The northern white-cheeked gibbon Nomascus leucogenys, which occurs in Vietnam, Lao PDR and China, is categorized as Critically Endangered on the IUCN Red List (IUCN, 2011). In China this species was once widely distributed in Mengla, Jiangcheng and Luchun counties, in south Yunnan, between the Lancang River (Mekong River) and the Yuan River (Red River; Ma & Wang, Reference Ma and Wang1986). Its population was estimated to be > 1,000 in the 1960s (Tan, Reference Tan1985) but by the 1970s its morning calls could no longer be heard in the county town of Mengla (Gao et al., Reference Gao, Wen and He1981). In the 1980s the population declined to c. 100 individuals as a result of deforestation and the expansion of rubber plantations, and the species only survived in Mengla County (Tan, Reference Tan1985; Yang et al., Reference Yang, Zhang and Li1985; Fooden et al., Reference Fooden, Quan and Luo1987; Ma & Wang, Reference Ma and Wang1988). By the late 1980s the population had declined to 36 individuals in nine groups in Mengla and Shangyong Nature Reserves (Hu et al., Reference Hu, Xu and Yang1989; Fig. 1). A field survey in 2003 confirmed that N. leucogenys had disappeared from Huanglianshan Nature Reserve, Luchun (Ni & Jiang, Reference Ni and Jiang2009).
In December 2008 we interviewed 78 people, mostly nature reserve rangers and former hunters, in 34 villages inside and in the vicinity of Mengla Nature Reserve (113,880 ha) and Shangyong Nature Reserve (33,307 ha), which were thought to hold the last remaining N. leucogenys population in China (Yang et al., Reference Yang, Zhang and Li1985; Hu et al., Reference Hu, Xu and Yang1989). Only three interviewees reported having seen or heard gibbons, at three different places within the Reserves (Zhaokanliang, Leigongyan and Nangongshan; Fig. 1), between 2006 and 2008 (Fan & Huo, Reference Fan and Huo2009).
We conducted a field survey in Zhaokanliang and Leigongyan during 7–23 December 2011. During this time we interviewed five more hunters, all of whom confirmed that they had not seen or heard gibbons in Nangongshan for 20 years, and therefore we did not survey this site.
In Zhaokanliang and Leigongyan an auditory survey technique was employed to assess the occurrence and population size of gibbons (Brockelman & Srikosamatara, Reference Brockelman and Srikosamatara1993). We set three or four listening posts 400–1,300 m apart on mountain ridges at each site to cover all areas that potentially supported gibbons (Table 1). One or two surveyors occupied each listening post from c. 7.00 (before sunrise) to 12.00 for 5 consecutive days. We also recorded signs of human disturbance (grazing, hunting, logging and agriculture) and any large animals.
During the survey we did not hear or see any signs of gibbons. On 11 December we saw a group of 20–30 macaques Macaca mulatta and, in Zhaokanliang, some fresh footprints of gaur Bos gaurus. No evidence of logging or agriculture was found at either site but local people grazed buffalos in Zhaokanliang. Illegal hunting was common at both sites. We heard 33 gunshots in 5 days and saw five hunters carrying a total of four guns on 11 December in Zhaokanliang. We heard 15 gunshots and saw eight campsites used by hunters in Leigongyan. We saw four hunters with a total of three guns on 23 December in Leigongyan; they had killed one Phayre's leaf monkey Trachypithecus phayrei, two silver pheasant Lophura nycthemera, one rufous-throated hill partridge Arborophila rufogularis, one giant flying squirrel Petaurista philippensis and an unidentified mammal.
It is possible that some gibbons still occur in these nature reserves and remained undetected by us, but the possibility is low. Habitat loss, degradation and fragmentation caused by deforestation and the expansion of rubber plantations between the 1960s and the 1980s have been reported as the main causes of the decline in the gibbon population in the area (Tan, Reference Tan1985; Yang et al., Reference Yang, Zhang and Li1985; Fooden et al., Reference Fooden, Quan and Luo1987; Ma & Wang, Reference Ma and Wang1988). In 1989 there were only 36 gibbons in nine groups, at seven sites isolated by roads and villages, in Shangyong and Mengla Nature Reserves (Hu et al., Reference Hu, Xu and Yang1989). The biggest subpopulation comprised eight individuals in two groups and was vulnerable to illegal hunting. We heard gunshots every day during this survey. The Yao and Aini ethnic groups hunt all large mammals in the reserves, including tiger Panthera tigris, elephant Elephas maximus, and gaur. They also hunt gibbons for food and traditional medicine (Fan & Huo, Reference Fan and Huo2009).
Although tiger, elephant, gaur and gibbon are all Class I Protected Animals in the Chinese Wildlife Conservation Law, illegal hunting of these animals occurs in nature reserves because of low awareness, poverty of local communities and poor management of the reserves. Without effective protection the small subpopulations recorded in the 1980s had little chance of survival under hunting pressure. By 2008 only three sites might still have supported very small populations of gibbons (Fan & Huo, Reference Fan and Huo2009). In Zhaokanliang and Leigongyan only one individual was seen by local people between 2006 and 2008. Even if individuals survived and simply remained undetected during our survey it is unlikely that the species could survive in the long term.
Given the absence of gibbons inside Mengla and Shangyong Nature Reserves and in Huanglianshan National Nature Reserve (Ni & Jiang, Reference Ni and Jiang2009) their chance of survival in unprotected forest is low. No gibbons have survived outside nature reserves in south-east Yunnan in recent years except for a population of four individuals in Bajiaohe, reported in 2009 (Ni & Jiang, Reference Ni and Jiang2009). In Bajiaohe killing a gibbon is considered a bad omen by local people. We conclude that N. leucogenys is extinct, or at least ecologically extinct, in China.
China once supported one of the world's richest gibbon faunas, with three genera and six species (Hylobates lar, Nomascus concolor, Nomascus nasutus, Nomascus hainanus, N. leucogenys, and Hoolock leuconedys; Geissmann, Reference Geissmann2007), second only to Indonesia (Grueter et al., Reference Grueter, Jiang, Konrad, Fan, Guan and Geissmann2009). However, H. lar and N. leucogenys now appear to be extinct from China (Grueter et al., Reference Grueter, Jiang, Konrad, Fan, Guan and Geissmann2009; present study), and small population size, habitat fragmentation and illegal hunting put all of China's remaining gibbon populations on the edge of extinction (Jiang et al., Reference Jiang, Luo, Zhao, Li and Liu2006; Fan et al., Reference Fan, Xiao, Huo, Ai, Wang and Lin2011). The small population of Hainan gibbons has been recovering following strict enforcement of anti-poaching measures in 2003 (Fellowes et al., Reference Fellowes, Chan, Zhou, Chen, Yang and Ng2008). Conservation activities aimed at saving the remaining gibbon populations include education to raise the awareness of the public and government, sustainable development of local communities, improved management of reserves, and monitoring and research to safeguard existing groups (Chan et al., Reference Chan, Fellowes, Geissmann and Zhang2005; Fellowes et al., Reference Fellowes, Chan, Zhou, Chen, Yang and Ng2008).
Acknowledgements
This study was supported by the Gibbon Conservation Alliance and Dali University. The survey was conducted with the permission of Xishuangbanna National Nature Reserve. We thank the survey participants, and we are grateful to Dr Thomas Geissmann for editing this manuscript.
Biographical sketches
Peng-Fei Fan has been studying the behavioural ecology and conservation biology of gibbons in China for 10 years. He has studied Nomascus concolor in the Wuliang Mountains, N. nasutus in Bangliang and H. leuconedys in Gaoligongshan. He has also surveyed N. leucogenys in Xishuangbanna, N. hainanus in Bawangling and H. lar in Nangunhe Nature Reserve. Han-Lan Fei studied N. nasutus in Bangliang for 1 year and is now studying H. leuconedys in Gaoligongshan. Ai-Dong Luo is a wildlife conservationist working in Xishuangbanna Nature Reserve.