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Chelonian Conservation and Biology, 2015, 14(1): 100–103 g 2015 Chelonian Research Foundation
Conservation Status of Freshwater Turtles in Hainan Island, China: Interviews and Field Surveys at Yinggeling Nature Reserve JAY PAK-HO WAN1, BOSCO PUI-LOK CHAN1,2, CHENGLE LIAO2, HONGXU MI2, MICHAEL LAU1,3, FEI LI1,2, HESHENG WANG2, AND YIK-HEI SUNG1,4,* 1
Kadoorie Conservation China, Kadoorie Farm and Botanic Garden, Lam Kam Road, Tai Po, N.T. Hong Kong [
[email protected];
[email protected];
[email protected];
[email protected]]; 2 Hainan Yinggeling Nature Reserve, Baisha County, Hainan Province, China [
[email protected];
[email protected];
[email protected]]; 3 Present address: WWF-Hong Kong, Central, Hong Kong SAR, China [
[email protected]]; 4 Present address: Department of Biology, Hong Kong Baptist University, Hong Kong SAR, China *Corresponding author
ABSTRACT. – Overexploitation has led to the drastic decline of most Asian freshwater turtle populations. We examined the distribution and current status of freshwater turtles using interviews and field surveys in Yinggeling Nature Reserve, Hainan Island. We captured 18 individuals of 4 species in over 8000 trap days. Based on our findings, interviews, and previous studies, illegal turtle harvesting is probably the major cause of population declines; we identified 2 key conservation areas within the reserve for regular patrols to reduce illegal activities. Overexploitation for traditional Chinese medicine, food, and pets has caused the drastic decline of Asian freshwater turtle populations (Cheung and Dudgeon 2006). Over 80% of species are listed as at least Threatened, with over 50% listed as Endangered or Critically Endangered by the IUCN Red List (IUCN 2013). Hainan Island, China’s southernmost land mass, has high turtle diversity, with 11 native freshwater species, 10 of which are listed as either Critically Endangered or Endangered (IUCN 2013). Field surveys of freshwater turtles in Hainan found that wild populations have been highly depleted (Gong et al. 2006a; Wang et al. 2011b), yet conservation efforts targeting Hainan’s freshwater turtles and their habitats are lacking. Therefore, prompt conservation action for Hainan turtles is needed. We conducted interviews to determine the historic and present distributions of freshwater turtle species and field surveys to examine the status of populations. We focus on the Yinggeling Nature Reserve (hereinafter
YGL) because it 1) is Hainan’s largest protected terrestrial area, at 505 km2, 2) is at the headwaters of the 2 largest catchment basins (Nandu and Changhua rivers), and 3) may still support freshwater turtle populations (based on anecdotal reports). YGL is located in the mountainous center of Hainan (Fig. 1) and has one of China’s largest tracts of primary rain forest. On its northern slope is the Nandu River, and on its southern slope is the Changhua River, providing abundant freshwater streams (Lau and Chan 2012). To facilitate management, YGL is divided into 7 sections that roughly follow its major watersheds. Before the reserve was established in 2004, turtle harvesting was common (Luo et al. 2013). We gathered information from interviews and field surveys to identify key areas for turtle conservation and formulate patrol programs that focus on these key areas. Methods. — We conducted the present study between March 2011 and October 2012, covering all management sections except Zayun, where no villages are adjacent to the reserve boundary. To investigate the current diversity and distribution of freshwater turtles, we interviewed collectors of non-timber forest products and ex-hunters living in villages adjacent to YGL. We showed photos of native and nonnative freshwater turtles to interviewees to identify which species were historically and currently found in the area. To verify the identification, we asked the interviewees to describe distinguishing characters of the species. We compiled data on the locality and date of each capture or sighting to document the distribution of each species present in the 6 surveyed management sections. Based on information from the interviews, we conducted forest and river surveys in each section. For forest surveys, we targeted species that use the terrestrial habitat and forest streams: Cuora galbinifrons, Cuora mouhotii, Cuora trifasiata, Platysternon megacephalum, and Sacalia quadriocellata. We focused our effort in 3 sections that interviews identified as having high turtle diversity: Gaofeng, Nankai, and Fanyang. We installed traps made of wire mesh, measuring 45 3 20 3 15 cm, on the forest floor and placed partially submerged traps on the edge of streams. Traps were baited with salted fish, meat, or cattle viscera and checked at least every 3 d. The trap design and bait choice have proven to be effective throughout southern China (Gong et al. 2005b; Sung et al. 2013). For river surveys, we targeted species inhabiting deeper water: Pelodiscus sinensis, Palea steindachneri, and Pelochelys cantorii. We focused on 3 sections— Yuanmen, Wanchong, and Maoyang—because of recent sightings of P. steindachneri and P. cantorii revealed in interviews. We installed large, floating cage traps made of wire mesh, measuring 2.5 3 1.5 3 0.7 m, in river regions with deep pools or large streams (cross-sectional width . 10 m; Som et al. 2006). Traps were baited with dead chickens. Because of high levels of human disturbance along large rivers, traps were checked every 4 hrs to
NOTES AND FIELD REPORTS
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Figure 1. Map of Yinggeling Nature Reserve, Hainan, with the 7 management sections. Dotted lines denote rivers adjacent to the reserve.
prevent vandalism and theft. We used binoculars to see whether turtles were captured in traps. Sampling was conducted during suitable weather (i.e., not during heavy rain), and each sampling sessions was between 4 and 22 consecutive days. Results. — We interviewed a total of 30 people in the 6 management sections of YGL. Eight of the 11 species native to Hainan were reported from YGL (Table 1). Geoemyda spengleri, Mauremys mutica, and Mauremys sinensis were unknown to the interviewees; thus, we believe them to be absent from YGL. Cuora mouhotii and P. megacephalum were the most widely reported species in the 6 sections. For field surveys, we conducted a total of 7999 and 531 trap days for forest and river surveys, respectively. We captured 18 individuals of 4 species, including C.
mouhotii, P. sinensis, P. megacephalum, and S. quadriocellata (Table 2). We do not disclose detailed information on where turtles were captured to ensure the safety of the populations (Stuart et al. 2006). Discussion. — The results of this study suggested that turtle populations in YGL are highly depleted, possibly attributable to intensive human exploitation. Most interviewees described turtle harvest in the last 20 yrs that caused drastic decline in turtle populations. From forest surveys, we captured 1 turtle for every approximate 666 traps days. By comparison, in Jianfengling Nature Reserve (another reserve in Hainan), it took , 200 trap days to capture an individual (Gong et al. 2006a). Despite considerable field effort (over 8000 trap days), we found only 4 species: C. mouhotii, S. quadriocellata, P. megacephalum, and P. sinensis.
Table 1. Interview data reporting the occurrence of turtle species in the six surveyed management sections of Yinggeling Nature Reserve (P 5 present at site). The conservation status of each species on the IUCN Red List (IUCN 2013) and China Species Red List (Wang and Xie 2004) is included also: CR 5 critically endangered; EN 5 endangered; VU 5 vulnerable. Species Cuora galbinifrons Cuora mouhotii Cuora trifasiata Geoemyda spengleri Mauremys mutica Mauremys sinensis Palea steindachneri Pelochelys cantorii Pelodiscus sinensis Platysternon megecephalum Sacalia quadriocellata
IUCN Red China Species List status Red List Gaofeng CR EN CR EN EN EN EN EN VU EN EN
EN EN CR EN EN EN EN CR VU EN VU
P P
P P P
Nankai
Yuanmen Wanchong Fanyang
P P P
P P
P P P P P
P P P
P
P
P P P P
P P P
Maoyang P P
P P P P
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Table 2. The species captured during field surveys in Yinggeling Nature Reserve, Hainan. Species Cuora mouhotii Pelodiscus sinensis Platysternon mgaecephalum Sacalia quadriocellata
No. of management sections
Forest survey
River survey
2 2 1 1
6 0 1 6
0 5 0 0
Cuora mouhotii and S. quadriocellata were the 2 most common species found in the forest survey—6 individuals per species—yet their densities were low. These are the only 2 species in Hainan with relatively high population densities, allowing for detailed ecological studies (Gong et al. 2005b; Wang et al. 2011a). Cuora mouhotii was and continues to be harvested in large volume for food and pet markets (Cheung and Dudgeon 2006; Gong et al. 2006b). The harvesting pressure for S. quadriocellata for food is relatively low because local people say it tastes bad, yet S. quadriocellata is still threatened by harvesting and is common in pet and food markets in cities (Cheung and Dudgeon 2006; Gong et al 2006b). Platysternon megacephalum, based on interviews, was common in all 6 sections of YGL, but populations have declined because of intensive hunting targeting this species. The common hunting technique for P. megacephalum is using baited hooks along stream pools. The results of field surveys—only one individual found— support the conclusion that populations in the reserve have been decimated. Pelodiscus sinensis is the only softshell turtle species that is relatively common in Hainan. It was reported that P. sinensis is found in rivers and irrigation ditches of farms around YGL. In our river surveys, we captured 5 adults and found 2 egg clutches on sandy banks adjacent to agricultural fields. From interviews, the density of P. sinensis has been in marked decline possibly attributable to hunting and habitat destruction; P. sinensis is a common food item, and individuals are eaten whenever they are found. In addition, increasing sand mining activities are reducing habitat quality and availability of nesting sites. Three Hainan species on the Turtle Conservation Fund Priority Species List, C. trifasciata, C. galbinifrons, and P. cantorii (Turtle Conservation Fund 2014), were not found in our surveys. From interviews, we identified several areas where C. trifasciata was captured in the last 10 yrs. Similar to most areas across its range, the density of wild C. trifasciata is extremely low (Horne et al. 2012). Cuora trifasciata are disappearing from the wild because of tremendous harvesting pressure—from interviews, the price of C. trifasciata in local villages has skyrocketed from around US$2500 10 yrs ago to over US$8000 in the last 3 yrs. The density of C. galbinifrons is also low in YGL, similar to elsewhere in Hainan (Wang et al. 2011b). According to interviews, there were no captures of C. galbinifrons from the reserve in the last 10 yrs; thus, we
Age classes 6 4 1 5
adults adults, 1 juvenile adult adults, 1 juvenile
speculate that the population is very close to extirpation in YGL. There is a chance that P. cantorii still exists in YGL. In 1995, 2000, and 2009, there were reports of P. cantorii captured near the reserve. It is likely that individuals survive in the deepest pools along the rivers, but they are undoubtedly very rare (Gong et al. 2006b). Priority has been placed on conserving these three species, therefore, it is imperative to locate and protect the remaining wild individuals of these species to prevent extirpation. Of the species on the freshwater turtle and tortoise checklists of Hainan, 4 additional species are not in YGL: M. mutica, M. sinensis, G. spengleri, and Manouria impressa. Both Mauremys species are typically found in rice paddies, marshes, and ponds (Yasukawa et al. 1996; Lovich et al. 2011), and their absence in the mountainous YGL is not surprising. In Hainan, G. spengleri remains a highly restricted species (Shi 2005), yet large numbers have been reported being sold in markets (Gong et al. 2005a). The current status of wild populations remains largely unknown. Also, we paid particular attention to M. impressa during our interview survey because its presence in Hainan is questionable; the only record is based on a specimen purchased from an animal trader in Haikou City (Buskirk 1989). We found no evidence of any large-sized tortoise present at any time in Hainan and similar investigations throughout Hainan over the last 12 yrs yielded similar results (B.P.-L.C., unpubl. data, 2014). Therefore, we believe that including M. impressa on species lists of Hainan is incorrect and that this species should be removed. Identification of key conservation areas with the highest turtle diversity or abundance is crucial to maximize the effectiveness of patrols and, thus, can be an effective measure to tackle illegal turtle hunting (Sung et al. 2013). In situ conservation actions, including setting up protected area with effective enforcement, have been recommended as crucial measures for conservation of freshwater turtles (Horne et al. 2012). However, antipoaching patrols may be ineffective, because of the limitation of manpower and the large size of protected areas. Since 2006, a team of almost 200 wardens has regularly patrolled YGL against illegal hunting. One job of wardens is to find and destroy turtle traps, and over the years, there seems to be a decreasing trend in the number of turtles traps found. Although promising, we believe it is difficult, if not impossible, to eliminate hunting completely because the reserve is large and incentive to hunt is very high. To safeguard the remaining turtle
NOTES AND FIELD REPORTS populations, we believe efforts should be concentrated in areas with relatively high turtle abundance and diversity. From the results of this study, we identified 2 key turtle conservation areas and started an intensive patrol and monitoring plan to halt the illegal trapping activities and aid the recovery of remnant populations. Acknowledgments. — We are thankful for a grant awarded by the European Association of Zoos and Aquaria Shellshock Campaign on behalf of the Turtle Conservation Fund. We thank Hainan Wildlife Conservation Bureau of Hainan Forestry Department for granting permits to conduct this study. Thanks to all the wardens and staff of YGL and volunteer Jackin Lam for conducting fieldwork. This project is partly funded by Kadoorie Farm and Botanic Garden. LITERATURE CITED BUSKIRK, J.R. 1989. New locality records for Chinese non-marine chelonians. Chinese Herpetological Research 2:65–68. CHEUNG, S. AND DUDGEON, D. 2006. Quantifying the Asian turtle crisis: market surveys in southern China, 2000–2003. Aquatic Conservation: Marine and Freshwater Ecosystems 16:751– 770. GONG, S., FU, Y., WANG, J., SHI, H., AND XU, R. 2005a. Freshwater turtle trade in Hainan and suggestions for effective management. Biodiversity Science 13:239–247. GONG, S., SHI, H., XIE, C., CHEN, C., AND XU, R. 2005b. Spring habitat selection by four eye-spotted turtle (Sacalia quadriocellata) in Limu Mountain of Hainan Island. Zoological Research 26:142–146. GONG, S., SHI, H., AND XU, R. 2006a. A survey of freshwater turtles in Jianfengling Nature Reserve, Hainan Province, China. Chinese Journal of Zoology 41:80–83. GONG, S., WANG, J., SHI, H., SONG, R., AND XU, R. 2006b. Illegal trade and conservation requirements of freshwater turtles in Nanmao, Hainan Province, China. Oryx 40:331–336. HORNE, B.D., POOLE, C.M., AND WALDE, A.D. 2012. Conservation of Asian tortoises and freshwater turtles: setting prioritiies for the next ten years. Recommendations and Conclusions from the Workshop in Singapore, 21–24 February 2011. INTERNATIONAL UNION FOR CONSERVATION OF NATURE (IUCN). 2013. IUCN Red List of Threatened Species. Version 2013.1. http://www.iucnredlist.org (21 May 2014). LAU, M.W.N. AND CHAN, B.P.L. 2012. Amphibian fauna of Hainan Yinggeling Nature Reserve, with new genus and
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