Somewhat Saved: a Captive Breeding Programme for Two Endemic Christmas Island Lizard Species, Now Extinct in the Wild

Home , Cryptoblepharus, Cryptoblepharus egeriae, Emoia atrocostata

Somewhat saved: a captive breeding programme for two endemic Christmas Island lizard species, now extinct in the wild

P AUL A NDREW,HAL C OGGER,DON D RISCOLL,SAMANTHA F LAKUS,PETER H ARLOW D ION M APLE,MIKE M ISSO,CAITLIN P INK,KENT R ETALLICK,KARRIE R OSE B RENDAN T IERNAN,JUDY W EST and J OHN C.Z. WOINARSKI

Abstract As with many islands, Christmas Island in the or diseases, or to other environmental modifications. Indian Ocean has suffered severe biodiversity loss. Its terres- Consequently, island species are over-represented among trial lizard fauna comprised five native species, of which four the world’s recent extinctions (Duncan & Blackburn, ). were endemic. These were abundant until at least the late In many cases, conservation management responses for s, but four species declined rapidly thereafter and were island species have been ineffective. Often, resources have last reported in the wild between  and . In response been inadequate to respond to synchronous declines of to the decline, a captive breeding programme was established many species. On many islands there are multiple threats in August . This attempt came too late for the Christmas and it is difficult to disentangle their relative or synergistic Island forest skink Emoia nativitatis,whoselastknownindi- impacts, and hence to target management responses most vidual died in captivity in , and for the non-endemic effectively. Furthermore, there may be limited options for coastal skink Emoia atrocostata. However, two captive popu- in situ conservation, and many threats may be difficult to lations are now established for Lister’sgeckoLepidodactylus control (Fritts & Rodda, ). listeri and the blue-tailed skink Cryptoblepharus egeriae.The The Australian Indian Ocean territory of Christmas conservation future for these two species is challenging: re- Island has high levels of endemism but many of these en- introduction will not be possible until the main threats are demic species have declined or become extinct. For example, identified and controlled. of five native mammal species, at least four of which were endemic, only the Christmas Island flying-fox Pteropus Keywords Christmas Island, extinction, gecko, Indian (melanotus) natalis, is known to be extant, and it is now Ocean, reintroduction, skink Critically Endangered (Woinarski et al., ). Notably, the Christmas Island pipistrelle Pipistrellus murrayi was abundant up to the s but declined rapidly to extinction slands provide many of the world’s most important con- in . The failure to conserve this species has been the servation opportunities and challenges. Many have a high I subject of critical review (Martin et al., ). complement of endemic species but these often have small  Christmas Island is a  km island in the Indian Ocean populations, limited genetic diversity and low reproductive (°′ S, °′ E),  km distant from the nearest land rates, lack immunity to novel diseases or are predator-naive. (Java, Indonesia). It was settled in the s, for phosphate These characteristics mean that island species have little mining; % of the island has been cleared but it has otherwise resilience to introduced predators, consumers, competitors mostly retained its original rainforest, and %isnationalpark. Many species have been introduced to Christmas Island and are now widespread even in intact native vegetation. PAUL ANDREW,PETER HARLOW and KARRIE ROSE Taronga Conservation Society Australia, Bradleys Head Road, Mosman, New South Wales, Australia Across much of the island super-colonies of the introduced yellow crazy ant Anoplolepis gracilipes have subverted the HAL COGGER Australian Museum Research Institute, Sydney, New South Wales, Australia previous crab-mediated ecology, leading to an ‘invasional ’ ’  DON DRISCOLL School of Life and Environmental Sciences, Deakin University, meltdown (O Dowd et al., ). The abundance of yellow Burwood, Victoria, Australia crazy ants has been periodically controlled through broad-

SAMANTHA FLAKUS,DION MAPLE,MIKE MISSO,CAITLIN PINK,KENT RETALLICK and scale application of insecticides. BRENDAN TIERNAN Parks Australia, Christmas Island, Indian Ocean, Australia Introduced species known or presumed to prey upon JUDY WEST Department of the Environment, Parks Australia, Canberra, Christmas Island lizards include the feral cat Felis catus (in- Australian Capital Territory, Australia troduced in the s), black rat Rattus rattus (), giant JOHN C. Z. WOINARSKI (Corresponding author) Threatened Species Recovery centipede Scolopendra subspinipes (s) and wolf snake Hub, Charles Darwin University, Casuarina, Northern Territory 0909,  Australia. E-mail [email protected] Lycodon capucinus (c. ). All are now common across Received  July . Accepted  September . First published online the island. An eradication programme is being implemented  November . for feral cats, but no broad-scale management for the other

Oryx, 2018, 52(1), 171–174 © 2016 Fauna & Flora International doi:10.1017/S0030605316001071 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.58, on 28 Sep 2021 at 07:45:25, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605316001071 172 P. Andrew et al.

predators has been undertaken. Three lizard species that may be potential competitors to and disease vectors for native reptiles have been introduced: the geckoes Hemidactylus frenatus (first recorded in ) and Gehyra mutilata () and skink Lygosoma bowringii (). The reptile fauna comprised six native species: the endemic Christmas Island blind snake Ramphotyphlops exocoeti,the Christmas Island forest skink Emoia nativitatis, the blue- tailed skink Cryptoblepharus egeriae, the giant gecko Cyrtodactylus sadleiri and Lister’sgeckoLepidodactylus listeri, and the non-endemic coastal skink Emoia atrocostata. The blue-tailed skink (snout–vent length c.  mm) FIG. 1 Changes in the size of captive-breeding populations of forages actively in low vegetation or on the ground. ’ ’  blue-tailed skink Cryptoblepharus egeriae and Lister s gecko Lister s gecko (c. mm) is nocturnal and arboreal. The for-    Lepidodactylus listeri from November to May on est skink (c. mm) occurred mostly in forest gap and edge Christmas Island and at Taronga Zoo. habitats. The coastal skink (c.  mm) occurred mainly in rocky littoral habitats (Cogger et al., ). Although there are only six records of the blind snake geckoes and  blue-tailed skinks (at November ) were since  (Maple et al., ), the five lizards were generally maintained at facilities on Christmas Island. common until at least  (Cogger et al., ). Declines of These have been treated as independent units (i.e. without the blue-tailed skink were first reported in  (Rumpff, interchange of individuals after establishment). Management ) and of the forest skink, coastal skink and Lister’s by Mean Kinship (Ballou & Lacy, ) was used to maximize gecko in  (Cogger & Sadlier, ), with ongoing de- retention of genetic diversity for Lister’sgeckoatTaronga, clines reported between  and  (James, ; and management by Maximal Avoidance of Inbreeding Schulz & Barker, ). For reasons not yet understood, (Princée, ) was used for blue-tailed skinks at both sites, the giant gecko remains abundant and widespread. and for Lister’s gecko at Christmas Island. Detailed husband- In response to the decline of four lizard species, a captive ry information is not presented here. breeding programme was initiated in . Here we describe Captive populations have been monitored since the progress and outlook of this programme. The role and November ; they have been stable at Taronga, and cost-effectiveness of captive breeding within a broader con- have increased on Christmas Island (Fig. ). These results servation context has been a focus of considerable global provide evidence of some success, but what are the local interest (Bowkett, ). In this case, it was justified by the and broader contexts of this programme, and how can rapid declines (Smith et al., ) and the likelihood that this limited success be consolidated? threats could not be controlled in the wild in the short time Reptiles are currently undergoing a severe global decline, period before the probable extinction of these species. Despite with increasing numbers of threatened species and extinc- a series of intensive and extensive searches, the last records of tions (Gibbons et al., ). Loss is particularly pronounced the Christmas Island population of coastal skink were in for species with small ranges, especially island species. September , of the forest skink and blue-tailed skink in Increasingly, captive breeding and translocation are likely August , and of Lister’s gecko in October . to be necessary mechanisms to forestall extinctions for the From August  as many individuals as possible of the most threatened species. The Christmas Island lizards pre- four declining species were collected from the wild. Three sent a sobering example. The five species were abundant and forest skinks (all females),  Lister’s geckoes and  blue- presumed secure in  (and perhaps remained so for at tailed skinks were captured and housed in purpose-built fa- least another decade), having withstood nearly  years cilities. No coastal skinks and no male forest skinks could be of human settlement and many introductions. But by  captured. The last of the three forest skinks died on  May four of these species had disappeared from the wild. The , the presumed extinction date for this species. The conservation response to this decline was mixed. Because coastal skink still occurs beyond Christmas Island. of limited monitoring, the decline was not detected until To reduce the risk of catastrophic loss, separate on- and  (localized; Rumpff, )or (more widely; off-island (at Taronga Zoo in Sydney, c.  km distant) Cogger & Sadlier, ), and its extreme extent was not re- captive populations were established for both the blue-tailed cognized until c.  (James, ; Schulz & Barker, ). skink and Lister’s gecko. From the wild-caught population Managers took several years to respond, partly because there and its F descendants,  Lister’s geckoes and  blue-tailed was some hope that the reptiles would benefit from exten- skinks were transferred to Taronga in three batches in May, sive control then being implemented for what was perceived June and November ; the remaining  captive Lister’s to be the main threat to the island’s ecology, the yellow crazy

ant (Green & O’Dowd, ). Delay was also a result of the DD, SF, PH, DM, MM, BT and JCZW. This article was absence of bureaucratic levers: the pace of decline out- drafted by JCZW, with subsequent inputs from all co- stripped formal assessment and listing of these species as authors. PA, PH and KR established and have maintained threatened. The forest skink and blue-tailed skink were the captive population at Taronga, and SF, DM, MM, CP, not listed as threatened under Australian legislation until KR and BT have maintained the captive population at January , only  months before the forest skink’s extinc- Christmas Island. tion. Furthermore, the pace of decline left researchers little opportunity to identify the primary cause, and hence little capacity for preventative management. When urgent action References (the captive breeding programme described here) was im-

plemented, it came too late for two species. BALLOU,J.D.&LACY,R.C.() Identifying genetically However, this programme has averted extinction for two important individuals for management of genetic diversity in species. Captive populations of blue-tailed skink and Lister’s pedigreed populations. In Population Management for Survival gecko are now secured, and are increasing. But this is only a and Recovery: Analytical Methods and Strategies in Small Population Conservation (edsJ.D.Ballou,M.Gilpin&T. holding pattern, and may be unsustainable. The current J. Foose), pp. –. Columbia University Press, programme represents a substantial investment (c. AUD New York, USA. , annual expenses and c. AUD , of infrastruc- BOWKETT, A.E. () Recent captive‐breeding proposals and the ture funding since ), and perennial support for main- return of the ark concept to global species conservation.  – taining it cannot be guaranteed. Conservation Biology, , . COGGER, H.G. & SADLIER,R.() The Terrestrial Reptiles of Captive breeding is a means to an end rather than an end-  Christmas Island: A Reappraisal of Their Status. The Australian point itself (IUCN/SSC, ). The ultimate objective of this Museum, Sydney, Australia. programme is the re-establishment of viable populations in COGGER, H.G., SADLIER,R.&CAMERON,E.() The Terrestrial the wild. However, that pathway has formidable challenges, Reptiles of Australia’s Island Territories. Australian National Parks mostly because the primary threat(s) remain unknown and and Wildlife Service, Canberra, Australia. DUNCAN, R.P. & BLACKBURN, T.M. () Causes of extinction in uncontrolled. Currently, we are using a small pool of surplus  –   island birds. Animal Conservation, , . male blue-tailed skinks in small-scale (c. m )predator- FRITTS, T.H. & RODDA, G.H. () The role of introduced species in exclosure trials on Christmas Island, to attempt to identify the degradation of island ecosystems: a case history of Guam. the critical threats, and assess whether these can be controlled Annual Review of Ecology and Systematics, , –. at least locally. However, there may be no option available im- GIBBONS, J.W., SCOTT, D.E., RYAN, T.J., BUHLMANN, K.A.,  mediately for broader-scale control of some threats, particu- TUBERVILLE, T.D., METTS, B.S. et al. ( ) The global decline of reptiles, déjà vu amphibians. BioScience, , –. larlyofwolfsnakesandgiantcentipedes. GREEN,P.T.&O’DOWD, D.J. () Management of invasive In many island conservation projects elsewhere, re- invertebrates: lessons from the management of an invasive alien ant. establishment has been staged through translocation to nearby In Invasive Species Management: A Handbook of Principles and small islands on which the primary threat is absent or can be Techniques (eds M.N. Clout & P.A. Williams), pp. –. Oxford controlled. This is not an option at Christmas Island, given its University Press, New York, USA. IUCN/SSC (IUCN Species Survival Commission) () Guidelines isolation and lack of satellite islands. With due regard to bio- on the Use of Ex Situ Management for Species Conservation. Version security concerns, we are currently evaluating translocation .. IUCN Species Survival Commission, Gland, Switzerland. options to islets in the Cocos (Keeling) group,  km west JAMES, D.J. () Christmas Island Biodiversity Monitoring of Christmas Island, which support no native reptile species. Programme: Third Quarterly Report for the Period April to June . Parks Australia North, Christmas Island, Australia. MAPLE, D.J., BARR,R.&SMITH, M.J. () A new record of the Acknowledgements Christmas Island blind snake, Ramphotyphlops exocoeti (Reptilia: Squamata: Typhlopidae). Records of the Western Australian  – We thank Parks Australia, Taronga Zoo, Foundation for Museum, , . MARTIN, T.G., NALLY, S., BURBIDGE, A.A., ARNALL, S., GARNETT,S. National Parks and Wildlife and Chris Bray Photography T., H AYWARD, M.W. et al. () Acting fast helps avoid extinction. safari tours for support; Mike Smith for help establishing Conservation Letters, , –. this programme; and Jane Hall, Paul Thompson, Frances O’DOWD, D.J., GREEN, P.T. & LAKE, P.S. () Invasional Hulst, Kimberly Vinette-Herrin, and Larry Vogelnest for ‘meltdown’ on an oceanic island. Ecology Letters, , –.  help managing the Taronga populations. PRINCÉE,F.( ) Overcoming the constraints of social structure and incomplete pedigree data through low-intensity genetic management. In Population Management for Survival and Recovery: Analytical Methods and Strategies in Small Population Conservation Author contributions (eds J.D. Ballou, M. Gilpin & T.J. Foose), pp. –. Columbia University Press, New York, USA. JW provided overall direction for this programme, with in- RUMPFF,H.() Distribution, Population Structure and Ecological dependent expert advice from a panel, including PA, HC, Behaviour of the Introduced South-East Asian Wolf Snake Lycodon

aulicus capucinus on Christmas Island, Indian Ocean. Australian Biographical sketches National Parks and Wildlife Service, Christmas Island, Australia. SCHULZ,M.&BARKER,C.() A Terrestrial Reptile Survey of JUDY WEST is Assistant Secretary, Parks Australia, and Chair of the Christmas Island, May–June . Parks Australia North, Christmas Christmas Island Reptile Advisory Panel. HAL COGGER,DON Island, Australia. DRISCOLL and JOHN WOINARSKI are independent advisors to the SMITH, M.J., COGGER, H., TIERNAN, B., MAPLE, D., BOLAND, C., Panel. PAUL ANDREW and PETER HARLOW manage the populations NAPIER, F. et al. () An oceanic island reptile community under held at TARONGA ZOO.KARRIE ROSE is a veterinary scientist man- threat: the decline of reptiles on Christmas Island, Indian Ocean. aging the Australian Registry of Wildlife Health at Taronga Herpetological Conservation and Biology, , –. Conservation Society Australia. SAMANTHA FLAKUS,DION MAPLE, WOINARSKI, J.C.Z., BURBIDGE, A.A. & HARRISON, P.L. () The CAITLIN PINK,KENT RETALLICK and BRENDAN TIERNAN are with Action Plan for Australian Mammals . CSIRO Publishing, Parks Australia, and oversee the programme there. MIKE MISSO was Melbourne, Australia. formerly Manager of Christmas Island National Park.