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S19-15-02.doc

CONVENCIÓN SOBRE EL COMERCIO INTERNACIONAL DE ESPECIES Decimonovena reunión del Comité de Fauna Conservación y comercio de tortugas terrestres y galápagos [Resolución Conf. 11.9 (Rev. CoP12) y Decisión 12.43] DESARROLLO DE MEDIDAS DE CONSERVACIÓN A MEDIO Y LARGO PLAZO PARA LAS TORTUGAS TERRESTRES Y GALÁPAGOS Este documento ha sido preparado por la Autoridad Administrativa de Alemania a tenor de losresultados técnicos de un proyecto de investigación y desarrollo realizado por TRAFFIC AsiaSudoriental1.
Numerosas autoridades en los países de importación y exportación han puesto de relieve en losúltimos años la precaria situación en materia de conservación de las tortugas terrestres y galápagos deAsia sudoriental. La drástica disminución en curso de la mayoría de las 90 especies, combinado con eldecidido interés en la cooperación entre los Estados del área de distribución para abordar la cuestión,condujo al establecimiento del Grupo de trabajo sobre tortugas terrestres y galápagos del Comité deFauna. Además, en un cursillo celebrado en Phnom Penh, Camboya, en 1999, se pusieron de relieveimportantes resultados sobre los mecanismos y los niveles de comercio. En la 11a. reunión de laConferencia de las Partes (CdP11), se adoptó la propuesta presentada por Alemania para incluir elgénero Cuora en el Apéndice II.
Alemania continuó las actividades de investigación sobre el comercio y la conservación de las tortugasterrestres y galápagos, lanzando un proyecto sobre “Desarrollo de medidas de conservación a medio ylargo plazo para las tortugas terrestres y galápagos” que fue llevado a la práctica por TRAFFIC AsiaSudoriental a través de WWF Alemania. Además de la elaboración de propuestas complementarias deinclusión para la 12a. reunión de la Conferencia de las Partes (CdP12), la finalidad del proyecto eracompilar y evaluar la información sobre las actividades de cría comercial en cautividad y susposibilidades para reducir al mínimo los incentivos de capturar especímenes en el medio silvestre, yabordar el riesgo que podría resultar del hecho de críar en cautividad especies no nativas.
Adicionalmente, se examinaron las actividades de cría en cautividad para la conservación existentes yrequeridas para las especies de Asia Sudoriental.
Los resultados preliminares se sometieron a la consideración de los órganos internacionalespertinentes (Comité de Fauna, Grupo de trabajo del AC, cursillo en Kunming, China, en 2002).
Alemania y TRAFFIC Sudoriental presentan ahora los resultados finales a fin de apoyar las actividadesen curso del Grupo de trabajo del AC y alentar a la comunidad internacional a proseguir sus esfuerzosen favor de la conservación de este grupo de especies críticamente amenazado.
Investigador principal: Peter Paul van Dijk (dirección actual: p/a Fjordhest-Gard, Krimweg 125, 7351 TL Hoenderloo, PaísesBajos) Durante el cursillo sobre comercio de tortugas asiáticas en Phnom Penh en 1999, se puso de relieveque la cría comercial en granjas de galápagos en Asia era sustancial y generalizada. La cría comercialde especímenes de Pelodiscus sinensis era una actividad conocida que remontaba al al siglo XIX enJapón, que había pasado por varios ciclos de expansión y recesión, concretamente en Taiwán, y quealcanzó su punto álgido en Malasia y Tailandia a finales del decenio de 1990. Asimismo, se informó alos participantes en la reunión de las operaciones de cría comercial en granjas a gran escala enTaiwán que producían cientos de miles de crías de Ocadia sinensis anualmente. Por último, quedóclaro que establecimientos pequeños y medianos en China continental producían cientos por no decirmiles de especímenes de tamaño comercial de Cuora trifasciata, Mauremys mutica y posiblemente deotras especies de galápagos de caparazón duro.
La existencia de actividades de cría comercial en granjas suscitó la preocupación generalizada de quela cría en granjas a menudo requiere especies que no son nativas del área en que se realiza la cría engranjas o su comercialización. Así, pues, las perspectivas eran que podían establecerse poblacionesviables a partir de animales que habían escapado o se había puesto en libertad deliberadamente. Seespeculó ampliamente acerca de los impactos de dichas poblaciones, desde la competición con lastortugas nativas debido a la contaminación genética hasta las alteraciones fundamentales de losecosistemas locales, pese a que se reconoció que existían escasos datos de campo objetivos.
En el Anexo 1 al presente documento se exponen dos estudios de campo sobre la cría en granjas detortugas que fueron completados como parte del estudio realizado por TRAFFIC Asia Sudoriental, ennombre del Organismo Federal de Alemania para la Conservación de la Naturaleza (Bundesamt fürNaturschutz, BfN). El primero de ellos, en octubre de 2001, se realizó en conjunción con la Universidadde Berkeley, California, a fin de investigar la genética de las tortugas criadas en granjas. En el curso deeste estudio se visitó una granja de tortugas de gran tamaño que albergaba 40 especies diferentes enel centro de la Isla Hainan, China; otros establecimientos de cría en la Provincia de Guangdong; elmercado Qing Ping en la ciudad de Guangzhou; y mercados de alimentos y animales de compañía enHong Kong. Este estudio confirmó el drástico aumento de los esfuerzos de cría en granjas de tortugasen China continental, que remontaban al menos al decenio de 1980. El segundo estudio se realizó enseptiembre de 2002 para evaluar la situación actual de la cría en granjas de tortugas de caparazónblando en Tailandia. Los resultados fueron sorprendentes, mientras que hacía tres años existían milesde granjas, sólo pudo encontrarse una que seguía teniendo un plantel de tortugas de caparazónblando; las demás granjas se dedicaban a la cría de camarones, tilapia, gouramis u otros peces.
Como parte del proyecto, se compiló información sobre la cría comercial en granjas de galápagos. Seconstató que había escasa información en la literatura técnica internacional, ya sea en obras sobreherpetología o acuicultura, así como en fuentes informales como periódicos, estadísticasgubernamentales o documentos informativos. Sin embargo, en los idiomas locales había ampliainformación en China y Tailandia en forma de manuales de instrucción para criadores de tortugasposibles o existentes, publicados con la participación de las empresas de equipo de acuicultura ysuministro de alimentos y los servicios gubernamentales de acuicultura correspondientes. Estosmanuales no solo se publicaban en forma de folletos poco caros, al precio de uno o varios euros, sinocomo discos video compactos en China, a precios similares.
En el Anexo 2 de este documento se presenta un examen de la cría en granjas para la conservaciónde los galápagos en el marco del mismo proyecto BfN/TRAFFIC Asia Sudoriental. La mayoría de lainformación se obtuvo a partir de las revistas para aficionados en el pasado decenio, pero gran partede la información complementaria sobre las actividades en curso se recibió por correo electrónico yotros contactos personales. De particular importancia fue el Simposio Internacional sobre tortugasterrestres y galápagos celebrado en Viena, en enero de 2002, al que asistieron aficionados y otrosamantes de las tortugas de más de 20 países, para asistir a unas 85 presentaciones sobre la cría encautividad de determinadas especies de tortugas, los avances en los cuidados veterinarios para lastortugas, y la situación y la historia natural de las tortugas silvestres. El investigador principal participó,en la medida de lo posible, en actividades de la Turtle Survival Alliance y trató de mantenerse al día delos últimos acontecimientos en los países europeos donde no se habla inglés y en Asia, lo queconstituye una tarea imposible dada la amplia gama de actividades realizadas, en curso o prevista entodas esas regiones. En la Sección 2 del Anexo se indican las tendencias y algunos de los logros de lacría en cautividad en favor de la conservación de esas especies.
(English only/ Seulement en anglais / Únicamente en inglés) Review of Commercial Breeding of Turtles concerning Asia
Species of freshwater turtles widely bred for Asian trade Turtle breeding operations in Asia are dominated by farming of the Chinese softshell turtle, Pelodiscussinensis (previously known as Trionyx sinensis or Trionyx japonicus), and its culture and trade history isdescribed in some detail below. This species is favoured for commercial culture by its combination ofsuitable characteristics, being rapid growth rate, relatively high annual reproductive output, widespreadconsumer acceptance, and extensive understanding of conditions for farming.
Other species of freshwater turtles are also bred commercially in varying quantities and at varyingdegrees of self-sustainability. Reasons for breeding species other than the Chinese softshell turtle includehigher value per animal or per kg for some species, convenient local availability of founder stock ofcertain species, or environmental conditions that are better suited for farming of particular species.
At least one farm exists in Hainan, China, whose owner claims to breed 10,000 hatchlings of the softshellturtle species Palea steindachneri. While it is difficult to verify the number, there is no doubt thatsignificant numbers of eggs and hatchlings are produced within the confines of the farm, and thatadditions of wild-caught founder stock, if any, are infrequent. Thus, this farm is well on its way to self-sustaining, closed-cycle captive breeding of this highly valuable species (Shi & Parham, 2001; Shi,Parham & van Dijk, pers. obs. 2001).
A number of enterprising individuals in Thailand and perhaps elsewhere have investigated thepossibilities to farm the native Amyda cartilaginea softshell turtle. This species, however, proved to haveslower growth and lower annual reproductive output than the Chinese softshell turtle, particularly undersimilar tropical conditions, and any increased value per kg of Amyda was insufficient to competefinancially with the higher productivity of Pelodiscus. All these operations eventually switched to farmingonly Chinese softshell turtles.
In rural parts of India, various forms of ranching and breeding of the Flapshell Turtle, Lissemys punctata,are undertaken by persons and communities. The primary aim of such activities is protein production forthe owner, as the species is partly vegetarian and ponds are stocked at such low densities that feeding isnot necessary. No quantitative information is available on the number of ponds involved or the totalquantities produced annually, but given the levels of subsistence consumption and the legal protectionstatus of the species under Indian legislation, trade in this species is not significant at present. Thespecies does, however, present a potential additional subject for large-scale farming, with a much lowerassociated risk of becoming an invasive species in its native range (Whitaker, 1998; Whitaker, pers.
comm. to van Dijk, Dec 2001).
Fewer farming operations concern themselves with hard-shelled freshwater turtles, mainly because mosthardshelled turtle species grow and reproduce significantly slower than soft-shelled turtle species whilefetching similar or lower market prices per kg. Farming hard-shelled turtles is thus a market that cannotcompete directly against softshell farming in the general food trade. It is thus restricted to niche markets,such as the supply of turtles to the medicinal trade, for release at temple ponds and other waters forpurposes of religious merit, and supply to the international pet trade, Species farmed in great quantitiesfor these purposes are predominantly Reeves’ Turtle Chinemys reevesii, and the Chinese Pond TurtleMauremys mutica in mainland China, and the Chinese stripe-necked turtle Ocadia sinensis, in Taiwan(Chen et al., 2000).
Beyond these species there is a wide variety of captive breeding efforts for a wide variety of turtle speciesin a wide variety of locations. These include pilot and small-scale projects to investigate the potential ofparticular species for mass or high-value production, as well as operations breeding small or modestnumbers of turtle species specifically for the international pet trade. Although the numbers may bemoderately significant in the pet trade and from a conservation perspective, these species and quantitiesare insignificant compared to the total commercial production for the mass consumption market.
Noteworthy in particular is that rearing and farming efforts have encompassed a range of North American species, including species such as Trachemys scripta elegans and Chelydra serpentina which haveraised concerns about their invasive potential elsewhere. Species recorded in farming statistics andobserved at turtle farms in China are listed in Table 1.
Table 1. Species of freshwater turtles involved in commercial farming in China.
[over 10,000 hatchlings produced annually, according to statistics of the Endangered Species Import andExport Management Office of P.R. China (Shi & Fan, [Annual hatchling production between 1000 and 10,000 Cuora amboinensis, C. flavomarginata – likely in thiscategory Observed in farms but not confirmed to be bred insignificant quantities Based on statistics from the Endangered Species Import and Export Management Office of P.R. China (Shi & Fan,2002), Shi & Parham (2001), and Shi, Parham & van Dijk (pers. obs. 2001).
A noteworthy amount of applied scientific research is carried out in China on refining farmingmethodologies for hardshelled turtles. Much of this research is unknown and almost inaccessible in theWest, but an indication can be gained from the observation that Volume 8 of Cultum HerpetologicaSinica, published in June 2000, contained a wide range of herpetological papers regarding taxonomy andgeographic distribution, but also a paper on advances in Chinese softshell culture (Li, 2000), two paperson different aspects of captive breeding of Cuora flavomarginata (Lu et al, 2000a, 2000b), a paper ontemperature sensitivity of ‘Color turtle of Brazil’ [=Trachemys scripta elegans] (Wang, 2000) and adetailed paper on inducing early oviposition in Chinemys reevesii and Mauremys mutica through injectingchorionic gonadotropin and its application to increased farm productivity (Li & Tang, 2000).
Noteworthy is that all commercial production systems involving freshwater turtles are closed or nearly-closed operations. Adult breeder animals are kept in enclosed conditions at the farm until their death, or sale. Additional adult brood-stock may be acquired from the wild, either from local native populations orthrough regional and international trade in wild-harvested turtles; however, no hatchlings or head-startedanimals are ever released and no attempts have been made for management of animals living free atpart of their life stages. This is likely to results from the combination of biological factors and issues ofcommunity resource stewardship (or more specifically, the lack thereof). In the case of small, high-value,tolerant animals, it makes economic sense to keep the animals under tight control and security at alltimes. Thus, ranching of freshwater turtles does not occur and does not appear to be a viable approach inthe near or medium-term future. The stock management at most Asian turtle farms examined appears tobe haphazard: additional breeder animals from varying sources are added whenever convenient.
Documentation of stock acquisition and stock movements are apparently absent. As a result, verificationof farms as Captive Breeding operations in the sense of CITES Resolution Conf. 10.16 (Rev), wherebyclosed-cycle reproduction to the second captive-bred generation is required, appears not feasible in thenear future except for most operations farming Pelodiscus sinensis.
Traditionally, farmed Chinese softshell turtles produced in Japan and Taiwan were mainly used fordomestic consumption as a delicacy, and very little exports occurred. Following the success of Chineseathletes coached by Ma Junren in the late 1980s and their widely-publicised diet including turtle blood,demand for turtle meat and “health supplements” containing turtle parts increased greatly in Eastern Asia.
To meet this demand, imports from abroad increased, as did domestic farming of Chinese softshell turtlesin mainland China. Demand also developed in Chinese communities elsewhere, as evidenced by theimport into the USA of 28,683 medicinal preparates involving softshell turtle between 1989 and July 1994(Bright in Salzberg, 1994).
During the 1990’s, almost the complete production of Chinese softshells in Thailand was exported toHong Kong, Taiwan and China, which were guaranteed markets. The domestic consumption market inThailand was insignificant, though as native Amyda stocks in Thailand declined, farmed Pelodiscus wereoffered more frequently in domestic markets in the mid-1990’s. By about 1997, wholesale export priceshad risen to levels that domestic Thai consumers were unwilling to pay, and softshells disappeared fromThai markets and domestic trade outside the seafood speciality sector. Farms in Malaysia and Indonesialikewise exported almost their entire production to mainland China, with Singapore being an importantadditional market.
An important secondary market for farmed turtles is the demand for turtles as part of medicinal preparations.
The full extent of the nature and preparation of turtles for medicinal purposes is poorly documented inwestern languages, but is known to involve jelly and powder preparations containing variously the shellbones of tortoises and hard-shelled freshwater turtles, shell bones of softshelled turtles, and whole tortoisesand freshwater turtles. The Pharmacopoeia of the People’s Republic of China specifies the use ofChinemys reevesii for this purpose (Liu et al., 1999). However, much of the demand for turtle shell bones isthought to be met by use of shells from a wide variety of wild-collected turtle species (Wu et al., 1998),which is partly a by-product of the consumption trade. Farming of Chinemys reevesii is extensive, asindicated by annual production of about 910,000 hatchlings per year, and increasing annual productionvalues of 266 to 427 metric tonnes in the period 2000-2002. The percentage of reported production which isspecifically destined for medicinal purposes is unknown. Ocadia sinensis also has significant potential formass production to meet the demand for turtle shell bone as a component in Traditional Oriental Medicine,particularly in Taiwan where the Pharmacopoeia does not prescribe the exclusive use of Chinemys reevesii(Chen et al., 2000).
The third significant destination for farmed freshwater turtles is the international pet trade. Hatchlings ofOcadia sinensis have been traded in significant numbers in recent years in Asian and global pet markets,and these are understood to have originated from the Taiwanese farming industry. The substantialnumbers of hatchlings and small juveniles of Cuora flavomarginata and Geoemyda spengleri on offer inpet markets in mainland China, Hong Kong and beyond are likely to originate from captive farmingoperations, as such hatchlings are extremely difficult to find and collect in the wild (e.g. Chen & Lue, inpress) and the animals are in good, healthy condition when traded. That hatchlings and juveniles ofCuora trifasciata and Mauremys mutica recorded in the pet trade originate from captive breeding iswithout much doubt given the documentation of extensive farming of these two species.
Commercial culture of freshwater turtles in controlled conditions was pioneered in Japan by a Mr. Hattorinear Tokyo, who started with locally native Pelodiscus sinensis softshells in 1866. At the turn of the 19th century, softshell farming was still a very small segment of aquaculture activities in Japan, involving theHattori business with about 13.6 hectares of pond devoted to the species and “several minor turtle farms”.
The Hattori establishments were expected to produce 82,000 eggs in 1904, expected to yield about60,000 animals of market size in 1907 (Mitsukuri, 1904).
Softshell farming developed in Taiwan in the 1950’s and was a small component of aquacultural activitiesuntil about 1970, when production increased quickly, to collapse during the early 1990s and increaseexponentially again in the late 1990s. Farming of softshell and other freshwater turtles in mainland Chinadeveloped with economic liberalisation in the 1980s. In the mid- to late 1980s, farming of Chinesesoftshells Pelodiscus sinensis also gained interest in tropical Asia. The origin of the initial founder stock isnot clear, but is likely to have originated from Taiwan.
In Singapore, Choo & Chou (1984, 1986, 1992) studied various aspects of aquaculture practices andbiological parameters of the Chinese Softshell and Singaporean entrepreneurs developed softshell farms innearby southern Peninsular Malaysia (Heng, 1998). Many of these farms initially experienced problemsdeveloping suitable husbandry practices and failed to succeed. By 1985, a few aquaculturists in Thailandalso experimented with the species, with varying dedication and success. In Thailand, the AgriculturalFoundation included a softshell farming manual (Kamneung, 1989) in its widely-sold series of illustratedbooklets advising rural farmers on agricultural opportunities and improvements. The Thai aquaculturesupply-industry noticed the emerging sector as well, and started publishing infomercials, booklets with tips,techniques and advertisements for food pellets, pumps and other items, and organised seminars. In the1990’s, farming of Chinese softshell turtles expanded exponentially in both Malaysia and Thailand and twotypes of ‘softshell turtle farm’ developed. A small number of farms maintained brood-stock of Chinesesoftshell turtles, usually imported from Taiwan, to produce eggs and incubate these. A small proportion ofthe resulting hatchlings were retained and raised for sale to the consumption trade and for expanding andrejuvenating the adult founder stock, while the larger part of the produced hatchlings were sold to thesecond type of farms, the rearing operations. These operators raise the purchased hatchlings to amarketable weight of about 500 grams each in about one year. The size of rearing farms in Thailand rangedfrom 24 to 3520 square meters pond surface (Anonymous, 1998). These rearing farms, mainly smallindependent aquaculturists working on commission or through co-operatives, were located all over Malaysiaand Thailand, but concentrated in Johor in southern Malaysia and Rayong, Chanthaburi and Trat in south-eastern Thailand. By 1998, Thailand contained over 10,000 farming and rearing operations(Plengmaneepun, 2001); the total number of turtle farms in Malaysia has not been reported but is likely tohave been hundreds if not thousands.
Perception of regulations in effect has limited farming developments in Indonesia, where rearing ofhatchlings imported from Thailand, Malaysia or Taiwan was initiated in North Sumatra in 1997 (Samedi &Iskandar, 2000).
In 1999, China imposed restrictions on imports of farmed softshell turtles because of contamination withSalmonella bacteria. This was followed by further restrictions on farmed softshell turtles as well as wild-collected turtles as part of China’s tightening of wildlife conservation and trade regulations. Around thesame time, domestic supply of farmed softshell turtles reached peak levels and prices began to dropthrough normal market mechanisms. By 2000, prices for softshell turtles and other high-value freshwateraquaculture products had diminished by as much as 50 percent (Wang, 2001).
As a result, export volumes from Thailand and Malaysia plummeted and wholesale prices slumpedcorrespondingly, leading many farmers to close or switch activities. Of over 10,000 farms operating inThailand in 1998, 6000 remained in 2001 (Plengmaneepun, 2001), and these were reduced to a handfulof moribund operations in September 2002, most operators having switched to culturing freshwaterprawns or fish. Of 30 farms operating in Langkap, Malaysia, in 1997, only 4 were left in May 2000 (MimiSyed Yusof, 2000).
As the main export market closed, softshell turtle farmers outside mainland China looked for alternativemarkets to sell their production. This remains a challenge, since consumption of turtle meat in HongKong, Korea and Japan combined has been reported as only 5% of the consumption in China(Plengmaneepun, 2001) and Singapore remains a limited market. Many hatchlings were traded into theglobal aquarium and pet trade. New markets are sought for prepared gourmet soups, meat and otherdishes from farmed Chinese softshell turtles, including internet marketing in Germany (Bennett's Trading,2002).
The only Asian country currently experiencing an increase in softshell turtle farming is Viet Nam, whereaquaculturists are understood to have started only recently to culture softshell turtles, presumablyPelodiscus sinensis, and where production mainly supplies the domestic market.
Chen (1990) pointed out that farming of softshell turtles (and most other turtles), like farming predatoryfish, is a net protein reduction. Turtles are a culinary novelty, to be marketed in up-market and exclusiverestaurants and to a lesser extent for high-end home-cooking. Softshell farming will not provide protein tothe starving poor, and while many rural aquaculturists earned well during the period of peak demand,many have subsequently been affected severely when turtle prices slumped below production costs andincomes were insufficient to meet loan obligations and operating expenses. Thus softshell farming hasproven a temporarily very profitable activity for some, but the very rapid developments have also broughtdebts and other problems to many farmers and investors.
Turtle farms usually have separate spawning ponds, hatching enclosures, nursery ponds and grow-outponds. Usually all walls are vertical concrete, often with a protruding lip at the top to avoid escape.
Mitsukuri (1904), Kamneung (1989), Chen (1990), Heng (1998) and Zhou (2000) provide detaileddescriptions of various pond constructions, feeding regimes and husbandry techniques in differentcountries. Open-air ponds are standard in tropical and sub-tropical areas, including southern China, butpartly or entirely enclosed and seasonally heated operations are widespread in areas with coolerclimates. Farms range in size from a few square metres on a balcony or a spare room to several hectaresin the countryside. At their peak, large farms in Thailand and Malaysia would each contain, at anyparticular moment, 10 to 25,000 turtles of marketable size (400-600 grams) (Mimi Syed Yusof, 2000).
Mitsukuri (1904) reported that in Japan the softshell turtles spent long periods in hibernation and grewslowly as a result of the climatic conditions in the Tokyo area, yet produced about 20 eggs per clutch and2 to 4 clutches per female per year. Hatchlings measure on average 27 mm, one-year olds 45 mm and 28g, two-year-olds 105 mm at 169 g, 3-yr animals 125 mm at 300 g, 4-yr-olds 160 mm at 563 g and five-year old animals to reach 175 mm Carapace Length (CL) at a weight of 750 g. These animals were fedon a diet of mainly crushed fresh clams, as well as dried fish scraps, silkworm pupae, boiled wheat grainetc. In Taiwan, hatchling turtles (2-3 cm, 2-4 g) are fed daily with a mixture of trash fish paste and eelfeed pellets. Daily feed ration is about 10% food weight per weight of stocked turtle for small animals, and5% for larger animals. The feed conversion factor is 8-12, meaning that 8-12 g fish paste is required toproduce 1 g of softshell turtle (Chen, 1990). Ideally, after 3 months their average size is 4-5 cm at 10gand after 10 months 10 cm and 40-70 g. Average survival during this period is 70%. Under goodconditions, with 2 feedings per day, 50% of hatchlings reach the “large” category (over 500 g), 35% reachmedium (300-500 g) and 15% stay below medium and are thus not marketable. In Taiwan, Chinesesoftshell turtles reach sexual maturity at the age of one year and a weight of about 500 g, but olderfounder stock (6-9 years) is preferred as eggs of young females are small and believed to hatch inferiorjuveniles. Up to 6 or 7 clutches (50-200 eggs) may be laid by a female annually (Chen, 1990). Similarrates of growth to marketable size and sexual maturity were reported for mainland Chinese turtle farmingoperations (Zhou, 2000).
Current productivity of commercial breeding In the past two decades, farming of freshwater turtles has developed and expanded exponentially inmainland China. Data on production levels and trends were not available outside the Chinese-languageliterature until very recently; the only available source of quantitative information are the statistics from theEndangered Species Import and Export Management Office of P.R. China (Shi & Fan, 2002, Table 2).
Some of these figures are unfortunately not entirely clear, particularly the reported quantities held andbred in Guangxi and Zhejiang Provinces appear optimistic. Including values for these provinces, some303 million Pelodiscus sinensis are held in P.R. China, of which 150 million in Guangxi and 120 million inZhejiang. From this, Zhejiang produced 25 million commercially traded animals in 2000, 30 million in2001 and 35 million in 2002, while the corresponding figures for Guangxi were 17.2, 13.0 and 10.8 millionanimals, respectively. In contrast, the 23 million animals held elsewhere led to market supplies of 46, 48and 52 million traded animals during those years. Such proportional differences are not fully consistentwith known growth rates in farm conditions, and it appears that hatchlings traded to rearing farms areincluded in the statistics for ‘commercial individuals’. Production statistics by weight are similarlydominated by the quantities provided for Zhejiang and Guangxi – of 52 thousand metric tons (mt)produced throughout P.R. China in 2000, 20,000 mt was produced in Zhejiang and 8,900 mt in Guangxi.
For 2001 the total was over 62 thousand mt, of which 30,000 mt from Zhejiang and 7,800 from Guangxi; in 2002 the quantities were over 67 thousand mt for the country as a whole, with 35,000 mt from Zhejiangand 6,500 mt from Guangxi. Thus, total production increases reported for all of China are caused solelyby reported production increases in Zhejiang.
Probably a better statistic to gauge the extent of Mainland Chinese softshell farming would be thereported numbers of adult breeder animals, a total of over 37 million animals, producing 375 million eggsfrom which 286 million hatchlings emerge.
Table 2 Total Production of Chinese Softshell turtles in P.R. China as recorded in statistics of theEndangered Species Import and Export Management Office of P.R. China (Shi & Fan, 2002).
Annual Pelodiscus sinensis production by number Annual Pelodiscus sinensis production by weight, in Thus, while most of P.R. China produces animals averaging 500 grams, Zhejiang consistently reportsproduction figures that represent an average value of 1 kg per animal. Production values in provincesother than Zhejiang and Guangxi show a very gradual increase over the 3-year period, though productionof Chinese softshells in Guangxi is actually reported to be in decline, while production in Zhejiang isincreasing in size at a proportionally very rapid rate, reputedly making annual gains greater than the restof China combined over the 3-year period.
Despite uncertainty in the available data, it appears evident that the People’s Republic of China,particularly in Hainan and the southern mainland, possesses an extensive sector in the aquacultureindustry producing Chinese Softshell Turtles. If reported figures are correct, Mainland China hassurpassed the combined production of Thailand, Taiwan and other formerly dominant turtle farmingregions by an order of magnitude.
In Taiwan, a few metric tons (mt) of Chinese Softshells were produced annually in the 1960s, increasingsteeply in the early 1970s to yield 323 mt in 1973 (Chen et al., 2000). Production declined slowly afterthat, and by 1978 172 ha of softshell culture ponds produced 282 mt of turtle. The decline continuedduring the 1980s, due to a declining market demand, with production down to 186 mt of turtles and downto “probably not much more than a handful” of turtle farms encompassing 32 hectares by the late 1980s(Chen, 1990). The deepest point was reached in 1991, when only 21 tons were produced. As domesticeconomic conditions improved, while exports to China, Hong Kong, Macao and Southeast Asiadeveloped since 1995, and thus demand grew throughout the 1990s, farm output shot up to reach 2237mt in 1997 (Chen et al., 2000). Available production figures for Taiwan are provided in figures 1 and 2; noquantitative data are available after 1997.
Figure 1. Annual production of hatchlings Chinese Softshells, Pelodiscus sinensis. From Figure 2. Annual production of ChineseSoftshells, Pelodiscus sinensis, by weight.
From Chen et al., 2000 The country that pioneered commercial culture of freshwater turtles, Japan, is not known to haveproduced significant quantities of Chinese softshells or other non-marine turtle species for a long time.
The total number of individual turtles recorded as exported by the Fisheries Department of Thailandpertains almost completely to farmed Chinese Softshells, since native turtle species are protectedunder domestic legislation and therefore should not be exported. Re-export numbers for exotic petspecies are negligible, and production and export of Red-eared Sliders, Trachemys scripta elegans,are not known to be significant in Thailand. Thus total turtle export records are assumed to indicateexports of farmed Chinese Softshells, Pelodiscus sinensis, and since only a minimal part of farmproduction was marketed domestically, these export records in Table 3 give a fair indication of totalproductivity. The number of just over 470,000 in the first 7 months of 1998 (van Dijk & Palasuwan,2000) does not include the bulk of that year’s export, as most harvesting occurs at the end of the wetseason, in time for the peak demand in East Asia as winter falls, thus most consumption exports occurat the end of the year.
Table 3 Total exports of turtles from Thailand asrecorded in statistics of the Fisheries Departmentof Thailand (in van Dijk & Palasuwan, 2000). Unitsare individual animals. Peak production levels for the Thai farming industry were probably even higher. By October 2001, theremaining 6000 farms in Thailand were reported to be producing 300,000 hatchling turtles and 25 metric tonsof market-sized turtles for consumption (about 55,000 animals of 450 grams each) per day, presumablyduring peak season only. These quantities were stated to be half the peak quantities produced in 1998(Plengmaneepun, 2001).
Production quantities for Indonesia, Malaysia and Viet Nam are not available.
Farmed softshell turtles generally fetch good prices. Mitsukuri, in 1904, noted softshell price in Japan asabout 6.50 to 7.50 yen per kwan (=8.25 lb/3.75 kg), equivalent to about USD 1.00 per kg (1904 dollar). In1995, price for softshell turtles in Thailand irrespective of species had increased to about THB 150 per kg ofwhole animal, about USD 6.00. At the peak of the trade, during 1997 and 1998, prices reached THB 500 toTHB 900 (USD 20-30) per kg in Thailand and MYR 43 (USD 11.30) per kg in Malaysia. Following thecollapse of exports to China, prices per kg slumped to MYR 15 (USD 3.95) in Malaysia in early 2000 and toTHB 80 (USD 2.00) in Thailand in late 2001, by which time production costs were THB 120 per kg (MimiSyed Yusof, 2000; Plengmaneepun, 2001). Prices of hatchling turtles shipped from Thailand to China forlocal rearing dropped from THB 7 (USD 0.18) to THB 1 (USD 0.03) over the same period, also suffering fromcompetition with hatchlings produced by large-scale Taiwanese farms (Plengmaneepun, 2001). BySeptember 2002, wholesale price for market-sized softshell turtles was no longer known as there was nowholesale demand anymore; it appeared unlikely that prices over THB 50 per kg could be realised. As notedpreviously, wholesale prices in China also reduced by up to 50% by the late 1990’s (Wang, 2001).
Production quantities for hard-shelled turtles in Mainland China are even more difficult to determine than forproduction of Chinese Softshells. The only available quantitative statistics, those from the EndangeredSpecies Import and Export Management Office of P.R. China (Shi & Fan, 2002), indicate remarkablyoptimistic population and production quantities in some provinces, notably Guangxi, while other productiondata (e.g. Cuora trifasciata in Hainan) appears underestimated from observed farm stock sizes. Given thevery high individual value of some of these species, farmers working with these species are extremelysecretive about their holdings and production (Shi & Parham, 2001; Shi & Fan, 2002).
With so much uncertainty associated with the available data, it is impossible to draw reliable conclusions onthe extent of farming of hard-shelled turtles, though all available information indicates that production isextensive and involves a multitude of species.
There is little doubt that mass farming and rearing of the American Red-eared Slider (Trachemys scriptaelegans) occurs in mainland China, as evidenced by significant quantities of obviously captive-born andraised animals being offered in East Asian food markets, including animals of captive-bred colour varieties.
According to statistics from the Endangered Species Import and Export Management Office of P.R. China(Shi & Fan, 2002), about half a million Trachemys scripta have been produced for commerce annually in thepast three years. This is still less than recorded exports of T. scripta hatchlings from the USA to P.R. Chinain recent years, which amount amounted to 4.65 million animals in 1998, 4.71 million in 1999, 7.50 million in2000, and 1.74 million in the first 10 months of 2001 (LEMIS data), suggesting rearing of imported hatchlings represents a very significant part of the total trade volume. The dynamics of this are likely to be significantlyaffected in the near future by China’s termination of allowing imports of turtles smaller than 10 cm shelllength (Endangered Species Import and Export Management Office of P.R. China, 2002).
Other hard-shelled turtle species are also apparently farmed in great numbers. These include Chinemysreevesii, an adaptable species native to temperate parts of China. Some 234 thousand adult breederanimals are reportedly in farms, nearly all in Hunan Province, producing some 1.88 million eggs annually,from which 910 thousand hatchlings emerge, producing from 630,000 to 93,000 animals for trade annually inthe past three years (Shi & Fan, 2002). Ocadia sinensis is farmed in both mainland China and Taiwan, withclose to 400,000 adult breeder animals mainly in Hubei and Guangxi producing between 1.5 and 2 millionanimals for trade annually in the past three years (Shi & Fan, 2002). Available data for Taiwan does allow anestimate of total annual production, but this is likely very substantial as many farms are thought to exist andthe largest of these produce over 30,000 hatchlings annually (Chen et al., 2000). Statistics from theEndangered Species Import and Export Management Office of P.R. China (Shi & Fan, 2002) indicate thatclose to a quarter of a million hatchlings of Mauremys mutica are produced annually, mostly in GuangxiProvince. Substantial production of this species, at a level of at least a thousand hatchlings in a single largefarm, has been verified independently in Hainan (Shi & Parham, 2001; Shi, Parham & van Dijk, pers. obs.
2001).
In mainland China there is a number of farms that concentrate on breeding an extremely valuable turtlespecies, the Chinese Three-striped Box Turtle Cuora trifasciata. This species is perceived to have cancer-preventing and cancer-curing properties (Lee, 1999), and may retail at USD 1500 for an adult animalweighing about one kg (2001 price). Given the very high value of these animals, farmers working with thesespecies are extremely secretive about their holdings and production, and reliable data are difficult to obtain.
There is little doubt, however, that production is extensive, given that dozens or hundreds of modest-sizedfarms exist, and that the largest of these may produce up to a thousand hatchlings annually from up to 500-700 adult breeding animals (Shi & Parham, 2001; Shi, Parham & van Dijk, pers. obs. 2001). Statistics fromthe Endangered Species Import and Export Management Office of P.R. China (Shi & Fan, 2002) generallycorrespond to these perceptions, while indications remain to be confirmed that some 60,000 hatchlings of C.
trifasciata
are produced annually in Guangxi province.
The issue of exotic turtle species and their potential as invasive species Chinese softshell turtles are easily cultured in the Southeast Asian tropics, and the animals have beentraded alive locally in Thailand, Malaysia, and Singapore (van Dijk & Palasuwan, 2000; Sharma & Tisen,2000), as well as China, Taiwan, Hong Kong and Macao. Escaped or liberated animals have been reportedfrom a number of places, including Thailand and Sarawak, and nests have been observed in the wild. Thespecies’ staying power can be observed in Hawaii, where small populations of Pelodiscus sinensis, and P.
steindachneri
, persist in limited habitat despite apparently incidental exploitation (Ernst et al., 1994). Onepossible result may be that feral tropical populations of Chinese Softshells will be larger, in numbers andpossibly in biomass, than current populations of native Amyda cartilaginea softshell turtles. Growing rapidlyand reproducing within one to three years, Chinese softshells have a much higher potential recruitment thannative A. cartilaginea, which may require a considerable size and up to a decade to reach sexual maturity. Atcurrent hunting pressures, most A. cartilaginea are caught before they reach reproductive age, andrecruitment is below what natural levels should be.
It is not certain what effect, if any, the anticipated establishment of Pelodiscus sinensis will have on tropicalecosystems. Precise data are lacking, but one may assume that P. sinensis ecologically approximatesjuvenile Amyda cartilaginea of similar size. The tropical Southeast Asian ecosystems, or what remains, haveevolved in the presence of softshells since at least the Miocene. It is worth noting that Pelodiscus species,which have been present in Central and East Asia for at least 12 million years (Kordikova, 1991), did notsuccessfully invade tropical ecosystems in the presence of larger native softshell turtle species. It is alsoworth noting that Thai softshell farmers consider that adult Chinese softshells are physically exhausted at theage of four or five years, in contrast to maximum ages of well over a decade attained in native subtropical ortemperate habitats; it appears that ‘Life in the Fast Lane’ in the tropics does not suit the species long-term.
Thus, while feral populations of Pelodiscus sinensis may establish themselves and reproduce successfully,particularly in human-dominated landscapes, it is far from certain that it would survive long-term in thepresence of healthy populations of native Amyda softshells. Whether feral populations of Chinese SoftshellTurtles would succeed in reaching and establishing themselves in the slope forest stream habitat inhabitedby the Malayan Softshell Turtle, Dogania subplana, in the Thai-Malay Peninsula and Indo-MalayanArchipelago remains to be determined.
Three other species of freshwater turtles have been widely traded and raised in Asia in recent years, all fromtemperate North America: The Red-eared Slider Turtle, Trachemys scripta elegans, the Snapping Turtle,Chelydra serpentina, and the Alligator Snapping Turtle, Macroclemys temminckii. In particular, the Red-eared Slider Turtle has established feral populations throughout the world through release or escape of petanimals, and these populations are seen with varying degrees of concern in many parts of the world,including France, Italy, California, South Africa, Israel, Taiwan, Thailand, Cambodia, Malaysia and Australia(e.g. Bouskila, 1986; Dupré, 1996; Ferri & di Cerbo, 1996; Chen & Lue, 1998). In the context of theEuropean situation, unsupported speculation that the larger Red-eared Slider Turtles would be significantcompetitors for the smaller native species, and could predate juvenile of the native species, has assumedthe status of incontrovertible fact. The European Union went as far as to prohibit the importation of thesubspecies in 1997 because it is assumed to represent a potential threat to European native freshwaterturtle species. Yet in its documentation on the import ban, the European Union admitted that it was notaware of documented ecological damage. Luiselli et al. (1997) documented significantly lower wintersurvivorship of introduced juvenile Red-eared Slider Turtles compared to juvenile native European PondTurtles Emys orbicularis. Chelydra and Macroclemys have been traded in much smaller numbers andbecause of their cryptic lifestyle are unlikely to be noticed even if they established feral populations, but thepotential for establishment is high and particularly Chelydra serpentina shares the adaptability to a widerange of habitat, food and other ecological conditions that Trachemys scripta possesses. So do thesespecies represent a significant potential threat to native Asian turtle populations and ecosystems? Theinformation needed to give an answer with certainty does not yet exist, but a number of considerations arerelevant.
When considering the potential ecological impacts of established Sliders Turtles in tropical and subtropicalAsia, it is important to remember that in its native area Trachemys scripta is an integral part of a diversecommunity of freshwater turtles. It has evolved to share its habitat with many other turtle species, somelarger and some smaller than itself. These include turtles of the genera Chrysemys, Pseudemys, rarelyGraptemys, Deirochelys, Kinosternon, Sternotherus, Chelydra and Apalone, with varying degrees of overlapin habitat and food preferences (Gibbons, 1990; Ernst et al., 1994). Trachemys scripta is an opportunisticspecies, but generally does not occupy new opportunities to the exclusion of other turtle species, and haseven less success penetrating existing communities.
When humans create new habitats, such as reservoirs, within the natural range of Trachemys scripta, theturtle community that develops to take advantages of the new opportunities is closely related to the evolvedhabitat selection of the various species. In reservoirs in the Tennessee Valley, Trachemys scripta, normally aspecies of lentic water, occurs mainly at the shallow end of coves where creeks enter, Pseudemys concinnaoccurs further towards the main lake, while the riverine Graptemys pseudogeographica, P.ouachitensis andApalone mutica prefer the deep water area at the mouth of the cove (Lindeman, 1997).
One long-term experiment exists of the effects of Slider Turtle introduction into an ecosystem where Emydidturtles did not form part of the evolving community: the invasion of Meso-America by Slider Turtles since thePleistocene. As climatic and geological conditions permitted, Trachemys turtles have expanded their rangesouthwards from the USA and Mexico and now occur throughout Central America, Colombia, andVenezuela, and localised in Brazil, Paraguay, Uruguay and Argentina. As the Slider Turtle expandedsouthward, it encountered resident turtle communities of Staurotypus, Claudius, Dermatemys,Rhinoclemmys, Podocnemids and Chelids. Many of these turtles have very different habits and would notexperience potential impact from the invading Trachemys, but other species theoretically could be impactedby competition, viz. Dermatemys mawii and Podocnemis lewyana. Yet an overview of the region’s fossilturtles and the present distribution and natural history of turtles in Central and South America shows that theestablished groups have largely stood their ground, and Trachemys is an uncommon species restricted topond habitats in isolated areas (Moll & Legler, 1971; Wood & Diaz de Gamero, 1971; Pritchard & Trebbau,1984; Iverson, 1992). The fact that the species has diversified greatly in colouration and sexual dimorphismin the course of its invasion (a dozen or more subspecies in Latin America: Legler, 1990) while apparently noevolutionary pressures worked to force reproductive adaptation to a tropical climate (Moll & Legler, 1971)suggests that Slider Turtle populations were relatively small and isolated for much of the history of their LatinAmerican venture.
So what developments can be predicted resulting from the existing or imminent establishment of SliderTurtles in Asia? Asia has developed rich and complex turtle faunas in adjoining regions. Relatively few turtlefossils are known from Asia, but known information indicates that species, genus and family ranges haveexpanded and contracted, invaded and become extinct. A dynamic community formed under such conditionsis likely to adjust to the arrival of another species. The Red-eared Slider Turtle, faced with this residentcommunity, will likely find its niche where it has developed it in its native region and become a part of thefauna of vegetated lowland ponds, lakes, canals and other slow-flowing waterbodies. There is little chance of Red-eared Slider Turtles establishing dominant populations in either hill or forest streams or in large openrivers and reservoirs. Competition for food may occur with several native freshwater turtle species, but foodsupply seems hardly a limiting factor in Asian wetlands. Any competition for food will be between the variousspecies of turtles, fish, waterfowl, various invertebrates and other animals, rather than simply restricted tointer-turtle competition. The possibility that a large Red-eared Slider Turtle might prey on a hatchling of anative turtle species is undeniable, but the native turtle species have long proven to survive in an ecosystemwhere their young may be preyed upon by large native softshells or other turtles, monitor lizards, herons,storks and other large wading birds, raptors, large predatory fish and other predators. Hatchling predation ispartly a function of hatchling density and tendency to swim in open water and the density of predators, ratherthan the simple number of potential predatory turtle species present in the ecosystem. Conversely, Red-eared Slider Turtles may become food for native predatory species as well. Displacement of native turtlesfrom basking sites by boisterous Slider Turtles is a potential problem in areas where the native species bask,such as mainland China and Taiwan, yet only in exceptional circumstances are suitable basking sites alimiting factor. It seems very unlikely that Slider Turtle populations would not be controlled by the ecologicalcomponents that control native turtle populations. Slider Turtles are not inedible or poisonous, and are thussubject to density-related predatory controls. Indeed, humans may impact sufficiently on adult Red-earedSlider Turtles to keep their populations well below ecological tolerances.
It is obvious that feral Red-eared Slider Turtle populations are most likely to establish in areas intensivelyimpacted by humans, such as urban and agricultural areas, which are precisely the areas where native turtlecommunities have been most impacted. Declines of native turtle species in human-impacted landscapeshave been widely documented throughout the world. It is convenient to blame observed declines in nativespecies on the presence of a non-native species, but without a convincing causal link, this is not justified.
Thus, the potential ecological threat posed by the establishment of feral populations of Trachemys scriptaelegans, or Chelydra serpentina or Macroclemys temminckii by analogy, cannot be predicted based on ourcurrent understanding of the species’ biology in non-native areas. It is possible that these exotic freshwaterturtle species may never become properly established long-term in Asia, in which case they would notrepresent cause for concern. They might establish, locally or regionally, and become part of a balanced localcommunity of freshwater turtle species and other organisms. Or they might become a pervasive ecologicalmenace. Only continued monitoring of non-native freshwater turtle distribution combined with ecologicalstudies of turtle communities in Asia and beyond can provide answers and suggest methods for activemanagement of non-native freshwater turtle populations.
Outlook for the Asian turtle farming industry and its effects on conservation of Asian freshwater turtle species What has become clear is that the Asian freshwater turtle farming industry has been and continues to be avery dynamic aquaculture activity. Turtle farming, particularly of Chinese Softshells, has developed, grownand declined in Japan, Thailand, and Malaysia, it appears to be in a peak phase in mainland China, and maybe on the second decline cycle in Taiwan. Clearly, turtle farming has developed into an established activitywhere profits are made and lost by many farmers and investors based on the economic forces of supply anddemand. A vast consumer market exists, with deep-rooted traditions to consume turtles, and thus demand islikely to persist as long as the underlying cultural traditions of East Asia remain intact. The novelty ofconsuming turtle has worn off for a large part of the potential consumers, and farmed turtles have become amass commodity. Declining prices and relatively steady reported production quantities indicate that thedemand is not likely to increase further in East Asia. What may increase, though, is the demand for morevariety or better quality turtles for consumption, demands which are anticipated by current farmingdevelopments emphasizing high-quality product output (Zhou, 2000) and diversification of the number ofsoftshell and hardshell turtles farmed in significant numbers (Shi & Fan, 2002).
To the South, softshell turtles are esteemed as a delicacy among parts, though not all, of the humanpopulation of tropical Southeast Asia. Traditionally, a steady supply of Amyda cartilaginea softshells wascollected from the wild, partly through targeted collection and partly as by-catch from general rural fisheriesactivities and during agricultural activities. As this supply was diverted from domestic markets towards themore lucrative export trade, domestic restaurants and markets were supplied with production overruns fromfarms culturing Chinese Softshells. While many consumers professed a preference for wild-collected nativesoftshell turtles, few if any consumers were able to differentiate between the species when alive or wholefrozen, and even fewer when butchered or as prepared dishes. Wholesale export prices rose to record levelsby 1997-1998, exactly at the time that Southeast Asian countries were trying to recover from the regionaleconomic collapse of October 1997. Thus, the entire production of farmed and wild-collected softshells wasexported, and softshell turtle disappeared from domestic markets for several years. When the Chinesemarket for farmed softshells began to close incrementally from 1999, there were no active domestic marketsto divert local farm production supply to. A combination of factors seems to have prevented re-establishing softshell turtles as a mainstream consumption item in Southeast Asia, particularly Thailand; these factorsprobably included continuing economic austerity, a reduction of conspicuous consumerism, an increasedgeneral awareness of and sympathy towards wildlife conservation, and a shift towards acquiring moreprepared meals and raw produce from supermarkets rather than wet markets.
Farming of the Chinese softshell turtle is almost completely self-sufficient wherever farming occurs. Adultbreeder animals are rarely collected from the wild to be added to farm brood-stock. As such, the industrydoes not appear to represent a significant threat to the species’ existence, but neither does it encourageeffective protection and conservation of remaining wild populations of this species.
What has become apparent is that in the past few years, the numbers and volumes of freshwater turtlesproduced in farms has substantially exceeded the numbers that are collected from the wild for internationaltrade. At peak levels, the international trade in Asian freshwater turtles was estimated to amount to 12 to 20million turtles annually in the late 1990’s, of which half was farmed (van Dijk, 2002). Current productionstatistics indicate that up to 125 million freshwater turtles may be farmed for consumption (Shi & Fan, 2002),exceeding even the highest estimates of collection levels from the wild by an order of magnitude. While suchfarmed supplies do not eliminate the demand for wild-collected turtles entirely, indications are that the supplyof farmed turtles has stabilised market prices and prevented excessive prices leading to excessiveexploitation of all wild turtle populations.
To what extent the availability of Viagra has led to a reduction in demand for wildlife dishes reputed toincrease sexual performance is impossible to assess at present, but this development has been claimed tohave played a role in the trends of demand for tiger products.
More importantly, though, is that current farm production levels are sufficient to meet consumer demand, andthat farming practices are diversifying and improving to offer the consumer a wider variety of better-qualityproducts. No longer dependent on imports to meet consumer demands, regulatory authorities in majorimporting countries can now take measures to address negative international perceptions that their citizens’purchasing power is ravaging Southeast Asian and global biodiversity. Combined with an understandabledesire to protect their domestic aquaculture industry from the threat of diseases introduced through importedfreshwater turtles, and the desirability to reduce the outflow of currency as payment for importedcommodities, imports into major Asian consumer states have gradually been restricted in recent years, and itis likely that that trend will continue. As the major export markets for South and Southeast Asian turtletraders disappear, so will the incentive to collect their native turtle populations for the export trade.
Subsistence exploitation and regional trade will continue, but no longer driven by the power of internationalcommerce.
Can turtle farming supply enough turtles to meet all market demand for turtles? No, because demand is open-ended and turtle farming will never be able to compete economically withfish or chicken production.
Can turtle farming replace imports of wild-collected turtles for the Asian consumption markets? Most likely, because already farm production is significantly larger than the total amount of turtlescollected from the wild for export to East Asia. Consumer demand for more variety and better qualityturtles for consumption are challenges that turtle farmers are already addressing.
Can turtle farming reduce exploitation pressures on wild populations of freshwater turtles? Probably, because 1. farmed turtles represent a consumer alternative that keep overall turtle pricesstable, and thus prevent excessive price developments leading to excessive exploitation pressures onwild populations, and 2. farming supplies are large enough that importing nations are no longerdependent on import supplies and are increasingly free to restrict imports of wild-collected freshwaterturtles, which represent veterinary, economic and public relations liabilities.
Are there any negative aspects to turtle farming? Yes, founder stock collection, genetic pollution and invasive exotics are but three of the potential threatsassociated with turtle farming. The alternative, however, is unmanaged exploitation of remaining Asianand global tortoise and freshwater turtle populations, which is vastly worse.
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(English only/ Seulement en anglais / Únicamente en inglés) A Review of Conservation Breeding of Threatened Asian Tortoises
and Freshwater Turtles
A widespread and widely accepted definition of Conservation Breeding is not yet available, but for thepurposes of this report the concept of Conservation Breeding is considered to refer to breeding of animals inconfined and controlled conditions whose primary objective is to maintain or increase the number ofindividuals for purposes of biological conservation. Thus the objectives of Conservation Breeding are distinctfrom commercial breeding or recreational animal keeping, although the practical actions may have much incommon. In an ideal world, Conservation Breeding would not be necessary because species conservationaction at the habitat level would be sufficient to safeguard species survival; in the real world, however,populations and species may be depleted faster than they could recover in Nature, through a variety ofreasons, and maintaining a number of animals in secure conditions acts as a safeguard. Should primary,habitat-based conservation actions fail to secure the species in Nature, then the species could be re-introduced to the wild with animals bred in captivity. Captive-bred individuals can also strengthen populationnumbers of declining or depleted populations. Re-introduction generally can only occur successfully whenthe original factors leading to the decline and/or extinction of the population or species no longer operate, atleast not at levels that threaten the survival of the re-introduced population. Examples of successfulconservation breeding programs include the Père David’s Deer, the Arabian Oryx, the Pink Pigeon ofMauritius, and the Hood Island (sub-species of Galapagos Tortoise (Geochelone [nigra] hoodensis).
Conservation breeding and the Asian turtle crisis As the Asian Turtle Crisis developed during the 1990’s, many people with an interest in tortoises andfreshwater turtles became gravely concerned that the economic forces for exploitation, combined withextensive habitat degradation, would lead to the extinction of a number of populations and even species ofAsian turtles. The severity of the threats facing Asia’s turtles became clear during the Phnom Penhworkshop: more than half of all species were considered more threatened in 1999 than in 1996, including 18Critically Endangered species among 67 threatened species, out of a total of 90 species. ConservationNGOs obviously took notice and began or continued to address some of the threats. Yet many of the mostconcerned people were not professional conservationists, but European and American hobbyists whoobjected to the thought that a species that they lovingly keep in their home might become extinct in Nature.
Among these people, who in their daily lives were occupied with a regular job, children’s education and amortgage, a determination developed to do something tangible to help the survival of Asia’s threatened turtlespecies, something where THEY can make a difference. The problem is simple: too many turtles aredisappearing from Nature. The solution can also be simple: more turtles can be produced. But neither theproblem nor the solution are that straightforward.
The solution to the Asian Turtle Crisis is not to produce more individuals of as many turtles species aspossible; in this respect, conservation breeding efforts could never match the production levels ofcommercial farms. When addressing conservation issues regarding Asia’s turtles, the goal should be toensure the long-term occurrence of turtle species in their natural range and habitat. If some turtle species arethreatened with extinction in the wild throughout their range, then it is desirable to establish a captiveassurance colony in a different place, to allow the species to survive until the threats have been eliminated orat least reduced substantially. When threats have ceased, animals from the assurance population can be re-introduced to the wild to re-establish the species in Nature. Thus the goal of conservation breeding is tomaintain a captive population whose individuals are maximally suited to eventual re-introduction. Theprincipal aim of any re-introduction should be to establish a viable, free-ranging population in the wild of aspecies, subspecies or race, which has become globally or locally extinct, or extirpated, in the wild. It shouldbe re-introduced within the species’ former natural habitat and range and should require minimal long-termmanagement (IUCN, 1998).
Assurance animals maintained in captivity with the eventual aim of re-introduction into depleted or extirpatedpopulations therefore must have maximal chances of survival in their original range and habitat, and must not do damage to any remaining wild population of the species or its ecosystem. Specifically, this means thatanimals in assurance colonies must meet a number of criteria (IUCN, 1998), among which the most pertinentare: • Release animals drawn from captive or artificially propagated stock should be from a population which has been soundly managed demographically and genetically, according to the principles ofcontemporary conservation biology.
• Prospective release stock must be subject to a thorough veterinary screening process before shipment from the original source; animals with less than ideal health should not be used. Transport should occurin a manner that minimises risk of contagion or disease during shipment.
Clearly, these conditions are fundamental to the establishment and management of assurance populationsfor Asian tortoises and freshwater turtles. There is a strong case for the establishment and management ofex-situ assurance colonies of certain species of Asian tortoises and freshwater turtles, a case that has widesupport among many conservationists and concerned individuals. But the need to move beyond maintainingin captivity a large number of individuals of a large number of species is not always understood clearly.
A particular concern with conservation breeding of Asian turtles is that most efforts occur in facilities where avariety of species are kept together or in close proximity. As a result, transmission of bacteria, viruses andmulticellular parasites between different species is almost unavoidable, and a number of cases are known orsuspected where a non-damaging commensal organism associated with one tortoise species has given rise toserious disease problems in another species. Nevertheless, veterinary issues can be dealt with at the level ofindividuals or populations in particular facilities, and should not represent systemic concerns for re-introductionfrom assurance populations.
Genetic issues concerning conservation breeding of turtles A more pervasive concern for assurance colonies for Asian tortoises and freshwater turtles involves theirgenetics. Several of the species where assurance colonies are highly desirable are widespread but severelydepleted in Nature; examples include Batagur baska, Chinemys reevesii, Cuora galbinifrons, C. trifasciata,Mauremys mutica, Pyxidea mouhotii and Sacalia quadriocellata. These species, and even more of thespecies currently under lower threat levels, are known or suspected to have differentiated into locally distinctforms at finer, more complex resolution than current taxonomy recognizes. Thus, assurance colonies forsuch species must take this into account and consist of founder stock from natural genetic units. For knownor suspected diverse species, several separate assurance colonies may be required, representing riverbasins, mountain ranges or other geographical units defining natural genetic units. Collecting suchgenetically compatible founder stock is probably the greatest challenge to the development of true assurancecolonies for Asian tortoises and freshwater turtles, because what are currently developed into conservationbreeding colonies is dependent on present-day practicalities: what is available as potential founder stock arepredominantly animals acquired through international trade with no reliable indication of geographic origin.
Because of the realities of recent taxonomic research concerning turtles, there remains concern that evencoarse determination of an individual animal’s origin through its subspecies status is not always reliable,since some species or subspecies may not be taxonomically distinct but instead be selected individualsshowing particular morphological characteristics (e.g. Platysternon megacephalum, or the Cyclemyscomplex), and for many taxa the exact range of distribution remains poorly defined or meaningless (e.g.
several of the Cuora species). Strategies to collect genetically compatible founder stock for assurancecolonies could be implemented by specific collection of a suitable number of animals from a single distinctpopulation; there are of course substantial legal, biological, practical and logistic issues to be addressed insuch a scenario, but it is possible. A proxy approach would be to acquire founder stock from a singlecommercial shipment, in the assumption or at least hope that the animals were collected from the samepopulation and stocked and shipped as a group; such assumptions can subsequently be tested withmolecular genetic tools. A practical complication with genetic testing of animals is that there is very little fielddata to ‘anchor’ such genetic results from captive animals: very few, if any, Asian turtle species have beenproperly profiled genetically, meaning determination of genetic variability and diversity within individualpopulations and among different populations throughout species’ range. Such data is slowly accumulating,however, and with long-lived animals like turtles there is time to collect the data and adapt captive populationmanagement to the results.
The alternative to careful genetic management is the approach that ‘in the absence of anything, something isbetter than nothing’. There is something to be said for breeding whatever animals are available right now,regardless of their geographic origin and genetic affinity. It can be argued that it is better to acquire at least some offspring from mature animals of unknown origin, than to wait for science to sort out the population andindividual genetics and run the risk that the animal dies in the meantime. There is always hope that geneticresults arrive early enough that animals can be re-assigned to more suitable partner animals, and theirgenes contributed to a proper genetically compatible assurance population, possibly after a sufficiently long‘quarantine’ period to address the issue of sperm storage in female turtles. Any previous offspring, if laterproven genetically undesirable, can be removed from the bloodline and conservation breeding program. Atthe very least, these offspring have contributed to refining captive husbandry, incubation and raisingpractices and skills, as well as encouraging continuing enthusiasm among the people keeping and caring forthe animals and the wider public.
There are other genetic concerns inherent in ex-situ captive breeding for conservation or other purposes. Asignificant challenge is long-term genetic diversity, to prevent inbreeding. The particular details of inbreedingare not always fully clear, and inbreeding risks apparently differ among taxonomic groups, with reptiles beinggenerally less susceptible to inbreeding defects than mammals, but a minimum population of 500 unrelatedmature reproductive animals is generally considered appropriate in conservation biology. This is a twinproblem facing many prospective assurance colonies of Asian tortoise and freshwater turtle species: 500mature reproductive animals do not exist in captivity in the case of many species, regardless of relatedness.
Also, the facilities and expertise to care for 500 adults plus several hundred offspring are simply notavailable. Add to this the desirability of assurance colonies for some 25 to 40 species, many with differentsubspecies or otherwise distinct management units, and suddenly a task of caring for some 25,000 individualturtles is faced by perhaps one hundred dedicated hobbyists, zoos and other facilities. This would clearly bean impossible prospect.
Thus, choices must be made, in the number of species and genetic groups for which assurance colonies canbe managed, and in the number of individual turtles that can realistically be managed. Optimal managementof available animals and available facilities will be crucial. Studbooks are needed to manage availableindividuals, genetics and bloodlines, and taxon management plans are needed to make optimal use ofavailable facilities and other resources. These resources, and the people in possession of them, form thetaxon management group. Widest possible participation in the taxon management group is desired becausethis increases the numbers of participating individual turtles and thus genetic diversity, and it increases theamount of enclosures available.
Studbooks for a small number of tortoises and freshwater turtles, including several Asian taxa, were initiatedby the Dutch Turtle & Tortoise Society in 1992, as they realised that wild turtle populations were decliningand increasing European legislative restrictions would lead to a situation where various species would nolonger become available through imports. To keep the species available for hobbyists, they had to becomeself-supporting, and sharing of husbandry information, inventorization of animals and genetic management ofbreeding were considered essential for this. Over the years the number of species for which studbooks weredeveloped grew, as did the geographical spread of the participants. A management structure was neededand an umbrella organization, the Overkoepelend Orgaan Stamboeken (OOS) or Coordinating BodyStudbooks, was established as a charitable foundation in 1997. By September 2000, studbooks were activein the Netherlands, Germany, Austria and Switzerland for 32 Asian turtle taxa. Through conservationpriorities and personal interests, Chinese species became a focus of attention within the OOS, leading to theestablishment of the Europäische Erhaltungszuchtinitiative für Chinesische Schildkröten (ECS) or EuropeanConservation Breeding Initiative for Chinese Turtles, in 1997, with participation of dedicated organizationsand individuals from the Netherlands, Germany, Austria, Switzerland, Hungary, the Czech Republic andSlovenia.
Similar concerns led to similar conclusions in the United States, and an all-inclusive alliance dedicated toconservation breeding of endangered species of Asian tortoises and freshwater turtles formed at the IUCNAsian Turtle Workshop: Developing Conservation Strategies Through Captive Management, held at the FortWorth Zoo, Texas, on 26-28 January 2001. Initially named Chelonian Captive Survival Alliance (CCSA) andlater renamed Turtle Survival Alliance (TSA), it aims to bring together all involved in maintenance andbreeding of endangered species of tortoises and freshwater turtles (a global expansion from its initial Asianremit) and link these ex-situ captive activities to turtle-focused and habitat conservation actions in thecountries where these species occur. The TSA has likewise structured itself into an umbrella organisationcovering a substantial number of active and incipient Taxon Management Groups (TMG), with co-ordinationwith and partial integration of the European studbooks. While clearly dominated by North Americanparticipation as a reflection of its origin and the strength of the American conservation movement, the TSA isan inclusive global organisation that actively seeks to establish and promote links with partners in allcountries, particularly in range states of threatened turtle species. The TSA itself has formalised its relations to the IUCN Tortoise & Freshwater Turtle Specialist Group and a number of other organisations by its keyposition within the newly-formed Turtle Conservation Fund (TCF). Thus, the organisational structure tomanage conservation breeding of endangered Asian tortoises and freshwater turtles has been established.
For a successful captive conservation breeding program, a variety of technical aspects need to beaddressed, including marking and recognition of individual animals, suitable enclosures in which to maintainthe animals, understanding of suitable food and feeding, knowledge and provision of appropriatetemperature, humidity and other environmental parameters, appropriate equipment and practices to incubateeggs, availability of veterinary care, legal permission to transfer captive animals between different countries,and options to bring in fresh bloodlines from range countries, Marking and recognition of individual tortoises and freshwater turtles To mark and recognize tortoises and freshwater turtles, a wide variety of techniques has been developedand applied. The oldest is the system of Cagle (1939) which marks the animal by drilling, cutting or grindingan unique arrangement of marks in the marginal scutes of a turtle. This technique, initially developed fornatural history research in Nature, has been implemented by the TSA for the animals under its control. Whilevery effective for many, but not all, turtle species, it defaces the animal in the eyes of many keepers andthere is some reluctance to adopt this method universally. On the positive side, the method makes animalsinstantly recognizable, facilitating animal management, and also acts as a deterrent to diverting animals intotrade or other avenues of loss from the program.
Another option is to implant small glass-encased Passive Integrated Transponders, also called PIT tags or‘microchips’, which are implanted in muscle mass by the use of a specially-sized syringe. Implanted invisiblyunder the skin, it returns a unique code number when a transceiver is passed over the implant. The methodis widely used for the identification of dogs, cats, horses and other domestic animals and, when implementedproperly, is tamper-resistant to a high degree, but not impossible to alter. Identification through‘microchipping’ is compulsory for certain species in certain countries. Unfortunately, the smallest availabletransponders still measure 12 mm long with a diameter of 2 mm, and cannot be implanted in small turtles; awidespread view is that no turtles smaller than 500 grams should be microchipped. This would exclude allhatchlings and many juveniles of every turtle species, and even the mature adults of several species oftortoises and freshwater turtles. Particularly in breeding programs where individual identity is important atevery time, and animals remain small for several years, reliance on PIT tagging would open up variousavenues for confusion. The cost of individual transponders continues to decline, but still represents asignificant cost, particularly when a breeding program produces dozens of offspring annually.
A third approach relies on recognizing unique morphological features of each animal in a standard protocol.
These features are usually color pattern or shape and arrangement of scutes and/or scales, but could beother features depending on species. The method has been used extensively for recognition of animals fornatural history field research, particularly in salamanders and frogs, but has also been used as asupplementary recognition tool in turtle field research. Perhaps one of the earliest applications was to putSlider turtles on a photocopier at the Savannah River Ecology Lab in the USA. Recently, visualdocumentation of tortoises has been investigated in detail by Bender (2001) and the results demonstrate thatstandardized photographs of a number of tortoise species can be used to identify individual animals with avery high degree of reliability. It remains to be determined how reliable the method is to monitor individualchanges as young turtles grow, and unique identifying characteristics need to be found and verified for eachspecies, but so far the method appears promising for identification of animals of all sizes for a number ofspecies, without physically harming or defacing the individual animal.
Maintenance of tortoises and freshwater turtles in captivity The primary determining factor for almost any individual or institution maintaining tortoises and/or freshwaterturtles in captivity is the available amount of space. The available space not only determines how manyanimals can be maintained in suitable conditions, but also of which species. Clearly, species reaching largemaximum sizes require larger enclosures than smaller species, and for similar-sized species, species withan active lifestyle require more space than species that move little. Also of fundamental importance is thetemperament of the species and the individual animal; some animals can be kept in groups in company ofother species, while others can only be kept with one or more animals of the same species, or in nearly-permanent solitary confinement. Minimum sizes for appropriate enclosures have been determined for a widerange of turtle species (Bundesministerium für Ernährung, Landwirtschaft und Forsten, 1997), and thesehave been codified into legal requirements in Germany; proposals for similar measures exist in theNetherlands and presumably throughout the European Union.
While minimum standards are relevant, conservation breeding projects often require additional husbandrytechniques to house animals in conditions that are most suitable for long-term health and wellbeing andreproduction of the animals. The extent to which enclosures are sized and structured varies widely, andoptimal sizes are determined through experience and possibilities. Hofer (2000) arrived at optimal housing ofGeoemyda spengleri by building five relatively spacious terrariums for a group of seven animals whichtogether would fit along two walls of a small room, while H. Meier (2002) built a conservatory to the side ofthe house and filled it with several basins, the largest of which measures 10 square metres and contains6000 litres of water heated to 24°Celsius to house a group of eight Chelus fimbriatus and a pair of Chelodinasiebenrocki.
Similar care is taken to provide appropriate temperature, humidity and other environmental parameters toduplicate the conditions experienced by the species in its natural habitat. The Climate Atlas of Müller (1983) isfrequently cited in hobbyist reports describing captive maintenance as guiding their temperature profiles, andcomputer-controlled systems to achieve both daily fluctuations and seasonal trends in temperature, humidityand light intensity are no longer beyond reach of many hobbyists.
Incubation of eggs is likewise a subject of much consideration and experimentation, described in hobbyistjournals and extensively discussed at meetings. In the past decade, prospects for eggs during incubation haschanged from uncertain to near-certain success for many species, although the issue of diapause continues tobe a challenge for some species.
Food and feeding is another topic receiving extensive attention. Feeding has become both cleaner andhealthier with the development of gelatin-based pudding-type foods. The exact nutrient intake requirements arebeing studied for several species; result for Cuora amboinensis and Heosemys spinosa have just becomeavailable (Helmink & Kuperus, 2002) and a comparable study regarding food and feeding of Heosemysgrandis, Orlitia borneensis and Siebenrockiella crassicollis.
Ensuring good health of captive animals remains a challenge with many turtles. Wild-collected turtles carry awide range of parasites, commensals and actual and potential diseases. Current veterinary understandingand treatment of health problems of turtles are not exactly in their infancy, but are certainly far behind thosefor mammals. As turtles are ectotherm, i.e. ‘cold-blooded’, and usually aquatic creatures, many of theirdiseases and health concerns are very different from ailments that afflict economically important species,and research and applied practices concerning turtle veterinary care will always remain a minor subject.
Nevertheless, many parasites and diseases can be treated successfully by known and publicized veterinarytreatments, and the animals themselves also assist by having robust immune systems that can tolerate andeliminate many health concerns.
Maintenance conditions as described by Elmar Meier (2000, 2002a, b) for Cuora zhoui, C. trifasciata andClemmys muhlenbergii, by Victor Loehr (2002) for Homopus signatus and by Buley & Gibson (2002) forPyxis planicaude at the Jersey Zoo are just some examples of the remarkable detail and effort that dedicatedconservation breeding programs will go to.
Legal restrictions on captive stock management A significant concern among many private individuals is what they perceive as increasing administrationrequirements and legal restrictions on keeping, breeding and transferring of animals. This concernsparticularly those species that are included in the CITES Appendices and in the European import legislation(EG) Nr. 1968/1999. Whereas legislative regulatory authorities primarily aim to prevent or restrictunregulated, unsustainable or otherwise undesirable imports, the effect is at times counterproductive when itimpedes transfer of captive-bred offspring of species on CITES Appendix I. Proper pathways to obtain legalpermission and documentation to transfer animals between breeders and between countries do exist, but thehurdles to be surmounted can be high, and expensive, for an individual, and the inclination to then stopbreeding such species is understandable. Similarly there are significant but not insurmountable obstacles toacquiring additional wild-collected animals to bring fresh bloodlines into breeding programs, These concernswill probably be resolved over time as authorities and applicants become more familiar with the processesand when both parties understand that each is trying to make its own contribution to the same goal, theconservation of turtles.
One message that the hobbyist community has to bring across is that they are not net consumers whosupport the removal of wild animals by their personal desire to possess animals at home. They need toemphasize the contribution that their captive observations make to general understanding of the naturalhistory of turtle species, they need to involve themselves with and support conservation activities and research in the range states, and they need to present the animals that bring such fulfilment to their lives asambassadors for their imperiled species and imperiled native ecosystems to a wider audience.
The contribution and prospects of conservation breeding to the conservation of threatened Asian turtles In summary, conservation breeding of threatened Asian tortoises and freshwater turtles is a dynamic fieldwhere many individuals and institutions participate to work towards very ambitious goals that requireenormous effort, space, money and other resources to meet very demanding requirements. Noteworthy isthat much of those resources are voluntarily contributed by most of the participants, all for the vision of lettinginconspicuous little turtles carry on with their lives in secure populations in the wild. Yet with all these efforts,how many Asian turtle species are actually the subject of long-term self-sustaining conservation breedingprogrammes anywhere in the world?

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