Distribution , Natural History , and Exploitation of Leucoc Ephalon Yu

948 C!-tE LONIAN CONSERVATION AND BIOL OGY, Volume 4, Number 4 - 2005

of the Testudinesof the AyeyarwadyBasin. Repon to Turtle The Sulawesi forest turtle is listed by IUCN as Critically Recove1yProgram. The WorldCo nservation Union-IUCNSSC Endangered (IUCN, 2004, www.redlist.org) and is a species Tonoise& FreshwaterTurtle Specialist Group,34 pp. of conserva tion concern. While visiting central Sulawesi in VAN DuK.P.P. 1997.Tunle conservaiion in Myanmar:Pa st, present, February 2002 we were given the opportunity to accompany and fu1ure.In: Abbema,J.V. (Ed.). Proceedings: Conservation. commercial turtle collectors on one of their forays into the restoration. ,rndm,rnagement of tortoises,u1d twtle s - An lntema- 1ional Conference.New York: New York Tunle and Tonoise turtle's natural habitat. We also visited three commercial Societyand WCSTurtle Recovery Program, pp. 265-271. turtle holding facilities. Here we report habitat descriptions, VAN DuK,P .P. ln press.Kacl111ga trivi11ma (Dumeril & Bibron, 1835). behavior, and morphology of L. yuwo,wi, as well as some TheConservation Bi ologyofFreshwa1erTu11les. Vol. I. vanDijk. insights into local commercia l trade and possible conserva­ P.P., Pii1chard.P.C.H, and Rhodin, A.G.J. (Eds.). Chelonian tion measures. Research Monographs. Methods. - Data were collected from 23 to 26 February VERNAY.A.S. 1935. Exploring the ·'Mighty Chindwin". Natural 2002 in Donggala County, central Sulawesi, Indonesia. On History 35:37-50. the evening of 24 February 2002 we were permitted to W11EELER, J.T. 1871. Journal of a Voyage up the Irr-.iwaddyto accompany four commercial turtle collectors into the low­ Mandalayand Bhamo.Rang oon: GovernmentPrinter s. 102pp. land forest of the Santigi region (00°35'N. 120°54'E) on a Received: 24 June 2002 nocturnal search for L. yuwo,wi. We searched a small stream Revised and Accepted: 30 October2004 and tributaries near the Kanggol River for 4.5 hours ( 1930 to 2400 hrs) and surveyed approximately 4 km of the stream.

Cllrltmiau Omsrn ·mum muf 8;11/fl~~- :2005. Jf-.l>:9-18-95 I Turtles were located and captured by hand by wading 0 2005 b) Chelomun Rc ...ca~h Founda.uon and searching in the stream bed. Midline carapace lengths (CL) and maximum carapace widths (CW) were recorded, Distribution , Natural History , and a well a water and air temperatures. Exploitation of Leucoc ephalon yu.wouoi We also visited temporary holding and dealer facilities in Central Sulawesi, Indonesia where turtles were examined. Also, reptile dealers and local turtle collectors were interviewed for anecdotal information

12 1 concerning their knowledge of L. yuwono i. CR 1s HAGEN • AN D h VALAN I Y.S. Cm NG Study Sire. -The stream and small tributaries that we surveyed were clear and shallow, allowing high visibility by 1 T1mle Dreams - Chelonian Resc11e, day and easy flashlight viewing at night. The stream aver­ Rehabili1ation, Education a11dConservation Facility. aged about 30 cm deep and 4 to 5 m wide. The small P.O. Box 3432, Ventura, Cal(fomia 93006 USA I £-mails: [email protected]; iwa/[email protected]/ tributaries were only about J m wide, very shallow ( < 10 2Present Address: Savm11wl,River Ecology Labora/ory. cm), and heavily shaded by vegetation. Water and air tem­ Drawer£, Aiken, 5011thCarolina 29802 USA peratures ranged from 25.2 to 26.9°C and 25.0 to 27.2°C, I £-mail: [email protected]/11} respectively. The substrate of the stream was pebbles,gravel, and cobble sized stones with large slabs of protruding rock. AB STRACT. - The SuJawesi forest turtJe, Leuco• Intenni ttent rock pools were encountered along the stream, cepha /011y 11wo 11oi, is Critically Endangered and averaging about 0.5- 1 m in depth and I m in width. The exploited for the food and pet trade, but little is stream and tributaries also contained some woody debris known of its ecology. We accompan ied a group from tbe stmounding secondary growth forest. Along the of commercia l turtle collector s into the wild and tributaries surveyed, the slope of the surrounding forest obtain ed preliminary data on habitat, diet , and banks generally ranged between 60 to 80° inclination. The exploitation. maximum elevation of the area does not exceed 300 m (Platt et al.. 200 1). Our guides indicated that this was typical The Sulawesi forest turtle (Leucocepha/011ymvonoi) is a habitat for L. yu111011oiwith in its local range. poorly known species from central and no1thwestem Sulawesi. Results. - We encou ntered 4 L. yuwonoi in the stream lndone ia. laitially described and named Geoemydtt yuwonoi and small tributaries between 2030 and 2345 hrs. Three of (McCord et al., 1995). Fritz and Obst ( 1996) later placed both the four were found sleeping/resting at the bottom of rock G. y11wo11oiand C. depressa in the genus Heosemys. conclud­ pools. According to our guides, they can also be found in the ing that morphological characters shared with Geoemyda deeper (30-50 cm) still-water sections of the stream chan­ species arose via homopla :,. Based on mitochondrial gene nel. A juveni le (CL= 70 mm. CW= 70 mm) was found along sequence variation and distinctive morphological characters, the main stream channel, at a water depth of 35 cm, within McCord et al. (2000) reas~igned H. yuwo11oi Lo the new some deadfall at the sUJface against the bank (Fig. I). An monotypic genus Leucocepha/011.and reported a close rela­ adult female (CL = 2 10 mm. CW = I 70 mm) was encoun­ tionship with Norochelysplar_, ·11ora.In spite of a clearer under­ tered along a small ( < 2 111wide) tributary sleeping/resting at standing of taxonomic relationships. observations in the wild the bottom of a solid rock pool that was 1.5 111wide at a depth remain scant and little is known of the Sulawesi forest tu111e·s of 45 cm (Fig. 2). In addition, another adult female and an natural history and ecology (Plan et al.. 200 I: Innis. 2003). adult male (no morphometric data recorded) were found NOTES AND FrELD REPORTS 949

Figure 1. Juveni le Leucocephalon yuwonoi as encountered in stream during nocturnal survey in Santigi, central Sulawesi.

Figure 2. Adult female Leucocephalon yuwonoi as encountered in Figure 3. Adu ltLeucocephalonyuwonoi in bolding facility in Palu, stream during nocturnal survey in Santigi, central Sulawesi. Sulawesi, awaiting sbipment to Jakarta, Indonesia.

Figure 4. Captive adult male Leucocephalon yuwonoi displaying characteristic white head. 950 CHELONIAN CONSERVATION AND B10LOGY, Volume 4, Number 4 - 2005 toge ther in a different small ( < 2 m wide) tributary in a pool in Gorontalo and Poso as report ed by McCo rd et al. ( 1995) I m wide at a depth of 60 cm. Both appea red to be sleeping/ may have originated from within Dongga la County. resting on the bottom of the pool approx imately20 cm apart. As described by McCord et al. ( 1995). capt ives are We found fallen fruits (possibly Artocwp us heterophyllus) exce l lent climbers, sem i-aquatic, and herbiv orous. Our field­ in the water that appeared to have turtle bites taken from them, work tends to agree with these observations. Leucocepha/011 but we did not observe turtles feeding. Also, the juvenile yuwonoi must be an adept climber to cope with the rough. captured during our field survey defecat ed and the feces stee p, and rocky terrain that surround s Lhe stream s we were found to contain insect parts, co nfirmin g juvenile surveyed. These turtles tend not to be found in the strea ms carnivory as noted from captive observations (B. Bonner, durin g daylight hours (local tu1tle co llectors, pers. comm.). pers. comm .; J. Vaughan. pers. comm.). We and others familiar with the spec ies be lieve that L. All four L yuwonoi encountered were collected by our yuwonoi forage on Ficus spp. (figs) and other fallen fruit s in guides for commercial purpo ses. Another adult female L. the strea ms and surroundin g forests (F. Yuwono , pers. yuwonoi was collected by a local villager from a different comm.). Plan et al. (200 l ) noted that four unidentified fleshy nearby stream on the same night, also for commercia l reasons. fruits , possibly Ficus spp., were found in L. yuwonoi stool ln addition to our field survey, we obse rved many L. sample s during their survey. Acco rding to Kinn aird et. al. yuwonoi in three co mmercial holding facilities throughout ( 1999) at least 37 fig species occur in north Sulaw es i and are DonggaJa County. We visited a dea ler's house and reptile­ found in the highest densities repo11ed for Southeast Asia 2 holding facil ity in Palu. There. we examined 25 juvenile and ( I J 63 indi viduals/km ). Several Ficus spp. bea r fruit year 48 adult L. yuwonoi, an adult male and female lndorestudo rou nd and the fig s are espe cially rich in ca lcium and Jors/e11ii.a nd I adult male Trachemys scripta elegans . This magne sium compared to other fruit s in the reg ion. The dealer. as of 2002. was the principle organizer of the L. gen us Ficus is reported to be the single most important yuwonoi trade in central Sulawesi. He would apparently visit food resource for Sulawesi· s fruit -ea tin g birds and mam ­ villages throughout the reg ion once or twice a month to mal s ( Kinn aird et al., I 999). purcha se turtles and other rept iles . Loca l co llectors were Local com mercial turtle co llectors indicate hatchLing paid 15,000 Rupiah (ca.$ I .50 US) per hatch ling or juvenile and juveni les are more aquatic and carnivorou s than adults. and 40 ,000 Rupiah (ca. $4.00 US) per adult L. yuwo n.oi. eating aquatic larvae and insects. as well as other small rega rdless of gender. Occasionally, village co llectors would aquatic prey. This co incides with captive observations by us travel to Palu themselves and drop off their turtles. When and others (B. Bonner , pers. comm.; J. Vaughan, pers. enough tu1tles were stockpiled at the hold ing facility in Palu comm.). Hatch lings and juv eniles are also known to readil y they were shipped to a commercial rep tile farm in Jakarta accept a wide variety of fruits and leaves in captivity (J. where they would await distribution. The dealer in Palu was Vaughan, pers. comm.), and are likely to do the same in the paid 50,000 Rupi ah (ca. $5 .00 US) per juv enile and I 50,000 wild. Local turtle collectors also claim that with 3 or 4 people Rupiah (ca. $ 15.00 US) per adu lt by the proprietor of the searching it is co mmon for them to find 5 or 6 L. yuwonoi per reptile farm in Jakart a (app rox imate prices in 2002). night. They have co nducted hunts up to 8 Limes per month. We observed 2 adult male L. yuwonoi (repo rted ly co l­ throughout the year. in the same stream and as of 2002 lected in a nearby forest stream) for sale at a local collector's claimed to find 5 or 6 turtles in a single night. They also house near the sma ll village of Tinombo. We also observed stated that when the moon is bright or full, many turtle s stay an adult female L. yuwonoi and severa l Cuora a111boi11ensis in the forest at night instead of entering the streams. at a reptile dealer's house near the town of Santigi where a Conservarion. - Previously, L. yuwo noi was lega lly sign adve1tised the sa le of kura-kura (Indones ian for fresh­ managed by Indones ia as a fishery reso urce and not afforded water tu11les). This was the only locati on we visited in any spec ific protective status (Sa medi and Iska ndar, 2000). central Su lawes i where turtl es and other reptiles were open ly In 2002 L. _rn1ro11oiwas assigned to CITES Appendix II in sold dome rically (reportedly for pets or food). order to regu late international Lrade and listed as Critically In torn!. we observed 81 L. _,·1111•011oiin transit at captive Endangered by the flJCN Red List of Threatened Species. holding focilitie throughout central Sulawe si. Unfortu­ Also in 2002, based on lndonesia's quota system, no L. nately, we were unable to collect morphological data on yuwo11oi were permitted to be expo 1ted. Howeve r, some these animal:.. All,, ere said to be collected from December Indones ian expo rters still held unused expo rt pennits from 200 I through Februar: 200}. The overcrowded and unsani­ previo us years, exp laining why some L. yuwonoi were tary condi tionsofthe!>e facilitie in which the turtle s are held impo1ted into the USA dmin g 2002 (A. Weinberg, pers. for weeks or months like!~ help exp lain the high mortality comm.). Quotas for 2003 and 2004 were set at 100 animal s rate of some pet trade spec imens (Fig. 3). for each year (www .cites.org). Addit ionally, because of the Discussion. - According to loca l commercial turtle lack of proper species identification trainin g of both export co llectors, literatur e report s, and our obse rvations, the range (D. lskandar , pers. comm.) and import inspec tors, as well as of L. yuwo noi extends at least from the Santigi region in the the phenotypic resemb lance and close geog raphic proximity north of Don gga.la County south to Lore Li_nduNational Park of L. yuwo11oi to other turtles such as Cyclemys spp. and (Platt et al. , 200 I; Colijn, 200 I; F. Taula. pers. comm.). We Norochelys platy 1101a, some misidentified specimens are believe that the type spec imens purchased by Frank Yu wono likel y to be traded. NOTES AND FI ELD REPORTS 95 1

We recommend that more field studie s are needed to Pt.An.S.G .. LEE,R.J .. ANDKL EMENS. M.W. 2001. Noteso n the distribu­ better define thedisoibution and natural histo ry of L. yuwo noi, tion, life history.and exploitation of turtlesin Sulawesi, Indon esia,with especially for conse rvation applications. Captive obse rva­ emphasison lndotestudofor.wen ii and Leucocephalony 11wo11oi.Che­ IonianConse 1vation and Biology 4( I):54- 159. tions of the reproductive biology of this spec ies note that SAMEDIAND lsKANDAR, D.T. 2000. Freshwater turtle and tortoise only one large (48-52 g) egg . occas ionall y two, is laid per conservation and ucilizationin Indonesia. In: van Dijk. P.P.. Stuart. clutch , with up to 3 clutches per year (Innis. 2003; B. Bonner , B.L.. and Rhodin, A.G.J. (Eds.). AsianTurtle Trade: Proceedings of pers. comm.; ]. Vaughan, pers. comm.). This reproducti ve a Workshop on Conservationand Trade of FreshwaterTunles and strategy hou ld be considered when determining prote ctive Tortoises in Asia. Chelonian ResearchMonographs 2: 106-111. sta tus for this spec ies . Lf L. yuwo noi generally lays one egg per clutch then any sustainabl e harvest of adults would be Received: 26 September 2002 Revised and Accepted: 18 May 2004 co nsidered impo ss ible (Co ngdo n et al., 1993, 1994 ). Leucocepha /011yuwo noi is endemic to Su lawes i and rela­ tively access ible to local turtle colJectors. We agree with Platt et aJ. (200 I) that this spec ies should be afforded the Chdtmimr Crmst:n'i,titm(md Biology. 200S. -1(4):951-954 0 2005 by Chelonian Resc.arc:hFoundation highest level of protection under Indonesian law.

Acknowledgements. - We wou ld like to thank the Genetic Analysis of Mitochondrial DNA following for helping us find and observe this species in the Variation in Eastern and Western African wiJd: Robert J. Lee , Steven G. Platt , Faudin Taula , and the Spurred Tor toises, Geocheloue sulcata turtle collectors of Santigi. For setti ng up loca l contacts. we thank Kamuran Tepedelen. We also thank W.P. McCo rd, B ARBARA LrvoREn, 1 AND Barbara B. Bonner, Indran eil Das, Djoko T. lskandar, Frank 2 Yuwon o, Damien C. Schneider, Jea nie Vaughan , and A~TOL'\ETI'E C. VAN DER KUYL Jonathan Ril ey for advice, assistance, and technical and moral suppo rt. Manuscript preparation support was pro­ 'Centre fo r Research a11dCo11se111a1io11 of Chelo11icms. SOPTOM. BP 24. 83590 Gonfaron, France vided by the University of Georgia's Savannah Ri ver Ecol­ f Fax: 33-./9./-78-2427; £-mail: Blivorei/@aol.com/ ogy Laboratory and with Financial Assistance Award Num­ "Department of Human Retrovirology. Academic Medical ber DE-FC09-96SR18546 from the U.S. Depa rtment of Cemre. U11irersiryof Amsterdam, Meibergdreef 15, I 105 AZ Ene rgy to the University of Georgia Resea rch Foundation. Amsrerdam. Netherlands {£ -mail: [email protected]} Also, we thank W.P. McCo rd, Steven G. Platt, Kun A. Buhlmann , Peter C.H. Pritc hard, Anders G.J. Rhodin. and ABSTRACT. - Genetic analysis of mtDNA in the Thomas S.B. Akre for reviewing drafts of this repon. widespread African tortoise, Geochelo ne sulcata, revealed three closely related haplotypes, two of LIT ERATURE CITED them specific to animals from, respective ly, Sudan in the eastern range and Senegal in the CoLIJN,E. 200 l. The Lndonesia conservation database. Checkfot of the reptiles of Lore Lindu National Park. http:1/users.ban.nl/ west. One common haplotype was also found in ---edcolijn/lindu.html. animals from Sudan, Senegal, and Mali. CONGDON. J.O., DUNHAM.A. E.. ANDVAN LOB EN SELS,R.C. 1993. Delayed sexual maturity and demographics of Blanding'stun le~ The African spurr ed tortoise , Geoche/011.e sulcata (Emydoideab landingit):implications for conservationand manage­ (1liller, l 779) is tbe largest con tinent al tortoise species, mentof long-livedorga nisms. ConservationBiology 7(4):826-833 . weig hing up to 100 kg (Lamb ert, 1993). Its disn·ibution CONGDON,J.D .. DUNIIAM,A.E .. ANDVAN LoBEN SELS.R.C . 199-t. ranges from Senegal in the west to Eritrea (Erythrea) in the Demographicsof common snapping tunles (Chelydraserpe111ina 1: eas t, which co1,-espo nds to a be lt about 500 km wide across implications for conservation and management of long-lived or­ ganisms. American Zoologist 34(3):397-408. the sub-Saharan African co ntine nt (Loveridge and Will­ FRITZ.U. ANDOssT. F.J. 1996. Zur Kennrnis der Celebes­ iams, 1957; Iverso n, 1992; Deva ux , 2000a). Although con­ Erdschildkrote.H eosemysy 11wo11oi(McCord , Iverson and Boeadi. sidered common and abundant several decades ago, popula ­ 1995). Herpetofauna I 8( I02):27-34. tions have declined since the early I 990s, and they are now L'INIS, C.J. 2003. Preliminary observations on reproductive param­ highly fragmented (Fig. 1). Ca uses of decline are mostJy eters of Lhe Sulawesi forest turtle (Leucoceplwlo11y 11wo11oi) in related to the explosio n of human population and domestic captivity. Chelonian Conservation and Biology 4(3):720-721. herds, with enhanced desertification triggered by severe K1NNA1RD,M.F., O'BRIEN,T .G., ANDSURYADI. S. 1999.The impor­ droug hts in the 1970s (Devaux, 2000a). Geochelone sulcata tance offigs to Sulawesi's imperiledwild Ii Fe. Tropical Biodi ve rsit y is now included in Appendix ll of CITES and benefits from 6( l /2):5-18. McCORD,W.P., lvERsoN,J. B. . ANDBoEADI. 1995. A new batagurid spec i ficconservation program (Stubbs, l 989; Devaux, l 993) . tunle from nonhem Sulawesi, Indonesia. Chelonian Conservation The wide distribution of G. sulcata cou ld possibly be and Biology I (3): 11-3I 6. associated with morphologic and genetic differences among Mc-CORD,W.P. , lvERSoN,J.B .. SPINKS,P.Q ., ANDSHAFFER. H.B. 2000. A populations. A study of size and weight relationships between new genus of geoemydidtUJtle from Asia.Hamad ryad25(2):86-90. anima ls from Sudan and Mali , from opposite ends of the