Wisdom of Crowds Reveals Decline of Asian Horseshoe Crabs in Beibu Gulf, China

Wisdom of Crowds reveals decline of Asian horseshoe crabs in Beibu Gulf, China

Y ONGYAN L IAO,HWEY-LIAN H SIEH,SHUQING X U ,QIUPING Z HONG J UAN L EI,MINGZHONG L IANG,HUAIYI F ANG,LILI X U ,WUYING L IN X IAOBO X IAO,CHANG-PO C HEN,SIU G IN C HEUNG and B ILLY K. Y. KWAN

Abstract Population decline among Asian horseshoe crabs in Supplementary material for this article can be found at Asia is increasingly reported, but knowledge of their popula- https://doi.org/./SX tion and ecological status in China is limited. We conducted community interviews in  fishing villages around Beibu Gulf in Guangxi, China, to collect distribution information about the potential spawning/nursery grounds of Tachypleus Introduction tridentatus and Carcinoscorpius rotundicauda,andanyimmi- ecording changes in population status and identifying nent threats to their populations. Based on the results from anthropogenic factors responsible for species declines  respondents we identified  potential spawning/nursery R are fundamental for evaluating potential risks to biodiver- grounds distributed widely along the shores of Beibu Gulf. We sity and developing effective conservation management ac- visited  of these sites and verified the presence of juvenile tions (Segan et al., ; Turvey et al., ; Bland et al., ). horseshoe crabs by field surveys. Nearly all respondents re- However, it can be difficult to obtain direct information on ported an overall depletion in horseshoe crab populations such parameters for species of conservation concern, par- from these  sites, which they attributed mainly to unsustain- ticularly in geographical regions that have large human po- able fishing practices. Respondents who reported having seen pulations but little focus on formal scientific research or horseshoe crab mating pairs on shores were mostly older peo- monitoring of exploitation (Turvey et al., ). One such ple, which may suggest a considerable reduction in horseshoe case is the limited population research conducted on the crabs coming to the shores to spawn in recent years. The mean Chinese horseshoe crab Tachypleus tridentatus and man- daily harvest of adult T. tridentatus offshore, as indicated by grove horseshoe crab Carcinoscorpius rotundicauda in fishers, has declined from c. –, in the sto– China, despite China being largely responsible for driving individuals during –. Our Wisdom of Crowds the recent decline in horseshoe crab populations across approach, supported by confirmatory field surveys, is a Asia (Liao & Li, ; Weng et al., ; Gauvry, ). cost-effective method for assessing the population status of Tachypleus tridentatus occurs in the Seto Inland Sea of horseshoe crabs, and the level of threat they face. Similar ap- Japan, along the coast of China, and southwards to Borneo proaches with other species are likely to be particularly valu- and Sumatra in Indonesia, whereas C. rotundicauda is com- able in the Asia–Pacific region, where well-structured monly recorded in Indonesia, Malaysia, Singapore, the population monitoring is largely unaffordable. Philippines, Thailand, Cambodia, Vietnam and the Bay of Keywords Beibu Gulf, Carcinoscorpius rotundicauda,data Bengal in India (Sekiguchi, ). Horseshoe crabs are eco- deficient, horseshoe crabs, local ecological knowledge, mat- logically important in coastal ecosystems, serving as both ing pairs, Tachypleus tridentatus prey and predators, hosts for epibionts, and bioturbators for sediment–water nutrient exchanges (Botton et al., ; Botton, ). They also have high commercial value in

YONGYAN LIAO* and BILLY K. Y. KWAN* (Corresponding author) Guangxi Key the manufacture of Tachypleus amoebocyte lysate, which is Laboratory of Beibu Gulf Marine Biodiversity Conservation, Qinzhou used in the testing of bacterial contamination in biomedical ’ University, People s Republic of China. E-mail [email protected] products (Walls et al., ; Gauvry, ). Despite being HWEY-LIAN HSIEH and CHANG-PO CHEN Biodiversity Research Center, Academia listed as Key Protected Aquatic Wildlife in four provinces Sinica, Taipei, Taiwan of China, T. tridentatus populations are heavily exploited SHUQING XU,QIUPING ZHONG,JUAN LEI,MINGZHONG LIANG,HUAIYI FANG and LILI to meet the increasingly high demands for Tachypleus amoe- XU Ocean College of Qinzhou University, People’s Republic of China bocyte lysate production and local food consumption (Liao WUYING LIN and XIAOBO XIAO Guangxi Biodiversity Research and Conservation    Association, People’s Republic of China et al., ; Hong, ; Gauvry, ). Other factors contrib- uting to the depletion of horseshoe crab populations include SIU GIN CHEUNG Department of Biology and Chemistry, City University of Hong Kong, Hong Kong the destruction of their spawning shores as a result of coastal *Also at: Ocean College of Qinzhou University, People’s Republic of China reclamation, and marine pollution, as reported in Taiwan   Received  April . Revision requested  May . (Hsieh & Chen, ), Hong Kong (Kwan et al., ) and Accepted  July . First published online  November . Japan (Seino et al., ). Carcinoscorpius rotundicauda

Oryx, 2019, 53(2), 222–229 © 2017 Fauna & Flora International doi:10.1017/S003060531700117X Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.19, on 30 Sep 2021 at 22:56:36, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S003060531700117X Wisdom of Crowds 223

populations in Hong Kong and Singapore are also decreas- towns around the three coastal cities (Fangchenggang, ing, mainly as a result of the loss of mangrove and mudflat Qinzhou and Beihai) along Beibu Gulf in Guangxi habitats (Shin et al., ; Cartwright-Taylor et al., ). Zhuang Autonomous Region, China (Table ). Beibu Gulf Tachypleus tridentatus and C. rotundicauda are currently is a semi-closed gulf located in the northern South China categorized as Data Deficient on the IUCN Red List Sea between China and Vietnam. The Gulf is  km wide  (WCMC, a,b), but based on the available evidence it at its widest and has a total area of , km (Chen et al., is likely that their populations will decline further because ). It has extensive estuarine ecosystems, with consider- their protection is a low priority for local governments able freshwater input from seven major rivers (Fangcheng, (Bland et al., ). In general, public awareness of the con- Qin, Dafeng, Nanliu, Red, Beilun, Changhua; Chen et al., servation of marine invertebrates is low (Cardoso et al., ). The rivers carry a significant load of nutrients from ). There is an urgent need for up-to-date information the land, which are essential for phytoplankton growth, on the distribution and population trends of Asian horse- which in turn supports the rich biodiversity and productive shoe crabs in China, and the threats they face, to protect fisheries in the northern South China Sea (Yu & Mu, ). remaining populations across their distribution range. To Both T. tridentatus and C. rotundicauda are recorded fre- this end, a broad approach that facilitates rapid, inexpensive quently in mangrove-dominated estuaries with patchy sea- and wide-scale collection of population data must be devel- grass beds and extensive sandy mudflats along the coastline oped. An important means of addressing information gaps of Beibu Gulf (Hu et al., ; Chen et al., ). In general, regarding species conservation and management, especially horseshoe crabs require three types of coastal habitats dur- in data-poor situations, is the collection of local knowledge ing their entire life cycle: adults nest on open, sandy beaches (Segan et al., ; Nash et al., ; Pan et al., ). This near the high water mark or along the edge of mangrove for- so-called Wisdom of Crowds technique is based on a mech- ests, juveniles forage and grow within the intertidal zones of anism that aggregates knowledge of a large sample popula- the same shores or their adjacent flats, and subadults and tion to generate quantitative estimates and spatial reasoning adults inhabit shallow subtidal areas (Chen et al., ; (Whitmore, ). Although the application of this method Smith et al., ). During the spawning season local people is relatively new, the merits of the approach, including its encounter adult C. rotundicauda mating pairs in amplexus independence, diversity of opinion, decentralization and burrowing in the mud along the edges of mangrove forests. aggregation, are recognized as of value for informing natural Mating pairs of T. tridentatus are occasionally entangled in resource management and conservation (Surowiecki, ; fishing nets cast along the coastline to harvest fish when the Arlinghaus & Krause, ). Previous studies have found tide recedes. that fishers’ perceptions about population trends matched scientific data reasonably well in some circumstances   (Rochet et al., ; Daw et al., ; Arlinghaus & Krause, Methods ). In the case of Asian horseshoe crabs, local community members, especially fishers, may be able to report the histor- The  villages and towns were chosen for the interviews be- ical and recent status of a species as well as underlying dri- cause sightings of horseshoe crabs on the beaches nearby vers of species decline (sensu Ainsworth et al., ). had been reported in the grey literature. Respondents were We conducted a study in three coastal cities along Beibu intercepted at random as the survey party walked through Gulf in south-western China to obtain data on the potential each village. We aimed to survey people of both sexes and distribution of spawning/nursery grounds of T. tridentatus of various ages, to capture potentially diverse knowledge and C. rotundicauda, and anthropogenic threats to the popu- and experience of horseshoe crabs across the sampling loca- lations, through community interviews. Beibu Gulf is consid- tions. Only one person per household was surveyed, to min- ered to be the most critical spawning/nursery ground for imize the chance of double counting the same information Asian horseshoe crab populations, particularly T. tridentatus from various family members. We interviewed  people (Hu et al., ;Li,). We verified our findings on the dis- in total, and the number of respondents from each village tribution of the two species by surveys of intertidal habitats for varied (– individuals), depending on people’s willingness juvenile populations. Such findings can strengthen our under- to participate in the interviews. Interview methods followed standing of the extent to which local knowledge can assist in the guidelines of the American Sociological Association, in- the conservation of Asian horseshoe crabs in locations where cluding informing all respondents at the outset about the these species are under intense anthropogenic pressure. study’s general aims, assuring them that the data would be anonymized, and conducting the interviews only after par- Study area ticipants had given verbal consent. Interviews were conducted by research team members and student helpers, all Community interviews were conducted during  of whom were native Mandarin Chinese speakers. There September– October  in  fishing villages and small was also at least one team member present during each

TABLE 1 Villages and towns along the shores of Beibu Gulf in Chinese were assisted by the researchers through oral com- Guangxi Zhuang Autonomous Region, China (Fig. ), where inter- munication in either Mandarin Chinese or native dialects. view surveys were conducted to gather local knowledge about the As horseshoe crabs may utilize sandy mudflats as their Asian horseshoe crabs Tachypleus tridentatus and Carcinoscorpius spawning and/or nursery grounds, the potential shores in- rotundicauda, with the number of responses collected at each location. dicated by the respondents were considered to be a mixture of spawning and nursery grounds. Based on the information Village name (by area) No. of responses provided by the respondents, and given budget constraints, Fangchenggang West a total of  potential spawning/nursery shores were chosen Zhushan 11 at random and verified by field surveys conducted at each Wutou 11 site in March and June . The sites were chosen to Banai 9 cover at least two potential spawning/nursery grounds Jiaodong 24 from each of the three coastal cities in Beibu Gulf. In Shijiao 27 Xinji 25 Southern China, summer is the best season to conduct ju- Wanwei 9 venile population surveys, as the crabs feed actively in the Fangchenggang East intertidal habitats after prolonged hibernation in winter Shankuaishi 13 and early spring (Chiu & Morton, ; Hu et al., ). Niutou 18 During each field visit a team of five trained researchers Yuzhouping 10 walked at random and searched for juveniles within the Zhouwei 10 intertidal area, .–. m above chart datum (i.e. the lowest Qisha 13 Leshan 15 astronomical tide as defined by the UK Hydrographic Office) for  minutes. The total monitoring area for each Shaluoliao 17  Qinzhou shore was ,–, m . Juvenile T. tridentatus were dis- Longmengang 22 tinguished from C. rotundicauda by the triangular cross sec- Maoling 20 tion of their telson, as well as the presence of three distinct Kangxiling 6 immovable spines above the telson insertion and three spines Dahuan 20 growing along the central ridge on the dorsum of the Shajiao 19   Paotai 20 opisthosomal carapace (Chen et al., ; Hu et al., ).   Beihai West Statistical analysis was performed using SPSS v. . Zhakou 4 (SPSS, Inc., Chicago, USA), after data had been checked Beihai Pier 4 for normality and homogeneity of variance using the Zhulinyanchang 5 Shapiro–Wilk and Levene’s tests, respectively. If these tests Beihai East failed, data were logarithmically transformed. An independ- Baishatou 16 ent samples t-test was applied to analyse the difference in Pangxietian 17 the age of respondents who had or had not observed mating Chongmei 4 Dabudun 8 pairs of horseshoe crabs on shores, and who had or had not Hongkan 11 eaten adult T. tridentatus before. Shankou 6 Shatian 6 Results

visit who could speak local dialects. All respondents were We interviewed  men and  women, with a mean age of interviewed one-to-one using a standard anonymous ques- . ± SD . years (range –). According to their re- tionnaire in simplified Chinese characters, containing sponses, juvenile and/or mating pairs of horseshoe crabs descriptive and multiple-choice questions in three sections: had been observed at a total of  sites (Fig. a). Field mon- present occurrences, population trends and threats, and fish- itoring confirmed the presence of juvenile T. tridentatus ing activities targeted at horseshoe crabs (Supplementary and/or C. rotundicauda at all  of the sites selected for Material). Respondents could choose more than one answer monitoring (Fig. b). These sites were previously believed for questions regarding the horseshoe crab species observed, to be spawning/nursery grounds for T. tridentatus only; perceived causes of the population decline, and fishing meth- however, juvenile C. rotundicauda were recorded at five of ods used for harvesting adult crabs (Supplementary the sites, along with juvenile T. tridentatus (Fig. a, b). Material). To improve the accuracy of the information col- This may reflect the difficulty for non-experts of distin- lected, responses were included in the analysis only if the re- guishing juvenile C. rotundicauda from T. tridentatus. spondent had seen a horseshoe crab in the wild. The Only T. tridentatus were found at Zhakou, and only C. ro- respondents who could not read or write in simplified tundicauda were found at Shankou during the two field

FIG. 1 (a) Locations of potential spawning/nursery grounds of the Asian horseshoe crabs Tachypleus tridentatus and Carcinoscorpius rotundicauda in Beibu Gulf, Guangxi, China, as indicated by interviews with local people in  villages and towns along the coast, and (b) locations of spawning/nursery grounds of T. tridentatus and C. rotundicauda reported in the literature (, Liang, ; , Chen et al., ; , Hu et al., ; , Hu et al., ) and confirmed by field monitoring in this study.

visits (Fig. b). Considering our findings along with the pre- among horseshoe crabs in Beibu Gulf in the previous viously published population data (Liang, ; Hu et al.,  years, .% stated that the population had increased, and , ; Chen et al., ), there are  known nursery .% did not perceive any obvious change (Fig. a). Only one sites for juvenile Asian horseshoe crabs in Beibu Gulf respondent could provide a specific location where there (Fig. b). This is a conservative number, as more spawn- had potentially been an increase in the population. ing/nursery grounds may be confirmed by field surveys. Respondents attributed the decline of horseshoe crabs to Respondents who had seen a mating pair of horseshoe overharvesting (.%), followed by industrial pollution crabs on the shore were significantly older (. ± SD . (.%) and coastal reclamation (.%; Fig. b). Mass har- years) than those who had not (. ± SD . years; vesting of adult T. tridentatus had been witnessed by .% df = , t = .,P=.). Ninety-five percent of the re- of respondents (n = ). The methods used to catch horse- spondents agreed that there had been a population decline shoe crabs included bottom trawling (.%), gill-netting

FIG. 2 (a) Respondents’ perceptions of the population trend of adult horseshoe crabs in Beibu Gulf, China (Fig. ), and (b) perceived causes of population decline. The number of responses is indicated above the bars.

(.%) and purse-seine fishing (.%). According to the beaches and shallow waters in Beibu Gulf at least until the respondents’ observations, .%ofT. tridentatus harvested s. In the s T. tridentatus production could reach were adults or subadults (prosomal width .  cm), and .–. million individuals per year (Liang, ; Liao & .% were th-instar or larger juveniles. The mean daily Li, ). Despite the species’ unusually high occurrence catch rate during – as estimated by the interviewees in Beibu Gulf, information about its abundance and distri- was – individuals (n =  respondents), which was sig- bution is limited. The first quantitative data on the daily har- nificantly lower compared to the mean catch rate in the vest of T. tridentatus and C. rotundicauda on five shores s, which was –, individuals per day (n = ). within Beibu Gulf were reported in  (– pairs; Liang, Respondents reported that the consumption of adult ). During –, Hu et al. () discovered three T. tridentatus was common practice (.%; n = ). The previously unknown nursery grounds of T. tridentatus and majority (%; n = ) considered T. tridentatus to be ed- C. rotundicauda (Fig. b), with a juvenile density of .–  ible, although %(n=) had heard of food-poisoning in- . individuals per  m . Chen et al. () found two cidents caused by other horseshoe crab species. There was more new nursery grounds on the west coast of Beibu no statistical difference between the age of respondents Gulf, and recorded a juvenile density of .–. indivi-  who habitually ate horseshoe crabs and those who did not duals per  m . By gathering local knowledge from  fish- (df = , t = −.,P=.). ing communities, we identified  potential spawning/ nursery grounds, distributed widely along the shores of Beibu Gulf,  of which were confirmed by surveys. This Discussion suggests that local knowledge is useful and effective in identifying potential habitats for juvenile T. tridentatus and In mainland China horseshoe crabs occur in the south of the C. rotundicauda. Yangtze River Delta, along the coastline of Shanghai, Previous studies have reported declining trends in popu- Fuzhou, Xiamen and Shantou Cities, and southwards to lations of Asian horseshoe crabs along the coastline of Leizhou, Beibu Gulf and Hainan Island (Liao et al., ). Zhejiang, Fujian, Guangdong, Guangxi and Hainan pro- Beibu Gulf is believed to accommodate the highest density vinces (Liao & Ye, ;Li&Hu,; Weng et al., ). of T. tridentatus globally (Liao & Li, ; Brockmann & It is estimated at least a million pairs of adult T. tridentatus Smith, ; Weng et al., ). According to the grey litera- are exploited each year to satisfy the demand for consump- ture and other information sources, Asian horseshoe crabs tion and biomedical applications (Liao & Ye, ; Li & Hu, were probably distributed extensively over all mudflats, ), and these are mainly imported from Vietnam. Such

intense harvesting pressure in addition to habitat destruc- conservation status. Fishing communities identified the tion may have driven horseshoe crab populations to the possible extent of occurrence for both species, which are dis- edge of extinction. Our interview results indicated that the tributed widely along the shores of Beibu Gulf. However, horseshoe crab population in Beibu Gulf has declined sub- despite their widespread occurrence, there is a perception stantially: () nearly all interviewees reported an overall re- among fishers that horseshoe crab populations are in de- duction in the abundance of horseshoe crabs in the previous cline, based on their direct observations of mating pairs  years; () older respondents were more likely to have seen on the shores, and the catch rate of adult T. tridentatus off- horseshoe crab mating pairs on the shores than younger re- shore. The causes of the decline, including unsustainable spondents; and () the respondents reported a mean daily fishing, industrial pollution and coastal reclamation, may catch rate of – adult T. tridentatus, which is a significant be irreversible, and the available evidence should be suffi- decline compared with –, individuals per day in the cient to urge the provincial Chinese authorities to imple- s. The reduction in population abundance was attribu- ment management conservation actions, particularly to ted mainly to unsustainable fishing practices. Our findings ensure sustainable use of horseshoe crab resources by fishers are consistent with previous reports of T. tridentatus decline and the Tachypleus amoebocyte lysate industry. Other re- (Liao & Li, ; Huang et al., ; Weng et al., ), and commendations for local authorities include () reducing il- indicated that most people in the region, regardless of their legal trade of horseshoe crabs; () promoting establishment age, consumed adult T. tridentatus, despite the species being of protected areas for horseshoe crabs; () implementing ef- listed as Key Protected Aquatic Wildlife in Guangxi prov- fective management and restoration of breeding/nursery ince. In general, local people avoid consuming adult C. ro- habitat; () strengthening research and conservation cap- tundicauda and unlaid eggs, following reports of food acity; and () raising public awareness of horseshoe crab poisoning caused by the presence of saxitoxin and tetrodo- conservation. Regarding the increasing need for cheap and toxin (Shumway, ; Liao et al., ). However, the cul- rapid population assessment tools, Wisdom of Crowds tural norm of consuming horseshoe crab as a delicacy methods are an overlooked but potentially valuable tool may impede efforts to motivate local communities to con- for conservation, particularly in the Asia–Pacific region, serve the remaining T. tridentatus population in Beibu where conventional field survey methods are largely un- Gulf. Long-term and local-based conservation education affordable and human disturbance of horseshoe crab popu- programmes (e.g. raising laboratory-cultured juvenile lations is intense. horseshoe crabs at secondary schools, as described by Kwan et al., ) are useful in promoting positive changes ’ in students behaviour and attitudes towards horseshoe crab Acknowledgements conservation. Such participatory educational activities, supported by public awareness programmes, could have a sig- This project was funded by the National Natural Science nificant influence in deterring local communities from Foundation of China (), Guangxi Natural Science eating horseshoe crabs. Foundation (GXNSFDA), Guangxi Marine As the problems of increasing human disturbance and Science and Technology Fund (GXZC-G--GXJX), overharvesting are expected to persist, there is an immediate Guangxi Key Laboratory of Beibu Gulf Marine Biodiversity need for a management strategy for T. tridentatus conserva- Conservation, Qinzhou University (ZA)and tion. At the  IUCN World Conservation Congress, a Guangxi Colleges and Universities Innovation Research motion for the conservation of Asian horseshoe crabs was Team. We are grateful to the students from the Ocean passed unanimously, with a recommendation encouraging College of Qinzhou University for their assistance in con- members to identify critical habitats and to protect them ducting community interviews and field surveys. using appropriate integrated marine and coastal management approaches (IUCN, ). However, territory-wide distribution surveys of Asian horseshoe crabs in China Author contributions would be costly and require significant effort, particularly given limited baseline data. Gathering local knowledge YL led the research project, developed the overall research could be of particular use in countries or areas where con- framework and methods, compiled and clustered data for servation budgets are insufficient to support well-structured analysis, and prepared the article. SX, QZ, JL, ML, HF, LX, quantitative monitoring (Whitmore, ). Follow-up con- WL and XX conducted community interviews and field firmatory field surveys, as described here, have the potential population surveys. HLH and CPC provided input on to attract funding for further studies. Given that both T. tri- local context to ensure the research framework and methods dentatus and C. rotundicauda are categorized as Data were relevant. SGC conducted statistical analysis and pre- Deficient, the Wisdom of Crowds method could be used pared the figures. BKYK supervised the research to ensure to collect data and facilitate assessment of the species’ it met scientific requirements. HLH, CPC, SGC and

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