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Origins of softshell turtles in Hawaii with implications for conservation

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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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References

  • Asian Turtle Trade Working Group (2000). Palea steindachneri. The IUCN Red List of Threatened Species. Version 2014.3

  • Booth D, Provan J, Maggs CA (2007) Molecular approaches to the study of invasive seaweeds. Bot Mar 50:385–396

    Article  CAS  Google Scholar 

  • Brasher AM, Luton CD, Goodbred SL, Wolff RH (2006) Invasion patterns along elevation and urbanization gradients in Hawaiian streams. Trans Am Fish Soc 135(4):1109–1129

    Article  Google Scholar 

  • Brock VE (1947) The establishment of Trionyx sinensis in Hawaii. Copeia 1947:142

    Article  Google Scholar 

  • Byers JE, Reichard S, Randall JM, Parker IM, Smith CS, Lonsdale WM, Atkinson IAE, Seastedt TR, Williamson M, Chornesky E, Hayes D (2002) Directing research to reduce the impacts of nonindigenous species. Conserv Biol 16:630–640

    Article  Google Scholar 

  • Chiaverano LM, Holland BS (2014) Impact of a predatory invasive lizard on the endangered Hawaiian snail Achatinella mustelina: a threat assessment. Endanger Species Res 24:115–123

    Article  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  PubMed  CAS  Google Scholar 

  • Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) (2014) Appendices I, II and III valid from 14 September 2014

  • Engstrom TN, Shaffer HB, McCord WP (2004) Multiple data sets, high homoplasy, and the phylogeny of softshell turtles (Testudines: Trionychidae). Syst Biol 53:693–710

    Article  PubMed  Google Scholar 

  • Ernst CH, Barbour RW (1972) Turtles of the United States. The University Press of Kentucky, Lexington

    Google Scholar 

  • Ernst CH, Barbour RW (1989) Turtles of the world. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • Feldman CR, Parham JF (2004) Molecular systematics of old world stripe-necked turtles (Testudines: Mauremys). Asiat Herpetol Res 10:28–37

    Google Scholar 

  • Fong JJ, Parham JF, Shi H, Stuart BL, Carter RL (2007) A genetic survey of heavily exploited, endangered turtles: caveats on the conservation value of trade animals. Anim Conserv 10:452–460

    Article  Google Scholar 

  • Fritz U, Auer M, Bertolero A, Cheylan M, Fattizzo T, Hundsdörfer AK, Martín Sampayo M, Pretus JL, Široký P, Wink M (2006) A rangewide phylogeography of Hermann’s tortoise, Testudo hermanni (Reptilia: Testudines: Testudinidae): implications for taxonomy. Zool Scr 35:531–543

  • Fritz U, Gong S, Auer M, Kuchling G, Schneeweib N, Hundsdorfer AK (2010) The world’s economically most important chelonians represent a diverse species complex (Testudines: Trionychidae: Pelodiscus). Org Divers Evol 10:227–242

    Article  Google Scholar 

  • Geller JB, Darling JA, Carlton JT (2010) Genetic perspectives on marine biological invasions. Annu Rev Mar Sci 2:367–393

    Article  Google Scholar 

  • Gering E, Johnsson M, Willis P, Getty T, Wright D (2015) Mixed-ancestry and admixture in Kauai’s feral chickens: invasion of domestic genes into ancient Red Junglefowl reservoirs. Mol Ecol 24:2112–2124

    Article  PubMed  CAS  Google Scholar 

  • Groombridge JJ, Raisin C, Bristol R, Richardson DS (2012) Genetic consequences from reintroductions and insights from population history. In: Ewen JG, Armstrong DP, Parker KA, Seddon PJ (eds) Reintroduction biology: integrating science and management, 1st edn. Wiley-Blackwell, Oxford, pp 395–440

    Chapter  Google Scholar 

  • Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474

    Article  PubMed  Google Scholar 

  • Hasegawa M (ed) (2011) Reptiles and Amphibians. In: The Committee of the Red Data Book Chiba, The Important Species for Protection in Chiba Prefecture, pp 125–144. Nature Conservation Division, Environmental and Community Affairs Department, Chiba

  • Holland BS, Dawson MN, Crow GL, Hofmann DK (2004) Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Mar Biol 145:1119–1128

    Article  Google Scholar 

  • Holland BS, Montgomery SL, Costello V (2010) A reptilian smoking gun: first record of invasive Jackson’s chameleon (Chamaeleo jacksonii xantholophus) predation on native Hawaiian species. Biodivers Conserv 19(5):1437–1441

    Article  Google Scholar 

  • Holsbeek G, Mergeay J, Hotz H, Plötner J, Volckaert FAM, De Meester L (2008) A cryptic invasion within an invasion and widespread introgression in the European water frog complex: consequences of uncontrolled commercial trade and weak international legislation. Mol Ecol 17(23):5023–5035

    Article  PubMed  CAS  Google Scholar 

  • Honda M, Yasukawa Y, Hirayama R, Ota H (2002) Phylogenetic relationships of the Asian box turtles of the genus Cuora sensu lato (Reptilia: Bataguridae) inferred from mitochondrial DNA sequences. Zool Sci 19:1305–1312

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MrBAYES. Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Ichihashi Y (1932) Japanese in the United States. Stanford University Press, Stanford, pp 28–29

    Google Scholar 

  • IUCN (2014) The IUCN red list of threatened species. Version 2014.3. http://www.iucnredlist.org. Accessed 1 Aug 2014

  • Johnson JR, Thomson RC, Micheletti SJ, Shaffer HB (2011) The origin of tiger salamander (Ambystoma tigrinum) populations in California, Oregon, and Nevada: introductions or relicts? Conserv Genet 12(2):355–370

    Article  Google Scholar 

  • Jousson O, Pawlowski J, Zaninetti L, Zechman FW, Dini F, Di Guiseppe G, Woodfield R, Millar A (2000) Invasive alga reaches California. Nature 408:157–158

    Article  PubMed  CAS  Google Scholar 

  • Kalinowski ST, Muhlfeld CC, Guy CS, Cox B (2010) Founding population size of an aquatic invasive species. Conserv Genet 11:2049–2053

    Article  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in mammals: amplification and sequencing with conserved primers. Proc Natl Acad Sci 86:6196–6200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kraus F (2002) New records of alien reptiles in Hawaii. Occas Pap Bernice P Bishop Mus 69:48–52

    Google Scholar 

  • Layhee M, Marchetti MP, Chandra S, Engstrom T, Pickard D (2014) Impacts of aquatic invasive species and land use on stream food webs in Kaua’i, Hawai’i. Pac Conserv Biol 20(3):252–271

    Google Scholar 

  • Le M, Raxworthy CJ, McCord WP, Mertz L (2006) A molecular phylogeny of tortoises (Testudines: Testudinidae) based on mitochondrial and nuclear genes. Mol Phylogenet Evol 40:517–531

    Article  PubMed  CAS  Google Scholar 

  • Lind AW (1955) Hawaii’s people. University of Hawaii Press, Honolulu

    Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • May B, Marsden JE (1992) Genetic identification and implications of a second invasive species of dreisennid mussel in the Great Lakes. Canad J Fish Aquat Sci 49:1501–1506

    Article  Google Scholar 

  • McKeown S, Webb RG (1982) Softshell Turtles in Hawaii. J Herpetol 16:107–111

    Article  Google Scholar 

  • Mitsukuri K (1906) The cultivation of marine and fresh-water animals in Japan. In: Rogers HJ (ed) Congress of arts and science: Universal Exposition, vol 4. Houghton Mifflin and Co, St. Louis, pp 696–704

    Google Scholar 

  • Nakamura K, Ueno SI (1963) Japanese amphibians and reptiles in colour. Hoikusha, Osaka

    Google Scholar 

  • Nylander J (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University

  • Nylander J, Wilgenbusch J, Warren D, Swofford D (2008) Awty (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581–583

    Article  PubMed  CAS  Google Scholar 

  • Parham JF, Shi H (2001) The discovery of Mauremys iversoni-like turtles at a turtle farm in Hainan Province, China: the counterfeit golden coin. Asiat Herpetol Res 9:71–77

    Google Scholar 

  • Parham JF, Simison WB, Kozak KH, Feldman CR, Shi H (2001) New Chinese turtles: endangered or invalid? A reassessment of two species using mitochondrial DNA, allozyme electrophoresis and known-locality specimens. Anim Conserv 4:357–367

    Article  Google Scholar 

  • Parham JF, Papenfuss TJ, van Dijk PP, Wilson BS, Marte C, Schettino LR, Simison WB (2013) Genetic introgression and hybridization in Antillean freshwater turtles (Trachemys) revealed by coalescent analyses of mitochondrial and cloned nuclear markers. Mol Phylogenet Evol 67(1):176–187

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45

    Article  PubMed  Google Scholar 

  • Purcell KM, Ling N, Stockwell CA (2012) Evaluation of the introduction history and genetic diversity of a serially introduced fish population in New Zealand. Biol Invasions 14:2057–2065

    Article  Google Scholar 

  • Radford CC (2011) The endangered wattle-necked softshell turtle (Palea steindachneri) throughout the Hawaiian Islands. Master’s thesis, California State University, Chico, California

  • Rambaut A, Drummond AJ (2007) Tracer v1.4. http://beast.bio.ed.ac.uk/Tracer

  • Reece EJ (1914) Race mingling in Hawaii. Am J Sociol 20:104–116

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sax DF, Gaines SD (2008) Species invasions and extinction: the future of native biodiversity on islands. Proc Nat Acad Sci 105:11490–11497

    Article  PubMed  PubMed Central  Google Scholar 

  • Sax DF, Gaines SD, Brown JH (2002) Species invasions exceed extinctions on islands worldwide: a comparative study of plants and birds. Am Nat 160:766–783

    Article  PubMed  Google Scholar 

  • Shi H, Parham J (2000) Preliminary Observations of a large turtle farm in Hainan Province, People’s Republic of China. Turt Tortoise Newsl 3:4–6

    Google Scholar 

  • Shi H, Fan Z, Feng Y, Yuan Z (2004) New data on the trade and captive breeding of turtles in Guangxi Province, South China. Asiat Herpetol Res 10:126–128

    Google Scholar 

  • Shi H, Parham J, Lau M, Chen TH (2007) Farming endangered turtles to extinction in China. Conserv Biol 21:9–10

    Google Scholar 

  • Shi H, Parham JF, Fan Z, Hong M, Feng Y (2008) Evidence for the massive scale of turtle farming in China. Oryx 42:147–150

    Google Scholar 

  • Siler CD, Oaks JR, Cobb K, Ota H, Brown RM (2014) Critically endangered island endemic or peripheral population of a widespread species? Conservation genetics of Kikuchi’s gecko and the global challenge of protecting peripheral oceanic island endemic vertebrates. Diver Distrib 20(7):756–772

    Article  Google Scholar 

  • Simberloff D (2003) How much information on population biology is needed to manage introduced species? Conserv Biol 17:83–92

    Article  Google Scholar 

  • Spinks PQ, Shaffer HB (2007) Conservation phylogenetics of the Asian box turtles (Geoemydidae, Cuora): mitochondrial introgression, numts, and inferences from multiple nuclear loci. Conserv Genet 8:641–657

    Article  Google Scholar 

  • Spinks PQ, Shaffer HB, Iverson JB, McCord WP (2004) Phylogenetic hypotheses for the turtle family Geoemydidae. Mol Phylogenet Evol 32:164–182

    Article  PubMed  CAS  Google Scholar 

  • Spinks PQ, Thomson RC, Zhang Y, Che J, Wu Y, Shaffer HB (2012) Species boundaries and phylogenetic relationships in the critically endangered Asian box turtle genus Cuora. Mol Phylogenet Evol 63:656–667

    Article  PubMed  Google Scholar 

  • Steadman DW (2006) Extinction and biogeography of tropical pacific birds. University of Chicago Press, Chicago

    Google Scholar 

  • Stejneger L (1907) Herpetology of Japan and adjacent territory. Bull US Natl Mus 58:1–577

    Google Scholar 

  • Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction. Am J Hum Genet 73:1162–1169

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stepien CA, Tumeo MA (2006) Invasion genetics of Ponto-Caspian gobies in the Great Lakes: a ‘cryptic’ species, absence of founder effects, and comparative risk analysis. Biol Invasions 8:61–78

    Article  Google Scholar 

  • Strong EK Jr (1934) The second-generation Japanese problem. Stanford University Press, Stanford

    Google Scholar 

  • Stuart BL, Parham JF (2004) Molecular phylogeny of the critically endangered Indochinese box turtle (Cuora galbinifrons). Mol Phylogenet Evol 31:164–177

    Article  PubMed  CAS  Google Scholar 

  • Stuckas H, Fritz U (2011) Identity of Pelodiscus sinensis revealed by DNA sequences of an approximately 180-year-old type specimen and a taxonomic reappraisal of Pelodiscus species (Testudines: Trionychidae). J Zool Syst Evol Res 49:335–339

    Article  Google Scholar 

  • Suzuki D, Hikida T (2014) Taxonomic status of the soft-shell turtle populations in Japan: a molecular approach. Curr Herpetol 33:171–179

    Article  Google Scholar 

  • Temminck CJ, Schlegel H (1835) Reptilia. Chellonii. In: De Siebold, PF (ed) Fauna Japonica, pp 1–80. Amsterdam

  • Thibault I, Bernatchez L, Dodson JJ (2009) The contribution of newly established populations to the dynamics of range expansion in a one-dimensional fluvial-estuarine system: rainbow trout (Oncorhynchus mykiss) in Eastern Quebec. Divers Distrib 15:1060–1072

    Article  Google Scholar 

  • Turtle Taxonomy Working Group (van Dijk PP, Iverson JB, Rhodin AGJ, Shaffer HB, Bour R) (2014) Turtles of the World, 7th edition: annotated checklist of taxonomy, synonymy, distribution with maps, and conservation status. In: Rhodin AGJ, Pritchard PCH, van Dijk PP, Saumure RA, Buhlmann KA, Iverson JB, Mittermeier RA (eds) Conservation biology of freshwater turtles and tortoises: a compilation project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelon Res Monogr 5(7):329–479

  • van Dijk PP, Stuart BL, Rhodin AGJ (eds) (2000) Asian turtle trade: Proceedings of a workshop on conservation and trade of freshwater turtles and tortoises in Asia. Phnom Penh, Cambodia, 1–4 December 1999. Chelon Res Monogr vol 2, pp 1–164. Chelonian Research Foundation, Lunenberg

  • Vitousek PM, D’Antonio CM, Loope LL, Rejmanek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. New Zeal J Ecol 21:1–16

    Google Scholar 

  • Webb RG (1980) The trionychid turtle Trionyx steindachneri introduced in Hawaii? J Herpetol 14:206–207

    Article  Google Scholar 

  • Weisrock DW, Janzen FJ (2000) Comparative molecular phylogeography of North American softshell turtles (Apalone): implications for regional and wide-scale historical evolutionary forces. Mol Phylogenet Evol 14(1):152–164

    Article  PubMed  CAS  Google Scholar 

  • Wilcove DS, Rothstein E, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615

    Article  Google Scholar 

  • Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666

    Article  Google Scholar 

  • Yang P, Tang Y, Ding L, Guo X, Wang Y (2011) Validity of Pelodiscus parviformis (Testudines: Trionychidae) inferred from molecular and morphological analyses. Asian Herpetol Res 2(1):21–29

    Article  CAS  Google Scholar 

  • Zhang C, Xu XJ, Zhang HQ, Mu CK, He ZY, Wang CL (2014) PCR-RFLP identification of four Chinese soft-shelled turtle Pelodiscus sinensis strains using mitochondrial genes. Mitochondr DNA 26(4):538–543

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Acknowledgments

We thank Molly Hagemann (Bishop Museum) for facilitating a tissue sample loan and access to specimen records, and Robert Creamer and Keevin Miniami for donating specimens. Áki Laruson, Van Wishingrad, and Amber Wright provided valuable assistance in the field. We also thank Nicolai Barca, Don Heacock, Keevin Miniami, Chris Radford, Ted Shanks, and Shannon Smith and for helpful correspondence regarding softshell turtle sightings. Anthony Barley, Brenden Holland, and Amber Wright provided helpful comments on the manuscript. This work was supported by a Hampton and Meredith Carson Fellowship (to C.M.D.) through the University of Hawaii at Manoa.

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  1. Department of Biology, University of Hawaii, 2538 McCarthy Mall, Edmondson Hall Rm 216, Manoa, Honolulu, HI, 96822, USA

    Caroline M. Dong & Robert C. Thomson

  2. Biological Sciences, California State University, Chico, CA, 95929, USA

    Tag N. Engstrom

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Dong, C.M., Engstrom, T.N. & Thomson, R.C. Origins of softshell turtles in Hawaii with implications for conservation. Conserv Genet 17, 207–220 (2016). https://doi.org/10.1007/s10592-015-0772-7

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