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Origins of softshell turtles in Hawaii with implications for conservation

Authors:
Caroline Dong at Tulane University
Caroline Dong
Tag N. Engstrom at California State University, Chico
Tag N. Engstrom
Robert Thomson at University of Hawaiʻi at Mānoa
Robert Thomson
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Abstract

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.
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... The binomen Trionyx axenaria was first proposed by Zhou et al. (1991) in the English abstract of a Chinese-language paper dealing with soft-shelled turtles called by the local populace 砂鳖 (sha bie = sand soft-shelled turtle) inhabiting rivers in the following counties and cities of Hunan Province, China: Taoyuan, Pingjiang, Rucheng, Lingling, and Shaoyang. Even though the diagnostic morphological features of 'sha bie' remain unclear to date, molecular genetic studies (Chen et al. 2005(Chen et al. , 2006Dong et al. 2016;Fritz et al. 2010;Gong et al. 2018;Yang et al. 2011) have confirmed the distinctiveness of the sand soft-shelled turtle, and it has been treated as a valid species of the genus Pelodiscus in all major turtle taxonomy checklists published after 2007 (Fritz & Havaš 2007;Rhodin et al. 2008;TTWG 2007TTWG , 2009TTWG , 2010TTWG , 2011TTWG , 2012TTWG , 2014TTWG , 2017TTWG , 2021. ...
Disentangling the Pelodiscus axenaria complex, with the description of a new Chinese species and neotype designation for P. axenaria (Zhou, Zhang & Fang, 1991)
Article
Full-text available
  • Apr 2022
  • ZOOTAXA
We describe a new species from the Pelodiscus axenaria complex from Hunan and Jiangxi Provinces, China. Also, the application of the name P. axenaria (Zhou, Zhang & Fang, 1991) is clarified by designating a neotype for this species. Besides its genetic divergence, the new species differs from all other Pelodiscus species, including the two other taxa constituting the complex (P. axenaria, P. huangshanensis), in the following combination of morphological traits: (1) small adult size, <15 cm carapace length; (2) carapace distinctly keeled, more or less strongly tuberculated, usually olive clay-coloured and adorned with greenish black marbling; (3) plastron yellowish white, typically immaculate except for a blurred-edged blotch behind each axilla that does not extend to the entoplastron and some slight black suffusion along its anterior border; (4) underside of the leathery margin of the carapace with varying amounts of dark pigmentation; (5) head olive clay-coloured with numerous black splotches; (6) chin grey brown with pale stipples, throat dark grey, finely spotted with black; (7) neck with a wide yellow lateral band stretching from the tympanum posteriorly, which tends to fade with age; (8) entoplastron boomerang-shaped, the amount of bending of the transverse bar between the two posteriolaterally directed rami >90°.
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... The homologous sequences of all species of the genus Pelodiscus and five outgroup species (Palea steindachneri, Apalone spinfera, A. mutica, Rafetus swinhoei, and R. euphraticus) were downloaded from GenBank (Engstrom et al. 2004;Jung et al. 2006;Fritz et al. 2010;Yang et al. 2011;Ihlow et al. 2013;Ihlow et al. 2014;Suzuki & Hikida 2014;Dong et al. 2016;Gong et al. 2018) and aligned with the newly generated sequences using the software MEGA X (Kumar et al. 2018). The downloaded sequences of FR851459 (cyt b) and FR851460 (ND 4) were sequenced from the lectotype of P. sinensis , and the mtDNA complete sequence of MK867844 (considered as P. axenaria, Yu et al. 2019) should be assigned to Pelodiscus huangshanensis sp. ...
A new species of the Genus Pelodiscus Fitzinger, 1835 (Testudines: Trionychidae) from Huangshan, Anhui, China
Article
Full-text available
  • Oct 2021
A new species of the soft-shelled turtle genus Pelodiscus is described based on seven specimens from Huangshan, southern Anhui Province, China. The new species, Pelodiscus huangshanensis sp. nov., is distinguished from other species in the genus Pelodiscus by the following characteristics: (1) Small size (maximum carapace length of 101.16 mm and maximum body length of 190 mm); (2) keel high; (3) tiny yellowish-white spots on the throat; (4) no black pinstripes around the eyes; (5) white longitudinal bands on both sides of the neck in juveniles, absent in adults; (6) plastron yellowish-white, and only a dark patch on each side of the armpit; (7) many tubercles on the dorsal surface, but indistinct in the center; and (8) entoplastron “⌒” shaped. The phylogenetic relationships of the species in Pelodiscus were reconstructed using the sequences of cytochrome b (cyt b) and NADH dehydrogenase subunit 4 (ND4) genes. The new species formed a monophyletic clade with strong support. The uncorrected pairwise distances between the new species and other representatives of Pelodiscus ranged from 5.4% to 9.2% for cyt b and 4.1% to 7.6% for ND4. The new species brings the number of species of the genus Pelodiscus to six; five species are distributed in China, with three species endemic to China.
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... This list includes one snake, four turtles, six frogs, and fifteen lizards (Mckeown, 1996;Kraus et al., 1999;Dong et al., 2015;Van Kleeck and Holland, in review). Surprisingly, however, scientific attention has only recently been given to any of these species, and to date this number of invasives includes only the Jackson's chameleon, Trioceros jacksonii xantholophus (Holland et al. 2010;Goldberg and Kraus 2011;Kraus et al. 2011;Van Kleeck et al., 2015 in press) and the coqui frog, Eleutherodactylus coqui (Kraus et al., 1999;Beard and Pitt 2005;Beard, 2009). ...
Van Kleeck dissertation 2016
Thesis
Full-text available
  • May 2016
Biological invasions provide opportunities to investigate micro-evolutionary change and the relative roles of key factors that lead to differentiation. Following introduction, release from native selective pressures and exposure to novel evolutionary forces can reduce morphological and physiological constraints and impose new ones, resulting in rapid micro-evolutionary changes. Studying ecosystem and geographic variation in invasive taxa on an ecological time scale can help provide conservation relevant information for management. I investigated ecological and evolutionary questions involving adaptation and ecomorphological variation and the roles of habitat characteristics on form, function and behavior of an invasive lizard in Hawaii. In Chapters 1 and 2 I evaluate substantial variation in head-size and horn-length among and within islands, and between native and introduced ranges. Larger heads are associated with low precipitation, and consumption and higher availability of hard prey, while longer horns are exhibited by chameleons in their native range and are associated with fight success and higher precipitation in the introduced range. Results may suggest rapid ecomorphological adaption to introduced microhabitats and release from natural selective pressures influencing sexually dimorphic characters in the native range. Chapter 3 examined predatory behavior in chameleons in response to prey size and type. Instead of the well-documented lingual prehension mechanism in Chamelaeonidae, a novel feeding mechanism is described, in association with both prey/predator size and prey type. Finally, for Chapter 4, I present the first proposed control strategy for T.j. xantholophus in Hawaii. We tested a method based on an approach using acetaminophen deployed by resource managers to control the invasive brown tree snake on Guam. We determined minimum dosage necessary to cause >95% mortality in <48 hours. Additionally, I propose methods of field delivery, including use of introduced snail shells as a vessel for ingestion. Although there is a massive and increasing body of invasion ecology research, this study provides new insights into trait adaptation of invasive predators and how this information can help develop management strategies. In addition, this study presents a framework by which biological invasions can be used to examine evolutionary questions on an ecological rather than evolutionary time-scale.
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... Previous studies on the taxonomy of Chinese softshell turtles focused either on morphological comparisons (Chkhikvadze 1987;Tang 1997;Zhou et al. 1991) or relied largely on variation of mtDNA (Fritz et al. 2010;Stuckas and Fritz 2011;Dong et al. 2016). Unfortunately, the morphological studies did not contribute to a better understanding of variation. ...
Millennium-old farm breeding of Chinese softshell turtles (Pelodiscus spp.) results in massive erosion of biodiversity
Article
Full-text available
  • May 2018
  • NATURWISSENSCHAFTEN
Chinese softshell turtles (Pelodiscus spp.) are widely distributed, ranging from the Amur and Ussuri Rivers in the Russian Far East through the Korean Peninsula, Japan, and eastern, central, and southern China to southern Vietnam. In East and Southeast Asia, Chinese softshell turtles are traditionally exploited for food and have been farm-bred in China since the Spring and Autumn Period, more than 2400 years ago. Currently, the annual production of Pelodiscus amounts to 340,000 t in China alone. Using mitochondrial DNA (2428 bp) and five nuclear loci (3704 bp), we examined broad sampling of wild and farm-bred Pelodiscus to infer genetic and taxonomic differentiation. We discovered four previously unknown mitochondrial lineages, all from China. One lineage from Jiangxi is deeply divergent and sister to the mitochondrial lineage of Pelodiscus axenaria. The nuclear loci supported species status for P. axenaria and the new lineage from Jiangxi. Pelodiscus maackii and P. parviformis, both harboring distinct mitochondrial lineages, were not differentiated from P. sinensis in the studied nuclear markers. The same is true for two new mitochondrial lineages from Zhejiang, China, represented by only one individual each, and another new lineage from Anhui, Guangdong, Jiangxi and Zhejiang, China. However, Vietnamese turtles yielding a mitochondrial lineage clustering within P. sinensis were distinct in nuclear markers, suggesting that these populations could represent another unknown species with introgressed mitochondria. Its species status is also supported by the syntopic occurrence with P. sinensis in northern Vietnam and by morphology. In addition, we confirmed sympatry of P. axenaria and P. parviformis in Guangxi, China, and found evidence for sympatry of P. sinensis and the new putative species from Jiangxi, China.We also discovered evidence for hybridization in turtle farms and for the occurrence of alien lineages in the wild (Zhejiang, China), highlighting the risk of genetic pollution of native stock. In the face of the large-scale breeding of Pelodiscus, we claim that the long-term survival of distinct genetic lineages and species can only be assured when an upscale market segment for pure-bred softshell turtles is established, making the breeding of pure lineages lucrative for turtle farms. Our findings underline that the diversity of Pelodiscus is currently underestimated and threatened by anthropogenic admixture. We recommend mass screening of genetic and morphological variation of Chinese softshell turtles as a first step to understand and preserve their diversity.
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Development and characterization of 68 SNPs markers in the critically endangered species, Palea steindachneri
Article
Full-text available
  • May 2024
The Wattle-necked Softshell Turtle (Palea steindachneri) is the only species in the genus Palea, and is listed as a critically endangered species by IUCN Red List due to the extreme decline in its natural populations as a result of human capture and trade activities. However, the lack of studies on molecular markers is not conducive to the genetic diversity assessment and population conservation of P. steindachneri. Here, a total of 68 novel polymorphic SNP markers were developed and characterized based on whole-genome sequencing of P. steindachneri. The observed heterozygosity, expected heterozygosity, and polymorphism information content of the 68 SNP markers ranged from 0.1250 to 0.6875, 0.3047 to 0.5000, and 0.2583 to 0.3750, respectively. Only five SNPs significantly deviated from the Hardy-Weinberg equilibrium (PHWE<0.05). These novel polymorphic SNP markers will be useful for future genetic management and population conservation of P. steindachneri.
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Impacts of aquatic invasive species and land use on stream food webs in Kaua’i, Hawai’i.
Article
Full-text available
  • Jan 2014
Anthropogenic disturbance is restructuring ecosystems and changing interactions within ecological communities. On the Hawaiʼian Islands, habitat degradation is linked to the establishment of invasive species; and together these stressors may lead to declining native populations and changes in food webs. In this study we employed stable isotopes to examine the structure of multiple Hawaiʼian stream food webs with varying levels of these stressors to illustrate interactions between native and non-native organisms that may represent drivers of community change. Limahuli stream contains all five species of native Hawaiʼian gobies, has a small number of introduced species, and minimal human disturbance. ʻOpaekaʼa, Hul¯eʼia and Kapaʼa streams are more heavily invaded than Limahuli and have greater human influence. We found increased species richness, increased trophic diversity, and increased total niche area in the more heavily invaded stream food webs relative to Limahuli. We also found non-native predatory species inhabiting top trophic positions in the three more heavily invaded streams and isotope mixing model estimates suggest that several species of non-natives have overlapping prey sources with native gobies in these sites. Lastly, we found that native stream organisms were nearly absent in ʻOpaekaʼa stream which also had the highest percent urban development of the streams sampled. Our results suggest significant trophic changes have occurred as the result of introduced species and possibly related to increased human disturbance.
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Validity of Pelodiscus parviformis (Testudines: Trionychidae) Inferred from Molecular and Morphological Analyses
Article
Full-text available
  • Jan 2011
The validity of Pelodiscus parviformis within the genus is still not very clear. In this study, molecular and morphological data were combined to evaluate the validity of P. parviformis. The phylogeny of some species in Pelo-discus was reconstructed by maximum parsimony, maximum likelihood and Bayesian inference analyses based on fve mitochondria DNA fragments (5308 bp of 12S rRNA, 16S rRNA, ND4, CO1 and Cyt b). The results of ML, MP and Bayesian analyses suggest that P. parviformis might be paraphyletic to P. sinensis, whereas the partitioned Bayesian analyses support the reciprocal monophyly of P. parviformis and P. sinensis. Considering the advantages of heteroge-nous characteristics of sequence evolution, we choose the result of partitioned Bayesian analyses. Furthermore, the morphological data lend support the distinct species status of P. parviformis and P. sinensis, such as tubercles on carapace skin, color of plastron skin, dark spots on plastron, basisphenoid characteristics (ratio of the smallest width to the largest width; the smallest width of basisphenoid is restrained by two holes on each side) and the shape of entoplastron. Combining the molecular and morphological data, we inferred that P. parviformis is a valid species. In addition, the results of this study suggest a new record of P. axenaria in Guangxi, China.
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