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![A comparison of Mauremys iversoni plastra from the type description with turtle farm hybrids and putative parental species: A) Mauremys mutica from a turtle farm in Tunchang, Hainan Province (MVZ 230477); B-D) Mauremys iversoni from the type description. They are either from Fujian or Guizhou Province; E-F) Intentionally produced hybrids from a turtle farm in Tunchang, Hainan Province; G) Mauremys iversoni from the type description. It is either from Fujian or Guizhou Province; H) An intentionally produced hybrid from a turtle farm in Tunchang, Hainan Province (MVZ 130475); I) Cuora trifasciata from Tai Pin, central Hainan Province (MVZ 23932); J) Cuora trifasciata from the pet trade (MVZ 230636). Photos by JFP [a,e-f,h-j] and Pritchard and McCord (1991)[b-d,g].](profile/James-Parham/publication/255483633/figure/fig3/AS:297891013906436@1448034160329/A-comparison-of-Mauremys-iversoni-plastra-from-the-type-description-with-turtle-farm.png)
A comparison of Mauremys iversoni plastra from the type description with turtle farm hybrids and putative parental species: A) Mauremys mutica from a turtle farm in Tunchang, Hainan Province (MVZ 230477); B-D) Mauremys iversoni from the type description. They are either from Fujian or Guizhou Province; E-F) Intentionally produced hybrids from a turtle farm in Tunchang, Hainan Province; G) Mauremys iversoni from the type description. It is either from Fujian or Guizhou Province; H) An intentionally produced hybrid from a turtle farm in Tunchang, Hainan Province (MVZ 130475); I) Cuora trifasciata from Tai Pin, central Hainan Province (MVZ 23932); J) Cuora trifasciata from the pet trade (MVZ 230636). Photos by JFP [a,e-f,h-j] and Pritchard and McCord (1991)[b-d,g].
Contexts in source publication
Context 1
... trifasciata, M. mutica, and even a Chelydra serpentina. When asked if any of the turtles ever hybridized, the workers of the farm pro- duced several animals that closely resembled Maure- mys iversoni. One of these hybrids, a subadult male, was procured as a voucher (MVZ 230475; Fig. 2, 3h). JFP was given permission to photograph two other hybrids (Fig. ...
Context 2
... 127181) that also has a clear horse- shoe-shaped coalescence of blotches. Even without this character, M. iversoni can be distinguished from M. mutica by its more rounded anterior lobe that lacks a prominent gular projection. Furthermore, many M. iversoni specimens, including some of the type series of M. iversoni and the Hainan farm hybrids (Fig. 3b-f) have transverse trending blotches on the pectorals, a feature not known to occur in Mauremys, but common in juveniles of C. ...
Context 3
... variation among the figured specimens in the type description is extreme (Fig. 3b-d,g). It is not stated whether these specimens are from Fujian or Guizhou. Comparisons of the plastral figures from Pritchard and McCord (1991) with the specimens from the Tunchang farm show that the latter speci- mens lie within the range of variation of M. iversoni. The most notable differences are that one (Fig. 3e) has more irregularly ...
Context 4
... type description is extreme (Fig. 3b-d,g). It is not stated whether these specimens are from Fujian or Guizhou. Comparisons of the plastral figures from Pritchard and McCord (1991) with the specimens from the Tunchang farm show that the latter speci- mens lie within the range of variation of M. iversoni. The most notable differences are that one (Fig. 3e) has more irregularly shaped plastral blotches and MVZ 230475 ( Fig. 3h) has only a narrow, light, central fig- ure on the plastron. Perhaps the most important fea- ture to be noted is that no two specimens look alike. In the type description, Pritchard and McCord (1991) describe the plastral pigmentation as "very variable in ...
Context 5
... specimens are from Fujian or Guizhou. Comparisons of the plastral figures from Pritchard and McCord (1991) with the specimens from the Tunchang farm show that the latter speci- mens lie within the range of variation of M. iversoni. The most notable differences are that one (Fig. 3e) has more irregularly shaped plastral blotches and MVZ 230475 ( Fig. 3h) has only a narrow, light, central fig- ure on the plastron. Perhaps the most important fea- ture to be noted is that no two specimens look alike. In the type description, Pritchard and McCord (1991) describe the plastral pigmentation as "very variable in intensity", but it is unclear whether the figured speci- mens represent the most ...
Citations
... More hybridization has been reported in Mauremys sensu lato, such as O. glyphistoma being a hybrid of M. sinensis and M. cf. annamensis [35] and M. pritchardi being hybrids of M. reevesii and M. mutica, respectively [36,37]. Therefore, the interspecific gene flow may have been increased by the turtle trade, escape from farms and release activities, which led to the genetic diversity of wild populations being lost. ...
Mauremys sensu lato was divided into Mauremys, Chinemys, Ocadia, and Annamemys based on earlier research on morphology. Phylogenetic research on this group has been controversial because of disagreements regarding taxonomy, and the historical speciation is still poorly understood. In this study, 32 individuals of eight species that are widely distributed in Eurasia were collected. The complete mitochondrial (mt) sequences of 14 individuals of eight species were sequenced. Phylogenetic relationships, interspecific divergence times, and ancestral area reconstructions were explored using mt genome data (10,854 bp). Subsequent interspecific gene flow level assessment was performed using five unlinked polymorphic microsatellite loci. The Bayesian and maximum likelihood analyses revealed a paraphyletic relationship among four old genera (Mauremys, Annamemys, Chinemys, and Ocadia) and suggested the four old genera should be merged into the genus (Mauremys). Ancestral area reconstruction and divergence time estimation suggested Southeast Asia may be the area of origin for the common ancestral species of this genus and genetic drift may have played a decisive role in species divergence due to the isolated event of a glacial age. However, M. japonica may have been speciated due to the creation of the island of Japan. The detection of extensive gene flow suggested no vicariance occurred between Asia and Southeast Asia. Inconsistent results between gene flow assessment and phylogenetic analysis revealed the hybrid origin of M. mutica (Southeast Asian). Here ancestral area reconstruction and interspecific gene flow level assessment were first used to explore species origins and evolution of Mauremys sensu lato, which provided new insights on this genus.
... Scientists have never observed C. picturata in the wild, and its origin remains unknown. Some poorly known Asian turtles that were recently described as new species on the basis of trade animals have since been shown to be only recent hybrids of better known species, including inter-generic hybrids (Parham et al., 2001; Dalton, 2003; Stuart and Parham, 2007). Some of these hybrids have a wild origin (Shi et al., 2005), while others originated from farming operations (where parental species are co-housed) that supply the Chinese turtle trade (Parham and Shi, 2001; Parham et al., 2001; Shi et al., 2008). ...
... Three other species of very rare Asian box turtles, Zhou's box turtle C. zhoui, McCord's box turtle C. mccordi, and the Yunnan box turtle C. yunnanensis, are found in commercial trade in China but remain unknown in the wild (Parham and Li, 1999; Parham et al., 2001, 2004; Zhou and Zhao, 2004). Like C. picturata, both C. zhoui and C. mccordi are known to science only from animals obtained in trade (Parham et al., 2001). A reported provenance for C. mccordi based solely on interviews of turtle hunters and traders (Zhou et al., 2008) is unreliable without field observations given that traders are motivated to hide localities of commercially valuable turtles (Parham and Li, 1999; Parham et al., 2001). ...
Asian turtles are overharvested for food, medicinal purposes and pets, and most species are now at risk of extinction (‘Asian turtle crisis’). As a result of high levels of trade, some species of Asian turtles are known to science mostly or only from animals found in trade. The Vietnamese box turtle (Cuora picturata) was described in 1998 and is known only from markets. This species is likely to be highly threatened, and identifying the origin of this “market species” is imperative if it is to be conserved. We used evidence from phylogeny, biogeography and trade patterns to focus field searches for this species, and in July 2010–January 2011 found it in the wild at three localities on the Langbian Plateau of southern Vietnam. This discovery provides the first opportunity to conserve the Vietnamese box turtle, and provides hope for determining the wild origin of other rare Asian turtles that remain known only from commercial trade.
... Recent Asian turtle research has uncovered the ability of distantly related species in the family Geoemydidae to hybridize (see Buskirk et al. 2005 for a review). This propensity for reticulation combined with a lack of detailed study of Asian geoemydids has sometimes confused herpetologists ; at least five newly described species have turned out to be the result of recent, human-mediated hybridizations (Parham et al. 2001; Spinks et al. 2004; Stuart and Parham 2007). Asian turtles face extinction due to the turtle trade (van Dijk et al. 2000), and anthropogenic hybridization complicates the situation by polluting gene pools and exploiting precious research and conservation resources (Allendorf et al. 2001; Fong et al. 2007). ...
... Whereas most hybrids are thought to be formed in Chinese turtle farms (Parham and Shi 2001; Parham et al. 2001; Shi et al. 2007, 2008), there have been reports of turtle hybrids appearing in the wild (Otani 1995; Shi et al. 2005; Haramura et al. 2008). These studies reemphasize the point that understanding the origin of Chinese turtle hybrids may require multiple explanations (Parham et al. 2001). Detailed surveys of turtle populations throughout Taiwan (Chen and Lue in press) have identified two likely hybrids (Fig. 1). ...
Field surveys in Taiwan have uncovered turtles presumed to be hybrids based on their intermediate morphology. We sequenced
a mitochondrial (ND4) and nuclear (R35) gene of two putative hybrid individuals, along with representatives of the potential
parental species (Mauremys mutica, M. reevesii, M. sinensis), to determine their genetic identity. Based on our data, both individuals are hybrids, with independent, recent origins
resulting from the mating of a female M. reevesii and a male M. sinensis. Since we question whether the highly traded M. reevesii is endemic to Taiwan, this hybridization could represent human-mediated genetic pollution. We also discuss the implications
of our findings on turtle conservation in Taiwan.
Keywords
Mauremys mutica
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Mauremys sinensis
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Mauremys reevesii
-Asian turtle crisis-Introduced species-Conservation
... Asian turtles face an extinction crisis (van Dijk, Stuart & Rhodin, 2000; Turtle Conservation Fund, 2003), underscoring the importance of accurately determining species diversity to guide conservation strategies (Parham et al., 2001; Stuart & Parham, 2004). Unfortunately, determining species boundaries of Asian turtles has proven challenging because of the widespread hybridization of distinct lineages in the wild and in captivity (Parham et al., 2001; Spinks et al., 2004; Shi et al., 2005; Stuart & Parham, 2007; Spinks & Shaffer, in press), a phenomenon that is exacerbated by the pervasive transportation and captive propagation of turtles for profit (Parham et al., 2001; Shi & Parham, 2001). ...
... Asian turtles face an extinction crisis (van Dijk, Stuart & Rhodin, 2000; Turtle Conservation Fund, 2003), underscoring the importance of accurately determining species diversity to guide conservation strategies (Parham et al., 2001; Stuart & Parham, 2004). Unfortunately, determining species boundaries of Asian turtles has proven challenging because of the widespread hybridization of distinct lineages in the wild and in captivity (Parham et al., 2001; Spinks et al., 2004; Shi et al., 2005; Stuart & Parham, 2007; Spinks & Shaffer, in press), a phenomenon that is exacerbated by the pervasive transportation and captive propagation of turtles for profit (Parham et al., 2001; Shi & Parham, 2001). These challenges faced by systematists are directly relevant to the captive-breeding efforts that are increasingly being championed as one of the long-term solutions to the survival of Asian turtles (Hudson & Buhlmann, 2002; Turtle Conservation Fund, 2003). ...
... Asian turtles face an extinction crisis (van Dijk, Stuart & Rhodin, 2000; Turtle Conservation Fund, 2003), underscoring the importance of accurately determining species diversity to guide conservation strategies (Parham et al., 2001; Stuart & Parham, 2004). Unfortunately, determining species boundaries of Asian turtles has proven challenging because of the widespread hybridization of distinct lineages in the wild and in captivity (Parham et al., 2001; Spinks et al., 2004; Shi et al., 2005; Stuart & Parham, 2007; Spinks & Shaffer, in press), a phenomenon that is exacerbated by the pervasive transportation and captive propagation of turtles for profit (Parham et al., 2001; Shi & Parham, 2001). These challenges faced by systematists are directly relevant to the captive-breeding efforts that are increasingly being championed as one of the long-term solutions to the survival of Asian turtles (Hudson & Buhlmann, 2002; Turtle Conservation Fund, 2003). ...
Asian turtles face an extinction crisis, and so it is imperative that systematists accurately determine species diversity in order to guide conservation strategies effectively. We surveyed mitochondrial and nuclear DNA (mtDNA and nuDNA) variation of the heavily exploited Mauremys mutica complex, a clade of Asian turtles that contains the endangered M. mutica from Japan, Taiwan, China and Vietnam, and the critically endangered Mauremys annamensis from central Vietnam. We discovered extensive mtDNA and nuDNA variation among samples that did not correspond to the currently recognized taxonomy. Both nuDNA and mtDNA data suggest that M. mutica is paraphyletic with respect to M. annamensis. Surprisingly, M. annamensis exhibits a previously unknown mtDNA structure in the form of two clades that are paraphyletic to M. mutica. These data reveal that the currently recognized taxonomy of the mutica complex does not reflect the genetic diversity of our samples. Unfortunately, many conservation-oriented captive-breeding efforts for turtles are also based on trade samples such as the ones studied here. These efforts include plans to breed trade-rescued individuals and release their progeny into the wild. Because our genetic survey reveals that the taxonomic identity of these samples does not reflect genetic diversity, we raise serious questions about the efficacy of these programs. In order to address conservation issues and provide more accurate estimates of evolutionary lineages within Mauremys, we recommend continued surveys for wild populations of the mutica complex to provide new genetic material and additional distributional data, attempts to extract DNA from historic museum specimens and a shift in conservation focus to in situ preservation of wild populations and associated habitat.
... Turtles are heavily exploited in Southeast Asia for food, traditional medicine, and pets (van Dijk et al. 2000), and now more than half of Asian species are listed as endangered or critically endangered in the wild (Stuart and Thorbjarnarson 2003; IUCN 2004). At the same time, these demands have fueled large-scale turtle farming operations in southern China (Shi and Parham 2001; Shi et al. 2004), a development that has greatly increased the potential for hybridization and genetic admixture of turtles found in trade. ...
... During the last two decades, 14 new species of geoemydid turtles were described from China (Parham et al. 2001; Spinks et al. 2004), and these represent a significant proportion of China's turtle diversity (Stuart and Thorbjarnarson, 2003). Most of these newly described taxa were based on specimens purchased from a Hong Kong pet dealer named Yuk Wah " Oscar " Shiu (Parham et al. 2001; Dalton 2003). ...
... During the last two decades, 14 new species of geoemydid turtles were described from China (Parham et al. 2001; Spinks et al. 2004), and these represent a significant proportion of China's turtle diversity (Stuart and Thorbjarnarson, 2003). Most of these newly described taxa were based on specimens purchased from a Hong Kong pet dealer named Yuk Wah " Oscar " Shiu (Parham et al. 2001; Dalton 2003). Three of these species, " Mauremys iversoni, " " M. pritchardi, " and " Cuora serrata, " are now known to be hybrids based on morphology, mitochondrial DNA, and nuclear DNA data (Parham et al. 2001; Wink et al. 2001; Stuart and Parham 2004; Spinks et al. 2004). ...
Three rare geoemydid turtles described from Chinese tradespecimens in the early 1990s, Ocadia glyphistoma, O. philippeni, andSacalia pseudocellata, are suspected to be hybrids because they are knownonly from their original descriptions and because they have morphologiesintermediate between other, better-known species. We cloned the allelesof a bi-parentally inherited nuclear intron from samples of these threespecies. The two aligned parental alleles of O. glyphistoma, O.philippeni, and S. pseudocellata have 5-11.5 times more heterozygouspositions than do 13 other geoemydid species. Phylogenetic analysis showsthat the two alleles from each turtle are strongly paraphyletic, butcorrectly match sequences of other species that were hypothesized frommorphology to be their parental species. We conclude that these rareturtles represent recent hybrids rather than valid species. Specifically,"O. glyphistoma" is a hybrid of Mauremys sinensis and M. cf. annamensis,"O. philippeni" is a hybrid of M. sinensis and Cuora trifasciata, and "S.pseudocellata" is a hybrid of C. trifasciata and S. quadriocellata.Conservation resources are better directed toward finding and protectingpopulations of other rare Southeast Asian turtles that do representdistinct evolutionary lineages.
... Cuora galbinifrons serrata Iverson and McCord, 1992 is known only from animals in trade that were claimed to have Here we use mitochondrial DNA sequence data to test if the five named forms of C. galbinifrons represent evolutionary lineages. We use the same genes studied in Parham et al. (2001), but with an additional 188–254 bp. Because the sister taxon of C. galbinifrons has been hypothesized to be a clade containing most other Cuora species (Honda et al., 2002), we include samples in our phylogenetic analyses of all but one of the nine currently recognized, extant species of Cuora. ...
The Indochinese box turtle Cuora galbinifrons is a polytypic, critically endangered species from Vietnam, Laos, and Hainan Island, China. We analyze up to 1790bp of mitochondrial DNA under maximum parsimony and maximum likelihood criteria to test if the five historically recognized subspecies represent evolutionary lineages, and to elucidate the relationship of C. galbinifrons to other Cuora. C. galbinifrons is composed of three major mitochondrial DNA clades corresponding to the three subspecies galbinifrons, bourreti, and picturata. These three lineages are also morphologically diagnosable, and consequently we recommend elevating each to full species. Cuora galbinifrons hainanensis nests within the galbinifrons clade, and we retain it as a synonym of galbinifrons, as supported by morphology. Cuora "serrata" is known to be a hybrid of male Cuora mouhotii and female C. galbinifrons, and our findings show that C. "serrata" originates from both female galbinifrons and bourreti. Little or no mitochondrial DNA variation was found among the morphologically distinct species Cuora aurocapitata, Cuora pani, and Cuora trifasciata, for which hypotheses are proposed. Recognizing galbinifrons, bourreti, and picturata as separate species has consequences for ongoing ex situ captive breeding programs and prioritization of in situ conservation activities, particularly in Vietnam.
Sea turtles are threatened by climate change and human activity, and their global populations continue to decline sharply. The Chinese government encourages artificial breeding of sea turtles to reduce the use of wild populations. However, artificial breeding of sea turtles is still fairly difficult, and some facilities may illegally purchase wild turtle eggs and then sell incubated turtles by marketing them as artificially bred turtles, which adds another threat to an already endangered species. Therefore, it is necessary to find a reliable method to distinguish the authenticity of artificially bred individuals. In this study, we investigated a turtle farm in southern China, that contained more than 400 green turtles, which were claimed to have been bred in captivity. Parentage testing of turtles from this farm was successfully conducted using two nuclear microsatellites combined with a mitochondrial D-loop DNA marker. Genetic matching of all 19 adults and randomly selected 16 juvenile turtles revealed that none of the juvenile turtles had a matching parent combination among the adult turtles. Therefore, we speculated that the green turtles in this farm were from the wild and that their origin of birth was mainly the Sulu Sea. The methods and molecular markers used in this study could be a reference for rapid authenticity testing of green turtles in future forensic enforcement and population management.
The Kinmen Islands on the coastline of China represent a recent case of the protection of endangered wildlife in a demilitarized zone. These islands represent the last remaining habitat in southeastern China that supports a healthy natural population of Reeves’ turtle Mauremys reevesii. However, human‐mediated dispersal appears to have aided the establishment of an introduced population of the Chinese stripe‐necked turtle M. sinensis since the late 1990s, resulting in population mixture of the two congeners. To evaluate the potential impacts of hybridization, we evaluated the magnitude of genetic introgression in ponds on Kinmen using mitochondrial cytochrome b sequences and 13 microsatellite loci. We further used eight environmental and biological factors of the ponds to conduct general linear regression model analysis between environmental factors and the magnitude of genetic introgression. Among the 41 sampled ponds, M. reevesii was recorded in 21, of which 12 ponds (57.1%) contained genetic hybrids or backcrosses, corresponding to 11.3–12.7% of the total individuals on the islands. The magnitude of genetic introgression was positively correlated with the amount of introduced M. sinensis occurring in a pond, and marginally negatively associated with the shortest distance from the pond to secondary roads. We conclude that this considerable genetic introgression is attributable to human‐mediated dispersal of M. sinensis; roads and habitat modification may increase the likelihood of unexpected encounters between these two congeners.
Turtles are of high value as pharmaceuticals, food, in scientific research, and the shells are used for making ornaments and jewelry accessories. There are various turtle culture models in China, depending on the intensity and the value of the overall facilities. The Chinese three‐keeled pond turtle and Chinese stripe‐necked turtle are relatively low‐valued species, and are usually cultured in ponds along with fish. The Asian yellow pond turtle, Chinese three‐striped box turtle, and Yellow‐margined box turtle are high valued, and are usually cultured in cement pools planted with vegetables or flowers. The complete value chain for turtle culture consists of larval production, culture, feed production, product manufacturing, trade, and consumption. An assumption is made is that the sustainable and fast development of turtle culture relies on progress in technology. Research and generalization of technology in the areas of efficient reproduction, culture and germplasm identification, provide the basis for sustainable turtle culture.
Non-native species have the potential to induce large-scale ecological changes that threaten native ecosystem biodiversity, particularly on islands. However, aside from the most conspicuous invasive taxa, the majority of non-natives receive relatively little scientific attention making it difficult to predict the severity of their impact. In addition to ecological and natural history data, genetic approaches can help address the status of non-natives, particularly for introductions that involve multiple sympatric and morphologically cryptic species to clarify their taxonomic identities and geographic origins. We used a molecular systematic approach to investigate softshell turtles (family: Trionychidae) introduced to the Hawaiian Islands in the late 1800s: Palea steindachneri and Pelodiscus sinensis. In light of extended importation and inter-island dispersal, recent taxonomic revisions in P. sinensis, unknown ecosystem impacts in Hawaii, and native range conservation concerns, a comprehensive characterization of the populations in Hawaii was warranted. Field surveying efforts revealed a distribution markedly different from the historical one, with the current ranges of P. steindachneri limited to Kauai and that of Pelodiscus limited to Oahu. Analysis of the 12S rRNA, ND4, and Cyt b gene regions revealed two species of the Pelodiscus complex (P. sinensis sensu stricto and P. maackii) and low genetic diversity in P. steindachneri. These results suggest the importance of continued study to assess impacts on Hawaiian species with the aim of developing management policies to either protect them as ‘assurance colonies’ for the declining native populations or alternatively to support the control and eradication efforts aimed at these introduced aquatic predators.
