Journal of Mammalogy, 97(1):128–134, 2016
DOI:10.1093/jmammal/gyv162
Published online October 21, 2015
Abiotic and biotic factors affecting the denning behaviors in Asiatic
black bears Ursus thibetanus
Toshiaki Yamamoto,* Hiroo Tamatani, Junpei Tanaka, Gen Oshima, Serina Mura, and Masaru Koyama
Department of Veterinary Nursing and Technology, Nippon Veterinary and Life Science University, Musashino, Tokyo 180-8602,
Japan (TY, SM)
Department of Bear Management, Picchio Wildlife Research Center, Hoshino Karuizawa, Kitasaku-gun, Nagano 389-0194,
Japan (HT, JT, GO)
Department of Tourism and Economy, Karuizawa town office, Karuizawa, Kitasaku-gun, Nagano 389-0111, Japan (MK)
* Correspondent: [email protected]
For bears, numerous associations between biotic and abiotic factors have been reported to correlate with the
timing of den entry and emergence; however, an analysis showing which factors influence the timing of den entry
and emergence has not been performed enough. In this study, a generalized linear mixed model was generated
using 66 entry dates for 26 females and 40 entry dates for 26 males, and 56 emergence dates for 26 females and 25
emergence dates for 18 males between 1999 and 2012. Regarding factors for den entry, the average temperature
in November and mast production of Mongolian oaks were significant for both males and females. For the date
of den emergence, the average temperature in March affected strongly. For males, good mast production of
Mongolian oaks in the previous year was found to be associated with early den emergence. For females, the
presence of newborns had a significant influence on their den entry and emergence. This study indicated that
denning behavior appears to be regulated by several abiotic and biotic factors and regulation factors are sex
specific.
Key words: Asiatic black bear, den emergence, den entry, denning period, mast, Mongolian oak
© 2015 American Society of Mammalogists, www.mammalogy.org
Denning behavior of the genus Ursus is a phenomenon evolved
to minimize energy consumption by shutting down most of
the bear’s activities, including ingestion and excretion (Nelson
et al. 1973). This process markedly reduces metabolism and
enables Ursus spp. to survive harsh environmental conditions,
primarily a seasonal lack of food and unfavorable weather
(Mystrud 1983). This behavior has been observed in American
black bears (Ursus americanus), Asiatic black bears (Ursus thibetanus), brown bears (Ursus arctos), and polar bears (Ursus
maritimus—Hellgren 1998; Seryodkin et al. 2003; Tøien et al.
2011). Bears generally spend several months in the den, but
the duration of denning is a variable dependent upon location
and can vary from a few weeks to 7 months or more (Linnell
et al. 2000). Even within local populations, the duration of denning has been found to differ by as much as a month among
individuals (e.g., Tietje and Ruff 1980; Haroldson et al. 2002).
Understanding the factors that influence the timing of den entry
and emergence thus may provide insights regarding the variation in ursid life histories.
Previous studies have clarified associations between the timing of denning behavior and various other factors. For example,
it has been long believed that snowfall is associated with den
entry (e.g., Craighead and Craighead 1972; Reynolds et al.
1976), but others have not corroborated this relationship (e.g.,
Judd et al. 1986; van Daele et al. 1990). There is, however, general agreement that low temperatures stimulate ursids to enter
their dens (Lindzey and Meslow 1976; Johnson and Pelton
1980). Other researchers have suggested that a reduction in
available food sources in autumn influences denning chronology, and that den entry begins earlier when the production of
acorn is low (Schooley et al. 1994; Kozakai 2009).
Denning behavior has also been reported to be influenced
by not only abiotic but also biotic factors. Delivery of newborn cubs influences the timing of den entry and emergence of
females. In ursids, pregnant females go into the den earlier than
other individuals and emerge from the den later (e.g., Lindzey
and Meslow 1976; Tietje and Ruff 1980; Haroldson et al.
2002). Variations dependent on age and sex among brown bears
have been observed. For example, the denning period was correlated positively with age in females (Friebe et al. 2001), but
the opposite result was found in males (Manchi and Swenson
2005). As described above, various biotic and abiotic factors
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YAMAMOTO ET AL.—TIMING OF DENNING BEHAVIORS IN BEARS129
for denning behavior have been individually reported in Ursus,
but a complex analysis to determine the most influential factors
for denning behavior has not been performed.
The duration of denning varies among Asiatic black bears,
which are widely distributed from the Middle East to East Asia.
In Japan, denning lasts for 5–6 months in Tohoku district (latitude of 36–42°N) but only for approximately 1 month in a section of Chugoku district (latitude of 33–35°N—Maita 1996;
Koike and Hazumi 2008; Yamazaki 2011). Except for pregnant
females, Asiatic black bears inhabiting Taiwan do not hibernate
(Hwang and Garshelis 2007), and the timing of den entry markedly varies by year in Asiatic black bears inhabiting in central
Japan (Kozakai et al. 2009), suggesting that various factors influence denning behavior. However, the factors associated with the
timing of den entry and emergence are poorly documented in
Asiatic black bears. In this study, we surveyed den entry and
emergence in Asiatic black bears inhabiting the foothills of Mt.
Asama in Nagano Prefecture, Japan, between 1999 and 2012,
and performed analyses of biotic and abiotic factors to identify
those associated with denning chronology in males and females.
Materials and Methods
Study site.—The survey was performed in the foothills of
Mt. Asama, located in the east of Nagano Prefecture in central Japan (approximately 400 km2; Fig. 1). The elevation of
the survey area was 600–2,500 m, and the forests consisted
of mixed foliage, including conifers, Larix kaempferi (syn.
Larix leptolepis), and broad-leaved trees: chestnut (Castanea
crenata), Mongolian oak (Quercus crispula), and Konara oak
(Quercus serrata). For Asiatic black bears, the hard mast production of these broad-leaved tree species is the most important food resource from early September to the end of October
and strongly affects feeding behavior (Izumiyama et al. 2004;
Nakajima 2012). Depending on the year and location, mast production of these species fluctuates widely and has a marked
correlation with the number of nuisance bears killed in northern
Japan (Oka et al. 2004). The annual rainfall is between 1000
and 1500 mm, and snowfall rarely exceeds 30 cm during winter
months. The average annual temperatures are 20 and −5°C in
summer and winter, respectively.
Tracking of individuals.—Data from 29 female and 26 male
Asiatic black bears tracked from 1999 to 2012 were used.
These animals were captured in culvert traps using honey and
honeycombs as attractants after obtaining permission from the
Ministry of the Environment and Nagano Prefecture. Captured
individuals were anesthetized (1:1 combination of tiletamine
and zolazepam, 100 mg/kg), and their gender was identified by
a genital examination. External physical measurements, including body length and body weight, were also taken, and a premolar was extracted to identify the animal’s age. Bears were
fitted with a collar (ATS Inc., Isanti, Minnesota) and released.
Research in live animals followed American Society of
Mammalogists’ guidelines (Sikes et al. 2011). A Yagi antenna
and portable receiver were used to track the bears’ movements
via locating the VHF signals emitted by collars; the location of
each bear was determined by triangulation (White and Garrott
1990). We located each bear approximately once every 10 days.
Estimation of den entry and emergence.—The date of den
entry was estimated as the midpoint between the first day, when
the animal was judged to have stopped moving, and the last day,
when the animal was assumed to be moving based on its location. Because telemetry error was previously estimated as 84.3
m (range: 20–161 m; Yamamoto et al. 2012), we concluded that
a bear was still moving when the current location was estimated
to be more than 100 m away from the denning site. The date of
den emergence was defined as the midpoint between the first
day that the animal moved more than 100 m and the last day
that its presence in the den was confirmed. Because the locations of the animals were confirmed at intervals of no more than
10 days during the denning period, errors in the estimated entry
and emergence dates were small. In addition, when the location
was not confirmed for 10 days or longer, data for the animal
were excluded.
Biotic factors.—Parturition was confirmed by physically listening for vocalizations of cubs near the dens during February
and March or directly observing the presence or absence of
cubs from April to November. Even when we had access to
the den and did not hear vocalizations of a cub, we did not
confirm the absence of cubs. When the presence or absence of
parturition could not be confirmed, the animal was excluded
from analysis.
In order to determine the age of individuals, the premolar
extracted during the capture was decalcified and thin-sectioned,
and the number of intensely stained layers in the cementum was
counted (see Willey 1974).
Abiotic factors.—We established an average of 50 sites per
year randomly within the survey area and examined the mast
production of Mongolian oak, chestnut, and Konara oak from
early September to early October from 1999 to 2012. At each
site, we selected 10 reproductive trees of similar size (20–
60 cm diameter at breast height) for each species and observed
the mast productions for a specific period of time (30 s to
1 min) using binoculars. The mast production was evaluated
based on the number of nuts counted per 30 s at each site and
was respectively judged as good, average, bad, or poor when
more than 20, 5–20, 1–4, or 0 nuts were observed (Wildlife
Management Research Center, Hyogo 2011). In total, 250–400
trees of each species per year were observed to estimate mast
production and the mean of the combined sites was used as the
amount of available food resources produced by each species
of tree per year (Fig. 2). The mast productions of each species
varied year by year, but no synchronization among the 3 species and sites was noted, unlike that reported in other regions
(Kuramoto et al. 1995; Wildlife Management Research Center,
Hyogo 2011).
The location of each den was individually plotted using
ArcGIS 10.2 (ESRI 2014), and the elevation was calculated
using 50-m digital elevation model. The average temperatures
in November and March and weather conditions on the first
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JOURNAL OF MAMMALOGY
Fig. 1.—Maps of the survey region. The lower map shows the elevation of the survey region; dark areas represent high elevations, and bright areas
represent low elevations. Point data represent denning sites of Asiatic black bears.
Fig. 2.—Changes in food availability (Mongolian oak, konara oak, and chestnut) for Asiatic black bears from 1999 to 2012.
YAMAMOTO ET AL.—TIMING OF DENNING BEHAVIORS IN BEARS131
day of snow were obtained from the database of the Japan
Meteorological Agency (Japan Meteorological Agency 2014).
Statistical analysis.—To compare timing of den entry and
emergence, and the denning duration among pregnant females,
non-pregnant females, and males, a 1-way analysis of variance
was performed, followed by Tukey’s multiple comparisons test.
The correlation between age and denning duration for each sex
was determined by Spearman rank correlation test. To analyze
the association of each factor with denning behavior, a general
linear mixed model (GLMM) was used, with the date of den
entry (regarding 1 November as day 1) as a response variable
and the following items as explanatory variables: the average
temperature in November; date of 1st snowfall; food sources,
namely Mongolian oak, chestnut, and Konara oak mast; elevation; presence or absence of pregnancy; and age (in males, the
same items excluding the presence or absence of pregnancy).
For the date of den emergence (regarding March 1 as day 1), the
GLMM included the following 6 items as explanatory variables:
average temperature in March, food sources, Mongolian oak
mast production in the previous year, elevation, age, and presence or absence of young (in males, the same items excluding
the presence or absence of young). To eliminate multicollinearity, Spearman’s rank correlation was analyzed beforehand, but
no strong correlation was noted between any variables (ρ < 0.5
in all cases). A Poisson distribution was employed for the error
distribution, and individuals were regarded as a random factor. For model selection, using the Akaike information criterion
(AIC), the model with the lowest AIC was regarded as optimal.
Analyses were performed using R.ver. 3.0 (R Development
Core Team 2013).
Results
Over the 14-year period, the date of den entry could be confirmed 21 times for 15 pregnant females, 45 times for 20 nonpregnant females, and 40 times for 26 males. The date of den
emergence could be identified 18 times for 12 females with
cubs, 38 times for 23 females without cubs, and 25 times for 18
males. The mean age was 7.3 ± 2.9 years for females with cubs,
8.9 ± 4.7 years for females without cubs, and 7.2 ± 3.5 years
for males. The mean elevation of the dens was 1,121 ± 204 m
for pregnant females, 1,078 ± 230 m for non-pregnant females,
and 1,174 ± 336 m for males (Fig. 1). Asiatic black bears in
our study area entered and emerged from their dens primarily
during November to December and April to May, respectively.
The average date of den entry was 3 December (SD = 11.4) for
females without cubs, 28 November (SD = 12.9) for females
with cubs and 2 December (SD = 10.8) for males (Table 1). The
date of den entry was not significantly different among the 3
groups (F2,103 = 1.17, P = 0.32). On the other hand, the average
date of den emergence was 25 April (SD = 13.0) for females
without cubs, 11 May (SD = 17.3) for females with cubs, and
17 April (SD = 9.3) for males (Table 1). Significant difference in the date of den emergence was detected among the 3
groups (F2,78 = 17.59, P < 0.001): males and females without
cub emerged earlier, and females with cub later. The duration
Table 1.—Average data of den entry, den emergence, and den duration in male and female Asiatic black bear by reproductive categories
during 1999–2012.
Category
Sex
N
Average (range)
Den entry
Females with cubs
Females with no cubs
Males
Females with cubs
Females with no cubs
Males
Females with cubs
Females with no cubs
Males
21
45
40
18
38
25
15
32
23
28 Nov (8 Nov–28 Dec)
3 Dec (12 Nov–2 Jan)
2 Dec (15 Nov–24 Dec)
11 May (4 Apr–12 Jun)
25 Apr (28 Mar–18 May)
17 Apr (2 Apr–27 Apr)
168.8 days (141–212)
141.1days (108–177)
135.1days (115–153)
Den emergence
Den duration
of denning was 135.1 ± 10.4 days for males, 141.1 ± 19.3 days
for females without cubs, and 168.8 ± 17.0 days for females
with cubs, with significant differences among the 3 groups
(F2,67 = 21.18, P < 0.001); duration was about on 1 month longer in females that gave birth compared to that of the others
(Table 1). Moreover, the duration of denning was negatively
correlated with age in males (ρ = −0.43, P = 0.04) and positively correlated with age in females (ρ = 0.31, P = 0.01).
The GLMM was used to analyze factors affecting den entry
and emergence. During model selection for the timing of den
entry in females, positive correlations were noted in parturition during denning and temperature in November and an
inverse correlation in the elevation (Tables 2 and 3). In years
with above average temperatures in November, den entry was
delayed at lower elevations, excluding females experiencing
parturition during the denning. The timing of den entry was
also strongly influenced by the mast production of Mongolian
oak. Similarly, the timing of den entry in males was positively
correlated with the temperature in November and inversely correlated with the mast production of Mongolian oak (Tables 2
and 3). On the other hand, timing of snowfall and age were not
in the best model for den entry. In the GLMM analysis of den
emergence, the average temperature in March was relevant in
both genders (Tables 2 and 3). In addition, den emergence was
markedly influenced by the elevation, parturition during denning in females, and the mast production of Mongolian oak in
the previous year in males (Tables 2 and 3). However, age was
not included in the parameters of the best model for the timing
of den emergence.
Discussion
In this study, temperature was associated with den entry and
emergence in both genders. Asiatic black bears are widely distributed in Japan. The duration of denning is about 5 months
in bears distributed in northern regions, whereas it is about
1 month in southern regions (Maita 1996; Oi 2009). Similar
variations in the denning period dependent on the latitude
have been reported in other ursid species, suggesting that
food resources remain available later in autumn as the latitude
decreases (Wooding and Hardisky 1992; Linnell et al. 2000).
For a similar reason, bears inhabiting Karuizawa enter the den
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JOURNAL OF MAMMALOGY
later and emerge earlier in warm years. Furthermore, snow
accumulates earlier at higher elevations in this area, which
makes it difficult for bears to forage. Thus, elevation was also
selected as a negative factor for females; however, elevation
was not selected for males. One reason may have been that,
in almost all cases, the locations of male dens were at higher
elevations, and the individual variation was too low to detect
this factor.
In both genders, mast production of Mongolian oak was also
strongly associated with the timing of den entry. We predicted
Table 2.—The top-ranked candidate (∆AICc<2) for den entry and
emergence of male and female. ID listed in the table indicates the identification code of each section. Numbers listed in the Variables column
represent the following entry (1–8) and emergence (5–9) factors: 1—
November temperature, 2—snowfall, 3—Konara oak, 4—Japanese
chestnut, 5—Mongolian oak, 6—elevation, 7—age, 8—parturition
during denning, 9—March temperature.
Model
Sex
Variables
AIC
∆AICc
Den entry
Male
1 + 5
1 + 3 + 5
1 + 5 + 7
1 + 4 + 5
1 + 2 + 5
1 + 2 + 4 + 5 + 6 + 8
1 + 2 + 4 + 5 + 6 + 7 + 8
1 + 4 + 5 + 6 + 8
1 + 2 + 3 + 4 + 5 + 6 + 8
2 + 5 + 9
2 + 9
2 + 5 + 7 + 9
6 + 8 + 9
6 + 8
6 + 7 + 8 + 9
2 + 6 + 8 + 9
82.3
83.0
83.1
83.6
84.3
0.00
0.77
0.77
1.30
1.99
0.00
1.53
1.68
1.99
0.00
0.81
1.68
0.00
0.81
1.29
1.97
Female
Den emergence
Male
Female
209.5
209.6
209.9
85.9
86.8
87.6
245.9
246.7
247.2
247.8
that denning behavior would start later when food sources were
scarce, because the energy stores needed to survive the winter
had not yet been secured. However, the situation was actually
the opposite; during years in which food sources were scarce,
denning behavior started early, perhaps to reduce the basal
metabolic rate to below the energy levels required for feeding.
A similar tendency was observed in the American black bear
(Schooley et al. 1994) and the Asiatic black bear (Kozakai et al.
2009). In Asiatic black bears inhabiting areas around the Ashio
Copper Mine in Tochigi Prefecture, where the food source
availability and denning behavior were compared over 2 years,
the results showed that denning started about 1 month earlier in
the year when the production of acorns was low (Kozakai et al.
2009). Such studies support the conclusion early den entry in
bears is at least in part the result of insufficient food resources
in autumn.
One interesting observation was that the mast productions
of Mongolian oaks in the previous year influenced the den
emergence of males. It has been reported that, based on fecal
analysis, bears feed on the acorns from the previous year after
emerging from their dens, suggesting that oak acorns are an
important source of food for males after den emergence (Koike
2010). Such evidence suggests that males emerge earlier from
the den to feed when they can feed on acorns from the previous
year, whereas when acorns are scarce, they continue denning
behavior in order to save energy in preparation for the breeding season. In future work, more attention should be given to
understanding the relationship between the timing of den emergence and available food resources.
A comparison of the duration of denning between males and
females confirms that pregnant females entered the den earlier.
Females tended to enter earlier, although the difference was not
always significant. Regarding den emergence, males emerged
earlier, and females with cubs emerged later. This sex-based
Table 3.—The parameters of the best model for den entry and emergence of males and females and the 95% confidence intervals (CI) of the
models. Variables indicated using asterisks mean that the value ranges of the 95% CI did not include zero.
Model
Sex
Den entry
Male
Female
Den emergence
Male
Female
Variables
Intercept
November temperature
Mongolian oak
Intercept
November temperature
Mongolian oak
Japanese chestnut
Elevation
Parturition during denning
Snowfall
Intercept
March temperature
Mongolian oak
Elevation
Intercept
March temperature
Elevation
Parturition during denning
Coefficient
SE
1.732
0.186
0.674
4.083
0.180
0.390
−0.099
−0.730
0.218
0.003
0.479
−0.188
−0.729
0.450
−0.547
−0.061
1.498
−0.307
0.363
0.037
0.181
1.000
0.025
0.128
0.040
0.320
0.061
0.002
1.688
0.076
0.257
0.241
1.249
0.030
0.399
0.067
Upper
lower
0.259
1.029
0.113
0.319
0.229
0.641
−0.021
−0.103
0.338
0.007
0.131
0.139
−0.177
−1.357
0.098
−0.001
−0.039
−0.225
0.922
−0.337
−1.233
−0.022
−0.002
2.280
−0.176
−0.120
0.716
−0.438
YAMAMOTO ET AL.—TIMING OF DENNING BEHAVIORS IN BEARS133
den emergence behavior has been previously noted in brown
bears, American black bears, and Asian black bears (e.g., Tietje
and Ruff 1980; Haroldson et al. 2002; Manchi and Swenson
2005; Oi and Yamazaki 2006). The shorter duration of denning in males than in females may generally be explained by
differences in body size and energy consumption. Reportedly,
the duration of denning is associated with the amount of fat
accumulation and the rate of fat catabolism in bears (Schwartz
et al. 1987), and the rate of metabolizing fat stores is proportional to the surface area to body weight ratio. Therefore, males
with a large body size than females use a smaller amount of
energy and accumulated fat to move and consequently spend a
shorter time in the den. Moreover, Manchi and Swenson (2005)
detected that the duration of denning decreased with increasing age and body mass in males. When age and body mass are
positively correlated in males, the duration of denning might
be correlated with both. Large adult males and small subadult
males were included in this study, and thus we could detect a
negative relationship between age and the duration of denning.
However, since age was not selected in the best model, age does
not appear to have a strong influence on the timing of den entry
and emergence.
On the other hand, there might be different reasons that
explain why pregnant females spent a longer time in their dens.
Similar trends in the timing of entry into and emergence out
of dens among female ursids occur elsewhere (van Daele et al.
1990; Friebe and Swenson 2001; Haroldson et al. 2002; Oi and
Yamazaki 2006, see Schooley et al. 1994). One of the major
objectives of pregnant females is to deliver and rear cubs safely
in the den. Hence, they enter the den earlier and emerge later
than males and females without cubs. Since reproductive status
was affected by age, the duration of denning was correlated
with age in this study, which is similar to the findings of Friebe
(2001).
Although many previous studies have shown that snowfall triggered denning behavior (e.g., Reynolds et al. 1976;
Hamilton and Marchinton 1980), no association has been noted
between snowy days and den entry in either gender. This may
be attributable to the low amount of snowfall in the survey area.
The burial of food sources by snow was believed to trigger
denning in other regions (Reynolds et al. 1976; Hamilton and
Marchinton 1980). However, in our survey region, the amount
of snowfall was relatively low in November and December,
which is the time that Asiatic black bears enter the dens (e.g.,
less than 10 cm in November 2012). In addition, the average
temperature was higher in some years, even when the first
snowfall came early. Thus, snowfall did not have any apparent
association with the denning behavior of Asiatic black bears in
this study.
In conclusion, annual variations in the timing of den entry
were attributed more to availability of autumn food sources,
autumn temperatures, and the elevation of denning, rather
than snowfall. Generally, the timing of den emergence varied
depending on spring temperatures, mast productions in the previous year, and the elevation of denning. Furthermore, sex and
female reproductive status also affected the timing of den entry
and emergence. This study indicated that denning behavior in
Asiatic black bears is a complex process and is regulated by
several abiotic and biotic factors.
Acknowledgments
This study was performed as part of the Karuizawa town project
for bear management and damage control. We thank the staff in
the Karuizawa town office for their assistance and advice in
the field and the Nagano Environmental Conservation Research
Institute for estimating the age of individuals. We also thank
T. Suzuki, Y. Kuroda, N. Izawa, and A. Mitsuke for supporting the fieldwork and D. Zmijewski for providing constructive
comments on the manuscript. This study was supported in part
by grants from the PRO NATURA FUND and the Mitsui &
Co., Ltd. Environment Fund.
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Submitted 7 January 2015. Accepted 1 October 2015.
Associate Editor was I. Suzanne Prange.