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SHORT COMMUNICATION Food habits of the Tibetan ( ferrilata) in the Kunlun Mountains, Qinghai Province, China Qunxiu Liua, Richard B. Harrisb, Xiaoming Wanga,Ã aCollege of Life Science, East China Normal University, Shanghai 200062, China bDepartment of Ecosystem and Conservation Sciences, University of Montana, Missoula, MT 59801, USA

Received 10 December 2008; accepted 8 February 2009

Keywords: China; Diet; Kunlun Mountains; Plateau pika; Tibetan fox

The Tibetan fox (Vulpes ferrilata) is restricted in noted that were rare within his category ‘‘pika geographic distribution to the Tibetan highlands of or small ’’. Thus, clarification of Tibetan ’ China and adjacent areas of , India, and potential dependence on plateau pikas has been based (Schaller and Ginsberg 2004; Clark et al. 2008). Studied largely on anecdotal observations of them preying on only during the past few years (Gong and Hu 2003; pikas, and on the apparent (but not-yet rigorously Wang et al. 2007), it has been assumed to prey examined) overlap between their areas of occurrence principally on plateau pikas, Ochotona curzoniae, which and areas of high pika density. achieve locally high densities on the Here, we report on food habits of Tibetan foxes in the (Smith and Foggin 1999), and with which it is invariably Kunlun Mountains of the northern Tibetan plateau, associated (Schaller 1998; Clark et al. 2008; Harris et al. Qinghai Province, China, based on an analysis of scats. 2008). Although plateau pikas clearly have an important Our study objectives were to quantify Tibetan fox diets, role in facilitating the existence of many other estimate the importance of plateau pikas for foxes, and (Smith and Foggin 1999), they are considered an examine if fluctuating pika numbers affected their agricultural pest by Chinese government bureaus, and importance in fox diets. We used foxes captured and have been subject to large-scale extermination cam- radio-monitored as part of a larger study (Harris 2007; paigns using various poisons since the 1950s (Smith Liu et al. 2007) to help us locate feces, which were later et al. 2006). Tibetan foxes have also been reported to examined. consume small rodents (e.g., Alticola, Cricetulus, and Our study was conducted in Gouli Township, Dulan Pitymys spp., and plateau zokors [Eospalax fontanierii]), County, Qinghai Province, China. The study area, and to scavenge carrion from wild (e.g., Tibetan centered on approximately 351300N, 981400E, covered [ picticaudata], blue sheep [Pseudois nayaur]) approximately 32 km2 of rolling mountainous terrain in and domestic ( [ mutus], sheep [ aries]) the eastern Kunlun Mountains at elevations of ungulates (Schaller 1998; Clark et al. 2008). Somewhat 3800–4500 m. Vegetation formations were alpine steppe surprisingly, quantitative documentation of Tibetan fox (dominated by Stipa purpurea), alpine meadow (domi- food habits is limited to that of Zheng (1985), who, nated by Kobresia spp.), and shrublands (dominated by unfortunately, lumped lagomorphs (including pikas) Salix spp.). The study area formed the winter grazing together with rodents, and Schaller (1998, p. 187), who area for approximately 10 households of Tibetan pastoralists who raised primarily domestic sheep and ÃCorresponding author. Tel./fax: +1 406 542 6399. along with a few domestic ( hircus)and E-mail address: [email protected] (X.M. Wang). horses (Equus caballus).

1616-5047/$ - see front matter r 2009 Deutsche Gesellschaft fu¨rSa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2009.02.002 Mamm. biol. 75 (2010) 283–286 Author's personal copy

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Blue sheep were common in the higher elevation and/ macroscopic fragments and to discard the inconspicuous or steeper slopes of the study area; a few Tibetan fragments (Ciucci et al. 1996; Reynolds and Aebischer gazelles were also year-round residents within home 1991). Prey determination was performed by micro- ranges of all of our radio-marked Tibetan foxes. Small scopic analyses on the basis of hair characteristics, bands of (Ovis ammon) and red ( feather and bone. Guard hairs were used to identify elaphus) were occasional visitors to the study area. prey. Macroscopic and microscopic structures Based on interviews with pastoralists, we believe that of hairs found in the scats were compared with reference both (Moschus chrysogaster) and wild yaks hairs (e.g., Brunner and Coman 1974; Reynolds and (Bos grunniens) were originally present in the area, but Aebischer 1991) obtained in the study area, or with had long since been extirpated by the time of our study. laboratory samples stored at East China Normal Other carnivores we observed within the study area were University in Shanghai or Northeast Forest University (V. vulpes), wolf ( lupus), (Lynx lynx), in Harbin. Because of the low presence of rodent Pallas’ cat (Otocolobus manul), and ( remains, and because differentiating among Eospalax, meles). We also observed tracks of brown ( Allactaga, and other rodent species was difficult, we arctos) and snow leopard (Uncia uncia; a separate study pooled them together as one category termed ‘‘rodents’’. had obtained a photograph of a free-ranging snow We were, however, able to reliably separate Marmota leopard using a remotely-operated camera in 2007, Jiang himalayana from other rodents, and pikas from all Zhigang, Institute of Zoology, personal communication, rodents. Undistinguishable fragments were labeled as 2007). ‘‘unidentified’’. We collected feces of Tibetan foxes during September We expressed diet composition as the percent 21–October 21, 2006, March 13–May 20, 2007, Septem- occurrence (PO), defined simply as the number of scats ber 15–October 17, 2007 and March 6–March 21, 2008. containing a prey item divided by the total collected To minimize the potential for species mis-identification, ( 100). We tested for difference in FO between our scats were considered to originate from Tibetan foxes hypothesized low (March–May) and high (September–- only when (i) they appeared fresh, (ii) they were found in October) pika density periods using a w2 test of close proximity to a known, radio-marked Tibetan fox, independence. Food niche breadth (B) was calculated (iii) they were collected from a known Tibetan fox den from the proportions of the 11 food categories in scats or , or (iv) we observed deposition by a radio- as suggested by Hurlbert (1978): marked fox directly. Scats collected were air-dried in the X 2 field, and stored in paper bags. B ¼ 1= ðpi Þ (i) s We captured 5 Tibetan foxes using Victor Soft-Catch where p is the proportion of food items made up by leg-hold (Woodstream Corporation, Lititz, Pennsylvannia, i s category i. USA), or Belisle leg-hold traps and immobilized them Shannon–Weaver diversity (H) and evenness (E) were with Ketamine hydrochloride (approximately 6 mg/kg) calculated: and Medetomidine (approximately 0.05 mg/kg). Foxes were fitted with VHF radio-collars (MOD-225, Telonics, Xs ¼ ð Þð Þ Inc., Mesa, Arizona, USA) weighing approximately 130 g H Pi log2 Pi (ii) ¼ and monitored 1–7 times/week. All capture and handling i 1 procedures complied with University of Montana E ¼ H=H (iii) Use Committee Protocols. max We also obtained an index of pika density by counting We analyzed 93 scats that included pika, rodent, large all pikas seen in 30-min time spans within 30 m radius mammal, bird, reptile, insect, vegetation, and unidenti- plots placed randomly within each 0.5 km2 cell of the fied animal remains (Table 1). Pika remains were found study area. Plots were surveyed both in early autumn in 84% of scats, representing the most frequently (September–October 2007 [n ¼ 54] when it was hypothe- occurring food item. Rodents, including Himalayan sized pika density would be high, and late winter , occurred in 26% of scats (Table 1). All other (March–May 2007 [n ¼ 77], and March–May 2008 prey items were found in only a few scats (Table 1). [n ¼ 61]), when it was hypothesized pika density would The pika density index was higher in September– be low, following the normal pattern of winter mortality October (x ¼ 4:15, 95% confidence interval 3.42–4.88) (Wang and Smith 1988). We tested whether the pika than in March–May (x ¼ 2:67, 95% confidence interval density index differed between seasons using a Mann– 2.31–3.03; Mean Ranks 86.7, 121.5, U ¼ 2376, Whitney U-test with a normal approximation. Z ¼3.961, Po0.001). However, we found no evidence In the laboratory, scats were autoclaved (30 min at of seasonal differences in diets of Tibetan foxes 120 1C), then oven-dried (at 80 1C). After being soaked (w2 ¼ 9.14, 11 df, P ¼ 0.609). The year-round food in water for 24–72 h, individual dried scats were filtrated niche breadth (B) was 1.32, Shannon–Weaver diversity with a 0.5-mm-mesh sieve to separate microscopic from and evenness indices were 2.29 and 0.66, respectively. Author's personal copy

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Table 1. Number and percent occurrence (PO) of Tibetan fox scats (n ¼ 93) containing various food items, collected in Gouli Township, Dulan County, Qinghai Province, China, September 15–October 17, 2007, March 13–May 20, 2007, March 6–March 21, 2008.

Items September–October (high pika density, n ¼ 52) March–May (low pika density, n ¼ 41)

n PO n PO

Plateau pika Ochotona curzoniae 45 86.5 33 80.5 Undifferentiated rodents 10 19.2 6 14.6 Marmota himalayana 4 7.7 4 9.8 Blue sheep Pseudois nayaur 0 0 4 9.8 Tibetan Procapra picticaudata 1 1.9 2 4.9 Domestic sheep Ovis aries 1 1.9 2 4.9 Domestic yak Bos mutus 3 5.8 0 0 Undifferentiated bird 1 1.9 1 2.4 Undifferentiated reptile 0 0 1 2.4 Undifferentiated insect 7 13.5 2 4.9 Vegetation 1 1.9 2 4.9 Unidentified animal 13 25.0 10 24.4

Our results confirm previous suggestions that Tibetan An additional shortcoming of basing diet estimates on foxes prey principally on plateau pikas, and secondarily raw frequency of occurrence in feces is that analysis of on various rodents (Schaller and Ginsberg 2004, Clark different size prey species may result in overestimating et al. 2008). Remains of wild ungulates found in fox the proportion of smaller because of their feces probably represent scavenging on carrion (Schaller higher surface: volume ratios (Floyd et al. 1978; and Ginsberg 2004); we believe it unlikely that Tibetan Geraldine 1978; Corbett 1989). Our research may foxes, at only 4–5.5 kg (Harris et al. 2008) are capable of therefore have overestimated the importance of plateau killing adult ungulates (although newly-born ungulates pikas and smaller rodents relative to larger-bodied prey. may be vulnerable to fox predation for a few days). Regression equations, such have been developed for Tibetan foxes are probably capable of killing young other carnivores, would be useful to assess this short- domestic sheep, but in informal interviews, pastoralists coming. Unfortunately, we are unaware of any Tibetan never reported that foxes were a depredation concern, foxes in captivity that could be used for such a even during lambing season. Marmot remains were controlled experiment. Notwithstanding these uncer- detected in fox scats collected in March, April and tainties, our results confirm the central role of plateau September. Himalayan marmots in our study area were pikas in the life-history of Tibetan foxes. rarely above ground before May or after August; thus, we speculate that, in addition to direct predation, foxes may have scavenged the carcasses of marmots killed at Acknowledgements other times of year, and possibly by other predators. In collecting feces in the field, we endeavored to Funding for this project came from the Robert M. ensure that they came from Tibetan foxes rather than Lee Foundation, the Research Fellowship Project (RFP) other sympatric carnivores; however, we cannot rule out of the Wildlife Conservation Society (WCS), the Denver the possibility of some mis-identification. Based on Zoological Foundation, and the doctoral training unquantified visual observations, Tibetan foxes ap- program at East China Normal University. We thank peared to be far more common in the study area than Zhou Jiake for assistance in the field, and Da Shenglin any other mammalian carnivore. The most likely mis- for administrative support. identification would have come from red foxes. How- ever, we only made 3 red fox observations during the 2 years of field work, whereas we observed Tibetan foxes References on well over 100 occasions even without the aid of telemetry. We captured only a single red fox in 4200 Brunner, H., Coman, B.J., 1974. The Identification of capture nights, compared with 7 captures of Tibetan Mammalian Hair. Inkata Press, Melbourne. foxes. This, coupled with our field procedures, suggested Clark Jr., H.O., Newman, D.P., Murdoch, J.D., Tseng, J., that we erroneously included very few red fox feces Wang, Z.H., Harris, R.B., 2008. Vulpes ferrilata. Mamma- within our sample. lian Species 821, 1–6. Author's personal copy

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