A Review of the European Pond Turtle, Emys Orbicularis (Testudines: Emydidae), As a Subject for Integrative Population Studies

Home , Emydidae

A Review of the European Pond Turtle, Emys orbicularis (Testudines: Emydidae), as a Subject for Integrative Population Studies

HIDETOSHI OTA

Abstract: The Proceedings of the EMYS Symposium, held at Dresden in 1996, were published in 1998 as the 10th issue of Mertensiella. This volume, consisting of 28 articles and seven notes all devoted to the systematics, ecology, physiology, and conservation of the European pond turtle (Emys orbicularis) populations, is reviewed in the light of its significance as a first step toward the international exchange of information/experiences for the comprehensive understanding of this widely distributed, but locally differentiated and threatened species. All the articles and notes, though arranged in a rather curious way, contribute much to our knowledges of this syste- matically interesting and conservationally important turtle, which, until recently, had been poorly studied from the viewpoint of population biology. Reading of this book, one can realize the importance of integrative approaches for the designation of effective conservation measures, especially for a wide-ranging polymorphic organism like this species. This volume is thus recommended for the bookshelves of all students interested in this and relevant fields of biology. Applications of a few other methods/techniques, such as the multivariate analysis of morphological characters and allozyme electrophoresis, are recommended to further improve the evaluation of taxonomic status and conservation priority for local populations of this turtle. Establish- ment of the criteria and guidelines for international translocation-based conservation procedures seems to be an urgent necessity. Key words: Review; Emys orbicularis; Testudines; Population biology; Conservation

The European pond turtle Emys orbicularis is um" was held from 4th to 6th October 1996 at the only native Old World representative of the Dresden to promote an exchange of information family Emydidae (as opposed to Bataguridae: relevant to various aspects of population biology Gaffney and Meylan, 1988), occurring from of E. orbicularis among international authori- northern Africa and southern Europe (including ties, and its proceedings were recently published. a few Mediterranean islands) northward to Den- In this essay, I review these proceedings with ap- mark and Lithuania, and eastward to northern preciation of their being the first step toward the Iran and the Aral Sea region of the former USSR comprehensive understanding of this systemati- (Iverson, 1992; Podloucky, 1997). Despite the cally interesting and conservationally important long-standing view of its being a monotypic spe- turtle. cies with a broad distributional range, recent The volume (Uwe Fritz, Ulrich Joger, Richard revisional studies by Uwe Fritz and his col- Podloucky, and Jean Servan [eds.]. 1998. leagues strongly suggested that the species is ac- Proceedings of the EMYS Symposium Dresden tually highly polytypic, consisting of some 13, 96. Mertensiella, Number 10. Published by more or less localized subspecies (e. g., Fritz, Deutche Gesellschaft fur Herpetologie und Ter- 1989; Fritz and Obst, 1995; Fritz et al., 1996). rarienkunde e. V. [DGHT]. i-vi+302 pages; Such a progress in the infraspecific taxonomy available from DGHT Geschaftsstelle, Postfach has lead to the increase of conservational con- 1421, D-53351 Rheinbach, Germany; price, cerns about this turtle in most of its range, where 29.80DM for DGHT members and 59.80DM populations belonging to particular localized for nonmembers; paperback), henceforth ab- subspecies are threatened by various human ac- breviated as PESD, is composed of 35 contribu- tivities. tions (28 articles and seven notes) by 54 authors. Under such a situation, "The Emys Symposi- Of these, ten articles and notes are chiefly or exclusively devoted to systematics, 11 to ecology, Accepted 20 May 1999 and 13 contributions and the remaining one arti- OTA-EMYS ORBICULARIS POPULATIONS 31 cle to issues relevant to conservation and physi- al., based on the results of morphological and ology of E. orbicuralis, respectively. The text molecular analyses, consider that the Majorcan of each contribution is written in plain, verbally population has originated not from the natural correct English: this seems to be at least partially dispersals from Iberian Peninsula, but from ar- attributable to efforts by James R. Buskirk as the tificial introductions from the more eastern parts Language Editor. A German abstract (Zusam- of Europe. Based on the morphometric analysis menfassung) is added to each contribution, and of several large samples and observations of an English abstract to each article. captive bred individuals, Zuffi and Ballasina recognize the presence of at least four divergent SUMMARYOF THE CONTENTS groups of populations within Italy. While Systematic studies.-Of the ten contributions referring to these groups as ecotypes, they argue devoted to systematics, the article by Fritz (p. 1- the necessity for re-evaluation of taxonomic sig- 27) provides an overview on the current taxo- nificances of color characters. nomic and geographical delimitations of subspe- From a viewpoint of population systematics cies and subspecies groups. Four pages of and historical biogeography, the article by Lenk, beautiful color photographs provided therein Joger et al. (p. 159-175) is of particular interest. show most, though not all, of the subspecies They analyse sequence variation of the recognized at present. He also refers to a few mitochondrial cytochrome b gene among sam- additional variant populations or groups of ples of E. orbicularis from broad geographical populations most likely representing yet un- ranges, and discuss the historical implications of described subspecies. In this article, fossil the phylogeographical pattern illustrated. A records of the Eurasian Emys are also reviewed, total of 187 specimens examined possess 13 and the historical biogeography of E. orbicularis different haplotypes composing six major assem- is discussed with the assumption that most, if blages, which largely correspond to their geo- not all, of those fossils are of direct ancestors of graphic arrangements but with a certain degree this species. He argued that the current geo- of mixture especially in the southeastern graphic range of E. orbicularis reflects influences Balkans. They attempt to explain the recog- of both the climatic changes during the latest nized phylogeographical patterns chiefly on the continental glaciation and recent human activi- ground of extinction of northern and inland ties. populations during the late Pleistocene glacia- Other systematic works include those by Far- tion, and of post-glacial range extensions from kas et al. (p. 89-101), Fritz, Baran et al. (p. 103- southern refugia along major river systems. 121), Fritz, Pieh et al. (p. 123-133), Taskavak The remaining three, all notes, by Ardizzoni and and Reimann (p. 267-278), and Zuffi and Balla- Fritz (p. 287-288), Fritz (p. 296), and Triperi sina (p. 279-286), which concern the taxonomic and Fritz (p. 299-302) refer to morphological status, relationships and/or diversity of popula- features in samples from Sicily, Catalonia, and tions in the Hungarian Lowlands, Turky, southern Italy, respectively. Majorca (a Mediterranean island east of the Ecological and physiological studies. -Six Iberian Peninsula), Turkey, and Italy, respec- contributions chiefly or exclusively focus on the tively. Of these, Farkas et al. highlight the reproductive ecology of populations in Germany differentiation of the Hungarian population (Andreas and Paul, p. 29-32; Schneeweiss, An- from the German and Polish populations in size dreas and Jendretzke, p. 227-234), Poland (Jab- and coloration, which contradicts results of a lonski and Jablonska, p. 141-146; Mitrus and molecular study, which suggested closer histori- Zemanek, p. 187-191), the former USSR cal relationships of the former two populations. (Snieshkus, p. 253-258), and France (Gay and Fritz, Baran et al., on the basis of external Lebraud, p. 297). Of these, Andreas and Paul, characters in a large series of specimens, assign while providing some quantitative data for some of the Anatolian populations, formerly clutches and dimensions of nests in northeastern considered to represent E. o. hellenica or colchi- Germany, report the massive deaths of hat- ca, to E. o. luteofusca, and others to a new sub- chlings and embryos in the nest during an ex- species, E. o. eiselti. Taskavak and Reimann tremely cold winter. Schneeweiss, Andreas, and also analyse morphometric and color variation in Jendretzke describe additional reproductive a different series of Anatolian specimens and, properties, such as the preferred nesting en- while assigning some to luteofusca, demonstrate vironments, incubation period, and the nest the intermediacy of one isolated population be- temperature during the embryonic development tween luteofusca and hellenica. Fritz, Pieh et for the northeastern German populations of E. 32 Jpn. J. Herpetol. 18 (1) 1999

orbicularis, and also report the massive deaths timates sizes and structures of populations that of hatchlings during a recent very cold winter. collectively compose a metapopulation in They argue that the breeding success of this tur- France. While further assuming that environ- tle is severely influenced by predators, agricul- mental heterogeneity influences the life history tural activities, and fluctuation of climatic fac- of turtles, he suspects that the significant differ- tors. Based on ten years of observations of the ences in carapace length between populations eastern Poland population, Jablonski and Jab- may reflect variability in the growth rate induced lonska report that egg-laying is most frequent by a few environmental constraints such as food during the first half of June, and that females availability and the type of microclimate. usually lay eggs in the evening and at same sites Szczerbak (p. 259-266) summarizes the bodysize for many years. They also claim that examina- (i. e., carapace length) variation, habitat proper- tions of nests by researchers often induce subse- ties, abundance, reproduction, diet, and other quent predation upon eggs, especially by crows aspects of natural history in the Ukraine popula- and ravens. Mitrus and Zemanek describe a tions of E. orbicularis. number of breeding properties, such as mating As the only contribution on the physiological (from late April to early May) and egg-laying aspect of E. orbicularis, Pieau (p. 199-207) seasons (from late May to middle June), and reports results of field experiments conducted in clutch size (10-18, usually 14 or 15), for the cen- France, which showed that gender of a hatchling tral Poland populations. They also reported an depends on the proportions of its development occasional death of neonates in the soil (as in the exposed to masculizing and feminizing tempera- case of northeastern German populations: see tures during the thermosensitive period. He above). The note by Gay and Lebraud, despite also confirmed that estrogens play a major role its brevity, provides an excellent summary of in gonadal differentiation. Based on these nesting records of E. orbicularis in France. It results, he suspects the presence of thermosensi- also lists factors causing threats to the survival tive regulation for aromatase (an enzyme that of southern French populations, and emphasizes promotes conversion of androgens to estrogens) the possible impact by the exotic turtle, gene in gonads of the turtle. Trachemys scripta elegans, which has already es- Directly conservation-oriented studies. - tablished a ferral population in this region. Eight articles and one note chiefly focus on the Keller, Andreu, and Ramo (p. 147-158) current distribution and/or status of E. or- present results of their progressive study on the bicularis populations in Russia (Bozhansky and size and age structures of an E. orbicularis Orlova, p. 41-46), France (Cheylan, p. 47-65; population in southwestern Spain. Their study Cheylan and Poitevin, p. 67-82; Devaux and indicates that the growth annuli observed on Bley, p. 83-88), Germany (Hanka and Joger, p. plastral scutes are not always formed annually, 135-140; Podloucky, p. 209-217; Schneeweiss, and that the age determined by counting these p. 219-226; Budde, p. 289-291), and Spain lines may thus suffer underestimation. Maxi- (Mascort, p. 177-186). Of these, Bozhansky mum female and male longevities, confirmed by and Orlova review the recent distribution of this the more reliable mark and recapture method, turtle in western Russia, and point out the possi- are 29 and 28 years, respectively. ble negative impact on the turtle populations Based on telemetry data, Paul and Andreas from the construction of irrigation and drainage (p. 193-197), while presenting home ranges of E. canals, and propose conservation measures to be orbicularis in Germany, report that females taken. Cheylan reviews the prehistoric and re- showed a rather long migration for nesting. cent distributional dynamics of E. orbicularis in Schneeweiss and Steinhauer (p. 235-243) also southern France on the basis of copious data report a long distance (up to 1650m) migration from osteological remains in post-glacial ar- by a female for oviposition near the field of the chaeological sites, writings on this turtle from former study. Interestingly, they also report the 19th and 20th century, and actual field sur- that the turtles recaptured with an interval of 24 veys. He argues that this species, having en- years migrated to, and oviposited in, the same joyed a much wider distribution in the pre- areas. It is argued that the loss of small Perma- historic era, has been reduced through direct hu- nent forest ponds and reforestation have recent- man exploitation as food during 11,000-5,500 yrs ly been causing deficiencies of favorable habitats BP, and more recently destruction and pollution for hatchlings and suitable nesting sites for adult of habitats. Now, most populations but two females, respectively. On the basis of ten years seem to be in more or less relict states and close of mark-recapture study, Servan (p. 245-252) es- to extinction. Cheylan and Poitevin, based on OTA-EMYS ORBICULARIS POPULATIONS 33 the analysis of population dynamics of the turtle where the species was common in the past, and in southeastern France after forest fires, report a removal of pollutants from the water in the mortality rate in the fires of approximately 60%, habitats of this turtle. over-mortality of young individuals during and Arvy and Servan (p. 33-40) report the range of immediately after the fire, and subsequent re- the exotic slider turtle, Trachemys scripta, in juvenation of populations. They also mention France, and compare ecological features be- the impact of fire upon the turtle's habitats tween this species and E. orbicularis on the basis through an almost total destruction of riparian of published data. They predict that T. scripta vegetation, rapid filling of the watercourse under is (or will be shortly) a formidable competitor of the effet of erosion, and an accentuation of the E. orbicularis in natural habitats, in which the torrential flow and a reduction in the run-off two species show a large niche overlap. They time. On the other hand, Devaux and Bley also suspect that the acclimatization in feral report the recent endangered status of the populations of T. scripta to natural environ- southcentral population of E. orbicularis in ments is already beginning in France. Ferri, France. These authors suspect that the proxim- Cerbo, and Pellegrini (p. 95-101), on the other ity of a rubbish dump and sewage deposit, hand, introduce the "Serranella Emys project", seasonal variations in the stream flow, and the which started in 1995 for the purpose of con- entry of chemicals from neighboring vineyards serving severely endangered populations of E. may have been unfavorably influencing this orbicularis in central Italy. This project in- population. Hanka and Joger, on the basis of volves several actions, such as censuses and as- genetic and morphological examinations of sessments of natural population, their direct several turtles from a nature reserve in western protection by habitat preservations, and collec- Germany, emphasize the extreme scarcity, or tion of individuals of badly endangered popula- nonexistence, of individuals representing a pure tions, their captive breeding, and repatriation. native population: those specimens may have Of the remainder, Delavaud, Seguin, and Veyss- been derived from hybridizations between native set (p. 292-295) briefly review the history of individuals of nominotypical subspecies and conservation activities for the E, orbicularis representatives of E, o. hellenica transported population in the coastal marsh area of Charente from southern Europe. Such a view is strength- Maritime, France, and Miquet (p. 298) summa- ened by Podloucky and Schneeweiss, who, on rizes a currently on-going project for the recov- the basis of extensive literature and field surveys, ery of a once eradicated E. orbicularis popula- and morphological examinations of available tion in eastern France by introducing individuals specimens, demonstrated an extreme from neighboring regions. predominance of escaped and released turtles (mostly from southern Europe) in western Ger- EVALUTION AND CRITICISMS many. Podloucky also points out the risk in the As summarized above, all papers in PESD project to augment native populations by in- should be of great use not only to those interest- troducing exotic individuals. On the other ed in the systematics, ecology, and conservation hand, Schneeweiss reviews other artificial factors biology of E. orbicularis, but also to students causing the decline of native populations, such and officers dealing with other taxonomically as overexploitation for food (up to the 19th cen- diverged and/or conservationally concerned spe- tury), and destruction of most freshwater cies as well. Those reading through this book, habitats and nesting sites. With respect to while benefiting from the large amount of useful populations in southwestern Germany, Budde information given therein, should realize the im- provides results of field surveys that are also portance of integrative international approaches strongly suggestive of extreme scarcity of "pure in developing effective conservation measures native" individuals. Mascort, on the other for such a wide-ranging, much differentiated or- hand, reports the results of surveys in north- ganism as E. orbicularis. I was also much im- eastern Spain, which demonstrate drastic pressed to see the active exchanges of relevant declines of almost all populations in this region, information among the authors, which is ex- most likely due to the abrupt reduction of avail- pressed by frequent mutual citations among the able habitats through freshwater pollution and contributions within this book. This is a very coastal development. He argues for the necessi- important issue for proceedings of symposia on ty of carrying out some conservation practices, particular topics like PESD, but always requires such as preservation of the sites that still main- editors to invest a huge amount of time and tain viable populations, restoration of areas effort. Indeed, the editors of this volume have 34 Jpn. J. Herpetol. 18 (1) 1999 done a splendid job in this regard. As such, this Ballasina in PESD, coloration may easily vary volume can be recommended for the book- through highly localized selection and/or in the shelves of all students interested in this and form of purely physiological responses to par- relevant fields of biology. ticular environmental factors in this species. I now turn to a few problematic points in Thus, I would like to recommend that tax- PESD, and also to problems relevant to those onomists re-analyse the morphological data of raised therein. The worst aspect of this book local samples by multivariate methods for fur- lies in the arrangement of articles and notes. ther revision of subspcific classifications of this Contributions on similar topics are often dis- turtle. Ratios and coloration, when convenient, tantly located within PESD. Locations of may be used to diagnose subspecies elucidated as papers by Fritz, Baran et al. (p. 103-121) and a result of such analyses in an a posteriori fashon Taskavak and Reimann (p. 267-278), both con- (see Yasukawa and Ota [1999] and Yasukawa et cerning the taxonomic status of Turkish popula- al. [1996] for examples of such procedure). tions of E. orbicularis, and those by Andreas In PESD, several authors use information and Paul (p. 29-32) and Schneeweiss, Andreas, from sequence variation in mitochondrial DNA and Jendretzke (p. 227-234), both on the to elucidate intraspecific phylogeography (e. g., reproductive aspect of populations in north- Lenk et al.), or to infer origins and subspecific eastern Germany, are among examples of such a allocations of individual specimens in question shortcoming. More careful arrangement of (e. g., Hanka and Joger). This method, deve- contributions would have saved serious readers loped to trace the maternal genealogy of individ- the labor of turning over pages so extensively. uals, is surely very useful for such purposes (A- Currently prevailing infraspecific classification vise et al., 1987). However, it would be even of E. orbicularis has been established only dur- much more effective if used in combination with ing the last decade, almost entirely through the nucleic genetic markers, such as sequence of efforts of Uwe Fritz and his co-workers (e. g., some parts of nucleic DNA and compositions of Fritz and Obst, 1995; Fritz et al., 1996; and allozyme alleles: the present species is likely to papers cited by Fritz in PESD). They seem to have frequently been involved in genealogical have made admirable efforts to access most, if reticulations (i. e., hybridization and introgres- not all, of the currently available materials from sion between individuals from more or less various localities fairly representing the wide diverged populations) through natural or artifi- distributional range of the species. They then cial dispersals, and combined use of markers delimited subspecies by an a priori use of color from mitochondrial and nucleic genomes is most characters and a few measurements, mostly con- effective in elucidating such events (Arnold, verted into ratios through the division by stan- 1992). Analysis of the nucleic genome is also dard length. Naturally, such an approach is very useful to diagnose within-population genet- also followed by several other contributors of ic diversity, which is considered as an indicator PESD. This procedure, however, suffers in two of the population viability (Haig, 1998). Allo- ways. First of all, statistical treatments of ra- zyme electrophoresis is one of the simplest, but tios, such as calculations of means and standard effective methods to address these issues (Ar- deviations (as are practiced by several authors in nold, 1992; Buth, 1984; Murphy et al., 1996). PESD), are beyond logical justifications (see At- Nevertheless, it has not yet been applied to stu- chley and Anderson [1978] and Atchley et al. dies of E. orbicularis (and seldom even to studies [1976] for detailed discussion on the problematic of other chelonians: see Buth and Rainboth attributes of ratios, which constrain their use in [1999] for review). I would like to recommend systematics). For the removal of size factor that the researchers working on the population from morphometric characters in univariate be- systematics, biogeography, and conservation of tween-sample comparisons, analysis of covari- this species attempt this method, along with re- ance (ANCOVA: e. g., Sokal and Rohlf, 1981) cently developed techniques for blood sampling should be employed (but also see the following without causing serious damages to live turtles criticism). Secondly, several recent studies (see Kuchling [1998] for review). demonstrated that the subdivision of a highly Several contributions in PESD refer to trans- variable taxon by univariate analysis for a limit- locations of E. orbicularis individuals in the ed number of characters easily fails to elucidate form of augmentations (sensu Reinert, 1991) to actual biological or historical entities (e. g., Wil- endangered populations (e.g., Ferni et al.) and lig et al., 1986; Thorpe, 1987; Wuster et al., reintroductions to areas where original popula- 1992). Furthermore, according to Zuffi and tions have already disappeared (e. g., Miquet). OTA-EMYS ORBICULARIS POPULATIONS 35

However, translocation and release of nonnative BUTH, D. G. AND W. J. RAINBOTH.1999. Gene ex- individuals, even though they "look" quite simi- pression in the desert tortoise, Gopherus agassizi; lar to native individuals, should be avoided, be- tissue sources and buffer optima for the gene cause such a manipulation is accompanied by products of 73 loci. Biochem Syst. Ecol. 27: 185- 200. considerable risk of reduction of between-popu- DODD, C. K., JR. AND R. A. SEIGEL. 1991. Reloca- lation genetic diversity and population decline tion, repatriation, and translocation of amphibians through deleterious genetic effects of mixing and reptiles: Are they conservation strategies that divergent gene pools (e. g., Templeton et al., work? Herpetologica 47 (3): 336-350. 1986; Burke, 1991; Reinert, 1991), as well as FRITZ, U. 1989. Zur innerartlichen Variabilitat von of the formation of a "false biogeographical Emys orbicularis (Linnaeus, 1758). 1. Eine neue Un- pattern" which would be badly confusing to terart der Europaischen Sumpfschildkrote aus future researchers (e.g., Sato and Ota, 1999). Kleinasien Emys orbicularis luteofusca subsp. nov. Moreover, the success ratio of translocation, ir- Salamandra 25 (3/4): 143-168. respective of repatriation or introduction, may FRITZ, U. AND F. J. OBST. 1995. Morphologische not be so high (Dodd and Seigel, 1991; but see Variabilitat in den Intergradationszonen von Emys Burke [1991] for different view). To avoid un- orbicularis orbicularis and E. o. hellenica. Salaman- dra 31 (3): 157-180. organized imprudent collecting and release of FRITZ, U., C. KELLER,AND M. BUDDE. 1996. Eine turtles under the excuse of conservation, estab- neue Unterart der Eupopaischen Sumpfschildkrote lishment of international criteria and guidelines aus Sudwestspanien, Emys orbicularis hispanica for the translocation-based conservation proce- subsp. nov. Salamandra 32 (3): 129-152. dure seems to be of urgent necessity. Recent GAFFNEY,E. S. AND P. A. MEYLAN.1988. A phylo- announcement of the Second International Sym- geny of turtles. In: M. J. Benton (ed.), The Phylo- posium on Emys orbicularis by Veysset and geny and Classification of the Tetrapods. Vol. 1. Livoreil (1999) lead me to expect that opportuni- Amphibians, Reptiles, Birds. p. 157-219. Clarendon ties for the international exchange of informa- Press, Oxford. tion and experiences on this turtle will be con- HAIG, S. M. 1998. Molecular contributions to conservation. Ecology 79 (2): 413-425. tinuously provided at certain intervals. I sin- IVERSON,J. B. 1992. A Revised Checklist with Distri- cerely hope for improvement in the above and bution Maps of the Turtles of the World. Privately other points through the discussion of authori- Printed, Richmond. 363 p. ties toward the better understanding and suc- KUCHLING,G. 1998. The Reproductive Biology of the cessful conservation of this species. Chelonia. Springer, Berlin. 223 p. MURPHY, R. W., J. W. SITES, JR., D. G. BUTH, AND ACKNOWLEDGMENTS. -I thank A. Kupfer for the C. H. HAUER. 1996. Proteins: Isozyme electropho- provision of this interesting volume for review, and M. resis. In: D. M. Hillis, C. Moritz, and B. K. Mable Toda and Y. Yasukawa for constructive discussion. (eds.), Molecular Systematics. 2nd edn. p. 51-120. Sinauer Associate, Sunderland. LITERATURE CITED PODLOUCKY,R. 1997. Emys orbicularis (Linnaeus, ARNOLD,M. L. 1992. Natural hybridization as an 1758). In: J. -P. Gasc, A. Cabela, J. Crnobrnja-Isai- evolutionary process. Ann. Rev. Ecol. Syst. 23: 237- lovic, D. Dolmen, K. Grossenbacher, P. Haffner, J. 261. Lescure, H. Martens, J. P. Martinez Rica, H. Mau- ATCHLEY,W. R. AND D. ANDERSON.1978. Ratios rin, M. E. Oliveira, T. S. Sofianidou, M. Veith, and amd the statistical analysis of biological data. Syst. A. Zuiderwijk (eds.), Atlas of Amphibians and Zool. 27 (1): 71-78. Reptiles in Europe. p. 170-171. Societas Europaea ATCHLEY,W. R., C. T. GASKINS,AND D. ANDERSON. Herpetologica & Museum National d'Histoire 1976. Statistical properties of ratios. I. Empirical Naturelle, Paris. results. Syst. Zool. 25 (2): 137-148. REINERT, H. K. 1991. Translocation as a conserva- AVISE,J. C., J. ARNOLD,R. M. BALL,JR., E. BERMIN- tion strategy for amphibians and reptiles: Some GHAM,T. LAMB, J. E. NEIGEL, C. A. REEB, AND comments, concerns, and observations. Herpetolog- N. C. SAUNDERS. 1987. Intraspecific ica 47 (3): 357-363. phylogeography: the mitochondrial DNA bridge be- SATO, H. AND H. OTA. 1999. False biogeographical tween population genetics and systematics. Ann. pattern derived from artificial animal transporta- Rev. Ecol. Syst. 18: 489-522. tions: A case of the soft-shelled turtle, Pelodiscus BURKE, R. L. 1991. Relocations, repatriations, and sinensis, in the Ryukyu Archipelago, Japan. In: H. translocations of amphibians and reptiles: Taking a Ota (ed.), Tropical Island Herpetofauna: Origin, broader view. Herpetologica 47 (3): 350-357. Current Diversity, and Conservation. Elsevier BUTH, D. G. 1984. The application of electrophoretic Science, Amsterdam. In press. data in systematic studies. Annu. Rev. Ecol. Syst. SOKAL, R. R. AND F. J. ROHLF. 1981. Biometry. 15: 501-522. W. H. Freeman and Co., New York. 887 p. 36 Jpn. J. Herpetol. 18 (1) 1999

TEMPLETON,A. R., H. HAMMER,G. MACE,U. S. SEAL, serv. Biol. 3 (2): 375-376. W. M. SCHIELDS,AND D. S. WOODRUFF.1986. Lo- YASUKAWA,Y. ANDH. OTA. 1999. Geographic varia- cal adaptation, coadaptation, and polulation boun- tion and biogeography of the geoemydine turtles daries. Zoo Biol. 5: 115-125. (Testudines: Bataguridae) of the Ryukyu Archipela- THORPE,R. S. 1987. Geographic variation: A synthe- go, Japan. In: H. Ota (ed.), Tropical Island Her- sis of cause, data, pattern and congruence in relation petofauna: Origin, Current Diversity, and Conser- to subspecies, multivariate analysis and phylogene- vation. Elsevier Science, Amsterdam. In press. sis. Boll. Zool. 54 (1): 3-11. YASUKAWA,Y., H. OTA, AND J. B. IVERSON.1996. WILLIG, M. R., R. D. OWEN, AND R. L. COLBERT. Geographic variation and sexual size dimorphism in 1986. Assessment of morphometric variation in Mauremys mutica (Cantor, 1842) (Reptilia: natural populations: The inadequacy of the univari- Bataguridae), with description of a new subspecies ate approach. Syst. Zool. 35 (2): 95-203. from the southern Ryukyus, Japan. Zool. Sci. 13 (2): WUSTER,W., S. OTSUKA,R. S. THORPE,AND A. MAL- 303-317. HOTRA.1992. Morphological variation in Russell's viper in Burma and Thailand. Herpetol. J. 2 (3): 99- 101. Tropical Biosphere Research Center, Universi- VEYSSET,A. ANDB. LIVOREIL.1999. 2nd Internation- ty of the Ryukyus, Nishihara, Okinawa, 903- al Symposium on Emys orbicularis. Chelonian Con- 0213 JAPAN