ISSN 1027-2992 no 1 KH^JSI .##/?. ? ?: original contribution SHENG Lfr, DAJUN WANG", ZHI LIT, WILLIAM J. MCSHEA2 Cats living with pandas The status of wild felids within giant panda range, China From 2002 - 2009, we conducted a camera-trapping survey in 11 nature reserves of the five mountain ranges within current giant panda distribution for a total sampling effort of 19,151 camera-days. Four felid species were recorded: Panthera pardus, Panthera uncia, Catopuma temminckii, and Prionailurus bengalensis. We found no significant correlation between the sampling effort and photographic rates of small felids, or medium- and large-sized felids, but a positive correlation between the pho- tographic rates of medium* and large sized felids and large-sized prey species. A well-designed systemic monitoring network using camera-trapping would be the best approach to obtain the critical information needed for setting felid conservation goals in China. Nine felid species have been recorded to oc- cur within the current giant panda Ailuropo- da melanoleuca range and adjacent areas in southwest China. These species include the tiger Panthera tigris, leopard, snow leopard, clouded leopard Neofelis nebulosa, Eurasi- an lynx Lynx lynx, Asiatic golden cat, Pallas's cat Otocolobus manul, leopard cat, and Chi- nese mountain cat Felis bieti (Hu & Wang 1984, Wang 1998, Smith & Xie 2008). Giant pandas have been long considered a flag- ship species in wildlife conservation (Schal- ler 1994, Leader-Williams & Dublin 2000, Loucks et a!. 2001). Immense financial and manpower resources, as well as public at- tention, have been devoted to the conserva- tion of giant pandas and their habitat, which is believed to be beneficial to sympatric species, including felids (Cam & O'Doherty 1999, Lu et al. 2000). From early 1960s to 2007, 62 nature reserves were established with emphasis on giant panda protection and covered an area of 29,000 km2 (Wang 2008). Current giant panda distribution co- vers one of the largest remaining forested areas in China, comprising five mountains in southern Shaanxi, western Sichuan, and a southern corner of Gansu province (Loucks et al. 2001, SFA 2006). Though a wildlife monitoring system based on sign transect has been recently established in the giant panda reserves (Gu et al. 2004, 2005, SFA 2007), our knowledge on the status of the felid species in this area is still poor due to lack of systematic survey and monitoring. In 2002, we initiated a large mammal survey within the giant panda distribution of Sichu- an and Shaanxi provinces using remote-trip cameras. We examined this dataset with re- spect to felids, and address three major que- Fig. 1. Surveyed nature reserves (NR). Label numbers and names referred in Table 1. stions: 1) what felid species are currently present in the giant panda nature reserves; 2) what is the spatial distribution pattern of these felids; and 3) what is the relative ab- undance of known prey for these felids. Methods Camera-trapping was used to determine the presence of large mammal species within our study areas. From the five mountain ranges, we selected one to five nature re- serves in each range as our study area (Fig. 1). A series of training courses on the ca- mera-trapping technique (once a year) were held by Smithsonian National Zoological Park, Peking University, and Sichuan Fore- stry Department in Sichuan province from 2003 - 2008. At each course, staff from 3 - 5 reserves were trained to operate the came- ra units, identify common mammal species based on the photographs, manage the camera-trapping data using a database, and design the survey plan of their own reser- ve within a Geographic Information System (GIS). Some camera units and funds were provided to each reserve after the training to initiate a survey focusing on large mam- The surveyed nature reserve was divided into 1x1 km2 sampling blocks using GIS. The major vegetation types of our sampled blocks were deciduous forest, deciduous- coniferous mixed forest, and coniferous forest. In three reserves (i.e. Wanglang, Wolong and Tangjiahe Nature Reserves), the sampling area was partly extended to alpine shrub and alpine meadow habitat above the tree-line. One or two passive infrared-triggered camera units were placed in each block for a sampling duration of one month. Adjacent camera units were set > 300 m apart. We used multiple camera mo- dels over the course of the surveys, inclu- ding three passive film models (DeerCairT DC-200, CamTrakker? Original 35 mm, and one film model manufactured by colleagues and based on similar specifications to the CamTrakker? Original 35 mm units), and two passive digital models (CamTrakker'" Digital Ranger, CuddeBack? Digital). Camera units were attached to trees along active ani- mal trails, 30-50 cm above ground and 3-5 m from the trail. All the units were set to record 24 hours per day with 0.5-2.5 minu- te delay between consecutive exposures, to film, memory storage or batteries being expended on a single detection. Carnivo- re scent lure (Montgomery Fur Company, CATnews 52 Spring 2010 cats living with pandas Table 1. Photographic rates of wild felids and their prey within surveyed nature reserves. Photographic rate was based on number of independent detections per 1000 camera-days. The survey effort is indicated in camera-days. Nature reserve Survey #1km! Camera- Photographic rate ? Mountain Leopard Asiatic Leopard Snow Small Medium Large range period blocks days cat golden cat leopard prey prey prey Qingling 1 .Changqing 4-12/08 54 4307 5.34 0.70 0.23 16.25 17.88 177.39 Minshan 2.Tangjiahe 3/02-10/04 9/08-3/09 112 4977 0.80 0.20 8.64 62.89 45.21 3!aohegoua 7/05-4/07 33 1008 0.99 50.60 23.81 43.65 4.Wanglang 9/04-10/05 6/08-11/08 120 4260 3.99 69.48 16.90 12.68 5.Xiaohegou 9/08-11/08 15 587 170 107.33 25.55 8.52 6.Xuebaoding 4/08-5/07 23 526 19.01 91.26 89.35 39.92 Qionglai 7,Wolong 8/05-5/07 10/08-3/09 56 2032 7.87 2.46 79.72 83.66 154.04 8.Anzihe 4/08-1/09 5 506 65.22 41.50 23.72 Xiangling g.Yele 6/08-12/08 26 547 1.83 731 89.58 14.63 Liangshan lO.Shenguozhuang 6/08-11/08 12 271 3.69 33.21 3.69 II.Mamize 4/08-8/08 5 130 69.23 15.38 "Timber area managed by a local timber company, stopped logging in 1998 and initialized wildlife monitoring in 2004. " Include the sample sites that are above tree-line. Ogden UT) was placed in front of the camera unit to attract the animal in the focal area to ensure photographs. The camera units were checked at the end of one-month sampling duration and moved to the next block after changing batteries, films, or memory cards if needed. The ani- mals in each photograph were identified to species by the authors and input to a MS Access database to track the date, GPS lo- cation, elevation, and habitat information of each photographic record. Photographic rate was calculated for each felid species, as well as potential small, medium and large prey species. We defined the photographic rate as: # independent detection/1000 camera-days where the independent detection of a spe- cies was defined as one photograph of the species taken during a 30-minute period at one camera site. Consecutive photographs of the same species within 30 minutes were considered a single detection. Small prey were those prey species with a body weight < 5 kg, medium prey were those species whose body weight 5-20 kg, and large prey were considered those species whose body weight > 20 kg. We tested the correlation between the photographic rates and the sampling ef- fort (number of camera-days) for all felids, and the correlation between the photogra- phic rates of felids and their prey. For this analysis, we combined the three southern nature reserves (Yele, Shenguozhuang and Mamize) due to low sampling effort in each individual reserve, and excluded the sample sites that were above tree-line. All variables were examined for normal distribution pri- or to analysis and no transformations were needed. Result From 2002-2009, 461 1x1 km2 blocks in 11 nature reserves were surveyed for a total sampling effort of 19,151 camera-days (Fig. 1, Table!), among which 6 blocks were abo- ve tree-line. The 11 surveyed reserves were not evenly sampled (sampling efforts varied from 130-4977 camera-days) due to logistic reasons. Tangjiahe, Changqing, Wanglang, and Wolong were the reserves with most sampling efforts (>2000 camera-days). Four felid species were detected during our survey: snow leopard [n = 2 sites, >3 indivi- duals, 1 reserve), leopard (n = 1 site, 1 indi- vidual, 1 reserve), Asiatic golden cat (n = 4 sites, 2 reserves), and leopard cat (n = 45 sites, 9 reserves) (Fig. 2-5). Leopard cat, the smallest but most detected species, was re- corded at 9 out of the 11 reserves. The ave- rage photographic rate of leopard cat among these reserves was 5.03 (range 0.80-19,01). Large- and medium-sized felids (i.e., leo- pard, snow leopard, and Asiatic golden cat) were only detected in Changqing, Tangjiahe, and Wolong with rather low photographic rates. Changqing Nature Reserve detected the most felid species (i.e., leopard, Asiatic golden cat, and leopard cat), followed by Wolong Nature Reserve (i.e., snow leopard and leopard cat) and Tangjiahe Nature Re- serve (i.e., Asiatic golden cat and leopard cat). The sampling effort (number of came- ra-days) prior to detection of felid species varied broadly among our survey reserves, from 50-1250 (average 200) camera-days for leopard cats to 600-5000 camera-days for the medium- and large-sized felids (Table 1), but there was no significant difference bet- ween small, medium- and large-sized felids (independent-samples t test, t - 1.170, v = 2.037, p - 0.361). No medium- or large-sized felids were detected in the three southern reserves {i.e., Yele, Shenguozhuang, and Mamize). Small prey detected in our survey included pheasant and grouse species, pika Ochotona spp., wooly hare Lepus oiostolus, small ro- dents, and squirrels. Medium prey included short-tailed porcupine Hystrix brachyura, hog badger Arctonyx collaris, golden monkey Hhinopithecus roxeliana, macaque Macaca spp., tufted deer Elaphodus cephalophus, Reeve's muntjac Muntiacus reevesi, and fo- rest musk deer Moschus berezovskii. Large 21 CATnews 52 Spring 2010 Sheng Li et al. prey detected were wild boar Sus scrota, blue sheep Pseudois nayaur, goral Naemor- hedus goral, Chinese serow Capricornis mil- needwardsii, and takin Budorcas taxicolor. Changqing Nature Reserve had the highest photographic rate of large prey, followed by Wolong and Tangjiahe Nature Reserves (Table 1). In the two southern reserves of Liangshan mountains (i.e., Shenguozhuang and Mamize), no large prey species were detected. We found no significant correlation bet- ween the sampling effort and photographic rates of small felid (leopard cat, Pearson test, r - 0.409, p = 0.667, n = 9), or medium- and large-sized felids (e.g. leopard, snow leopard and Asiatic golden cat combined, Pearson test, r - 0.763, p = 0.100, n= 9). We also found no significant correlation bet- ween the photographic rates of small felid (leopard cat) and small prey (Pearson test, r = 0.767, p = 0.319, n = 9), but a positive correlation among the photographic rates of medium- and large-sized felids and large- sized prey [Pearson test, r - 0.821, p = 0.047, n = 9). nn Discussion Our surveys provide current information on the status of felids and their prey within the study area. Our record of snow leopard in Wolong Nature Reserve (Fig. 2) was the first photographic evidence of this endan- gered species at the southeast edge of its distribution (Nowell & Jackson 1996, IUCN 2009). The photograph of an Asiatic golden cat at Tangjiahe Nature Reserve showed a rare coat pattern with rosettes and spots, which is the first field photo of this pheno- type in China and only occasionally reported elsewhere (Nowell & Jackson 1996, Wang 2007, Wilson & Mittermeier 2009, Fig. 3). These preliminary results indicate extending the sampling effort of these surveys would benefit felid research and conservation in China. There are three potential reasons under- lining the spatial pattern in our survey, in which more felids were detected in northern than in southern reserves: 1) sampling effort; 2) prey abundance; and 3) poaching pressu- re on these felids. We found no significant correlation between sample effort and car- nivore abundance but our sample effort was lowest in the south. Camera-trapping is con- sidered the most effective methodology to detect the presence of wild felids (Cutler & Swann 1999, Karanth & Nichols 1998), but nondetection cannot be directly considered absence, especially when the sampling ef- fort is low. Previous studies show that the number of camera-days required for de- tection of rare felid species varies broadly (e.g., 230-2945 camera-days for tiger and 16-4418 camera-days for clouded leopard in southeast Asia; Datta et al. 2008), so its possible our sampling effort in southern reserves (130-547 camera-days) was insuf- ficient to detect rare large felids. However, this sampling effort was sufficient to detect large mammals in the northern reserves and in other regional studies conducted by this research team (Wang et al. 2006, Li et al., in press), but detected no large prey spe- cies in these southern reserves, a finding in agreement with informal interviews with local people. Large mammals are probably missing from these reserves because most of the nature reserves in Xiangliang and Li- angshan mountains were established from 1993 to 2002 after a long history of commer- cial timber logging, and no control over har- vest of both the felids and their prey. Of our three probable reasons for lack of detection in these southern reserves, we consider low survey effort the least likely. All the surveyed nature reserves have an official mammal species list generated from baseline investigation and historical litera- ture. Two to seven felid species are listed in each nature reserve's formal species list (S0M T1), though there may be no evidence for the presence of some species within the reserve in recent decades. For example, six felid species are on the baseline species list of Tangjiahe (Hu 2005), but no photographs, sightings or dead/captured animal have been reported for three species (i.e., clou- ded leopard, Eurasian lynx, and Pallass cat) since the reserve was established in 1978 (Liu X., pers. comm.). Our large sampling effort (approximate 5000 camera-days), covering all possible habitat types within this 300 km2 reserve, indicates a conspicu- ous gap between the felid species detected and the official list maintained by the reser- ve. Similar discrepancies exist in all other surveyed reserves. During the 3rd National Giant Panda Survey from 1999-2003, only three felid species (i.e., leopard, Asiatic gol- den cat and leopard cat) were detected with an extensive sampling effort of 11,174 sign transects throughout the giant panda di- stribution (SPA 2006). Among the nine felid species historically recorded within current giant panda range (SOM Tl), the tiger has been probably extinct since the late 20th century (IUCN 2009), and the record of Chi- nese mountain cat remains doubtful (He et al. 2004). Though our camera-trapping effort didn't cover all possible felid habitat types in some reserves (e.g. above treeline), our results do highlight the need for detailed survey of felids in the major reserves rather than reliance on the reserve species lists to determine carnivore status and distribution. Studies on the distribution range of each in- dividual felid species need to be conducted prior to setting felid conservation goals in China. We think a well-designed systemic monitoring network using camera-trapping would be the best approach to obtain such information (Li et al., in press). Although none of our surveyed nature reser- ves were established for the conservation of felids, the giant panda may serve as an um- brella species for the sympatric felids and their prey (Schaller 1994, Lu et al. 2000). Ne- vertheless, there may be size limitations for reserves established for giant pandas that render the reserves of insufficient area for large carnivore species. Large felids normal- ly maintain low densities due to social inter- actions and large home ranges for foraging requirement. For example, the home range of individual snow leopard (McCarthy et al. 2005) and leopard (Norton & Lawson 1985) can exceed 500 km2, whereas the average size of giant panda reserve is 544 km2 (ran- ge: 83-4069 km2, SPA 2006). The area nee- ded to support a viable population for these large felids may require several adjacent nature reserves. Isolated reserves, such as those in the southern mountains, may be in- sufficient in size for large felid conservation. For an effective conservation of felid spe- cies, adjacent giant panda reserves should be considered an integrated management unit with connectivity between reserves of primary concern. Acknowledgements This study was financially supported by Smithso- nian National Zoological Park, Peking University, Shanshui Conservation Center, Conservation In- ternational and World Wildlife Fund. We thank Sichuan Forestry Department, Shaanxi Forestry Department, and local forestry bureaus for permis- sions and logistical support. We thank the staff of all involved nature reserves for their contribution on project management, field work, data collection and logistics. We cannot collect these high quality data without their hard work and effort. We also thank James Sanderson, Shu-Jin Luo, Li Zhang, CATnews 52 Spring 2010 cats living with pandas Eva Jutzeler, Urs Breitenmoser and an anonymous reviewer for reviewing our manuscript and provi- ding valuable comments. References Cam T. 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Handbook of the mammals of the world, Vol. 1: Carni- vores. Lynx Ediciones, Barcelona. Supporting Online Material SOM Table Tl at www.catsg.org College of Life Sciences, Peking University, Beijing, China;' corresponding author Smithsonian Conservation Biology Institute, National Zoological Park, USA Shanshui Conservation Center, Beijing, China 23 Fig. 4. Asiatic golden cat (spotted moiph), Tangjiahe NR, 2008 Fig. 5. Leopard cat, Wanglang NR, 2004 CATnews 52 Spring 2010