CONSERVATION 570 CONSERVATION

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1 570 CONSERVATION CONSERVATION Herpetological Review, 2017, 48(3), by Society for the Study of Amphibians and Reptiles Back From the Brink: Ex-situ Conservation and Recovery of the Critically Endangered Burmese Star Tortoise (Geochelone platynota) in Myanmar The Burmese Star Tortoise (Geochelone platynota) is a medium-sized tortoise (carapace length [CL] to ca. 300 mm) endemic to the dry zone of central Myanmar (Fig. 1; Platt et al. 2011b). Chronic over-harvesting of G. platynota, mainly for domestic consumption by rural Burmese (Blyth 1863; Theobald 1868), coupled with habitat loss has resulted in widespread, albeit gradual population declines throughout its range (Platt et al. 2011b). Harvesting greatly intensified during the mid-1990s, driven by the burgeoning demand from wildlife markets in southern China STEVEN G. PLATT Wildlife Conservation Society Myanmar Program, Aye Yeik Mon 1st Street, Yadanamon Housing Ave., Yangon, Myanmar KALYAR PLATT Turtle Survival Alliance Myanmar Program, Aye Yeik Mon 1st Street, Yadanamon Housing Ave., Yangon, Myanmar LAY LAY KHAING Conservation and Forestry, Minzontaung Wildlife Sanctuary, Natowgyi Township, Myanmar THIN THIN YU Conservation and Forestry, Shwe Settaw Wildlife Sanctuary, Minbu, Myanmar SHWE HTAY AUNG Conservation and Forestry, Lawkanandar Wildlife Sanctuary, Bagan, Myanmar SAN SAN NEW Conservation and Forestry, Minzontaung Wildlife Sanctuary, Natowgyi Township, Myanmar ME ME SOE KHIN MYO MYO TINT LWIN WIN KO KO SWANN HTET NAING AUNG Wildlife Conservation Society Myanmar Program, Aye Yeik Mon 1st Street, Yadanamon Housing Ave., Yangon, Myanmar THOMAS R. RAINWATER * Tom Yawkey Wildlife Center & Belle W. Baruch Institute of Coastal Ecology and Forest Science, P.O. Box 596, Clemson University, Georgetown, South Carolina 29440, USA *Corresponding author; trrainwater@gmail.com (Behler 1997; Altherr and Freyer 2000) where G. platynota was sold as food and incorporated into traditional medicines (Platt et al. 2000). Demand from Chinese markets was soon eclipsed by illegal collecting for the high-end international pet trade, which resulted in the near extinction of wild populations (Platt et al. 2011b). By the early 2000s viable populations could no longer be found and G. platynota was considered ecologically and functionally extinct in the wild, even for those populations within the national protected area network (Platt et al. 2011a, 2011b). Consequently, G. platynota was designated a member of extinction row along with other high-risk chelonian taxa (Buhlmann et al. 2002), listed among the 25 most endangered chelonians in the world (Rhodin et al. 2011), and assessed as Critically Endangered by the IUCN (IUCN 2014). Captive-breeding was recognized as the only remaining option for preventing biological extinction of G. platynota and ultimately restoring this species as a functional member of the dry zone ecosystem (Horne et al. 2012). In 2004 the Nature and Wildlife Conservation Division (NWCD) of the Myanmar Ministry of Environment, Conservation and Forestry, in collaboration with the Wildlife Conservation Society (WCS)/Turtle Survival Alliance (TSA) Myanmar Program established three ex-situ assurance colonies (defined as demographically and genetically viable captive breeding groups of imperiled taxa maintained as a hedge against the extinction of wild Fig. 1. Captive-bred Burmese Star Tortoise (Geochelone platynota) released in scrub forest of Minzontaung Wildlife Sanctuary. PHOTO BY ELEANOR BRIGGS

2 CONSERVATION 571 PHOTO BY STEVEN PLATT PHOTO BY STEVEN PLATT Fig. 2. Food is placed on wooden trays for sanitary reasons and to disperse feeding activity within the breeding enclosure. Note shallow pool for drinking and soaking in middle of photograph. Fig. 3. Tortoise eggs are incubated in-situ within the breeding enclosures. Temporary wooden markers denote the location of the buried clutch, number of eggs, date of laying, and identification number of the nesting female. populations; Buhlmann et al. 2002) of G. platynota at Lawkanandar, Minzontaung and Shwe Settaw wildlife sanctuaries (LWS, MWS, and SSWS, respectively) in Myanmar with the objectives of 1) ensuring the biological survival of G. platynota by establishing a secure captive metapopulation and 2) producing sufficient numbers of offspring for eventual reintroduction into protected natural habitat. We herein provide a brief history of these efforts, review husbandry practices, summarize progress towards attaining the objectives of the assurance colonies, and discuss the conservation implications of this program. Site Description The three wildlife sanctuaries (MWS, SSWS, and LWS) hosting the assurance colonies are located within the central dry zone of Myanmar, a desert-like region formed by the rain shadow of the western mountains (Platt et al. 2011b). The dry zone is characterized by a monsoonal climate (annual precipitation = mm) with a truncated wet season (mid-june through September) followed by a prolonged dry season (October to early June); most rainfall occurs during August and September. High diurnal temperatures (to 43 C) are typical of the dry season with low nocturnal temperatures (to 4 C) occurring during January and February (FAO/UNDP 1982). Physiographic descriptions of SSWS (46,500 ha) and MWS (2260 ha) are provided elsewhere (Platt et al. 2001, 2003). LWS is a small (47 ha) urban protected area of planted forest on the outskirts of Bagan, an archaeological and cultural site of international importance. All three wildlife sanctuaries are located within the presumed historic geographic range of G. platynota (Platt et al. 2011b); both SSWS and MWS harbored wild populations of G. platynota until these were extirpated in late 1990s (Platt et al. 2001) and early 2000s (Platt et al. 2003; Thanda Swe 2004), respectively. Founding Stock The majority of founding stock for the three assurance colonies included juvenile, subadult, and adult G. platynota, most of which were confiscated from wildlife traffickers by NWCD enforcement agents. Lesser numbers of wild tortoises were collected from MWS and SSWS during the early to mid-2000s and placed in the assurance colonies when it became apparent these populations could no longer be effectively protected in the face of overwhelming poaching pressure. With the exception of wild tortoises collected from MWS and SSWS, founder provenance cannot be determined with any degree of certainty. Additionally, precisely enumerating the founders is challenging because inadequate records were maintained, tortoises were not individually marked, stock was occasionally transferred among colonies, some tortoises were stolen, and others were released during a premature and ill-conceived reintroduction attempt (Platt et al. 2011a). All things considered, our best estimate is that the founding stock consisted of 175 tortoises of an approximately equal sex ratio. These numbers are in keeping with the recommendation of Horne et al. (2012) that chelonian assurance colonies should consist of at least three groups of 50 individuals each (1:1 sex ratio) maintained at separate locations in order to maximize genetic diversity and minimize the likelihood of catastrophic loss through disease, accident, or natural disaster. Housing Juvenile (> 2 years-old), subadult, and adult G. platynota are maintained in outdoor enclosures and exposed to ambient environmental conditions throughout the year. Housing initially consisted of makeshift enclosures of wood, chain-link fencing, and low concrete walls, but underwent significant redesign and improvement in the wake of repeated thefts of tortoises during the early years of the project. Security considerations and husbandry requirements have driven renovation of the enclosures and remain of paramount concern. The renovated enclosures consist of a high (to 3 m) perimeter wall constructed of concrete blocks and heavy gauge fencing, topped with concertina wire, sharpened bamboo (pungi) stakes, or electrically charged wires. Entry to each enclosure is through locked gates with round-theclock security provided by sanctuary staff, who reside on-site. No tortoises have been stolen from the assurance colonies since these security measures were implemented. Within each enclosure, low walls (ca. 80 cm high) divide the facility into separate pens of variable size. Overhanging thatch shelters along the interior wall of each pen, and piles of dried vegetation, leaves, and palm fronds provide tortoises with shade

3 572 CONSERVATION and concealment. These refugia are extremely important because the availability of secure hiding places is known to reduce stress among captive tortoises and enhance breeding success (Ebenhack 2012). Moreover, piles of vegetation buffer against temperature extremes and create a humid microenvironment which may be important for proper shell growth (Wyrwich et al. 2015). Each pen contains one or two shallow (maximum depth ca. 10 cm) concrete pools for drinking and soaking. The latter is a critical consideration during April and May when diurnal temperatures regularly exceed 40 C. Because tortoises frequently defecate while soaking, water is changed at least once daily. The ground is swept and feces are removed from pens twice daily; in the morning and again in late evening. PHOTOS BY STEVEN PLATT Diet and Feeding Little is known concerning the diet of G. platynota in the wild, although limited field observations suggest it consists largely of grass and other foliage, with lesser amounts of fruits, invertebrates, and on occasion, vertebrate carrion (Thanda Swe 2004; Platt et al. 2011b; Me Me Soe et al. 2016). The standard diet of G. platynota in the assurance colonies consists of water spinach (Ipomoea aquatica), various locally available grasses, carrot roots and tops, cucumber fruit, and Roselle (Malvaceae) foliage, augmented with banana leaves and stems, gourd foliage, pricklypear cactus pads, and fruits of tomato, gourd, cantaloupe, papaya, and watermelon, depending on availability. Oxalate-rich foods are fed sparingly (e.g., figs and squash) or avoided (e.g., legumes and cabbage). Foods are washed to remove any lingering pesticide residues, and then chopped and thoroughly mixed before being offered to tortoises. Food is provided every afternoon ( h) on wooden trays to reduce the likelihood of fecal contamination and parasite transmission. Several feeding trays are placed at widely scattered locations in each pen to disperse feeding activity and ensure each tortoise has access to sufficient food (Fig. 2). Uneaten food is removed from the pens and feeding trays are washed with dishwashing soap and sun-dried at the end of the day. Given the size of the captive population, individual prophylactic deworming is impractical. Therefore, fenbendazole (Panacur, Merck Animal Health, Madison, New Jersey, USA) is mixed with food at a dosage of 50 mg/kg of body mass and administered annually to tortoises > 2 years old. Although high doses of fenbendazole administered over longer periods can cause toxicosis in tortoises (Neiffer et al. 2005), the dosage we administer follows recommended guidelines (Carpenter and Marion 2013). Reproduction and Hatchling Care Breeding groups of approximately equal sex ratio are maintained together in outdoor enclosures; courtship and mating occurs throughout the year (Thanda Swe 2004; Platt et al., unpubl. data). Egg-laying begins in late September and continues through mid-may. During this period, keepers monitor breeding groups throughout the day, noting when females begin excavating nests. Upon completion of laying, a wooden marker is inserted at the nest and labeled with the identification number of the female, date, and clutch size (Fig. 3). Females reach sexual maturity when 7 8 years-old and deposit one to four clutches each season; mean (± 1SE) clutch size and annual reproductive output are 4.4 ± 0.4 eggs (range = 1 11) and 9.9 ± 3.2 eggs/female/year (range = 5 16 eggs), respectively (Thanda Swe 2004). Females Fig. 4. Neonates are kept in secure, rat-proof wooden boxes for three months (above) before being transferred to a nursery building (below). Neonate boxes are shaded for most of the day. Note high security fence (behind the boxes) topped with concertina to deter thieves (above). hatched before 2010 and reared at the assurance colonies were now laying eggs at the time of manuscript submission. Eggs are incubated in-situ under ambient environmental conditions at all three assurance colonies. Because enclosures are shaded at LWS and more open at MWS and SSWS, there is concern over how this might affect incubation temperatures and hence offspring sex ratio (pivotal temperature ca. 30 C; Kuchling et al. 2011). Although secondary sexual characteristics are not yet evident in most cohorts, we noted a moderate male bias among older cohorts at LWS and a similar degree of female bias at MWS when assembling groups of subadult tortoises for release at MWS and SSWS (Platt et al. 2014, 2015). Despite the apparent bias, adequate numbers of both sexes are available for reintroduction. Should it be deemed necessary to manipulate sex ratios in the future, eggs could be artificially incubated in solar-powered incubators (continuous electricity is unavailable at MWS and SSWS). Hatching occurs from mid-may through mid-july and hatching rates typically range between 50 75%. The hard-packed substrate is moistened with water every morning during this period to facilitate hatchling egress from nests. Hatchlings exit the nest unassisted and are collected soon after appearing aboveground. Staff excavate each nest 24 hours after the last neonates emerge

4 CONSERVATION 573 to low overnight temperatures. Because neonates often develop respiratory ailments at the onset of the wet season, a multivitamin containing vitamin B complex and vitamin C (Envervon C, United Pharma, Yangon, Myanmar) is administered to all individuals < 2 years-old during this period. Current Captive Population Fig. 5. Combined annual production of Burmese Star Tortoise hatchlings at three assurance colonies in Myanmar ( ). Table 1. Captive population of Burmese Star Tortoises held by three assurance colonies in Myanmar (October 2016). Assurance colonies: Minzontaung Wildlife Sanctuary (MWS); Lawkanandar Wildlife Sanctuary (LWS); Shwe Settaw Wildlife Sanctuary (SSWS). Three hundred subadult tortoises reintroduced into MWS and SSWS are not included in this stock assessment. Age class Assurance 2 yrs Subadults Breeding Total colony adults MWS LWS SSWS Total to ascertain that all hatchlings have exited the nest and determine the number of unhatched eggs. Neonates are separated into groups of 50 and kept in wooden rearing boxes (122 cm long 122 cm wide 25 cm high with access via a hinged top) for three months (Fig. 4). After three months, neonates are transferred to a more spacious nursery building and maintained there until reaching three years of age. Nurseries are open buildings exposed to ambient conditions, containing low-walled (ca. 30 cm high) enclosures housing groups of neonates (Fig. 4). Because rats (Rattus sp.) represent a serious threat to neonates, nursery buildings are sealed with small gauge wire-mesh and rat traps are maintained along exterior walls. Shelters within each pen provide neonates with shade and concealment, and sunken concrete pools are available for drinking and soaking. Owing to their small body size, neonates are particularly vulnerable to dehydration. Therefore, during the late dry season when air temperatures exceed 33ºC neonates are manually gathered and placed in shallow water-filled basins for about 1 hour every morning. Neonate diet and feeding protocols are similar to those of other age classes except that foods are finely chopped and laced with supplementary calcium. Food is provided daily on wooden trays or banana leaves and uneaten material is removed in late afternoon. The pens are swept daily to remove feces and other debris. Young tortoises have been found to be susceptible to chilling when nocturnal temperatures drop below 21 C, and repeated chilling has been associated with respiratory signs such as serous nasal discharge and dyspnea (K. Platt et al. 2014). The use of heat lamps to maintain optimal temperatures is precluded by the lack of a reliable electrical source so small tortoises are instead covered with dry straw and leaf litter to reduce exposure Since 2008 the number of hatchlings produced at the three assurance colonies has been increasing at an annual rate of 37% (Fig. 5; average rate of increase calculated from slope of the linearized relationship between hatchling production and year; Bayliss et al. 1987). At the time of this writing (mid-october 2016) the total captive population of G. platynota in Myanmar consists of 7150 individuals (Table 1) with an additional > 1000 eggs currently being incubated. The captive population is dominated by younger cohorts, reflecting the success of propagation efforts in the last 5 6 years. Captive facilities are expected to reach maximum capacity within the next 2 3 years, although the reintroduction of head-started subadults into the wild (Platt et al. 2014, 2015) will no doubt extend this period. Discussion Ex-situ conservation of G. platynota is proving extremely successful in Myanmar because husbandry is relatively straightforward, and the species adapts well to captivity and reproduces readily in confinement. Our ex-situ conservation efforts have averted the near-certain biological extinction of G. platynota and its continued survival is no longer in doubt, one of the original objectives of the assurance colonies. The second objective to produce offspring for eventual reintroduction has likewise been met and large numbers of captive-bred tortoises are now available for release into protected habitats. Limited success to this end has already been achieved at MWS and reintroduction efforts are now underway at SSWS (Platt et al. 2014, 2015, 2016). Most importantly, the ultimate, albeit long-term objective put forth in the national conservation action plan (K. Platt et al. 2014) of restoring viable populations of G. platynota in every protected area within the central dry zone is now biologically attainable, although social and political challenges remain to be resolved. Geochelone platynota, together with the endemic and Critically Endangered Eld s Deer (Cervus eldii thamin) are considered iconic focal species for preservation of dry zone landscapes (Republic of the Union of Myanmar 2011). To date there has been no genotyping of captive tortoises in Myanmar, largely due to the costs associated with screening such a large population. Nevertheless, genotyping of at least the reproductive adults is warranted to avoid potential inbreeding, maximize the effective population size, and maintain sufficient levels of heterozygosity among the captive population. Although a transition from herd-level to individual management is impractical, achieving these objectives may entail restructuring breeding groups to maximize the likelihood that genetically high-value tortoises produce offspring. To further diversify the genetic base, it may be advantageous to incorporate additional tortoises into the assurance colonies from collections outside of Myanmar, such as the Turtle Conservancy (Ojai, California) and Taipei Zoo (Taipei, Taiwan). Of course, any importation of tortoises into the Myanmar assurance colonies must follow strict quarantine protocols to prevent the introduction of novel pathogens. Exsitu programs in other countries are also important as bulwarks

5 574 CONSERVATION against the potential loss of assurance colonies in Myanmar due to disease outbreaks, natural disasters, or political upheaval and accompanying civil turmoil. Our ex-situ conservation efforts for G. platynota in Myanmar highlight several advantages of establishing captive breeding programs within the natural range of a species (Durrell and Mallison 1987; Derrickson and Snyder 1992). First, local venues have a microclimate and photoperiod already appropriate for native animals making investment in potentially expensive climate control equipment unnecessary. This is certainly the case for G. platynota at the three assurance colonies in Myanmar where tortoises can be maintained year-round under ambient environmental conditions. Second, captives are more likely to be adapted to the disease environment within the range country. Of course, the possibility of introducing diseases from captive into wild populations must also be considered during any reintroduction (Cunningham 1996; Aiello et al. 2014), although with G. platynota this risk has been considerably reduced through rigorous health screening of individuals selected for release (Raphael et al. 2016). Third, the transfer of animals within the borders of a single country can be accomplished without being hampered by cumbersome international trade restrictions. Conway (1995) rightly cautions that husbandry and medical expertise might be lacking in less developed range states; however, our close collaboration with technical experts in the international zoo and veterinary community has largely nullified this concern (Raphael et al. 2016). Furthermore, a continuing emphasis on training and capacity building by the WCS/TSA Myanmar Program (K. Platt et al. 2014) has produced a cadre of highly knowledgeable and experienced staff at each assurance colony in Myanmar. In conclusion, ex-situ conservation efforts have secured the biological future of G. platynota in Myanmar. Because stockpiling animals in captivity is of little conservation benefit, the ultimate goal of any conservation breeding program should be the restoration of the target species as a functional member of its native landscape (Tudge 1992). Given the high value G. platynota continues to command in both the illegal and legal wildlife trade, increasing human population density in the dry zone of Myanmar, and limited representation of this landscape in the national protected area system, restoring viable wild populations poses a daunting, but not insurmountable, challenge to conservationists. Despite the difficulties involved, progress towards realizing this objective is nonetheless being made using offspring produced in the assurance colonies in Myanmar (Platt et al. 2016). Finally, our experience in Myanmar suggests the ex-situ conservation model we outline here is broadly applicable to other developing countries struggling to recover imperiled tortoises. Acknowledgments. Numerous people contributed to the success of this project since its inception in the early 2000s. We are especially indebted to U Nyi Nyi Kyaw (Director General) and U Win Naing Taw (Director) for their enduring commitment to Burmese Star Tortoise conservation. Turtle Survival Alliance is acknowledged for recognizing the pivotal role of ex-situ conservation in the recovery of the Burmese Star Tortoise and supporting the improvement of captive facilities at MWS and LWS. Than Myint, Rick Hudson, Colin Poole, Saw Htun, Bill Holmstrom, Lonnie McCaskall, Brian Horne, Andrew and Angie Walde, Cris Hagen, Bonnie Raphael, Shane Boylan, Katie Rainwater, and Paul Gibbons are thanked for their contributions. Financial support for tortoise conservation in Myanmar was generously provided by Andy Sabin and the Sabin Family Foundation, Helmsley Charitable Trust, Panaphil Foundation, Turtle Conservation Fund, Jeff and Mara Talpin, and Joan and Howard Oestreich. Deb Levinson and the interlibrary loan staff at Wildlife Conservation Society (New York) are thanked for obtaining literature, and Bonnie Raphael and Lewis Medlock commented on an initial draft of this manuscript. This paper represents technical contribution number 6544 of the Clemson University Experimental Station. Literature Cited Aiello, C. M., K. E. Nussear, A. D. Walde, T. C. Esque, P. G. Emblidge, P. Sah, S. Bansal, and P. J. 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