Content uploaded by Claudia Bieber
Author content
All content in this area was uploaded by Claudia Bieber
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) 96:165–171
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-wait’strategy 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? Capture–recapture 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°10′N, 16°20′E).
Mean air temperature at the enclosures during the study
period (2005–2007) 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 1.2–2 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, 0–28 days; interquartile range, 4–11 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 May–June 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) 96:165–171
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
“animal”for 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 2–4 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 7–21 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) 96:165–171 167
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, 49–157 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 “season”to 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= 336.20–15.94 × 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) 96:165–171
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 4–5 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 (4–5h,
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-wait’tactic 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) 96:165–171 169
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 resort’strategy 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 23:6972–6981
Bartholomew GA, Hudson JW (1961) Aestivation in the Mohave
ground squirrel (Citellus mohavensis). Bull Mus Comp Zool
124:193–208
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 113–125
Brunet-Rossini AK, Austad SN (2004) Aging studies on bats: a
review. Biogerontology 5:211–222
Buck CL, Barnes BM (1999) Annual cycle of body composition and
hibernation in free-living arctic ground squirrels. J Mammal
80:430–442
Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation
in a tropical primate. Nature 429:825–826
Fietz J, Schlund W, Dausmann KH, Regelmann M, Heldmaier G
(2004) Energetic constraints on sexual activity in the male edible
dormouse (Glis glis). Oecologia 138:202–209
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 175:45–55
French AR (1982) Effects of temperature on the duration of arousal
episodes during hibernation. J Appl Physiol 52:216–220
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 156:13–19
Geiser F (2007) Yearlong hibernation in a marsupial mammal.
Naturwissenschaften 94:941–944 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 68:935–966
Humphries MM, Thomas DW, Kramer DL (2003) The role of energy
availability in mammalian hibernation: a cost–benefit approach.
Physiol Biochem Zool 76:165–179
Kenagy GJ, Bartholomew GA (1985) Seasonal reproductive patterns
in five coexisting California desert rodent species. Ecol Monogr
55:371–397
Kirkwood TBL (2002) Evolution of ageing. Mech Ageing Dev
123:737–745
Luis AD, Hudson PJ (2006) Hibernation patterns in mammals: a role
for bacterial growth? Funct Ecol 20:471–477
Lyman CP, O’Brien RC, Greene GC, Papafrangos ED (1981)
Hibernation and longevity in the Turkish hamster Mesocricetus
brandti. Science 212:668–670
Millesi E, Prossinger H, Dittami JP, Fieder M (2001) Hibernation
effects on memory in European ground squirrels (Spermophilus
citellus). J Biol Rhythm 16:264–271
Mrosovsky N (1977) Hibernation and body weight in dormice: a new
type of endogenous cycle. Science 196:902–903
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 131:603–611
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 149–159
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 84:1784–1792
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 1–86
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:R1054–R1082
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:R1044–R1052
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 87:372–381
Schaub M, Vaterlaus-Schlegel C (2001) Annual and seasonal variation
of survival rates in the garden dormouse (Eliomys quercinus).
J Zool (Lond) 255:89–96
Schlund W, Scharfe F, Ganzhorn JU (2002) Long-term comparison
of food availability and reproduction in the edible dormouse
(Glis glis). Mamm Biol 67:219–232
Schmidt KA, Ostfeld RS (2008) Numerical and behavioral effects
within a pulse-driven system: consequences for shared prey.
Ecology 89:635–646
Silvertown JW (1980) The evolutionary ecology of mast seeding in
trees. Biol J Linn Soc 14:235–250
Turbill C, Law BS, Geiser F (2003) Summer torpor in a free-ranging
bat from subtropical Australia. J Therm Biol 28:223–226
170 Naturwissenschaften (2009) 96:165–171
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 166:325–330
Wilkinson GS, South JM (2002) Life history, ecology and longevity in
bats. Aging Cell 1:124–131
Williams GC (1957) Pleiotropy, natural selection and the evolution of
senescence. Evolution 11:398–411
Williams PD, Fletcher TQ, Rowe L (2006) The shaping of senescence
in the wild. TREE 21:458–463
Wilz M, Heldmaier G (2000) Comparison of hibernation, estivation,
and daily torpor in the edible dormouse, Glis glis. J Comp
Physiol B 170:511–521
Naturwissenschaften (2009) 96:165–171 171