien der Wildsäugetiere XIV, Jena, Germany
Webb PI, Skinner JD (1996) Summer torpor in African woodland
dormice Graphiurus murinus (Myoxidae: Graphiurinae). J Comp
Physiol B 166:325330
Wilkinson GS, South JM (2002) Life history, ecology and longevity in
bats. Aging Cell 1:124131
Williams GC (1957) Pleiotropy, natural selection and the evolution of
senescence. Evolution 11:398411
Williams PD, Fletcher TQ, Rowe L (2006) The shaping of senescence
in the wild. TREE 21:458463
Wilz M, Heldmaier G (2000) Comparison of hibernation, estivation,
and daily torpor in the edible dormouse, Glis glis. J Comp
Physiol B 170:511521
Naturwissenschaften (2009) 96:165171 171
... In hibernators maintaining T b above the setpoint there is also a strong decrease of TBD with increasing T b (Twente and Twente, 1965;Geiser and Kenagy, 1988;Buck and Barnes, 2000;Ortmann and Heldmaier, 2000;Bieber and Ruf, 2009;Nowack et al., 2019). According to the hourglass hypothesis, this effect would be expected from Arrhenius effects at higher T b or increased T b -T a gradients leading to elevated MR. ...
... Besides, it should be noted that mammals living at lower latitudes apparently avoid extremely long and deep torpor bouts. Whereas torpor results in enormous energy savings, it also apparently involves risks and trade-offs (Humphries et al., 2003;Munro et al., 2005;Bieber and Ruf, 2009;Bieber et al., 2014;Zervanos et al., 2014;Nowack et al., 2019). ...
... This applies not only to torpor phases, but also to arousals. For example, in the edible dormouse, which hibernates in relatively shallow burrows, decreases in burrow temperature lead to a profound shortening of the duration of arousals (Bieber and Ruf, 2009). This suggests that even within the same individuals MR affects not only the build-up of a metabolic imbalance, but also its clearance rate during IBE. ...
Article
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.
... Hence, it seems that T b acts on bout duration via increasing torpor oxygen consumption. This is in line with well-known effects of T b on arousal frequency (e.g., Bieber and Ruf, 2009). Possibly, hibernators may use T b as a proxy for metabolic rate, and for the speed by which a metabolic imbalance is approached. ...
Article
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.
... Thus, our key finding is that the dormitive prey can gain advantage and overtake in the competition under large-amplitude fluctuations. Indeed, prey dormancy has been observed in a variety of predator-prey systems including bacteria (Myxococcus as predator and Bacillus as prey) [47][48][49]; arthropods-spider mites [50,51]; and small rodents-dormice [52,53]. ...
Article
Full-text available
Background Dormancy is widespread in nature, but while it can be an effective adaptive strategy in fluctuating environments, the dormant forms are costly due to the inability to breed and the relatively high energy consumption. We explore mathematical models of predator-prey systems, in order to assess whether dormancy can be an effective adaptive strategy to outcompete perennially active (PA) prey, even when both forms of the dormitive prey (active and dormant) are individually disadvantaged. Results We develop a dynamic population model by introducing an additional dormitive prey population to the existing predator-prey model which can be active (active form) and enter dormancy (dormant form). In this model, both forms of the dormitive prey are individually at a disadvantage compared to the PA prey and thus would go extinct due to their low growth rate, energy waste on the production of dormant prey, and the inability of the latter to grow autonomously. However, the dormitive prey can paradoxically outcompete the PA prey with superior traits and even cause its extinction by alternating between the two losing strategies. We observed higher fitness of the dormitive prey in rich environments because a large predator population in a rich environment cannot be supported by the prey without adopting an evasive strategy, that is, dormancy. In such environments, populations experience large-scale fluctuations, which can be survived by dormitive but not by PA prey. Conclusion We show that dormancy can be an effective adaptive strategy to outcompete superior prey, recapitulating the game-theoretic Parrondo’s paradox, where two losing strategies combine to achieve a winning outcome. We suggest that the species with the ability to switch between the active and dormant forms can dominate communities via competitive exclusion.
... Thus, our key finding is that the dormitive prey can gain advantage and overtake in the competition under largeamplitude fluctuations. Indeed, prey dormancy has been observed in a variety of predator-prey systems including bacteria (Myxococcus as predator and Bacillus as prey) [39][40][41], arthropodsspider mites [42,43], and small rodents-dormice [44,45]. 15 An obvious limitation of this work is that, because of the wide variation of the parameters of predator and prey populations, the evolutionary dynamics derived from the real-world data [11,14,27] might substantially differ from that predicted by the model. ...
Preprint
Full-text available
Dormancy is a costly adaptive strategy that is widespread among living organisms inhabiting diverse environments. We explore mathematical models of predator-prey systems, in order to assess the impact of prey dormancy on the competition between two types of prey, a perennially active (PA) and capable of entering dormancy (dormitive). Both the active form and the dormant form of the dormitive prey are individually at a disadvantage compared to the PA prey and would go extinct due to their low growth rate, energy waste on the production of dormant prey, and inability of the latter to grow autonomously. However, the dormitive prey can paradoxically outcompete the PA prey with superior traits and even cause its extinction by alternating between the two losing strategies. This outcome recapitulates the game-theoretic Parrondo's paradox, where two losing strategies combine to achieve a winning outcome. We observed higher fitness of the dormitive prey in rich environments because a large predator population in a rich environment cannot be supported by the prey without adopting an evasive strategy, that is, dormancy. In such environments, populations experience large-scale fluctuations, which can be survived by dormitive but not by PA prey. Dormancy of the prey appears to be a natural evolutionary response to self-destructive over-predation that stabilizes evolving predator-prey systems through Parrondo's paradox.
... The HPA axis function seems to be down-regulated during periods of prolonged food limitation to avoid energy-consuming behavior and metabolism (Reeder and Kramer 2005) which supports the energy saving mode. Obviously, the edible dormouse is perfectly adapted to cope with extended periods of fasting and overcome these energetic challenges by adjusting their energy expenditure and activity (Bieber and Ruf 2009;Langer et al., 2018). The most drastic adaptation to keep energy consumption low during periods of limited food availability is obviously to remain reproductively quiescent and skip reproduction (Ruf et al., 2006). ...
Article
Our knowledge of the perception of stress and its implications for animals in the wild is limited, especially in regard to mammals. The aim of this study was therefore to identify sex specific effects of reproductive activity, body mass, food availability and hibernation on stress hormone levels in the edible dormouse (Glis glis), a small mammalian hibernator. Results of our study reveal that reproductive activity and pre-hibernation fattening were associated with high cortisol levels in both sexes. During the mating season, in particular individuals with low body masses had higher stress levels. Elevated levels of cortisol during pre-hibernation fattening were even higher in females that had formerly invested into reproduction compared to non-reproductive females. Previously observed impairments on health parameters and reduced survival rates associated with reproduction emphasize the functional relevance of high stress hormone levels for fitness. Prolonged food limitation, however, did not affect stress levels demonstrating the ability of dormice to predict and cope with food restriction.
Article
Small insectivorous bats often enter a state of torpor, a controlled, reversible decrease in body temperature and metabolic rate. Torpor provides substantial energy savings and is used more extensively during periods of low temperature and reduced prey availability. We studied torpor use and activity of a small (10.1 ± 0.4 g) fishing bat, Myotis macropus, during winter in a mild climate in Australia. We predicted that the thermal stability of water would make foraging opportunities in winter more productive and consistent in a riparian habitat compared to a woodland habitat, and therefore, fishing bats would use torpor less than expected during winter compared to other bats. Using temperature-sensitive radio transmitters, we recorded the skin temperature of 12 adult (6 M, 6 F) bats over 161 bat-days (13.4 ± 5.4 days per bat) during Austral winter (late May to August), when daily air temperature averaged 6.2–18.2°C. Bats used torpor every day, with bouts lasting a median of 21.3 h and up to 144.6 h. Multiday torpor bouts were more common in females than males. Arousals occurred just after sunset and lasted 3.5 ± 2.9 h. Arousals tended to be longer in males than females and to occur on warmer evenings, suggesting some winter foraging and perhaps male harem territoriality or other mating-related activity was occurring. The extensive use of torpor by M. macropus during relatively mild winter conditions when food is likely available suggests torpor might function to minimize the risks of mortality caused by activity and to increase body condition for the upcoming breeding season.
Chapter
The weather of most geographical regions changes substantially with the seasons. Therefore, alterations in the thermal environment, rainfall and other environmental variables require a responsive adjustment of the physiology of animals to enable survival. However, geographic regions of the world differ substantially in their seasonal challenges. Whereas temperate and high latitude/altitude regions are characterised by warm Tas in summer and often high primary productivity, Tas in winter are low resulting in little or no primary productivity. Untimely, this low Ta and low productivity occur in the season when energy expenditure of animals often is high. In contrast, tropical areas may remain rather warm in winter, but often show strong seasonal changes in rainfall with almost all precipitation in summer and none in winter (Dausmann and Warnecke 2016). In subtropical areas the high summer heat may limit plant productivity. During the mild subtropical winter nectar production can be much higher than in summer (Ford 1989). In deserts Tas are often too hot, evaporation too high and/or precipitation too low in summer for significant plant growth, whereas winters can be rather mild during the day, at least in deserts not too far from the equator, as for example in the Australian deserts. The seasonal change in photoperiod, a reliable environmental signal for seasonal change in physiology, also differs enormously between high and low latitudes. Such regional differences are reflected in the seasonal expression of torpor.
Chapter
In this chapter, the diversity of heterotherms, where they live and how they differ from each other is covered in detail. When data from free-ranging animals were available these were used preferentially, but information on captive animals is also included. As the extent of available data differs substantially among taxa, the information provided reflects what is known about a specific group to a large extent. To put the information on heterothermic endotherms into context with other organisms, I will address terrestrial ectotherms first.
Chapter
Torpor is not only highly diverse in the manner it is used and found in many birds and mammals, it is also expressed by animals all over the world under different climatic conditions. Animals living in different regions will be exposed to the prevailing thermal conditions and therefore, to some extent, torpor expression should reflect their distribution. On average, hibernators are distributed at higher latitudes (~35°) than are daily heterotherms (25°) (Ruf and Geiser 2015). Both the maximum and mean TBD of hibernators are significantly affected by latitude, with the shorter bouts observed at lower latitudes (Fig. 7.1). The predicted mean TBD for hibernators from the regression line (Fig. 7.1) is ~32 hours at 0° latitude and ~ 680 hours at 70°, or an increase by ~108 hours for every 10° increase in distance away from the equator. To a large extent the longer TBDs at higher latitudes may simply reflect exposure to lower Tas (Chap. 5), but it is probable that the colder winters further north result in selection for deeper and longer torpor bouts. In contrast, TBDs in daily heterotherms are not affected by latitude. In both birds and mammals the average maximum TBD is 10.1 hours in birds and 12.9 hours in mammals, whereas the mean TBD is 6.3 hours in birds and 8.2 hours in mammals (Ruf and Geiser 2015). This suggests that because of their largely daily foraging, the time daily heterotherms allocate to torpor is not affected by latitude, although their TBD is affected by Ta.
Chapter
Torpor is used by many birds and mammals. However, despite the number and diversity of species, it seems only two major patterns have been favoured by natural selection. In most heterothermic endotherms torpor is characterized by either a daily occurrence (‘daily torpor’ in the ‘daily heterotherms’), which often use torpor throughout the year, or multiday torpor in the ‘hibernators’ with often a seasonal occurrence (Fig. 1.7). In many species these two patterns of torpor differ ecologically and functionally. Only a few species appear to display intermediate torpor patterns. However, the comparison between the two torpor patterns is complicated by the strong temperature-dependence of most physiological variables of torpor, which therefore may overlap especially at high Tas (see below). Moreover, long-term studies that have reliably characterised patterns of torpor of species are not always available.
Article
Full-text available
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
Article
Full-text available
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.
Article
Full-text available
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.
Article
Full-text available
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.
Article
Full-text available
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.
Article
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.