Behavioral
Ecology
The official journal of the
ISBE
International Society for Behavioral Ecology
Behavioral Ecology (2015), 26(5), 1345–1351. doi:10.1093/beheco/arv083
Original Article
Temporal shift in activity patterns of
Himalayan marmots in relation to pastoralism
Buddi S. Poudel, Peter G. Spooner, and Alison Matthews
School of Environmental Sciences, Institute for Land, Water and Society, Charles Sturt University,
PO Box 789, Albury, NSW 2640, Australia
Received 11 December 2014; revised 22 May 2015; accepted 26 May 2015; Advance Access publication 20 June 2015.
Activity patterns of wildlife are often associated with the risk of predation, foraging requirements, and impacts of anthropogenic disturbance. Animals may adjust their temporal niche by shifting their activity patterns in relation to anthropogenic disturbance activities;
however, few studies have recorded this response. We investigated the extent to which disturbances associated with pastoralism
changed the timing of foraging and activity patterns of Himalayan marmot, a widely distributed rodent that inhabits alpine meadows
in the mountains of central Asia. Using a scan-sampling observational approach, we collected data from 30 marmot sites in the Upper
Mustang region of Annapurna Conservation Area, Nepal. We developed an index of pastoralism intensity for each site, based on the
presence of livestock, herders, guard dogs, distance from pastoralist camps, and density of major tracks. Using this index, marmot time
spent above-ground, and foraging distance from burrows, was compared between high and low pastoralism sites. Using a linear mixed
modeling approach, there was no significant difference between areas of high and low pastoralism in either the total daily activity time
or foraging distance from burrows. However, marmots adjusted their diurnal patterns of activity and the distances moved from their
burrows in relation to the timing of pastoralist activities (temporal niche shift). In areas experiencing high levels of pastoralism, marmots were less active during periods of herding activity, and compensated by increasing activity when herding activity was less. By
changing foraging behaviors, any increase in pastoralism may have significant consequences in terms of marmot population viability.
Key words: diurnal activity, foraging distance, livestock grazing, pastoralism, temporal niche shift, transhumance.
INTRODUCTION
Predation risk plays a prominent role in shaping the activity patterns of many foraging animals (Halle and Stenseth 2000; Creel
et al. 2014). Such animals may shift their activity patterns to avoid
or reduce the risk of predation (Fenn and Macdonald 1995; Fraser
et al. 2004), or extent of interference competition for resources by
other species (Valeix et al. 2007; Harrington et al. 2009). Temporal
partitioning is one way a species can differentiate their ecological niche (Schoener 1974; Kronfeld-Schor and Dayan 2003),
avoid predation risk, and coexist with other animals (Fenn and
Macdonald 1995; Harrington et al. 2009)—the basis of the “risk
allocation hypothesis” (Lima and Bednekoff 1999; Beauchamp and
Ruxton 2011).
For many species, temporal niche adjustment is also an advantageous strategy for avoiding high levels of human disturbance
(Schwartz et al. 2010). Theoretical studies suggest that wild animals often perceive humans as a potential predator, and therefore
respond to their presence as a threat (Frid and Dill 2002; Beale and
Monaghan 2004). For example, Kitchen et al. (2000) found that
coyotes (Canis latrans) in Colorado altered their activity patterns in
Address correspondence to B.S. Poudel. E-mail: [email protected].
© The Author 2015. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved. For
permissions, please e-mail: [email protected]
response to changes in human disturbances. Likewise, Pangle and
Holekamp (2010) found human pastoralist activities in Kenya had
a strong influence on changes in the activity patterns of hyenas
(Crocuta crocuta). However, temporal shifts in the activity patterns of
animals can incur a cost because many species are rarely adapted
to foraging effectively at different times of the day (Kronfeld-Schor
and Dayan 2003).
Animals that are forced to forage in suboptimal activity periods
to avoid the risks associated with human activities often experience
problems in balancing their energy budgets (Kronfeld-Schor and
Dayan 2003; Houston et al. 2012; Christiansen et al. 2013). For
example, species with a limited ability to move away from a threat,
such as those with small home ranges or tied to a burrow, are more
vulnerable to risks associated with human disturbances (Gill et al.
2001). Therefore, further knowledge of the mechanisms through
which human disturbances influence the activity patterns of wild
animals is critical to enhance conservation management activities.
Trans-Himalayan rangelands have been shaped over millennia
by the grazing of wild and domesticated animals (Schaller 1998;
Miehe et al. 2009). These high-altitude rangelands are among the
least productive grassland ecosystems in the world (Mishra 2001),
but are essential in supporting human populations, and a diverse
flora and fauna which includes many threatened and endangered
Behavioral Ecology
1346
species (Schaller 1977; Joshi et al. 2013). Pastoralism is an ageold strategy of subsistence livelihood in this region (Miller 1987;
Bhasin 2011), which is expected to increase due to human population growth (Namgail, Bhatnagar, et al. 2007; Parajuli et al. 2013).
Wild animals that occupy the region are likely to be exposed to a
variety of forms of human disturbance associated with pastoralism
(Namgail, Fox, et al. 2007). Resultant increase in human–wildlife
conflict has the greatest potential to affect the behavioral ecology
of the local wildlife (Manor and Saltz 2003; Woodroffe et al. 2005).
Numerous studies have described the negative impacts of livestock grazing on wild animal behavior (e.g., activity patterns)
(Chaikina and Ruckstuhl 2006; Brown et al. 2010; Reid et al.
2010). These changes are often caused by the physical presence of
livestock and herders (Welp et al. 2004; Namgail, Fox, et al. 2007).
Livestock and their herders are therefore considered a form of disturbance (Namgail, Fox, et al. 2007), and animals have to adjust
their behavior to cope with both acquiring food/energy and avoiding disturbance. Because human activity in the rangelands varies
throughout the day, the intensity of any interference competition
with other species will vary temporally, with some times being more
highly disturbed than others. Consequently, wild animals often
adapt by altering their natural patterns of activity (Kitchen et al.
2000; Schwartz et al. 2010); however, few studies have documented
this phenomenon (Valeix et al. 2007).
The aim of this study was to investigate the diurnal activity patterns of Himalayan marmots (Marmota himalayana Hodgson 1841) in
relation to risks associated with pastoralism. Marmots depend on
burrows as a refuge to escape from potential predators (Blumstein
and Arnold 1998; Armitage 2000). Therefore, both activity outside
the burrow and the distance from the burrow (hereafter referred to
as “foraging distance”) may be related to the perceived predation
risk (Holmes 1984; Berryman and Hawkins 2006). We designed
this study to address the following questions: 1) to what extent does
marmot activity levels differ between areas experiencing high and
low levels of pastoralism and 2) in response to disturbances from
pastoralists, do marmots adjust their above-ground activity patterns
through changes in the timing of their foraging behavior, that is, is
there a temporal shift in their diurnal activity patterns.
MATERIALS AND METHODS
Study species
The Himalayan marmot (M. himalayana) is a diurnal, burrowing
ground squirrel that lives colonially in alpine and subalpine meadows
throughout the Trans-Himalaya region (Armitage 2000; Nikol’skii
and Ulak 2007). Himalayan marmots are important prey for many
predators, including for Panthera uncia, Ursus arctos, Canis lupus, and
Aquila chrysaetos (Schaller 1977; Oli et al. 1993; Aryal et al. 2012).
Marmots hibernate, so in summer they must obtain sufficient food
to replace energy reserves, breed, and then build up energy reserves
again for the next winter. They are often stressed during summer
time, as human pastoralists and predators are active and compete for
similar resources. They cannot avoid livestock grazing and human
disturbances because they are diurnal, have a small home range,
and form a high dependence on a complex burrow system. The
Himalayan marmot is one of the least-understood marmot species
in the world (Le Berre and Ramousse 2007), whose population trend
is largely unknown (Molur and Shrestha 2008). Little is known about
its ecology (Nikol’skii and Ulak 2007), nor of the potential impact of
pastoralism on its behavior and activity patterns.
Study area
This study was conducted in the Upper Mustang region (29°10′N,
83°54′E) of the Annapurna Conservation Area in northern Nepal
(Figure 1). The study area lies in the rain shadow of the Himalayas,
at altitudes of around 4000 m a.s.l., and forms part of the TransHimalaya high desert region of Nepal. The area is characterized
by a cold arid alpine climate, with average annual rainfall below
200 mm. Most precipitation occurs in the form of snow during
winter, whereas some rainfall occurs during the monsoon (June–
August). Average monthly temperatures range from −4 to 13.9 °C.
Snow cover lasts 4–5 months from late October or early November
until March. The mean maximum temperature reaches up to
20.8 °C in summer. The minimum temperature drops to subzero
between October and April (Ohba et al. 2008).
The vegetation of the area is predominately Trans-Himalayan
steppe (Ohba et al. 2008). Three broad vegetation types can be
identified: 1) alpine meadows, distributed in flat pockets and basins,
dominated by grasses and forbs; 2) alpine grasslands, located at
higher elevations, mainly on northern slopes, dominated by Stipa
spp., Kobresia spp., and Carex spp.; and 3) scrublands; widespread
on dry rugged slopes, dominated by dwarf shrubs. Sedges, such as
Carex and Kobresia, are common along streams. Rugged slopes are
sparsely vegetated with dwarf shrubby cushion plants (e.g., Caragana
spp., Astragalus spp., and Lonicera spp.).
The region has experienced a long history of animal husbandry
and pastoralism in these high-altitude rangelands (Schaller 1977;
Miehe et al. 2009). Present-day livestock assemblages include goat
(Capra hircus), sheep (Ovis aries), cow (Bos indicus), yak (Bos grunniens),
and horse (Equus caballus). At the commencement of the study,
observations were made to characterize the present grazing regime
and determine the distribution and abundance of domestic livestock herds. It was estimated that approximately 8500 livestock
(5600 goats/sheep, 800 cows, 600 horses, and 1500 yaks) occurred
in the area during the study period. Livestock were corralled every
evening inside villages or near to the nomad’s camp and moved out
to surrounding grazing areas each morning. Yaks were semi-freeranging, that is, herders released the yaks for grazing in the morning and herded them back to campsites in the evening, but did not
follow the yak herds throughout the day, whereas the goats/sheep
and cows were herded at farther distance from campsites (or villages) by herders and brought to the campsites (or villages) in the
evening.
The Tibetan woolly hare (Lepus oiostolus) is the only wild herbivore that shares the study area with marmots during summer. Snow
leopard (Panthera uncia) and brown bear (U. arctos) are known by
herders to use this area especially during winter, but no terrestrial
predators were observed during the fieldwork period. The golden
eagle (A. chrysaetos) is the only avian predator known to feed on
marmots.
Observation sites
Observations were made during the summer active months
(June–August) of 2014 at each of 30 sites. The average area of
a family group of Himalayan marmot generally ranges 0.5–1.7
ha (Nikol’skii and Ulak 2007). A pilot study was conducted in
2013 to study marmot colonies and ascertained that the maximum distance marmots traveled from their burrows was less
than 50 m (Poudel B, unpublished data). Therefore, we defined
a marmot “site” as an area encompassing the burrows occupied
by a family group or interacting family group within a radius
Poudel et al. • Temporal shift in activity patterns of Himalayan marmots
N
1347
(b) Annapurna Conservation Area
Nepal
Chhonhup
Lhomanthang
Jomsom
Chhoser
Charang
Ghami
Surkhang
Chhusang
(a)
NEPAL
Legend
Study area
Rivers
VDC
2500 - 3500 m
3500 - 4500 m
4500 - 6000 m
Above 6000 m
0
5
10
20
km
Kathmandu
Figure 1
Upper Mustang region of Annapurna Conservation Area, Nepal; the location of the study area is indicated by the box. The map on the inset shows (a) the
location of the Annapurna Conservation Area (demarcated) in Nepal, and (b) the location of the Upper Mustang region in Annapurna Conservation Area
(shaded) in Nepal.
of approximately 100 m that was separated from other marmot
sites by a minimum of 270 m. This criterion was developed in
order to avoid resampling the same individual in more than 1
site and to ensure that sites were independent of each other. The
group size of adult marmots in a site ranged between 2 and 7
individuals.
For each marmot site, an index of the extent of disturbances
from pastoralist activities was calculated (Supplementary Table S1)
based on the following attributes: 1) presence of livestock, humans,
and dogs (Griffin et al. 2007; Namgail, Fox, et al. 2007); 2) distance
to camps (Sasaki et al. 2009; Dorji et al. 2013); and 3) the density
of major foot trails/tractor trails (Cingolani et al. 2008; Paudel and
Andersen 2010). At each site, the number of livestock, humans and
dogs that stayed on or passed through, was recorded continuously
during daylight hours (0700–1900 h) over 2 consecutive days, and
then, each factor’s values were averaged to generate 1 set of values
per site. The total length of major human/tractor trails was visually estimated in each site. The distance of each site to the nearest camp was measured from GPS locations of sites and camps
in ArcGIS v. 10.0 (ESRI Inc.). Each attribute was first scaled and
assigned an ordinal value between 0 and 5 based on their intensity of effects. We then calculated a combined index of pastoralism
for each site (see Supplementary Table S1). As the index showed a
bimodal distribution, we then categorized the sites based on index
as having “low” (disturbance indices of 2.0–9.5) or “high” pastoralism effects (disturbance indices of 11.5–16.5). This process resulted
in a total of 20 “low” and 10 “high” pastoralist intensity sites for
subsequent marmot observations.
Table 1
Salient characteristics of 2 categories of sites in the Upper
Mustang, Nepal
Attributes of pastoralism
Low pastoralism
High pastoralism
Distance to nearest camp (m)
No. of livestock grazing daily on
the site
No. of pastoralists observed daily
on the site
No. of dogs observed daily on
the site
Length of major trail (m)
1672 ± 211
224 ± 33
319 ± 21
435 ± 53
1.6 ± 0.4
3.6 ± 0.6
0.3 ± 0.2
1.4 ± 0.2
64.5 ± 49.0
125 ± 18.0
Values are average ± standard errors.
High pastoralism sites referred to those sites that were generally
closer to nomads’ camps; that had high levels of livestock, human,
and dogs; and that contained well-defined human and/or tractor
trails (Table 1). In contrast, low pastoralism sites were further away
from campsites and had a low occurrence of livestock, humans, and
dogs (Table 1). The 2 categories of sites also differed substantially
in terms of their duration of time, where they were observed for
longer time in high pastoralism sites, as compared with low sites.
Field observations
The daily activity patterns of adult marmots (≥2 years old) were
recorded using binoculars (8 × 42) and a telescope (×20 to ×60).
Marmot activity patterns were determined using a scan-sampling
Behavioral Ecology
1348
The dataset consisted of 3347 observations in 2940 scans (30 sites ×
2 days/site × 49 scans/day) from 30 sites. For each site, the proportion of time marmots spent above ground was calculated as an index
of overall activity. The maximum number of marmots observed in
any one scan on any day was used as an estimate of the total number of marmots in each study group (site). For each site, we averaged the proportion of the total individuals seen above ground at
each scan to obtain a single value per site. This averaged proportion
was equivalent to the average time spent above ground per individual. Temporal patterns of marmot activity and movement were
analyzed during 3 time periods: morning (0700–1000 h), midday
(1001–1600 h), and evening (1601–1900 h). These periods followed
the local time of livestock herders and represented different periods
of risk to marmots. The pattern of pastoralist activities showed a
marked temporal pattern, with maximal activity during the morning
and the evening and minimal during the midday in high pastoralism
sites, and opposite in low pastoralism sites (Figure 2a). We then compared the activity and movement patterns of marmots between 2
levels of pastoralism (high and low) and among 3 periods of the day.
Data were checked for outliers, normality, and homogeneity
according to protocols described by Zuur et al. (2010). Activity percentage data were square-root transformed, and average distance
traveled was log-transformed to satisfy assumptions for normality
and heterogeneity of variances. A Shapiro–Wilk’s test (P > 0.05)
and visual inspection of histograms, normal Q–Q plots, and box
plots were performed to confirm that the transformed data were
normally distributed.
General linear mixed models (LMM) were used to assess the
influence of pastoralism and time of day on marmots’ activity time
and foraging distance. The function lmer of the library lme4 (Douglas
et al. 2014) in the R package was used for fitting the LMM, where
pastoralism (factor with 2 levels), time of day (factor with 3 levels),
and their interaction (pastoralism × time of day) were included as
fixed factors for both analyses. The random effect entered into the
models was site. Study site was used as a random factor to account
for potential correlation among observations within site through
periods and uneven sample sizes (Pinheiro and Bates 2000; Bolker
et al. 2009). Marginal R2 (proportion of variance explained by the
fixed factors) and conditional R2 (proportion of variance explained
by both the fixed and random factors) were calculated according to
Nakagawa and Schielzeth (2013). Results were considered statistically significant at P < 0.05. All data are reported as means ± 95%
confidence intervals (CI) unless otherwise stated. All the analyses
were conducted in R 3.1.2 (R Core Team 2014).
RESULTS
Effects of pastoralism on diurnal activity patterns
Overall, adult marmots were above ground for a mean of 33.7%
(95% CI = 4.0%) of daylight time, averaging approximately 4 h
10
Activity (%)
8
6
4
2
0
700
900
1100
1300
1500
1700
1900
1100
1300
1500
1700
1900
1300
1500
1700
1900
(b) Marmot activity
60
50
Activity (%)
Data analysis
(a) Pastoralist activity
40
30
20
10
0
700
900
(c) Foraging movements
25
Mean distance (m)
approach (Altmann 1974; Martin and Bateson 2007), where the
activities of all visible marmots were recorded during 15-min intervals in daylight hours over 2 days at each site. For each scan, the
foraging distance from burrow for all active marmots was recorded.
Observations were made from vantage points (≥60 m from the
marmots), at which they showed no evidence of reactions to
observers. A total of 735 h of direct observations of 103 different
marmots was accumulated during this study.
20
15
10
5
0
700
900
1100
Time of the day (hrs)
Figure 2
Temporal activity patterns of pastoralist (a) and marmots (b), and average
distance traveled by Himalayan marmots from their burrows (c) in high
(solid line) and low pastoralism sites (dashed line) in the Upper Mustang
region, Nepal.
(±29 min) per day. Contrary to expectations, there was no significant difference in marmot activity (total time above ground)
between high and low pastoralism sites (LMM: χ2 = 0.85, degrees
of freedom [df] = 1, P = 0.35). In general, marmots showed a
bimodal activity pattern, where they were mostly inactive during
the midday period. The proportion of time marmots spent above
Poudel et al. • Temporal shift in activity patterns of Himalayan marmots
ground reached up to 50% during the peak morning and afternoon
periods (Figure 2b). However, time of the day also had no significant influence on marmot total activity (LMM: χ2 = 2.88, df = 2,
P = 0.23).
Model results showed that there was a significant interaction between pastoralism and time of the day (LMM: χ2 = 6.82,
df = 2, P = 0.03), where marmot activity was greater during the
midday period in high pastoralism sites, whereas this pattern was
opposite in low pastoralism sites (Figure 2b). Compared with high
pastoralism sites, mean activity in low pastoralism sites was significantly greater during the morning period (P = 0.007). Pairwise
comparisons revealed that all other differences in marmot activity
for different time periods were not significant (all P > 0.05). Sites
explained about 31% of the total variation in activity pattern (R2
marginal = 0.09, R2 conditional = 0.40).
Effects of pastoralism on foraging movements
from burrows
When above ground, marmots spent most of their time
(90.7 ± 3.2%) within 18 m from a burrow. Marmots were either
resting or vigilant when they were near the burrow. The average
foraging distance in high pastoralism sites (8.6 ± 2.4 m) was approximately 13% greater than that of low pastoralism sites (7.6 ± 1.3
m); however, this difference was not significant (LMM: χ2 = 0.06,
df = 1, P = 0.79). The maximum distance traveled we recorded
was 48 m.
Time of the day had a significant effect on average foraging distance (LMM: χ2 = 9.76, df = 2, P = 0.007). The average foraging
distance was greater during the midday period (P = 0.03). There
was a significant interaction between pastoralism and time period
on foraging distance (LMM: χ2 = 9.63, df = 2, P = 0.008). The
distance traveled by marmots in high pastoralism sites was greater
around midday and lower during the morning and the evening, as
compared with marmots at low pastoralism sites (Figure 2c). Model
results explained 43% of the total variation in the distance traveled
(R2 conditional = 0.43).
DISCUSSION
Our results show a temporal adjustment in the activity pattern and
foraging behaviors of Himalayan marmots in relation to pastoralism. Although marmot activity levels and foraging distances were
similar between areas experiencing high and low levels of pastoralism, there was a significant change in the timing and nature of
their above-ground activity.
Effects of pastoralism on diurnal activity patterns
of Himalayan marmots
Marmots avoided high-risk times when the herders, their livestock,
and guarding dogs were in the vicinity, especially during early morning and late evening—when disturbances associated with pastoralism reached a peak. Marmots were more active during times of the
day when disturbances from pastoralism were low, especially during the middle of the day in high pastoralism sites. This behavioral
adjustment suggests that marmots perceive disturbances associated
with pastoralism as a threat. Our findings are consistent with previous studies (Kitchen et al. 2000; Kolowski et al. 2007; Schwartz
et al. 2010), which have showed that animals can adjust their temporal patterns of activity to avoid interactions with humans. We
contend that the stress and fear associated with pastoralism partly
1349
explains the temporal niche switching we observed with Himalayan
marmots.
The bimodal activity pattern we recorded for Himalayan marmots (Figure 2b) has been commonly observed for other Marmota
species: such as the hoary marmot (Taulman 1990), yellow-bellied
marmot (Belovsky and Slade 1986), golden marmot (Blumstein
1994), alpine marmot (Turk and Arnold 1988), and black-capped
marmots (Semenov et al. 2001). Although several studies have
explained the nature of this bimodal activity pattern in terms of
warm temperatures (Turk and Arnold 1988; Halle and Stenseth
2000), these findings are not applicable to our species because the
temperature never reaches the reported critical limit (22–25 °C)
in our study systems (Nikol’skii and Ulak 2006). Marmots reduced
their activity around midday to take rest, and thus, their daily activity pattern becomes bimodal. A resting period in middle of the day
could be explained by strong afternoon winds that are commonly
experienced in such high-altitude environments (Ohba et al. 2008).
Our results also show that Himalayan marmots spend very
little time out of their burrows as compared with other rodents
(Taulman 1990; Semenov et al. 2000; Everts et al. 2004). Adult
Himalayan marmots averaged 33.7% of the daylight hours above
ground—approximately 4 h per day. In contrast, Belovsky and
Slade (1986) reported that yellow-bellied marmots spend 6 h per
day above ground, alpine marmots 7 h per day (Turk and Arnold
1988), and hoary marmots spend approximately 70% of their
time above ground (Taulman 1990). However, such comparisons
in activity are difficult because Himalayan marmots share pastures
with other livestock. Therefore, the lower proportion of time spent
in activity by Himalayan marmots in comparison with other species
may be related to pastoralism, in conjunction with the harshness of
the environment (Mishra 2001; McNamara and Buchanan 2005).
Marmots have to conserve energy to survive through winter hibernation (Kuhn and Vander Wall 2008). The results indicate that
marmots are conserving energy by reducing activity time, as energy
expenditures during activity are greater than during rest in burrows
(Halle and Stenseth 2000).
Effects of pastoralism on foraging movements
from burrows
We found that marmots adjusted their foraging movements in
relation to pastoralism. In sites experiencing high levels of pastoralism, marmots increased their mean foraging distances during
midday than in mornings and evenings. This is most likely related
to the temporal activity patterns of pastoralists, livestock, and most
importantly the guarding dogs, as livestock are led to pastures in
the morning and returned to their sheds in the evening. These
results suggest that marmots avoid high-risk times and forage much
closer to their burrows during periods of high risk when herders,
livestock, and guarding dogs are in the vicinity.
The mean foraging distance we recorded for Himalayan marmots (7.6–8.6 m) was similar to reports for hoary marmots (5–12 m;
Barash 1980; Karels et al. 2004) and yellow-bellied marmots (<20
m; Frase and Armitage 1984). However, our findings contrast to
those by Holmes (1984) for hoary marmots in south-central Alaska
(49.9 m) and Carey and Moore (1986) for yellow-bellied marmots
in California (up to 300 m). Such differences are most likely associated with environmental conditions, associated energy constraints,
and predation risk.
In this study, marmots exhibited short movement patterns. This
could be because the study area provides forage for a large number
of domestic livestock, and the distance may be determined by risk
1350
associated with pastoralism. Alternatively, livestock may facilitate quality food availability (Farnsworth et al. 2002; Retzer 2007). Although
food availability can affect the foraging movements, it appears unlikely
to have caused the diurnal difference we observed in foraging distance
because vegetation does not change according to a diurnal pattern.
Because we selected both sites in the same valleys and same altitudes,
there were no substantial differences in vegetation cover. The habitat
structure or availability of refugia also can affect the perceived risk
of predation, and hence foraging movements (Blumstein et al. 2006).
However, this study could not disentangle the potential effects of disturbance and habitat structure on foraging distance.
CONCLUSIONS
An understanding of the effects of pastoralism on the diurnal activity patterns of wild animals is an essential step toward conserving a
species in an environment where livestock grazing is pervasive. Low
activity levels and short foraging movements could be interpreted as
marmot’s energy-saving strategy. Himalayan marmots adjusted their
temporal niche by shifting their activity patterns and foraging movements to avoid high-risk times associated with pastoralism. Marmots
responded to pastoralism by compensating the timing of their activity
and above-ground movements. Marmots appear flexible in the timing of their activity patterns. In high-altitude arid areas such as Nepal,
where conditions are harsh and resources are scarce, even small differences and shifts in activity or movements could have significant ecological implications and evolutionary significance. Additional research
quantifying these consequences would further enhance our understanding of the relationship between pastoralism and wildlife conservation. Future studies should also examine the time and energy budgets
of Himalayan marmots in relation to pastoralism, to determine the
relative effect of grazing on wildlife in such an extreme environment.
SUPPLEMENTARY MATERIAL
Supplementary material can be found at http://www.beheco.
oxfordjournals.org/
FUNDING
This work was supported by the Holsworth Wildlife Research
Endowment of the ANZ Trustees Foundation (CT#22178) and
Charles Sturt University (Postgraduate Research Scholarship to
B.S.P.). The research was undertaken under an approved protocol
(13/013) from the Animal Care and Ethics Committee of Charles
Sturt University.
We would like to thank Iain Taylor for his advice with the conceptual design
and for useful comments on an earlier draft of this MS. Thanks to Wayne
Robinson for his statistical advice, and Deanna Duffy for her assistance with
GIS mapping. We also thank Hem S. Baral for his support during the early
design of this research, and Prabin Shrestha, Mahesh Neupane, Shankar
Tripathi, and Thokme Lowa for their assistance in the data collection.
We are grateful to National Trust for Nature Conservation/Annapurna
Conservation Area Project for allowing permission to conduct this research.
A special thanks to the community of the Upper Mustang who provided
generous hospitality during field work.
Handling editor: Bob Wongon
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