Mauremys annamensis is protected by national legislation in Viet Nam. It is included in Schedule IIB of Decree 32/2006/ND-CP, dated 30 March 2006, on Management of Endangered, Precious, and Rare Species of Wild Plants and Animals. Schedule II includes species whose utilisation is restricted to scientific research, establishing breeding populations, and international exchange; any such activities require a collection permit from the Ministry of Agriculture and Rural Development. Wildlife also needs permits to be transported nationally; such transport permits can be issued by provincial Forest Protection Department offices. A veterinary health certificate may also be required. Viet Nam’s Decree No. 159/2007/ND-CP sets out penalties for forest and wildlife crimes. Substantial strides have been made in enforcement of wildlife laws in Viet Nam, and recent confiscations of the species by government authorities have been transferred to a conservation programme (McCormack and Nguyen 2009, McCormack et al. 2014). Mauremys annamensis is also listed as a priority species for protection in Viet Nam under Decree 160/2013/ND-CP, dated 12 November 2013, on Criteria to Determine Species and the Regime of Managing Species Under Lists of Endangered, Precious and Rare Species Prioritized Protection. This law creates a system for identifying protected species, provides principles for the protection of listed species, and establishes a mechanism for managing the exploitation of these species.
Mauremys annamensis was included in CITES Appendix II at CoP 12 (Proposal 21, Santiago, Chile, 2002), which came into effect by 13 February 2003. A zero quota was imposed at CoP 16 (CoP16 Prop.32), effective 12 June 2013. The species was uplisted to CITES Appendix I in 2019, which came into effect on 26 November 2019. It is also included in Annex B of EU Commission Regulation no. 709/2010 (amending EC Regulation 338/97), which requires that a corresponding import permit must be issued by the country of import before a shipment of the species can enter the European Union.
In recent years, ex situ efforts to breed the species in captivity have developed from isolated attempts at reproduction towards coordinated breeding programmes, involving information exchange and management of genetics. A European studbook for the species has been established. Captive breeding at some European facilities has been so successful, with placement options being limited, that some institutions have started incubating only a portion of the eggs produced (Meier and Raffel 2011). In North America, a studbook and a Species Survival Plan for M. annamensis have been created through the Association of Zoos and Aquariums (Stern 2014).
Since 2006, an international programme has taken shape to reintroduce a viable population of M. annamensis into its native range. This project is led by the Asian Turtle Programme (ATP), and supported by local and national authorities, national universities, and the global turtle conservation community. Captive-bred turtles produced in Hong Kong, Europe and North America have been repatriated to Viet Nam, boosting the captive assurance population in the country in terms of numbers and genetic lineages. Field surveys in central Viet Nam have failed to confirm the species’ presence in any existing protected areas, and its occurrence in these protected areas seems unlikely due to a lack of suitable habitat (McCormack et al. 2014). To secure protected habitat, the ATP has been working with the Forest Protection Department of Quang Ngai Province and the local People’s Committee to establish a small Species Habitat Conservation Area (SHCA) for M. annamensis (McCormack and Ngyuen 2009). Approximately 100 hectares of suitable habitat have been identified by the ATP and its partners for the reintroduction programme (Horne et al. 2012). This project also includes a large outreach component to generate local support for conservation of the species through awareness and community engagement, a training component for local authorities, and a population monitoring programme (McCormack and Hendrie, 2007, McCormack and Ngyuen 2009, McCormack et al. 2014).
Mauremys annamensis is endemic to central Viet Nam, where it occurs in a narrow strip of coastal lowlands between the South China Sea to the east and the Annamite Mountains to the west. Eastward extensions of mountains reaching to the sea form the northern (Hai Van Pass) and southern (Ca Pass) boundaries of the species' distribution (Iverson 1992, Le et al. 2004, Fritz and Havas 2007, Nguyen et al. 2009, McCormack et al. 2014). Published records of M. annamensis exist from Quang Nam, Da Nang, and Gia Lai Provinces (Siebenrock 1903, Bourret 1941, Parham et al. 2006, Dawson et al. 2013, TTWG 2017). A wider range for the species has been suggested in some literature, although this idea appears to have been based on traded or misidentified specimens (McCormack et al. 2014).
The extent of occurrence (EOO) for M. annamensis is estimated at 12,500 km2 using the Delaunay triangulation technique. However, the area currently occupied by the species within this EOO is considerably smaller. At best, the estimated area of occupancy (AOO) is 10 km2 and continuing to decline. In recent decades, M. annamensis has only been reliably recorded from a single wild animal at one restricted location, although the species is suspected to occur in a few locations.
There are no quantifiable data available on the historic or present population sizes of Mauremys annamensis. However, Bourret (1941) described the species as abundant in ponds and streams at one site in the late 1930s. Over the next several decades, armed conflicts and politics in Viet Nam largely prevented additional fieldwork, and only one specimen, caught in 1966, has been documented from this time period (Dawson et al. 2013). Nevertheless, during recent interviews conducted by the Asian Turtle Programme (ATP), local residents indicated that the species was locally common in many areas through the 1970s and early 1980s; turtles would wander into houses and were even considered pests as large individuals trampled rice plants (McCormack 2012 in CITES AC 28 Doc. 20.3.9, McCormack et al. 2014).
Over the past 30–45 years (equivalent to approximately 2–3 generations of M. annamensis), a 99% reduction in the species' population is estimated to have occurred. Interviewees have reported to the ATP that when collection of turtles for trade first began locally in the mid-1980s, rice sacks filled with turtles (including M. annamensis and other species) could be collected in a single night (McCormack 2012 in CITES AC 28 Doc. 20.3.9, McCormack et al. 2014). Collection of the species intensified rapidly, and by the late 1990s, the M. annamensis population appeared to have declined steeply from prior years. Hendrie (2000) noted that “where once this species was observed more frequently in trade seizures, only a few specimens have been observed in 1998 and 1999. This reduction in observed occurrence within the trade, combined with loss in habitat and continued hunting pressures within its extremely limited known range, would suggest that M. annamensis is under serious threat of extirpation.”
Field surveys for M. annamensis in recent years have been mostly unsuccessful, indicating that the species is now extremely rare in the wild (Hendrie 2000 in CITES Proposal 12.21) In 2006, one individual was trapped by scientists within natural habitat McCormack et al. 2014). The species has continued to appear occasionally in illegal trade, but only in small numbers (Le et al. 2004; McCormack and Hendrie 2007; McCormack and Nguyen 2009). At one site in Quang Ngai Province closely monitored by the ATP, fewer than five new turtles were observed each year between 2008 and 2013 in local village households (McCormack et al. 2014). Given the economic value of M. annamensis in the trade, it is almost certain that any wild animal encountered by local people will be collected, and the species’ population is suspected to continue to decline by 50% over the next 15 years. By combining the population trends over the past two turtle generations and the one future generation, the ongoing population decline in this species is estimated to be 99%.
No specific details of the population structure of M. annamensis in the wild are known. However, a notable discovery occurred in 2012, when seven turtles identifiable as hybrids between M. annamensis and Mauremys sinensis were found in the wild (Blanck and Braun 2013). Genetic analyses have demonstrated the hybrid origin of such specimens, which previously received the name ‘Ocadia glyphistoma’ (Spinks et al. 2004, Stuart and Parham 2007). Mauremys annamensis appears to be sympatric with M. sinensis over much of the former’s range, and local people have portrayed M. annamensis as naturally being fewer in number, with a 10:1 ratio of M. sinensis to M. annamensis described during ATP interviews (McCormack 2012 in CITES AC 28 Doc. 20.3.9). The occurrence of hybrid offspring in the wild suggests that adult M. annamensis may now be so scarce that the few remaining individuals cannot locate suitable mates, leading to the interbreeding with other species (McCormack et al. 2014). It is likely that no more than 50 mature individuals remain in the wild.
The greatest threat to the survival of Mauremys annamensis is unsustainable exploitation as part of the so-called Asian Turtle Crisis (Hendrie 2000) – the expansive international trade in Asian chelonians for food, traditional medicine, and pets (van Dijk et al. 2000). Collection of the species for trade reportedly began in the mid-1980s. Local people interviewed by the Asian Turtle Programme (ATP) state that during that time, rice sacks filled with turtles (including M. annamensis and other species) could be collected in a single night (McCormack 2012 in CITES AC 28 Doc. 20.3.9, McCormack et al. 2014). Collection intensified rapidly, and by the late 1990s, the species’ population appeared to have dropped sharply. Most M. annamensis that entered the trade were destined for consumption in China, while smaller numbers were locally consumed in Viet Nam or entered the international pet trade (McCormack et al. 2014).
In recent years, M. annamensis has rarely been observed in wildlife trade shipments of central Viet Nam. Only modest numbers (less than 10) of the species have been seen annually in local trade since 2007 (McCormack and Hendrie 2007, McCormack and Nguyen 2009). This low volume of trade is probably due to a reduction in the number of wild turtles, which has made collection more difficult. However, although few turtles seem to remain in the wild, the high economic value of the species in trade means that people continue to have financial incentive to collect every individual encountered. Since 2007, the ATP has observed hatchling and juvenile turtles being collected from the wild and entering the trade. These small turtles are kept with the intention of raising them to a larger size before sale (thereby increasing their value) or in hopes of being able to breed the species in the future. Often, the realisation that the species is becoming rare is cited by local people as the reason behind collecting such small turtles, before someone else has the opportunity to capture the animals (McCormack 2012 in CITES AC 28 Doc. 20.3.9).
Another major threat to M. annamensis is habitat destruction (Dawson et al. 2013, McCormack et al. 2014). The lowlands of central Viet Nam have an extended history of human occupation. Despite this long period of settlement and the anthropogenic changes to the landscape (such as agricultural conversion) that occurred over time, M. annamensis has persisted in the wild until relatively recently. However, the loss of habitat to intensive rice cultivation and urban areas has increased dramatically as the human population of Viet Nam has grown tremendously in the 20th century. The central lowlands are now a major socio-economic centre of Viet Nam, containing cities such as Da Nang, one of the country’s largest and most densely populated urban areas. Many watercourses in the area have been substantially impacted by channelization, filling of low-lying areas, and draining of wetlands (McCormack et al. 2014). At one location where M. annamensis formerly occurred, suitable habitat no longer appears to exist (Dawson et al. 2013). Although the species could potentially still inhabit some modified habitats (e.g. flooded rice fields or urban canals), turtles in these areas have a greater chance of human contact, leading to an increased potential for collection. Development also poses the problem of environmental contamination from sewage, industrial effluents, and other pollution (McCormack et al. 2014).
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Mandai Wildlife Group (category and featured image)