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Zoological Journal of the Linnean Society, 2002, 134, 401–421. With 7 figures Electrophoretic delineation of species boundaries within the genus Chelodina (Testudines: Chelidae) of Australia, New Guinea and Indonesia ARTHUR GEORGES1*, MARK ADAMS2 and WILLIAM McCORD3 1Applied Ecology Research Group, University of Canberra, ACT 2601, Australia 2Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, SA 5001, Australia 3East Fishkill Animal Hospital, 285 Rt 82, Hopewell Junction NY 12533, USA Received February 2001; revised and accepted for publication June 2001 A total of 281 specimens of long-necked chelid turtles (Chelodina) were obtained from drainages of Australia, Papua New Guinea and the island of Roti in Indonesia. Ten diagnosable taxa were identified using allozyme profiles at 45 presumptive loci. Chelodina expansa, C. parkeri, C. rugosa and C. burrungandjii are in a Group A clade, C. longi- collis, C. novaeguineae, C. steindachneri, C. pritchardi and C. mccordi are in a Group B clade, and C. oblonga is in a monotypic Group C clade, with each clade thought to represent a distinct subgenus. Chelodina siebenrocki is syn- onymised with C. rugosa. An eleventh taxon, C. reimanni, could not be distinguished from C. novaeguineae on the basis of allozyme profiles, but it is morphologically distinct. Its status is therefore worthy of further investigation. Three instances of natural hybridization were detected. Chelodina rugosa and C. novaeguineae hybridize in the Gulf country of Queensland, with evidence of backcrossing to C. novaeguineae. Chelodina longicollis and C. novaeguineae hybridize in central coastal Queensland, and C. rugosa and C. burrungandjii hybridize along their zone of contact in the plateau escarpment streams and pools. A phylogeny for the Chelodina is presented. © 2002 The Linnean Society of London, Zoological Journal of the Linnean Society, 2002, 134, 401–421. ADDITIONAL KEY WORDS: Natural hybridization – Australian chelid phylogeny – phylogenetic species – long- neck turtle – Chelonia. INTRODUCTION acter states (Gaffney, 1977). Superficially, it is distin- guished from other chelid genera of the region by pos- The freshwater turtle fauna of Australia and adjacent session of only four claws on the front feet, regions is dominated by the family Chelidae, which exceptionally long necks (often longer than the shell) occurs only in Australia, New Guinea, the island of and gular shields which typically meet in front of the Roti in Indonesia and South America. Its fossil record intergular or nearly so in all species (Cogger, 2000). extends back to the Upper Cretaceous of South The genus was thought to have its closest extant rel- America (de Broin, 1987) and the Miocene of Australia atives among the long-necked forms of South America (Gaffney et al., 1989), but no fossil chelids are known (Gaffney, 1977), but the long necks and associated from outside the present range of the family (Williams, modifications of the head and shell of Chelodina are 1953, 1954; Gaffney, 1991). The family is therefore now thought to have been independently derived considered to be of Gondwanal origin (Burbidge et al., (Pritchard, 1984; Seddon et al., 1997; Georges et al., 1974). 1998). Chelodina is one of six chelid genera recognized Six species of Chelodina are regarded as endemic to from the Australian region, a clearly defined mono- Australia (Goode, 1967; Cogger et al., 1983), four phyletic group with a long list of shared-derived char- are endemic to New Guinea (Goode, 1967; Rhodin & Mittermeier, 1976; Philippen & Grossman, 1990; Corresponding author: Arthur Georges. E-mail: Rhodin, 1994a), C. novaeguineae is found in both [email protected] Australia and New Guinea (Goode, 1967) and C. © 2002 The Linnean Society of London, Zoological Journal of the Linnean Society, 2002, 134, 401–421 401 402 A. GEORGES ET AL. mccordi is endemic to the island of Roti in Indonesia and suspected new taxa. This study follows a similar (Rhodin, 1994b). one addressing the issues of species delimitation in the These species fall into three subgeneric groups short-necked chelid genera of Australia (Georges & (Burbidge et al., 1974). Chelodina longicollis and C. Adams, 1996). Our approach is to use an objective steindachneri of Australia, C. pritchardi and C. procedure to identify diagnosable taxa within the reimanni of New Guinea, C. mccordi of Roti (Indone- genus (Davis & Manos, 1991; Davis & Nixon, 1992), sia) and C. novaeguineae belong to Group A with rel- which can be regarded as phylogenetic species. Levels atively narrow heads, shorter thinner necks and of divergence between these taxa, where they are broader plastrons (Goode, 1967; Rhodin, 1994a). Che- allopatric, are used to make judgements on whether lodina expansa, C. rugosa and C. burrungandjii of or not the phylogenetic species should be regarded as Australia, and C. siebenrocki and C. parkeri of New biological species. We also develop a phylogeny for Guinea belong to Group B with relatively broad heads, the genus, and identify three instances of natural longer thicker necks and narrower plastrons (Goode, hybridization. 1967; Rhodin & Mittermeier, 1976; Cann, 1998; Thomson et al., 2000). Chelodina oblonga of south- MATERIAL AND METHODS western Australia is superficially similar to species of Group B, and has often been placed in that group SPECIMEN COLLECTION AND IDENTIFICATION (Goode, 1967; Legler, 1981), however, we follow Bur- A total of 281 specimens of Chelodina were collected bidge et al. (1974) and place it in a third subgeneric from drainages in the five Australian mainland group, Group C. It is distinguished from other states and the Northern Territory, New Guinea and described Chelodina by a consistent set of well-devel- Indonesia (Fig. 1). Specimens of New Guinea species oped neural bones (Burbidge et al., 1974; Thomson & and C. mccordi of Roti Island were accessed through Georges, 1996). A brief historical account of the tax- the collection of live turtles maintained by William onomy of the Chelodina by Rhodin (1994a,b) reveals McCord at the East Fishkill Animal Hospital in New considerable confusion over the number of valid York State. All recognized species except C. kuchlingi, species and the correct designation of populations to and several forms thought to be distinctive, are rep- species. resented (Table 1). The sampling strategy involved The above taxonomy has been formulated only obtaining a minimum of five turtles (not always recently and, while rectifying many long-standing achieved) from each of several natural populations deficiencies, several issues remain unresolved. There of each species, though only single populations were is uncertainty as to whether C. rugosa of northern available for most New Guinea species. Samples for Australia and C. siebenrocki of New Guinea are dis- C. longicollis were supplemented from the Australian tinct species (Goode, 1967), whether populations of Biological Tissues Collection (ABTC), based at the C. novaeguineae from northern Australia and New South Australian Museum, and blood samples for Guinea are conspecific (Rhodin, 1994a), whether C. C. steindachneri were kindly provided by Gerald burrungandjii and populations of Chelodina from Kuchling. The tissues used in this study have been the Kimberley of northern Australia are distinct lodged with the ABTC. (Thomson et al., 2000), and whether the coastal and Turtles representing described Australian species inland forms of C. expansa represent two species or were identified with the aid of keys provided by Cogger subspecies (Cann, 1998). (2000). New Guinea forms, C. burrungandjii and C. Allozyme electrophoresis offers an alternative to mccordi, were identified by reference to original traditional morphological approaches to resolving descriptions. Distinctive populations and undescribed issues such as these (Avise, 1975; Buth, 1984; species were assigned to species using these references Richardson et al., 1986; Hillis, 1987; Buth & Rainboth, and on the basis of locality of collection. Chelodina 1999). It provides a large number of quantitative char- kuchlingi Cann (1997) is known from a single pre- acters that are genetically determined. The enzyme served specimen (WAM R29411) of doubtful origin, systems in use are sufficiently known to ensure that and was unavailable for allozyme analysis. Recent these characters are independent of each other and examination of the holotype of C. oblonga (BMNH any morphological characters used, and they are 1947.3.5.89) shows that it is a form of C. rugosa (C. usually expressed in all individuals regardless of age oblonga has precedence), as suspected by Cann (1998), or sex. Moreover, when compared with morphological and that C. colliei (Gray, 1856) should be the name studies, fewer individuals need be sampled per applied to the distinctive long-necked turtle species population to identify diagnostic character states. of south-west Western Australia (Thomson, 2000). In this paper, we use allozyme electrophoresis to Thomson plans to review and amend some of the con- delimit species within the Chelodina, testing the sequential changes in a submission to the ICZN, so the genetic integrity of both currently recognized species contemporary use of C. oblonga is retained here. © 2002 The Linnean Society of London, Zoological Journal of the Linnean Society, 2002, 134, 401–421 SYSTEMATICS OF CHELID TURTLES 403 Figure 1. Australian and New Guinean drainage basins showing the 46 basins from which samples were collected. Drainage basins are numbered
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