Asian Snake Farms: Conservation Curse Or Sustainable Enterprise?

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Asian snake farms: conservation curse or sustainable enterprise?

P ATRICK W. AUST,NGO V AN T RI,DANIEL J.D. NATUSCH and G RAHAM J. ALEXANDER

Abstract Snake farming in Asia has increased over the past were harvested from the wild and traded on a localized decade, and conservationists have expressed concerns that and sustainable scale (Pipeng et al., ). However, since farms may foster overexploitation of wild populations and the s the demand for snakes and snake products has in- create legal conduits for illegally harvested wild individuals. creased, driven primarily by the growth of Asia’s wealthy We conducted face-to-face interviews with snake farmers in middle class and increasing demand for luxury goods Viet Nam and China, with the aim of describing the basic (Zhou & Jiang, ; Auliya, ; Nijman, ; Jiang models under which snakes are farmed for meat. We et al., ; Cao et al., ). By the beginning of the st cen- synthesized this information to assess the feasibility of farm- tury demand for snake products had begun to outstrip sup- ing snakes for human consumption, drawing conclusions ply, and within a few years the stage was set for uncontrolled about the impact of this industry on the conservation of international trade, overexploitation of wild populations wild snake populations. The most commonly farmed snakes and escalating risks of a multi-species extinction event include the monocled cobra Naja kaouthia, the Chinese (Zhou & Jiang, , ; Pipeng et al., ). cobra Naja atra, the oriental rat snake Ptyas mucosus and Concerns regarding the increasing demand for snake the king cobra Ophiophagus hannah. These species have products have persisted over the last decade, during which life histories that are compatible with the demands of inten- time the Asian snake trade has become characterized by two sive livestock production, including early maturity, rapid key phenomena: () the work of the international conserva- growth rates, high reproductive output, efficient food assim- tion community to reverse the plight of threatened snake ilation rates and undemanding space requirements. Snake species (e.g. Auliya, ; CITES, ; Kasterine et al., farmers appear to be capitalizing on the unique energy-effi- ; Jiang et al., ), and () the evolution of closed-cycle ciency of snakes to produce meat for human consumption. snake farming systems operated by small-scale farmers re- We conclude that the ease and profitability of farming sponding to market forces (Pipeng et al., ; Natusch & snakes in China and Viet Nam make farming a viable sub- Lyons, ). Defined as the production of snakes within a stitute for harvesting wild snakes, with apparently minimal controlled environment without the introduction of speci- threat to wild populations. Snake farming offers a range of mens from the wild (Natusch & Lyons, ), closed-cycle novel agricultural opportunities and has the potential to snake farming is a relatively new industry and little is play a pivotal role in sustainable development. known about its role in sustainable development. A funda- mental lack of baseline information, coupled with a paucity Keywords Asian snake trade, conservation, snake farms, of comparative production models in other parts of the sustainable utilization, wildlife farming world, has fuelled concerns that snake farms may exacerbate The supplementary material for this article can be found at the overexploitation of wild populations and act as a conduit http://dx.doi.org/./SX. for wild-caught specimens entering the trade illegally (Lyons &Natusch,; Kasterine et al., ; Pipeng et al., ). CITES is responsible for regulating international trade for the majority of snake species that are traded in large Introduction numbers (CITES, ). In China and Viet Nam at least six CITES-listed snake species are commercially farmed nakes have been prized in Asia for centuries on government-registered farms. Unregistered snake (Dharmananda, ; Pipeng et al., ). Valued for S farms also exist, and a number of non-CITES species are their meat, skin and medicinal worth, traditionally they also farmed for commercial purposes; however, the scale of these activities is negligible compared to the legal produc-

PATRICK W. AUST (Corresponding author) and GRAHAM J. ALEXANDER School of tion of CITES-listed species. China and Viet Nam are con- Animal, Plant and Environmental Sciences, University of the Witwatersrand, sidered to be the largest and most important producers of, Johannesburg, South Africa. E-mail [email protected] and markets for, snake meat. Calculating the total size of the NGO VAN TRI National Key Laboratory, Institute of Tropical Biology, Vietnamese industry is difficult, although a conservative estimate for Academy of Sciences and Technology, Ho Chi Minh, Viet Nam China and Viet Nam suggests there are at least , closed- DANIEL J.D. NATUSCH School of Life and Environmental Sciences, University of  Sydney, NSW 2006, Australia cycle farms producing several million snakes of at least Received  December . Revision requested  February . taxa (CITES Management Authority, Viet Nam and Accepted  March . First published online  July . Guangxi Forestry Administration, unpubl. data).

Oryx, 2017, 51(3), 498–505 © 2016 Fauna & Flora International doi:10.1017/S003060531600034X Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.19, on 29 Sep 2021 at 01:55:42, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S003060531600034X Asian snake farms 499

In  the CITES Secretariat convened a technical work- interview process was rarely private, and interviews were shop to consider the conservation priorities and manage- often carried out in the presence of interested onlookers. ment and enforcement needs of the Asian snake trade. Each interview lasted c.  minutes. Questions were de- The results were presented at the th Meeting of the signed to give an overview of the key biological (e.g. growth, Conference of Parties to CITES in March , whereupon survival and reproduction) and economic parameters (e.g. the CITES Secretariat was instructed to carry out a series of food, environment and management systems) that defined tasks to ensure the overall sustainability, legality and trace- and determined farm inputs and outputs. Farmers often ability of the trade in CITES-listed snakes. Since that meet- kept multiple species within a single facility, but usually ing much attention has been focused on the closed-cycle under separate management regimes. For the analysis, sam- production of large pythons for their skins, and the role of ple size (n) represents the number of responses to each ques- snakes in the luxury leather industry (Kasterine et al., ; tion. Not all farmers answered all questions, and Natusch & Lyons, ). However, a number of snake farms species-specific data were pooled for more general analysis; in Asia are now producing CITES-listed snakes specifically thus sample size often varied according to question. Pythons for human consumption, and the demand for snake meat is were excluded from the analysis because they are farmed increasing. primarily for their skins rather than their meat. To address the lack of knowledge about closed-cycle snake farming, we visited snake farms in China and Viet Nam as part of a CITES initiative to better understand pro- Results duction systems for snakes farmed primarily for their meat. We aimed to address three questions regarding the conser- Species Excluding pythons, the four most commonly  vation implications of snake farming: ( ) What are the basic farmed snakes were the monocled cobra Naja kaouthia,  conditions under which snakes are farmed? ( ) Is snake the Chinese cobra Naja atra, the oriental rat snake Ptyas  farming biologically and ecologically feasible? ( ) Are mucosus and the king cobra Ophiophagus hannah. In total snake farms a sustainable option for meeting all current we surveyed  cobra,  oriental rat snake and four king and future demands for snake meat? cobra management regimes. We treated N. atra and N. kaouthia as a single species because of the difficulties in differentiating the two species during fieldwork (probably Methods as a result of hybridization). These study species are farmed primarily for their meat and are all listed in CITES –  During September January we conducted Appendix II (CITES, ). Naja atra and O. hannah are  face-to-face interviews with managers of independent also categorized as Vulnerable on the IUCN Red List snake farms. We used a targeted sampling strategy and a (Stuart et al., b; Ji & Li, ). semi-structured approach based on a standard series of questions (Supplementary Material ), with ethical approval from the University of the Witwatersrand, South Africa Farm characteristics Snake farms in both China and Viet (Human Non-medical Ethics clearance certificate H//). Nam are variable in terms of scale, ranging from We informed all potential interviewees about the aims of smallholder suburban plots raising a few hundred snakes the survey, and conducted interviews only with participants as a supplementary livelihood activity, to large-scale farms who had given their informed consent. We conducted  in- breeding and rearing tens of thousands of snakes as their terviews in the Vietnamese provinces of Ca Mau, Ho Chi primary business. Despite substantial variation among Minh City, Tay Ninh, Vinh Phuc and Phu Tho, and nine individual farms, similar species were farmed at both in the Chinese province of Guangxi. In Viet Nam we sur- Chinese and Vietnamese snake farms. We therefore veyed a broad spectrum of licensed snake farms, whereas pooled farms from the two countries for our descriptive in China our selection was skewed towards larger commer- analyses. Most of the farms surveyed were small, cial farms in an effort to gain a better understanding of the independent operations that bred, raised and sold their own  more technologically advanced sector of the industry that stock. Fifty percent of farms ( of )were, , m  has developed there. Nonetheless, we assume a random (mean =  ± SD  m ). Most farms kept more than one and representative sample of farms in both China and species (mean = . ± SD . species). Snake enclosure types Viet Nam. varied between farms, species and age groups, from small, Our survey team consisted of a principal investigator single-snake cages to large outdoor pits containing many from the University of Witwatersrand, South Africa, one snakes. The more advanced farms ( of ) used or more government officials, a CITES Management purpose-built rooms in which several hundred individual Authority representative, a biologist or herpetologist from snakes were housed within vertical towers of stacked a relevant in-country institution, and an interpreter. The wooden pallets. Stocking rates for adult snakes ranged

TABLE 1 Key life history and production attributes of the king cobra Ophiophagus hannah, the Chinese cobra Naja atra, the monocled cobra Naja kaouthia and the oriental rat snake Ptyas mucosus, which are farmed for their meat in China and Viet Nam.

Ophiophagus hannah Naja atra & N. kaouthia Ptyas mucosus Attribute No. of responses (n) Mean ± SD No. of responses (n) Mean ± SD No. of responses (n) Mean ± SD No. of breeding 3 0.9 ± 0.8 15 1.5 ± 0.7 16 2.8 ± 2.3 females to 1 male Clutch size 10 27 ± 6.1 21 23 ± 6.7 33 15 ± 2.8 Incubation failure rate 3 29 ± 20% 8 14 ± 10% 14 17 ± 17% Hatchling mortality rate 3 37 ± 5% 14 12 ± 10% 18 21 ± 15% Age at maturity (years) 3 2.1 ± 0.2 15 1.8 ± 0.6 17 0.9 ± 2.2 Mass at maturity (kg) 2 2.5 ± 0.5 13 1.6 ± 0.3 14 1.3 ± 0.2 Age at harvest (years) 3 5 ± 2 14 2.5 ± 1.3 11 1.5 ± 0.7 Mass at harvest (kg) 3 2.5 ± 0.1 12 2 ± 0.2 12 1.6 ± 0.3 Price per kg (USD) 3 81 ± 18 14 31 ± 6.1 11 28 ± 8 Feed conversion ratio (kg) 3 5 ± 0.8 12 5.6 ± 0.6 14 6 ± 1.2

− both within and between farms, from . kg m in − single-snake cages to  kg m in the communal tower block arrays. Forty-one percent of farms ( of ) provided supplementary heating for snakes through the use of electric heating elements or piped hot water, and four of the large commercial farms provided facilities for snakes to access natural sunlight. The use of various forms of insulation was common. Enclosures were cleaned by hand on average once per week. Only two farms used water to clean enclosures. The standard diet for all species comprised a variety of small vertebrates, fed whole, chopped into pieces or reconstituted into pellets or sausages. With the exception of king cobras, which showed a strong preference for snake meat, virtually all farmers reported generalist dietary tendencies for all species and age groups. We divided primary feed inputs into three categories: wild-harvested natural food (e.g. FIG. 1 Comparative reproductive output (no. of eggs) of the king amphibians and rodents), waste protein from other cobra Ophiophagus hannah, the Chinese and monocled cobras industries (e.g. poultry and pork) and formulated diets Naja spp. and the oriental rat snake Ptyas mucosus, farmed in China and Viet Nam. Year  represents the hatch date for all (reconstituted waste protein). Waste poultry was present species. Rat snake totals are the sum of up to three clutches per  in % of diets and wild harvested food was present in year, whereas the other species only have one clutch per year. % of diets (n = ). No live prey was provided; meat Trend line endpoints are a function of harvest and do not was provided either fresh or thawed from frozen. Adult necessarily represent senescence. snakes received food weighing a mean of  ± SD .%of their body weight (n = ) on average once every . ± SD . days (n = ), whereas juveniles were offered diet of fresh, whole vertebrate prey with a dry mass of   food more often (in some cases daily). Breeding adults c. % (Dierenfeld et al., ), this translates to an   were fed less and/or less often than non-breeding adults, equivalent dry food conversion ratio of c. . . Both and less in winter than in summer. All farms provided Chinese and Vietnamese farmers selected snakes with clean drinking water on a regular basis. desirable traits (e.g. rapid growth rates and aggressive feeding responses) for breeding purposes. Snakes were sold at a mean mass of  ± SD . kg (n = ) and we Snake biometrics Life-history attributes important for found no significant difference between the mean mass of production of the four snake taxa are summarized in individuals at sexual maturity and at sale size (two-sample Table  and Fig. . All farmers had a good understanding t test, t()=.,P=.). The mean price for a whole − of food conversion metrics, as these were used as a means live snake was USD  ± SD . kg (n = ). There was of estimating revenue. On average . kg of feed was used no significant difference between the price of rat snakes to produce  ± SD . kg of live snake (n = ). Assuming a and cobras (two-sample t test, t()=.,P=.) but the

TABLE 2 A comparison of the size (no. of snakes) and annual net profit of snake farms in Viet Nam and China.

Viet Nam China Mean no. of adult snakes per farm (range) 550 ± SD 527 (30–2,100) 27,288 ± SD 42,065 (400–130,000) Mean annual net profit per farm (range), USD 12,476 ± SD 13,714 (1,428–47,619) 350,716 ± SD 619,403 (7,392–1,968,000)

value of king cobras was greater than that of other species presence of an audience (e.g. family members, neighbours), (mean = USD  ± SD ). Estimates of the relative value of which may have compromised objectivity (e.g. legal issues, the snake farming industry in China and Viet Nam in terms social pressures). Secondly, the farm selection process was of farm size and economic output are in Table . potentially biased towards more successful farms, which may have positively skewed our conclusions. A third limitation applies mainly to the king cobra data, where a small  Resilience of snake farming Seventy-four percent of sample size and problems experienced during the first day farmers varied their management regime according to of fieldwork (which coincided with two of the four king prevailing environmental or economic conditions. This cobra interviews) may have compromised the data. included suspending feed inputs in response to Nevertheless, the findings demonstrate the parameters of a fluctuations in feed prices or seasonal availability. Sixteen viable industry and are broadly corroborated by existing lit-  farmers ( %) allowed their snakes to brumate for a mean erature (e.g. Haitao et al., ; Cunningham et al., ). of  ± SD . months (n = ), during which time management inputs were significantly reduced. The mean estimate of how long their stock could survive without Biological feasibility feeding, and without lasting consequences to production output (e.g. in the event of an environmental catastrophe) Conventional logic states that energy efficiency, and there- was . ± SD . months (n = ). fore production efficiency, decreases towards the apex of the trophic pyramid (e.g. Odum et al., ). Theoretically, snakes are unsuitable for commercial meat production be- Discussion cause they are predators and obligate carnivores. However, the ectothermic metabolic response of reptiles results in a Closed-cycle snake farming has emerged as a viable live- more efficient conversion of biomass compared to mam- stock industry supplying snakes to the international trade. mals and birds (up to % more efficient; Pough, ). In Viet Nam and China the four main species farmed for This feat is achieved through several unique adaptations, in- their meat are P. mucosus, N. atra, N. kaouthia and O. han- cluding efficient digestive physiologies (Bedford & nah. A variety of production models are used but all species Christian, ; Secor, ), judicious activity patterns have broadly similar life histories and are compatible with (e.g. Slip & Shine, ), the ability to regulate metabolic the biological prerequisites for commercial production. rate according to resource availability (Secor, ) and Snake farming is a profitable livelihood activity for rural the ability to harness solar energy to negate the cost of me- communities, and in some cases may offer novel opportu- tabolic thermoregulation (Seigel et al., ). Our findings nities because primary production parameters are resource suggest that snakes fed on a rudimentary diet may have efficient and resistant to environmental perturbations. dry feed conversion ratios comparable to poultry fed on Although studies have suggested that wildlife farming scientifically formulated diets (Steinfeld et al., ). enterprises may have a negative impact on wild populations The species of snakes included in our study grow rapidly, (e.g. Drury, ; Brooks et al., ; Lyons & Natusch, ; mature early and have a high reproductive output. These Cunningham et al., ), our study supports the hypothesis traits are generally more accentuated in farmed animals that in the right context wildlife farming can mitigate the compared to wild conspecifics (Fig. ; Stuart et al., a,b; drivers of uncontrolled wild harvests, and in some cases in- Ji & Li, ). The nutritional composition of the diets of centivize conservation action (e.g. Gordon & Ayiemba, farmed snakes was broadly similar to natural diets ; Hardouin et al., ; MacGregor, ; Nogueira & (Dierenfeld et al., ; Whitaker et al., ). In terms of Nogueira-Filho, ; Natusch & Lyons, ). Given the behaviour, several species of snakes tend to aggregate ease and economic viability of producing snakes within (Gregory, ; Reed & Rodda, ) and appear to be re- closed-cycle systems, it is likely that this industry poses latively tolerant of high stocking densities. Snakes are also minimal conservation threat to wild snake populations. adapted to exploit a three-dimensional spatial landscape, There were three primary limitations to our study. displaying dual terrestrial and arboreal tendencies (e.g. Firstly, our findings relied on information supplied by farm- Alexander & Marais, ). Thus stocking rates may be − ers themselves, and we typically conducted interviews in the nearly double the  kg m recommended for meat

chickens in the UK (DEFRA, ). In terms of biology, metabolic regulation pythons can digest and assimilate large snake farming could potentially offer a cheaper, more hu- meals relatively quickly and then survive for long periods mane and more resource-efficient solution to food security. with no food (Pope, ; Secor & Diamond, , , Snakes are relatively cheap and easy to produce in a captive ). Snakes are not only adept at exploiting seasonal setting, compared to the effort required to find and capture gluts, they are also capable of surviving periods of famine wild snakes on a commercial scale, and therefore snake (Pope, ), and this gives farmers the freedom to synchro- farming could reduce illegal wild harvests. nize feed inputs with trends in local resources; for example, some farmers rely on amphibians during the monsoon season and rodents during the rice harvest season to provide Ecological sustainability the bulk of their annual feed inputs. Famine is often asso- ciated with increasing variability in climate, and in this con- Direct measures of ecological sustainability were limited, text snake farming could be a unique buffer against the and thus we relied on a number of assumptions and infer- impacts of climate change. Snake farming has also proved ences to facilitate objective interpretation. The landscape in to be a resilient livelihood activity in the face of increasingly much of Viet Nam is dominated by a patchwork mosaic of frequent epidemics of HN-type avian influenza (P. Aust, small-scale agriculture and wetlands (Dang et al., ), and unpubl. data), as the virus only infects endothermic animals farming methods remain largely traditional (e.g. harvesting such as pigs and poultry (Peiris et al., ). is by hand). These mixed agroecosystems support a rich diversity of anthropophilic species (Brown et al., ;  Halwart, ), many of which are abundant and resilient Welfare issues to seasonal exploitation. Examples of such species include amphibians and commensal rodents (Lawler, ; Gray The livestock industry often attracts the attention of animal et al., ; Brown et al., ), which are important food welfare groups because it advocates the intensive production inputs for the snake farming industry. By placing a value of higher-order vertebrates. Snakes display markedly infer- on these species, snake farmers are indirectly creating a fi- ior cognitive abilities compared to endothermic species such nancial incentive for preserving holistic environment- as poultry and pigs (Burghardt, ), and although their friendly farming practices, particularly where these are aggregation behaviour facilitates comparatively high stock- threatened by the advance of monocultures. The other im- ing densities, overall the surface area per individual remains portant feed input in the snake farming industry comprises relatively high because of their arboreal behaviour; for − by-products from existing food production chains. Snake example, a stocking density of  kg m actually equates − farms essentially recycle low-value waste protein from the to . kg m after accounting for shelf space, which is poultry, pork and fish industries and repackage it into a well below the recommended stocking density for meat high-value protein suitable for human consumption in the chickens (DEFRA, ). Currently, most production para- form of snake meat. meters fall within the broader standards prescribed by Snake farms require relatively minimal freshwater or science-based snake husbandry guidelines (e.g. Pough, ) chemical inputs and produce low levels of biological but issues such as veterinary care, transport and slaughter waste. In terms of ecological imperatives, snake farming is could benefit from further animal welfare-focused research in line with the principles of agroecological land-use prac- and development. tices and conservation agriculture (e.g. Jat et al., ; Scialabba et al., ), and may be a potential livelihood strategy for communities living within the buffer zones of Direct conservation outcomes protected areas (Hardouin et al., ). Wildlife farming in South-east Asia is often perceived to have negative impacts on wildlife conservation because it re- Social impact lies on, or at least exacerbates, the overexploitation of wild populations (Drury, ; Brooks et al., ; Snake farming requires minimal land or start-up capital and Cunningham et al., ). However, our findings suggest is an accessible, low input livelihood option for rural and that closed-cycle snake farming is both possible and profit- peri-urban small-scale farmers. It is often carried out in par- able, and cheap, high-quality farmed snakes could poten- allel with other livelihood activities such as rice farming or tially reduce the demand for wild-caught snakes. paid employment, and in these situations it often represents Competition from snake farms combined with prohibitive a windfall income or insurance policy (Nossal et al., in legislation and improved law enforcement has already press). The unique physiology of snakes offers vulnerable forced some professional snake hunters to turn to snake farmers flexibility in the way they cope with volatile eco- farming as an alternative livelihood (P. Aust, unpubl. nomic and environmental conditions. By means of adaptive data). Furthermore, snake farmers appear to place

significant importance on selective breeding as a means of Specialist Group, the Carnegie Corporation of New York increasing productivity. The fear of contaminating carefully (Global Challenge Initiative) and the National Research selected genetics with wild-type genes, in addition to the Foundation of South Africa. We thank the following orga- risks of introducing parasites and infectious diseases, pro- nizations for their contribution of staff time and institu- vides at least some motivation for farmers to actively pre- tional support towards fieldwork: The Institute of Tropical vent wild snakes from entering the commercial farm Biology, Viet Nam; the CITES Management Authorities of environment. Nonetheless, there is little to prevent people Viet Nam and China; the Forest Protection Departments of from opportunistically capturing wild snakes and selling Ca Mau, Ho Chi Minh City, Tay Ninh, Vinh Phuc and Phu them into trade (possibly as captive-bred individuals), and Tho provinces (Viet Nam); The Endangered Species we should assume this occurs in some cases. Although such Scientific Commission Office, Institute of Zoology, small-scale harvest is unlikely to present problems for spe- Chinese Academy of Sciences; Shenyang Normal cies that thrive in anthropogenic environments (Boeadi University (China); The Endangered Species Import and et al., ; Shine et al., ; Auliya, ), it may create Export Management Office (China); The Endangered challenges for the conservation of less plastic species, such Species Scientific Commission, China CITES Scientific as the king cobra (Stuart et al., b). A similar harvest- Authority; The Division of Wildlife Conservation, related question arises over the industry’s use of wild ani- Guangxi Forestry Administration (China); and the mals as a food source for snakes, and whether or not this Lingshan Forestry Administration, Qinzhou City (China). constitutes a sustainable practice. Further research is needed We are also grateful to the many farmers, farm staff and to clarify the role snake farming plays in the conservation of other industry stakeholders who participated in interviews wild populations and identify strategies whereby snake and took time to answer our questions. farming enhances rather than jeopardizes incentives for the conservation of wild snakes.

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ZHOU,Z.&JIANG,Z.() Identifying snake species threatened by potential of reptiles within a sustainable food security context. NGO economic exploitation and international trade in China. Biodiversity VAN TRI is a conservation biologist specializing in herpetological tax- and Conservation, , –. onomy and wildlife forensics. DANIEL NATUSCH is a biologist work- ing on the ecology, conservation and trade of reptiles in the Asia– Biographical sketches Pacific region. GRAHAM ALEXANDER has a particular interest in elu- cidating causality of range limitation in reptiles, and using this infor- PATRICK AUST is a conservation biologist with a particular interest in mation for conservation purposes. He is currently focusing on the applied herpetology. He is currently exploring the agricultural importance of snakes as predators in South African ecosystems.