<<

Transboundary conservation of the last remaining population of the cao vit nasutus

C HANG- YONG M A * ,HOANG T RINH-DINH* ,VAN-TRUONG N GUYEN T RONG-DAT L E ,VAN-DUNG L E ,HUU-OANH L E ,JIANG Y ANG Z I -JIE Z HANG and P ENG-FEI F AN*

Abstract The cao vit gibbon Nomascus nasutus, also known Introduction as eastern black crested gibbon, is categorized as Critically Endangered on the IUCN Red List and was considered olitical borders rarely coincide with the natural one of the world’s  most threatened . The only Pboundaries of wildlife populations (Vitkalova et al.,  known population occurs along the border between ) and often artificially separate populations. and Viet Nam. Accurate information on population size and Transboundary populations that live along international dynamics is critical for the species’ conservation, but popu- borders are often subject to different management regimes  lation surveys conducted in only one country may over- on each side of the border (Gervasi et al., ; Linnell et al.,   or underestimate total population size because the home ; Thornton et al., ). Language barriers, lack of trust, ranges of cao vit gibbon groups often cross the international and differences in sampling designs and data collection border. In  and  we conducted two collaborative protocols can make transboundary information exchange  transboundary censuses of the cao vit gibbon populations difficult (Vitkalova et al., ), hindering the effective in the Trung Khanh Cao Vit Gibbon Species and Habitat conservation of such populations. Conservation Area in Viet Nam and the Bangliang The cao vit gibbon or eastern black crested gibbon Gibbon National Nature Reserve in China. The results Nomascus nasutus was once widespread in south China  showed a population size of – in , which in- and north-east Viet Nam, east of the Red River (Tien ;   creased to – in . Our results indicate that previous Geissmann et al., ; Rawson et al., ). Hunting and surveys conducted separately in Viet Nam and China habitat loss have led to a dramatic population decline   underestimated the global population size of this species. (Geissmann et al., ) and by the s the cao vit According to our more comprehensive surveys, the gibbon gibbon was thought to be extinct in both countries (Tan,   population is increasing slowly. The and their ; Geissmann et al., ). The species was rediscovered  habitat are legally protected in both countries. Hunting in in a small karst forest patch in Trung Khanh and charcoal making have not been reported in this area District, Cao Bang Province, Viet Nam, close to the  since . As habitat carrying capacity is a limiting factor, Chinese border (La & Trinh Dinh, ; Geissmann et al.,   habitat restoration is required. However, lack of funding to ). In the species was observed in the same forest  protect the cao vit gibbon remains a challenge. patch on the Chinese side (Chan et al., ), making it a transboundary population. Keywords Cao vit gibbon, China, Nomascus nasutus, popu- Because only one small population survives, the cao vit lation size, threats, transboundary conservation, Viet Nam gibbon is considered the second rarest species. Only Supplementary material for this article is available at the Hainan gibbon Nomascus hainanus has a smaller popu-   https://doi.org/./S lation size (ca. individuals; Bryant et al., ). The cao vit gibbon is categorized as Critically Endangered on the IUCN Red List (IUCN, ) and was considered one of the world’s  most threatened primates during – (Mittermeier et al., , , ). The species’ habitat CHANG-YONG MA and PENG-FEI FAN (Corresponding author) School of Life has been seriously degraded as a result of selective logging, Sciences, Sun Yat-sen University, No. 135, Guangzhou, 510275, China E-mail [email protected] charcoal making, farming and livestock grazing (Fan et al., ). To conserve the last population of the cao vit gibbon, HOANG TRINH-DINH,VAN-TRUONG NGUYEN,TRONG-DAT LE,VAN-DUNG LE and HUU-OANH LE, Fauna & Flora International—Viet Nam Programme, Hanoi, the Vietnamese government established the Trung Khanh Viet Nam Cao Vit Gibbon Species and Habitat Conservation Area in JIANG YANG The Administration Bureau of Guangxi Banglinag Gibbon National , and the Chinese government set up the Bangliang Nature Reserve, Jingxi, China Gibbon Autonomous Nature Reserve in  and upgraded ZI-JIE ZHANG Fauna & Flora International—China Programme, Nanning, China it to national protection level in  (Fig. ). *Contributed equally. Accurate information on population size and dynamics Received  October . Revision requested  November . is critical for conservation of threatened species. However, Accepted  December . First published online  September . population surveys conducted on only one side of a political

Oryx, 2020, 54(6), 776–783 © 2019 Fauna & Flora International doi:10.1017/S0030605318001576 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 30 Sep 2021 at 03:33:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001576 Conservation of the cao vit gibbon 777

FIG. 1 The study site and survey posts in the Trung Khanh Cao Vit Gibbon Species and Habitat Conservation Area, Viet Nam, and the Bangliang Gibbon National Nature Reserve, China.

border may overestimate total population size as individuals Nature Reserve in Guangxi Province, China, and the Trung or groups travel across the border and are counted by both Khanh Cao Vit Gibbon Species and Habitat Conservation countries (Vitkalova et al., ), and researchers may Area in Cao Bang Province, Viet Nam (Fig. ). The study underestimate total population size because areas adjacent area is characterized by a typical karst limestone landscape to political borders are avoided because of security con- consisting of densely packed outcrops, sharp-peaked moun- cerns. Since the rediscovery of the cao vit gibbon in , tains with steep slopes, ridges and vertical cliffs, interspersed several surveys and censuses have been conducted on the with lowland valleys. Altitude is – m and the vegeta- Vietnamese side of the border in the Trung Khanh Cao tion is monsoon tropical forest that has been degraded Vit Gibbon Species and Habitat Conservation Area. These by selective logging, fuelwood collection, charcoal making, surveys recorded a population with – individuals in and agriculture prior to the establishment of the nature re-  (Geissmann et al., ),  in  (Trinh Dinh, serves (Fan et al., ). On the Chinese side of the border, ), and – in  (Vu et al., ). These surveys  tree species and  woody liana and epiphyte species underestimated the species’ population size because three were recorded in   ×  m plots, and mean canopy more groups also exist on the Chinese side, as was discov- height was . m (Fan et al., ). Diversity of tree and ered in  (Chan et al., ). woody liana species was higher in the valleys and slopes To obtain an accurate estimate of the total population than on the cols and ridges (Fan et al., ). Previous studies size of the cao vit gibbon, two transboundary censuses found cao vit gibbons consumed foods from .  tree and were conducted, in  and , by the Management liana species, with  species accounting for .% of total Board of Trung Khanh Cao Vit Gibbon Species and feeding time (Fan et al., ). Fruits made up % of the Habitat Conservation Area and the Administrative Bureau gibbons’ diet, and leaves and buds accounted for . and of Bangliang Gibbon National Nature Reserve, with the .%, respectively (Fan et al., ). No comparable informa- support of Fauna & Flora International (FFI) Viet Nam and tion is available for Vietnamese cao vit gibbon groups, but China Programmes. Here, we report the results of these sur- we assume that habitat quality and gibbon ecology and veys, analyse population trends since the species’ rediscovery, behaviour are similar on both sides of the border. discuss factors that limit gibbon population increase, and propose potential solutions. Methods

Study area We applied auditory techniques that were developed especially for gibbon surveys (Brockelman & Ali, ) We conducted surveys along the Chinese and Vietnamese and were used in this area in previous surveys (Geissmann international border in the Bangliang Gibbon National et al., , ; Chan et al., ). In  we set up 

Oryx, 2020, 54(6), 776–783 © 2019 Fauna & Flora International doi:10.1017/S0030605318001576 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 30 Sep 2021 at 03:33:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001576 778 H. Trinh-Dinh et al.

TABLE 1 Survey results for the cao vit gibbon Nomascus nasutus population in  and .

No. of gibbon No. of transitory Total no. of No. of No. of Year groups individuals individuals Country Survey dates surveyors listening posts 2007 17–18 0 102–110 Viet Nam 07–19 Sep. 22 18 China 07–14 Sep. 17 6 2016 20–22 3–4 107–136 Viet Nam 11–24 Sep. 31 21 China 11–16 Sep. 16 8

survey posts in Viet Nam and six in China (Supplementary start and end time of the sighting, and the direction and dis- Table ), located on outcrop peaks and ridges, where we tance of the gibbons from the researchers. We also recorded could record gibbon vocalizations from several nearby val- the group size and composition (including adult male, adult leys. The surveys posts covered all potential gibbon habitats female, juvenile and infant), to distinguish between neigh- (Fan et al., ) and all locations where gibbons had bouring groups. Adult male cao vit gibbons were defined been recorded during previous surveys and routine patrols. as fully grown and black in colour. Adult females are yellow In  we used the same survey points from  and with a white facial ring and a large black crest extending set up three new posts in Viet Nam and two in China from head to the centre of their back. Juveniles are black, (Supplementary Table ), to sample an area of regenerating smaller than adult males, and fully independent from habitat that was considered suitable for gibbons (Fig. ). their mother. Infants are black and still dependent on The survey dates and number of researchers involved in their mother (Mootnick & Fan, ). In addition, we also the surveys are presented in Table . To ensure that the field recorded floating individuals; i.e. young adults that have teams used the same techniques for all surveys, all research- emigrated from their natal group and, at least temporarily, ers attended a -day training course prior to the field sur- live on their own. veys, although most had already participated in previous To avoid double counting groups that live along the gibbon surveys in this area and were familiar with the mor- border and could be heard simultaneously by both teams, phological characteristics and calls of cao vit gibbons. researchers from both countries exchanged and discussed A previous study of three groups found cao vit gibbons survey results after the field surveys, in May  and vocalized mostly (.% of recorded calls) in the mornings, October . We calculated mean group size based on from  minutes before to  hours after sunrise (Fei et al., groups that had been observed and counted, and then multi- ). Individual groups vocalized on a mean of .% plied mean group size by the number of groups to estimate of all monitoring days and the mean number of singing total population size. bouts on days when they did vocalize was . per day (Fei et al., ). As the sun rises at c. . in September in our survey area, we monitored all survey points during .– Results . for at least – successive days. We occasionally occu- pied the survey points until . to observe gibbons when Population size of cao vit gibbons they were foraging nearby. Once the gibbon songs were The combination of listening and sighting information from heard, researchers recorded the date, location of survey the surveys indicated there were – groups in  and posts, direction and estimated distance between survey – groups in  (Table ). In addition, we recorded posts and gibbon groups, and the start and end time of – floating individuals in  (none were recorded in each song bout. We recorded the call type and the number ). During the survey we counted all members of  of individuals producing a particular type of call. Call types groups in , and of  groups in . The mean group included duet song bouts, male solo song bouts, female solo size was . ± SD . (n = , range –)in, and song bouts, isolated great-calls, and alarm calls (Feng et al., . ± SD . (n = , range –)in (Tables  & ). ). Song bouts or isolated great-calls were defined as Consequently, the estimated population size was – distinct vocalization events if they were separated from in  and – in  (Table ). previous calls by an interval of at least  minutes. During the survey, we tried to locate and observe gibbon groups if they were calling close to the survey points. Group structure of cao vit gibbons Because gibbons are canopy dwellers and canopy height is low in our study area, researchers could observe gibbons Most groups had two adult females ( of  fully observed from survey points using binoculars (Fan et al., , groups in , and  of  groups in ). In ,we ). Once we located a gibbon group, we recorded the recorded one group with three females. Two females both

Oryx, 2020, 54(6), 776–783 © 2019 Fauna & Flora International doi:10.1017/S0030605318001576 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 30 Sep 2021 at 03:33:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001576 Conservation of the cao vit gibbon 779

TABLE 2 Group composition of cao vit gibbons recorded in .

Group composition Immature Group Adult male Adult female Adolescent Infant Total Record1 Locality2 G13,4 1 2 4 1 8 L, O North of Lung Gu G23 1 2 2 1 6 L, O West of Lung Gu G33,4 1 2 2 5 L, O West of Lung Nha Nhung G43 1 2 3 1 7 L, O West of Lung Ky Gia G5 2 2 2 1 7 L, O North of Lung Nguom G6 1 2 2 5 L, O West of Lung Chi G7 3 2 1 1 7 L, O North-west of Lung Che G8 2 2 3 2 9 L, O North of Lung Dac G9 1 1 1 3 L, O East of Lung Dac G10 1 1 1 3 O South-west of Lung Co (Nguom Dam) G114 1 2 (3)5 L South-east of Lung Hoai G12 2 2 2 6 L, O West of Lung Nam (Tap Toan) G13 2 2 3 2 9 L, O North-west of Tap Toan Lon G143 1 2 2 2 7 L, O Between Nguoc Man & Nguoc Ri G15 3 2 2 1 8 L, O Lung Gia Ray G16 2 2 2 2 8 L, O Lung Bong Bip G17 1 1 1 3 L, O Lung Tu Noc G18 1 1 (2)5 L, O China only

 L, listening; O, observation.  Local name of the valley.  These groups’ home ranges overlapped the border.  The total number of individuals in these groups is uncertain because they were observed only briefly or were not seen at all (group record based on vocalization only).  The number in parentheses is the minimum number of gibbons in this group (for groups that were observed only briefly and not all members could be counted, or where group size was estimated by vocalization only).

carrying infants were observed in four of the  bi-female the steep karst hills and low canopy, an unusual habitat groups in .In we recorded only one group with for gibbons, facilitated gibbon detection in this area. We two females that both carried infants. In  seven of  observed most groups while they were singing (Tables  & ). fully observed groups contained more than one adult In addition, we had monitored the population dynamics male. In  only one of  fully observed groups contained of gibbons on the Chinese side of the border every more than one male. month since December  and knew each of these groups, so this subpopulation provided a good control to evaluate the detection rate for our field surveys. We Discussion did not miss any known groups on the Chinese side during the surveys.  Global population size of the cao vit gibbon Based on the transboundary survey in we estimated the global population of cao vit gibbon to be .  indivi- Our results indicate the presence of c.  cao vit gibbon duals. However, population surveys recorded fewer than  groups with a total population size of .  individuals dur- individuals in Viet Nam prior to  (reported population ing the  and  surveys. It is unlikely that we missed sizes were –,  and – in studies by Geissmann et al., any groups living in this area, for a number of reasons. ; Trinh Dinh, ; and Vu et al., , respectively) Firstly, our survey posts covered all potential gibbon and only  individuals in China in  (Chan et al., habitats in the study area. Secondly, during a study of ). It is unlikely that the gibbon population doubled three cao vit gibbon groups, individual groups sang on during –. Cao vit gibbons mature at – years c. % of monitoring days (Fei et al., ). We monitored of age and the interbirth interval is – years (Fan et al., each survey point for – consecutive days. According to a ). The long juvenile period and long interbirth interval detection function, the chance of detecting a group during make gibbon population recovery a slow process. We there-  a -day survey is  − ( − .) . .. In addition, we fore conclude that surveys before  must have underes- conducted surveys in September, when cao vit gibbons timated the population size, possibly because they did not vocalize most frequently (P.F. Fan, unpubl. data). Thirdly, cover the area completely. For example, the three groups

Oryx, 2020, 54(6), 776–783 © 2019 Fauna & Flora International doi:10.1017/S0030605318001576 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 30 Sep 2021 at 03:33:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001576 780 H. Trinh-Dinh et al.

TABLE 3 Group composition of cao vit gibbons recorded in .

Group composition Immature Group Adult male Adult female Adolescent Infant Total Record1 Locality2 G1 4 2 1 7 L, O Lung Ky Gia G2 3 1 1 1 6 L, O Lung Ky Gia G33 1 1 2 1 5 L, O Lung Nguom G4 1 24 (3)5 L Lung Thenh, Lung Chi, Lung Kep That, Lung Chi Dong G5/24 1 2 2 1 6 L, O Lung Ky Gia G6 1 1 1 1 4 L, O Lung Bong Bip G77 1 2 4 1 8 L, O Lung Gu Nho G8 1 2 2 1 6 L, O Lung Nguom, Nguoc Man, Gia Ray G9 1 2 5 8 L, O Lung Day G10 1 24 (3)5 L Lung Tong On, Lung Dac G11 1 2 5 8 L, O Lung Che, Lung Day, Lung Dac Dong G12 1 2 2 1 6 L, O Lung San, Lung Chai Khuyet, Lung Co next to Lung Dac G138 1 1 1 (3)5 L Lung Co, Lung Dac, Lung Tam Deng G14 1 1 (2)5 L Lung Hoai, Lung Tau Lo, Lung Tong On G15 1 2 3 2 8 L, O Lung Tap, Lung Nam G167 1 2 2 5 L, O Lung May Ri G17 1 14 (2)5 L Lung Ngu Khop G18 1 2 2 1 6 L, O Lung Nam G197 1 2 2 5 L, O Nonglaolang (China only) G207 1 3 3 1 8 L, O Lung Ky Gia, Lung Ky Gia Nho G219 1 2 1 4 L, O Nongnianda, Nongnianxiao (China only) G2210 2 2 1 (5)5 L, O Lung Tong On 1 1 L Lung Gia Ray (near Lung Nguoc Man) 111 1 O Lung Ky Gia 1 1 L, O Lung Ky Gia 18 1 L, O Nongkou (China only)

 L, listening; O, observation.  Local name of the valley.  We were not able to count all gibbons in the group. There were at least three black individuals and a yellow female with an infant.  The number of females was uncertain.  The number in parentheses was the minimum number of gibbons in this group (for groups that were observed only briefly and not all members could be counted, or where group size was estimated by vocalization only).  Group  was possibly the same as Group  plus a female. These two groups were recorded in the same valley (Ky Gia) and it was not always possible to count all gibbons in a group during our observations.  These groups’ home ranges overlapped the border.  There was an immature male learning to sing.  These groups or individuals were recorded only in China.  Some individuals may have been missed during the observation and it is possible that this group was in fact Group  or Group .  A single female; it is possible that the animal just split from one of the groups in the valley.

discovered on the Chinese side close to the international third in  close to the border (Fan et al., ; Wei et al., border in  were not included in surveys in Viet Nam ; Ma Changyong, unpubl. data). In addition, five fe- (Chan et al., ). This supports our contention that unco- males from three groups gave birth to  infants during ordinated population surveys on only one side of the border –, but two infants died or disappeared (Fan et al., resulted in an underestimation of the population size. ). The mean interbirth interval for these  births was  Since  the cao vit gibbon population has been slowly months, which is comparable to other gibbon populations increasing. A Chinese research team led by PFF intensively (Fan et al., ). Although the cao vit gibbon population monitored gibbon population dynamics on the Chinese has been slowly increasing, this is the only known popula- side of the border since September . Three new groups tion of the species. Increased attention therefore needs to be formed during this period: one in ,asecondin and a focused on its conservation.

Oryx, 2020, 54(6), 776–783 © 2019 Fauna & Flora International doi:10.1017/S0030605318001576 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 30 Sep 2021 at 03:33:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001576 Conservation of the cao vit gibbon 781

Bi-female groups prevail amongst cao vit gibbons In rare situations, there could be three or even four adult- sized black individuals living in the same group. However, Although most gibbons live in monogamous groups, the based on behavioural observations, only one male mates majority of cao vit gibbon groups are polygynous and usu- with adult females in cao vit gibbon groups. This contrasts ally include two breeding females (Fan et al., , ; with bi-male lar gibbon and groups, in which both Guan et al., ; this study). The two adult females are adult males copulate with resident females (Lappan, ). generally nonaggressive towards each other and are com- monly observed grooming (Fan et al., ). In addition,  both females may breed at the same time (Fan et al., ). Transboundary conservation As a result, the mean group size of these bi-female groups was .–. individuals, which is comparable to bi-female Since the rediscovery of the cao vit gibbon in  in Viet groups of the western black crested gibbon Nomascus conco- Nam and  in China, no hunting of gibbons has been lor (Fan et al., ) and Hainan gibbon (Zhou et al., ), recorded in either country. The main threat to the species and larger than monogamous gibbon groups (normally with is habitat degradation caused by selective logging, charcoal four individuals, Bartlett, ). making, fuel wood collection and farming (Fan et al., ). During the  survey we observed one group with three Since the establishment of the Trung Khanh Cao Vit Gibbon females, which is rare in any gibbon population. We ob- Species and Habitat Conservation Area in Viet Nam and the served two groups with three females during the long-term Bangliang Gibbon National Nature Reserve in China, the behavioural study on the Chinese side of the border. In the gibbons and their habitat are legally protected. Logging, first group one female stayed in her natal group and replaced charcoal making, fuel wood collection and farming have an old female that was not her mother, so temporarily there been eliminated in the protected areas. Livestock grazing were three females in this group before the older female dis- is completely prohibited in the protected area in Viet Nam, persed. The second group contained an old female who had but still occurs inside the protected area in China. not given birth since  and lived in the group with a Since the rediscovery of the cao vit gibbon population, second adult female. In August , we identified a third conservation awareness education has been conducted female, a young adult, in this group. We are not certain annually with local communities in both Viet Nam and whether this young female was born in the group or immi- China. In addition, programmes that improved the liveli- grated into it. However, we have never observed a group hoods of the local people were implemented by local gov- with three adult females that all produced offspring. ernment and international NGOs, such as growing grass We recorded a mean of .–. infants per group for livestock, planting trees for firewood, expanding the (.–. infants per female) during our surveys. However, use of biogas, and the Community Seed Fund pilot the long-term monitoring of the gibbon population on the programme (FFI, ). Chinese side of the border indicates that females are breeding The governments of Viet Nam and China permit inter- at a rate comparable to that reported in other gibbon species national NGOs to conduct conservation projects in this area (. infants per female; Fan et al., ). A possible reason for and facilitate transboundary conservation of the cao vit gib- this discrepancy is that researchers may have misidentified bon. A memorandum of understanding between China older infants as small juveniles. As infants mature they spend and Viet Nam for cooperative conservation of the cao vit more time travelling independently from their mothers gibbon was signed by the Department of Forestry of (P.F. Fan & C.Y. Ma, unpubl. data), although they continue Guangxi Zhuang Autonomous Region and the Department to nurse. Thus, during a short observation period, an of Agriculture and Rural Development of Cao Bang older infant may be observed to travel independently and Province in . The two sides reached agreement on me- therefore be misidentified as a juvenile. chanisms of bilateral exchanges, collaborative approaches to Groups containing more than one adult male have been counter wildlife hunting, and emergency measures such as recorded in lar gibbons lar (Reichard et al., ) forest fire protection. Both countries take turns to host a and Symphalangus syndactylus (Lappan, ), joint meeting every  years, to exchange experience on mon- but are rare in Nomascus gibbons. During the  and itoring, programme management, public education, law en-  surveys we recorded few groups with more than one forcement and other aspects of daily administration. In fully grown adult male. Because we did not know the genetic addition, the two protected areas have held informal meet- relationships and life history of males, subadult males ings on the border twice per year since . Participants that are fully grown but remained in their natal groups from both contries did not need to apply for visas to travel may have been wrongly recorded as adults. Given that to the other country, which makes transboundary conser- there were two breeding females in most groups, one or vation flexible and cost-effective. A transboundary species both may have produced male offspring that could have conservation action plan – was developed for been subadult during our relatively short survey period. the cao vit gibbon. This includes plans to expand the

Oryx, 2020, 54(6), 776–783 © 2019 Fauna & Flora International doi:10.1017/S0030605318001576 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 30 Sep 2021 at 03:33:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001576 782 H. Trinh-Dinh et al.

conservation area, gibbon population and habitat monitor- Acknowledgements This work was carried out under the auspices ing, community development, publicity and education, sci- of the Conservation Projects of Fauna & Flora International entific research, and transboundary cooperation. (FFI) with funding from the FFI Species Fund and Arcus Foundation. The long-term field study in China was supported by the National Natural Science Foundation of China (#30900169; #31822049), the One Hundred Talent Program of Sun Yat-Sen Habitat restoration University, and the National Program for Support of Top-Notch Young Professionals in China. We thank Paul A. Garber for editing Fan et al. () evaluated habitat quality for the cao vit gib- the text, Liang Gang for supporting the surveys, and all survey participants for their contribution. bon population in both contries and suggested that the  remaining area of intact forest can support c. groups. Author contributions Study design and fieldwork: HTD, CYM, However, systematic habitat restoration in disturbed forests VTN, TDL, TCN, VDL, HOL, JY, ZJZ, PFF; data analysis and could increase suitable habitat to support  groups. The writing: HTD, CYM, PFF. current population size of – groups is approaching the Conflicts of interest None. estimated habitat carrying capacity. In saturated habitat with a high density of gibbon groups, transitory individuals are Ethical standards This research abided by the Oryx guidelines expected to replace resident individuals rather than establish on ethical standards. The research did not involve human subjects, new breeding groups (Brockelman et al., ). Two cases of experimentation with and/or collection of specimens. male replacement and one case of female replacement were recorded in two cao vit gibbon groups on the Chinese side of References the border, suggesting that this population is approaching

habitat carrying capacity (C.Y. Ma, unpubl. data). BARTLETT, T.Q. () The hylobatidae: small of Asia. In Primates To promote population recovery, Fan et al. () sug- in Perspective. nd edition (eds C.J. Campbell, A. Fuentes, gested habitat restoration. Three transboundary sympo- K.C. MacKinnon, R.M. Stumpf & S.K. Bearder), pp. –. siums on habitat restoration for the cao vit gibbon were Oxford University Press, New York, USA.  conducted, in ,  and , with the support of FFI BROCKELMAN,W.Y.&ALI,R.( ) Methods of surveying and sampling forest primate populations. In Primate Conservation in and the People Resources and Conservation Foundation. A the Tropical Rain Forest (eds C.W. Marsh & R.A. Mittermeier), framework for transboundary restoration of cao vit gibbon pp. –. Alan R. Liss, Inc., New York, USA. habitat was published in English in  and Chinese in  BROCKELMAN, W.Y., REICHARD, U., TREESUCON,U.&RAEMAEKERS, (FFI, ). Pilot habitat rehabilitation actions under this J.J. () Dispersal, pair formation and social structure in gibbons  – framework have been implemented at four sites, covering (Hylobates lar). Behavioral Ecology and Sociobiology, , .   BRYANT, J.V., BRULÉ, A., WONG, M.H.G., HONG, X., ZHOU, Z., HAN, . ha in China. Food trees for the gibbon have been planted W. et al. () Detection of a new Hainan gibbon (Nomascus in abandoned fields (. ha in six valleys) in the protected hainanus) group using acoustic call playback. International Journal area in Viet Nam (Uong Sy Hung, People Resources and of Primatology, , –. Conservation Foundation, pers. comm., ). Despite CHAN, B.P.L., TAN, X.F. & TAN, W.J. () Rediscovery of the these initial successes, the situation remains challenging Critically Endangered eastern black-crested gibbon Nomascus nasutus (Hylobatidae) in China, with preliminary notes on because habitat restoration requires time and continued population size, ecology and conservation status. Asian Primates funding. Progress and effectiveness of habitat restoration Journal, , –. and reforestation programmes need to be systematically FAN, P.F., JIANG, X.L., LIU, C.M. & LUO, W.S. () Polygynous evaluated. Livestock grazing continues inside protected mating system and behavioural reason of black crested gibbon reserves in China, and future research should examine the (Nomascus concolor jingdongensis) at Dazhaizi, mt. Wuliang, , China. Zoological Research, , –. potentially adverse effects of grazing on habitat restoration FAN, P.F., FEI, H.L., XIANG, Z.F., ZHANG, W., MA, C.Y. & HUANG,T. and gibbon recovery. () Social structure and group dynamics of the cao vit gibbon In summary, our results from two transboundary surveys (Nomascus nasutus) in Bangliang, Jingxi, China. Folia of the only known population of the Critically Endangered Primatologica, , –. cao vit gibbon indicate that previous surveys conducted sep- FAN, P.F., FEI, H.L., SCOTT, M.B., ZHANG,W.&MA, C.Y. () arately in Viet Nam and China have underestimated the glo- Habitat and food choice of the Critically Endangered cao vit gibbon (Nomascus nasutus) in China: implications for conservation. bal population of this species. According to the latest survey Biological Conservation, , –.  – ( ), this population is increasing slowly and has FAN, P.F., FEI, H.L. & MA, C.Y. () Behavioral responses of cao vit remaining groups containing c. – individuals. The gibbon (Nomascus nasutus) to variations in food abundance and gibbon population and its habitat in both countries are legally temperature in Bangliang, Jingxi, China. American Journal of  – protected and hunting and charcoal making have been Primatology, , . FAN, P.F., REN, G.P., WANG, W., SCOTT, M.B., MA, C.Y., FEI, H.L. eliminated in the past decade. As habitat carrying capacity et al. () Habitat evaluation and population viability analysis of is a limiting factor, habitat restoration needs to be expanded, the last population of cao vit gibbon (Nomascus nasutus): but lack of sufficient funding remains a major challenge. implications for conservation. Biological Conservation, , –.

Oryx, 2020, 54(6), 776–783 © 2019 Fauna & Flora International doi:10.1017/S0030605318001576 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 30 Sep 2021 at 03:33:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001576 Conservation of the cao vit gibbon 783

FAN, P.F., BARTLETT, T.Q., FEI, H.L., MA, C.Y. & ZHANG,W.() World’s  Most Endangered Primates –. IUCN/SSC Understanding stable bi-female grouping in gibbons: feeding Primate Specialist Group, International Primatological Society, and competition and reproductive success. Frontiers in Zoology, , . Conservation International, Arlington, USA. FEI, H.L., FAN, P.F., XIANG, Z.F., MA, C.Y., ZHANG,W.&HUANG,T. MITTERMEIER, R.A., SCHWITZER, C., RYLANDS, A.B., TAYLOR, L.A., () Effects of meteorological factors on singing behavior of CHIOZZA, F., WILLIAMSON, E.A. & WALLIS,J.() Primates in eastern black crested gibbons (Nomascus nasutus). Acta Peril: the World’s  Most Endangered Primates –. IUCN/ Theriologica Sinica, , –. SSC Primate Specialist Group, International Primatological Society, FENG, J.J., MA, C.Y., FEI, H.L., CUI, L.W. & FAN,P.F.() Call Conservation International, and Bristol Conservation and Science sonograms of eastern black crested gibbon (Nomascus nasutus). Foundation, Bristol, UK. Acta Theriologica Sinica, , –. MOOTNICK, A.R. & FAN,P.F.() A comparative study of crested FFI (FAUNA &FLORA INTERNATIONAL)() Cao Vit Gibbon gibbons (Nomascus). American Journal of Primatology , –. China- Trans-Boundary Conservation Action Plan – RAWSON, B.M., INSUA-CAO, P., NGUYEN, M.H., HOANG, M.D., . FFI Asia-Pacific, Hanoi, Viet Nam. MAHOOD, S., GEISSMANS,T.&ROOS,C.() The Conservation GEISSMANN, T., NGUYEN, X.D., LORMEE,N.&MOMBERG,F.() Status of Gibbons in Vietnam. Fauna & Flora International/ Vietnam Primate Conservation Status Review: Part . Gibbons. Conservation International, Hanoi, Viet Nam. Fauna & Flora International/Conservation International, Indochina REICHARD, U.H., GANPANAKNGAN,M.&BARELLI,C.() Programme, Hanoi, Viet Nam. White-handed gibbons of KhaoYai: social flexibility, complex GEISSMANN, T., LA, Q.T., TRINH DINH, H., DANG, N.C., PHAM, D.T. reproductive strategies, and a slow life history. In Long-Term Field &VU, D.T. () Report on an Overall Survey of Cao Vit Gibbon Studies of Primates (eds P.M. Kappeler & D.P. Watts), pp. –. Population Nomascus sp. cf. Nasutus in Trung Khanh District, Cao Springer, Berlin, Germany. Bang Province (Second Overall Survey). Technical Report, FFI TAN, B.J. () The status of primates in China. Primate Conservation, Asia-Pacific, Hanoi, Viet Nam. , –. GEISSMANN, T., LA, T.Q., TRINH DINH, H., VU, D.T., DANG, N.C. & TIEN, D.V. () On the north Indochinese gibbons (Hylobates PHAM, D.T. () Rarest ape rediscovered in Vietnam. Asian concolor) (primates: Hylobatidae) in north Vietnam. Journal of Primates, , –. Human Evolution, , –. GERVASI, V., BROSETH, H., GIMENEZ, O., NILSEN, E.B., ODDEN, J., TRINH DINH,H.() A Survey on the Cao Vit Gibbon (Nomascus FLAGSTAD,O.&LINNELL, J.D.C. () Sharing data improves nasutus) in Trung Khanh, Cao Bang Province: Survey Results and monitoring of trans-boundary populations: the case of wolverines in Training for Local People in Survey Techniques. Technical Report, central Scandinavia. Wildlife Biology, , –. FFI Vietnam, Hanoi, Viet Nam. GUAN, Z.H., MA, C.Y., FEI, H.L., HUANG, B., NING, W.H., NI, Q.Y. THORNTON, D.H., WIRSING, A.J., LOPEZ-GONZALEZ, C., SQUIRES, et al. () Ecology and social system of northern gibbons living in J.R., FISHER, S., LARSEN, K.W. et al. () Asymmetric cross-border cold seasonal forests. Zoological Research, , –. protection of peripheral transboundary species. Conservation IUCN () The IUCN Red List of Threatened Species. V. –. Letters, ,e. Http://www.iucnredlist.org [accessed  January ]. VITKALOVA, A.V., FENG, L.M., RYBIN, A.N., GERBER, B.D., LA, Q.T. & TRINH DINH,H.() Report on Survey Eastern Black MIQUELLE, D.G., WANG, T.M. et al. () Transboundary Crested Gibbon Nomascus sp. cf. nasutus in Trungkhanh District, Cao cooperation improves endangered species monitoring and Bang Province. Technical Report, FFI Asia-Pacific, Hanoi, Viet Nam. conservation actions: a case study of the global population of LAPPAN,S.() Social relationships among males in multimale Amur leopards. Conservation Letters, ,e. siamang groups. International Journal of Primatology, , –. VU, N.T., NGUYEN, X.D., NGUYEN, M.H., LUU, T.B. & NGUYEN, T.H. LINNELL, J.D.C., TROUWBORST, A., BOITANI, L., KACZENSKY,P., () Survey and Assessment of the Cao Vit Gibbon in Phong HUBER, D., RELJIC, S. et al. () Border security fencing and Nam—Ngoc Khe Proposed Species/Habitat Conservation Area, wildlife: the end of the transboundary paradigm in Eurasia? PLOS Trung Khanh District, Cao Bang Province. FFI Vietnam, Hanoi, Biology, ,e. Viet Nam. MITTERMEIER, R.A., WALLIS, J., RYLANDS, A.B., GANZHORN, J.U., WEI, S.G., MA, C.Y., TAN, W.J., YANG, J., CUI, L.W. & FAN,P.F.() OATES, J.F., WILLIAMSON, E.A. et al. () Primates in Peril: Discovery of a new formed group and current population status of the World’s  Most Endangered Primates –. IUCN/SSC eastern black crested gibbon in Bnagliang National Nature Reserve, Primate Specialist Group, International Primatological Society, Guangxi, China. Acta Theriologica Sinica, , –. and Conservation International, Arlington, USA. ZHOU, J., WEI, F.W., LI, M., ZHANG, J.F., WANG, D.L. & PAN, R.L. MITTERMEIER, R.A., RYLANDS, A.B., SCHWITZER, C., TAYLOR, L.A., () Hainan black-crested gibbon is headed for extinction. CHIOZZA,F.&WILLIAMSON, E.A. () Primates in Peril: the International Journal of Primatology, , –.

Oryx, 2020, 54(6), 776–783 © 2019 Fauna & Flora International doi:10.1017/S0030605318001576 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 30 Sep 2021 at 03:33:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001576