Temporal shift in activity patterns of Himalayan marmots in relation to pastoralismBuddi S. Poudel, Peter G. Spooner, and Alison MatthewsSchool of Environmental Sciences, Institute for Land, Water and Society, Charles Sturt University, PO Box 789, Albury, NSW 2640, AustraliaReceived 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 dis-turbance. 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, mar-mots 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.
INTRODUCTIONPredation risk plays a prominent role in shaping the activity pat-terns 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 ecologi-cal 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 advan-tageous strategy for avoiding high levels of human disturbance (Schwartz et al. 2010). Theoretical studies suggest that wild ani-mals 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
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 Address correspondence to B.S. Poudel. E-mail: [email protected].
species (Schaller 1977; Joshi et al. 2013). Pastoralism is an age-old strategy of subsistence livelihood in this region (Miller 1987; Bhasin 2011), which is expected to increase due to human popula-tion 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 live-stock 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 dis-turbance (Namgail, Fox, et al. 2007), and animals have to adjust their behavior to cope with both acquiring food/energy and avoid-ing 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 pat-terns 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 METHODSStudy 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 Trans-Himalaya 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 live-stock 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-free-ranging, that is, herders released the yaks for grazing in the morn-ing 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 vil-lages) by herders and brought to the campsites (or villages) in the evening.
The Tibetan woolly hare (Lepus oiostolus) is the only wild herbi-vore 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 maxi-mum 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
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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 visu-ally estimated in each site. The distance of each site to the near-est 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 inten-sity 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” pastoral-ism 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.
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
Legend
Study area
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Figure 1Upper 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.
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) 1672 ± 211 319 ± 21No. of livestock grazing daily on the site
224 ± 33 435 ± 53
No. of pastoralists observed daily on the site
1.6 ± 0.4 3.6 ± 0.6
No. of dogs observed daily on the site
0.3 ± 0.2 1.4 ± 0.2
Length of major trail (m) 64.5 ± 49.0 125 ± 18.0
Values are average ± standard errors.
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approach (Altmann 1974; Martin and Bateson 2007), where the activities of all visible marmots were recorded during 15-min inter-vals 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.
Data analysis
The dataset consisted of 3347 observations in 2940 scans (30 sites × 2 days/site × 49 scans/day) from 30 sites. For each site, the propor-tion 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 num-ber of marmots in each study group (site). For each site, we aver-aged 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 indi-vidual. 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 com-pared 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 per-centage 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 statisti-cally 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).
RESULTSEffects 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
(±29 min) per day. Contrary to expectations, there was no sig-nificant 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
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Figure 2Temporal 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.
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ground reached up to 50% during the peak morning and afternoon periods (Figure 2b). However, time of the day also had no signifi-cant influence on marmot total activity (LMM: χ2 = 2.88, df = 2, P = 0.23).
Model results showed that there was a significant interac-tion 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 sig-nificantly 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 approx-imately 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 dis-tance (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).
DISCUSSIONOur results show a temporal adjustment in the activity pattern and foraging behaviors of Himalayan marmots in relation to pastoral-ism. Although marmot activity levels and foraging distances were similar between areas experiencing high and low levels of pasto-ralism, 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 morn-ing and late evening—when disturbances associated with pastoral-ism reached a peak. Marmots were more active during times of the day when disturbances from pastoralism were low, especially dur-ing 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 pre-vious studies (Kitchen et al. 2000; Kolowski et al. 2007; Schwartz et al. 2010), which have showed that animals can adjust their tem-poral patterns of activity to avoid interactions with humans. We contend that the stress and fear associated with pastoralism partly
explains the temporal niche switching we observed with Himalayan marmots.
The bimodal activity pattern we recorded for Himalayan mar-mots (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 activ-ity 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 hiber-nation (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 pasto-ralism, 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 mar-mots (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 associ-ated 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
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associated with pastoralism. Alternatively, livestock may facilitate qual-ity 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 dis-turbance and habitat structure on foraging distance.
CONCLUSIONSAn understanding of the effects of pastoralism on the diurnal activ-ity 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 move-ments 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 tim-ing of their activity patterns. In high-altitude arid areas such as Nepal, where conditions are harsh and resources are scarce, even small differ-ences and shifts in activity or movements could have significant eco-logical implications and evolutionary significance. Additional research quantifying these consequences would further enhance our under-standing of the relationship between pastoralism and wildlife conserva-tion. 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 MATERIALSupplementary material can be found at http://www.beheco.oxfordjournals.org/
FUNDINGThis 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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