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1 Zootaxa 2393: (2010) Copyright 2010 Magnolia Press Article ISSN (print edition) ZOOTAXA ISSN (online edition) New localities of endangered Chinese turtles from museum specimens and the practical and ethical challenges using and reporting natural history collection data JONATHAN J. FONG 1 & GE-XIA QIAO 2,3 1 Museum of Vertebrate Zoology; University of California, Berkeley; Berkeley, CA 94720; USA. j_fong@berkeley.edu 2 National Zoological Museum of China, Institute of Zoology; Chinese Academy of Sciences, Chaoyang, Beijing ; China. qiaogx@ioz.ac.cn 3 Corresponding author The turtle fauna of Asia is one of the most diverse in terms of number of species, but is also the most endangered. This is a result of human activities such as habitat destruction and over-harvesting for the pet, food, and medicine trades (van Dijk et al., 2000). Effective conservation measures require adequate baseline data on the ecology, systematics, and geographic distribution of each species. Unfortunately, Asian turtle research is difficult because of the longstanding, high-volume Asian turtle trade that includes long-distance transport. Not only are wild turtles increasingly difficult to find, those found in the field may have escaped or been released into the wild. In particular, because of the turtle trade, reconstructing the natural distributions of turtles becomes a problem; turtle records from Asia need to be treated with caution. A specific example of this situation was pointed out by Parham & Li (1999), where some records from the pet trade proved to be misleading. Currently, Iverson (1992) and The EMYSystem (Iverson et al., 2000) are the main resources available for geographical distributions of turtles. These resources include most published records for Asian turtles, but the distributions for several species are relatively unknown, being represented by only a handful of point localities. With new field records and by sifting through Chinese museums and Chinese literature, researchers have begun to improve these distributions (Parham & Wang, 2000; Fong et al., 2002). Lessons learned from these studies are 1) current distributional data must be scrutinized due to the turtle trade, and 2) Chinese museums and literature hold valuable historical data, since many of the specimens pre-date the mass transport of turtles (~1980). Access to data in Chinese museums is often difficult, due to the distance (interested people must travel to the museums, since catalogues are not electronically available) and language barriers (almost all of the records are in Chinese). However, these museums house valuable and often rare specimens and their associated data that can be used for research. Herein we translate the specimen catalogue for turtles in the Institute of Zoology, Chinese Academy of Sciences (IOZ). We outline a set of explicit criteria to evaluate the reliability of each specimen record, and provide updated distribution maps for the species where there are new data. In addition, we discuss two important issues that field researchers face when documenting locality data: collecting detailed locality data and the dangers of published data leading to the exploitation of the organism (dual-use dilemma). A total of 12 pages of the IOZ catalogue, corresponding to the complete turtle collection, was translated and is presented in Appendix A. The appendix consists of verbatim Chinese data with English translations in parentheses. We have included three slight modifications to the catalogue. First, Chinese characters are converted from their original form in simplified characters to traditional characters. Next, common names, instead of being directly translated, follow the names found in Shi et al. (2008). Lastly, since the taxonomy of some species has changed, scientific names follow the current nomenclature by the Turtle Taxonomy Working Group (2007). Accepted by S. Carranza: 17 Dec. 2009; published: 9 Mar

2 Establishing reliable localities, when data on the specimen were incomplete, required assumptions; it is always possible that a reliable locality may be a result of the turtle trade or that a locality deemed unreliable represents a bona fide occurrence. For this study, we strived to be conservative in order to minimize the false positives, and use this opportunity to collect baseline data to guide future fieldwork. We present the full data (Appendix A) for other researchers and encourage them to confirm or refute our explicit assumptions based on additional data. Not all data were useable since many records were incomplete and/or deemed to be unreliable. Unreliable data were filtered based on the following criteria. Specimens were included only if locality data were more specific than province level and the date of collection was before Although it is useful to know if a species is present in a province (noted in Table 1), this information is too general for locating persisting wild populations. When the most specific data named was a county or city, the locality was mapped to the geographic center of that location, as it minimizes uncertainty (Wieczorek et al., 2004). For date of capture, since the turtle trade dramatically increased in ~1980, specimens collected before this time were tentatively considered reliable, while specimens collected after this time have a higher probability of being imported into the area. TABLE 1. Summary statistics of the turtle specimens in the Institute of Zoology, Chinese Academy of Sciences. Species # New Records # Reliable From Market Locality Problem Date Problem Testudo horsfieldii Cuora galbinifrons Cuora trifasciata Locality & Date Problem New Province Record Cuora mouhotii Yunnan (no date; BIZ00123) Cuora yunnanensis Geoemyda spengleri Mauremys mutica Mauremys reevesii Mauremys sinensis Platysternon megacephalum Pelodiscus sinensis Shanxi (BIZ ) Sacalia bealei Sacalia quadriocellata TOTAL A total of 169 turtle specimens consisting of 12 species from 15 provinces in China are present in the IOZ. Noteworthy are three specimens of Cuora yunnanensis, a speices that was previously believed to be extinct and which only 12 historical specimens exist worldwide. Based on our criteria, 110 of the turtle specimens were problematic: one was bought from a market, one had a problem with the locality (only data to the province level), 52 had problems with the date (missing data or post 1980), and 56 had problems with both locality and date (Table 1). What remained were 59 specimens that met our criteria. We plotted these new localities with previously known data for each species. Many turtle distributions were unchanged after adding the locality records from the IOZ, since the new data were similar to existing data. However, data from the IOZ improved the distribution records for three species: Platysternon megacephalum, Sacalia bealei, and Pelodiscus sinensis. For these three species, an updated distribution map is provided that adds the IOZ data to the existing data from Iverson (1992) and The EMYSystem (Iverson et al., 2000) (Figures 1 3). An additional two species (Geoemyda spengleri and Cuora mouhotii) had new locality data, but the validity of those data, based on our criteria, was questionable. For G. spengleri, the specimen was collected recently 60 Zootaxa Magnolia Press FONG & QIAO

(1987) in a large city active in the turtle trade (Nanning), while for C. mouhotii, the specimen had no date of capture data and is from the capitol of Yunnan Province (Kunming).

3 (1987) in a large city active in the turtle trade (Nanning), while for C. mouhotii, the specimen had no date of capture data and is from the capitol of Yunnan Province (Kunming). These facts associated with these records increase the probability that the turtle was bought in a market or was the result of an escape/release. FIGURE 1. Revised distribution of Platysternon megacephalum combining previously known localities (Iverson, 1992; Iverson et al., 2000) with records from the Institute of Zoology, China. Circles represent 41 previously reported localities, stars represent 11 new records. The issue of non-specific and/or incomplete locality data raises two important issues relating to specimen collection and documentation of ancillary data. The first is the need to increase the quality of data that is associated with museum specimens. The second issue pertains to the dual-use dilemma (Sommerville & CHINESE TURTLE LOCALITIES CHALLENGES Zootaxa Magnolia Press 61

4 Atlas, 2005; Stuart et al., 2006) and the hazards of providing too much data for fragile species that have monetary value. On the first issue, Remsen (1977) and Stebbins (2003) provided important discussion on the techniques and benefits of taking field notes. The key message in these publications is that more data associated with collected specimens is always desirable. An instructional guide written to the members of the Museum of Vertebrate Zoology (MVZ) by Joseph Grinnell (revised by Alden Miller in 1942) implores researchers to Write full [original emphasis] notes, even at risk of entering much information of apparently little value. One cannot anticipate the needs of the future, when notes and collection are worked up. Locality data should be standardized to maximize their effectiveness. The guidelines from the MVZ website ( mvz.berkeley.edu/locality_field_recording_notebooks.html) offer an excellent example. Today, with resources such as handheld GPS devices, Google Earth, and high-resolution paper maps, there is no excuse for incomplete locality data. In addition, collecting specimens should include tissue samples that can be used later for molecular studies. We hope that all researchers, not just those studying turtles, will strive to collect these data along with specimens. The lack of such data in collections limits a specimen s utility and presents challenges to their inclusion in online databasing efforts (e.g., HerpNet; FIGURE 2. Revised distribution of Sacalia bealei combining previously known localities (Iverson, 1992; Iverson et al., 2000) with records from the Institute of Zoology, China. Circles represent 6 previously reported localities, stars represent 5 new records. The second issue is the dual-use dilemma faced by researchers (Sommerville & Atlas, 2005; Stuart et al., 2006), where locality data for a new, rare, or commercially valuable species facilitates its exploitation. There have been several documented cases in the literature (Palomares et al., 2003; Shepherd & Ibarrondo, 2005; Nickerson & Briggler, 2007) where primary literature assists commercial collectors in harvesting. To make 62 Zootaxa Magnolia Press FONG & QIAO

matters worse, commercially valuable species (for pets and medicine) often experience the anthropogenic Allee effect, where increasing rarity increases value, sustains demand, and subsequently helps

5 matters worse, commercially valuable species (for pets and medicine) often experience the anthropogenic Allee effect, where increasing rarity increases value, sustains demand, and subsequently helps drive the species to extinction (Courchamp et al., 2006). Such a situation makes locality data increasingly valuable and sensitive. Although scientists have been trained to fully disclose data to allow others to re-test and check results, it would be naïve to think these locality data were not being used for commercial exploitation. Collecting detailed locality data should still be a necessity for field researchers, but care should be taken in disseminating these data to the public. Chapman and Grafton (2008) and the Global Biodiversity Information Facility provide guidelines for assessing, categorizing, and disseminating sensitive data. We hope that these data and guidelines set forth for using turtle museum records help in the research and conservation of Asian turtles. Also, we are optimistic that our discussion on data collection and dissemination will allow scientists to maximize the utility of specimens while minimizing the negative, anthropogenic impacts. FIGURE 3. Revised distribution of Pelodiscus sinensis combining previously known localities (Iverson, 1992; Iverson et al., 2000) with records from the Institute of Zoology, China. Circles represent 132 previously reported localities, stars represent 6 new records. CHINESE TURTLE LOCALITIES CHALLENGES Zootaxa Magnolia Press 63

6 Acknowledgements This work was made possible through funding from the National Science Foundation, EAPSI summer fellowship (JJF) and the Museum of Vertebrate Zoology, UC Berkeley (JJF). We would like to thank several people who were integral in helping complete this project: Sun Lihua andhuang Xiaolei (Institute of Zoology, Chinese Academy of Sciences) for help in accessing the specimens in the collection, and Jamie Huang (Sacramento, CA) and Janet Fong (Piedmont, CA) for help with the translation. Also we would like to thank James Parham (The Field Museum and California Academy of Sciences), John B. Iverson (Earlham College), Roberta Damasceno (UC Berkeley), and one anonymous reviewer for providing helpful comments on this manuscript. References Chapman, A. & Grafton, O. (2008) Guide to best practices for generalizing primary species-occurrence data, Version 1.0. Copenhagen: Global Biodiversity Information Facility. Courchamp, F., Angulo, E., Rivalan, P., Hall, R.J., Signoret, L., Bull, L., & Meinard, Y. (2006) Rarity value and species extinction: the anthropogenic Allee effect. PLoS Biology, 4, e415. Fong, J.J., Parham, J.F. & Fu, J. (2002) A reassessment of the Distribution of Cuora flavomarginata Gray 1863 on Mainland China. Russian Journal of Herpetology, 9, Iverson, J.B. (1992) A revised checklist with distribution maps of the turtles of the world. Privately Printed. Paust Printing, Richmond, Indiana. 363 pp. Iverson, J.B., Kimerling, A.J., Kiester, A.R., Hughes, L.E. & Nicolello, J. (2000) The EMYSystem. The Terra Cognita Laboratory. Available from: (23 March 2009). Nickerson, M.A. & Briggler, J.T. (2007) Harvesting as a factor in population decline of a long-lived salamander; the Ozark hellbender, Cryptobranchus alleganiensis bishopi Grobman. Applied Herpetology, 4, Palomares, M.L.D., Samb, B., Diouf, T., Vakily, J.M., & Pauly, D. (eds.) (2003) Fish biodiversity: Local studies as basis for global inferences. ACP-EU Fisheries Research Report, 14, 281 pp. Parham, J.F. & Li, D. (1999) A new locality of Cuora pani Song 1984 with comments on its known range. Asiatic Herpetological Research, 8, Parham, J.F. & Wang, Y. (2000) Palea steindachneri: distribution record for China. Herpetological Review, 31, 111. Remsen Jr., J.V. (1977) On taking field notes. American Birds, 31, Shepherd, C.R. & Ibarrondo, B. (2005) The trade of the Roti Island Snake-necked turtle Chelodina mccordi, Indonesia. TRAFFIC Southeast Asia. 42pp. Shi, H., Hou, M., Pritchard, P., Peng, J., Fan, Z., Yin, F., Chen, T., Liu, H., Wang, J., Liu, Y. (Eds.) (2008) Identification Manual for Traded Turtles in China. Contributors: P.P. van Dijk, J.F. Parham, J. Fong, B. Horne, H. Zwartpoorte, C. Schaffer, J. Tucker, B. Devaux, A. Cadi, S. Gong, G. Li. Encyclopedia of China Publishing House, Beijing. 166 pp. Sommerville, M.A. & Atlas, R.M. (2005) Ethics: A weapon to counter bioterrorism. Science, 307, Stebbins, R.C. (2003) A field guide to western reptiles and amphibians. Houghton Mifflin Harcourt, Boston, Massachusetts. 533 pp. Stuart, B.L., Rhodin, A.G.J., Grismer, L.L., & Hansel, T. (2006) Scientific description can imperil species. Science, 312, Turtle Taxonomy Working Group (2007) An annotated list of modern turtle terminal taxa with comments on areas of taxonomic instability and recent change. Chelonian Research Monographs, 4, van Dijk, P.P., Stuart, B.L., & Rhodin A.G.J. (Eds.) (2000). Asian turtle trade: proceedings of a workshop on conservation and trade of freshwater turtles and tortoises in Asia. Chelonian Research Monographs, 2. Wieczorek, J., Guo, Q., & Hijmans, R.J. (2004). The point-radius method for georeferencing locality descriptions and calculating associated uncertainty. International Journal of Geographical Information Science, 18, APPENDIX A. Original and translated text of the turtle catalogue at the Institute of Zoology, China. Chinese text has been converted from its original form in simplified Chinese characters to traditional Chinese characters and is followed by the English translation in parentheses. Common names follow Shi et al. (2008) and scientific names follow Turtle Taxonomy Working Group (2007). 64 Zootaxa Magnolia Press FONG & QIAO

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Freshwater turtle trade in Hainan and suggestions for effective management

Freshwater turtle trade in Hainan and suggestions for effective management 2005, 13 (3): 239 247 Biodiversity Science doi: 10.1360/biodiv.050021 http: //www.biodiversity-science.net 1 (, 100875) 2 (, 571158) 3 (, 570228) : 2002 2004,, 22, 19.6%; 64, 65.3%; 103, 48910, 90%, 3,