THREATENED SPECIES SCIENTIFIC COMMITTEE

Established under the Environment Protection and Biodiversity Conservation Act 1999

The Minister approved this listing advice and transferred this species from the Critically Endangered category to the Extinct category, effective from 03/03/2021 Listing Advice Emoia nativitatis

Christmas Island Forest Skink

Taxonomy The species is conventionally accepted as Emoia nativitatis (Boulenger, 1887).

Summary of assessment

Conservation status Following a listing assessment of Emoia nativitatis (Christmas Island Forest Skink), the Threatened Species Scientific Committee (the Committee) has determined that there is sufficient evidence to list the Christmas Island Forest Skink in the Extinct category under the Environmental Protection and Biodiversity Conservation Act 1999 (EPBC Act).

Species can be listed under state and territory legislation. For information on the listing status of this species under relevant state or territory legislation, see http://www.environment.gov.au/cgi- bin/sprat/public/sprat.pl

Reason for listing assessment by the Threatened Species Scientific Committee This advice follows assessment of new information provided to the Committee to list the Christmas Island Forest Skink.

Public consultation Notice of the proposed amendment and a consultation document was made available for public comment for 31 business days between 31 July 2020 and 11 September 2020. Any comments received that were relevant to the listing of the species were considered by the Committee as part of the assessment process.

Species/sub-species information

Description Emoia nativitatis (Christmas Island Forest Skink) was a moderately robust (80 mm snout-vent length, 10 gram) skink. The species had a rich metallic-brown colour, paler on flanks, with numerous irregularly scattered paler and darker scales. It differed from E. atrocostata (the sympatric coastal skink) in scalation and colour (the latter having silvery-grey ground colour and a diffuse dark lateral stripe) (Boulenger, 1887).

Distribution This species was endemic to Christmas Island, an Australian Territory in the Indian Ocean.

Extinction date This species was last seen in the wild in August 2010 at Egeria Point, Christmas Island (Smith et al., 2012). The last known individual died in captivity on 31 May 2014 (Woinarski et al., 2014). An overview of the extensive surveys and their findings is provided in Table 1.

On 20 February 2017, the species was listed as Extinct on the IUCN Red List of Threatened Species (Cogger and Woinarski, 2017).

Emoia nativitatis (Christmas Island Forest Skink) Listing Advice Page 1 of 10 Table 1. Summary of survey history and reported declines in the Christmas Island Forest Skink leading to the conclusion that it is extinct.

Year Surveys and status reports Reference

1979 The Christmas Island Forest Skink was reported to be Cogger and the most abundant and widespread of the diurnal lizards Sadlier (1981) on Christmas Island. The species was found to be present at 16 sites across the Island.

1998 The first reported declines in the Christmas Island Forest Cogger and Skink occurred, but the skink was also reported to be Saddlier (1999) common and abundant in some areas in June with more than 80 individuals seen basking and foraging on the trunk of a large tree.

2001 - Island wide surveys were undertaken recording all Director of 2006 reptiles on an ad-hoc basis. Monitoring between 2003 National Parks, and 2005, which sampled 320 sites across the Island, 2008); Director reported the Christmas Island Forest Skink to have National Parks “declined severely” and that it was likely to be confined to (2012); James scattered, localised pockets in more remote areas of the (2004) coastal terraces and inland cliffs.

2005- Targeted monitoring for the Christmas Island Forest Director of 2006 Skink started at long-term biodiversity monitoring sites National Parks each month by National Park officers, following programs (2012) established by David James.

2007 The range of the Christmas Island Forest Skink had James (2007); contracted to scattered populations on remote coastal Director of terraces, of North West Point, Egeria Point and South National Parks Point having disappeared from inland rainforests. (2012)

Mid An island-wide survey took place in which reptiles were Smith et al., 2007 recorded as present or absent at 900 sites spread (2012) equidistantly across the Island. Only a few native reptiles (and no Forest Skinks) were recorded.

2008 Further declines in the Christmas Island Forest Skink Schulz and were reported. The skink had disappeared from North Barker (2008); West Point and South Point between mid to late 2008 Director of and early 2009. The Christmas Island Forest Skink was National Parks reported from only one of the 35 sites sampled in 2008. (2012) The total adult population size of the Christmas Island Forest Skink was considered likely to be substantially fewer than 1000 individuals.

Early The Christmas Island Forest Skink was noticeably Smith et al., 2009 declining in the semi-deciduous closed forest at Egeria (2012) Point, and by mid to late 2009 they were mostly found in Pandanus forest. The species then contracted in a southerly direction within the Pandanus forest.

Late Island wide surveys by National Park staff did not record Andrews et al., 2009 the Christmas Island Forest Skink at any of the 900 sites (2016); Director sampled in mid-2007. From August 2009 to August 2010 of National Parks efforts were made to collect as many individuals of the (2012)

Emoia nativitatis (Christmas Island Forest Skink) Listing Advice Page 2 of 10 Year Surveys and status reports Reference

Christmas Island Forest Skink as possible, which amassed only three females and one individual of unidentified sex. These were then housed in purpose- built facilities on Christmas Island, but the individual of unidentified sex failed to establish in captivity leaving only three females.

Relevant biology/ecology The Christmas Island Forest Skink was known to occur in the litter of the forest floor and also on low vegetation and amongst the buttress roots of rainforest trees, whilst foraging. The species appeared to be as abundant on the plateau as it was on the terraces and the low forest backing onto the rocky coastline (Cogger and Sadlier, 1981).

The Christmas Island Forest Skink was solitary, but historic records suggest that in suitable habitat (forest clearings and forest areas where the sunlight penetrates the canopy), it may have occurred locally in “large numbers” (Cogger and Sadlier, 1981). The species’ diet included a wide range of small terrestrial invertebrates (Cogger and Sadlier, 1981). In areas where yellow crazy ant (Anoplolepis gracilipes) super colonies existed, food availability for the Forest Skink was markedly reduced (TSSC 2014). The species was diurnal and actively foraged on the ground and in low vegetation (Director of National Parks, 2012).

The Christmas Island Forest Skink was not particularly conspicuous and relatively hard to detect. During sunny periods there was a higher chance of detecting the Forest Skink when it could be seen basking or active on and around fallen timber (Director of National Parks, 2012). Although there is no reproductive information for the Forest Skink, a similar species, E. atrocostata, attains sexual maturity between nine and nine and a half months of age and lives for between 3 and 10 years (Alcala and Brown, 1967).

Threats Initially, the rapid decline in population numbers of E. nativitatis was believed to be a result of direct and indirect impacts on the island's forest ecosystems of super colonies of the invasive Yellow Crazy Ant (Anoplolepis gracilipes) (Cogger and Woinarski, 2017). The speed of the decline in both E. nativitatis and other endemic lizards suggested however that the threatening processes causing these declines were multiple and complex (Emery et al, in revision a). Declines took place in most native lizard species on the island following the introduction of the Oriental Wolf Snake (Lycodon capucinus) in the early 1980s (Andrew et al. 2016) and Wolf Snake predation is now believed to be the proximate cause of this skink's extinction (Cogger and Woinarski, 2017).

Due to mining on the island, there has been a loss of 25% of forest habitat, a possible contributing factor to the decline of the species (TSSC 2014). Despite the number of likely and actual threats identified as contributing to the decline and extinction of the Christmas Island Forest Skink, there is no quantitative evidence apportioning the relative impacts of threatening processes (Smith et al., 2012).

Likely causes of decline and extinction are from threats known to have occurred on the Island when the last known Forest Skink was extant (see Table 2).

Emoia nativitatis (Christmas Island Forest Skink) Listing Advice Page 3 of 10 Table 2. Threats which likely led to the extinction of the Christmas Island Forest Skink.

Threat factor Threat type Evidence base and status Invasive species Predation by Wolf Actual, past An expert elicitation project considered the Wolf Snake Snakes (Lycodon to be the primary cause for the collapse of Christmas capucinus) Island’s native lizard community as its temporal and spatial spread across the island closely matched patterns of lizard disappearance (Emery et al., in revision b). Upon arriving on Christmas Island with no predators, no competitors and a hyper-abundance of naive skinks at the point of arrival, the Wolf Snake population rapidly increased, and by 1992 reached extraordinary densities of between 45 and 500 individuals per hectare in the Settlement (Rumpff 1992; Emery et al., in revision b). In the mid-2000s and 2017 over 200 Wolf Snake were dissected, and many had reptiles in their stomachs (James, 2007; Sleeth 2017). Whilst there was no evidence of Forest Skink remains from these dissections or of predation in the wild on the Forest Skink, Rumpff (1992) undertook a captive trial where various reptile species were offered as prey items to Wolf Snakes, whereby the Forest Skink was taken. Feral cats (Felis Actual, past Several studies have confirmed cats as a major catus) predator of the Christmas Island Forest Skink with specimens found in cat stomach contents (Tidemann et al., 1994; and Van der Lee (1997). Cats were also identified as a significant threat to the last remaining populations of the Christmas Island Forest Skink by James (2007). Predation by Giant Actual, past There is inference of predation on another Christmas Centipedes Island skink, the blue-tailed skink (Emery et al., in (Scolopendra revision b). Giant centipedes have also been subspinipes) demonstrated to be a serious threat to two reptile species in captive colonies on the island, including the blue-tailed skink (Smith et al., 2012). Evidence from dietary studies of centipedes confirms they consume small reptiles, and are likely to be predatory (Rumpff, 1992; Donnellan et al., 2011, Emery, in revision b). Yellow Crazy Ant Actual, past Crazy ants were introduced sometime between 1915 (Anoplolepis and 1934. Since the 1990s they have formed high gracilipes) density, multi-queen super colonies at many places over the island (Director of National Parks, 2012) and as a result the habitat of the Christmas Island Forest Skink underwent broad-scale ecological change associated with outbreaks of Yellow Crazy Ants. These outbreaks caused a reduction in the Island’s endemic Red Crab (Gecarcoidea natalis) population, which resulted in an increase in the cover of understorey and ground litter, potentially leading to an increase in the abundance of some exotic species that predate on the Christmas Island Forest Skink and compete for food (Director of National Parks, 2012). A recent assisted colonisation trial of another small

Emoia nativitatis (Christmas Island Forest Skink) Listing Advice Page 4 of 10 Christmas Island species, the Blue-tailed Skink, to Pulu Blan Madar, a small island on the Cocos archipelago was impacted by a colony of Yellow Crazy Ants, with ant bites leading to necrosis (Kristen Schubert, unpublished data). Black rat (Rattus Likely, past Rats were introduced around the time of settlement rattus) and they quickly spread across the island (Tidemann, 1989). There is no direct evidence of predation of the Forest Skink, but rats are a serious threat to reptile species on other islands (Harper & Bunbury 2015). Expert elicitation has identified rats as a potential threat to reptiles on Christmas Island (Emery et al., in revision a) and ex-situ conservation efforts for two Christmas Island lizard species have gone to great lengths to remove Black Rats as a threat. Introduced potential, Introduced disease has been identified as a potential disease past threat to Christmas island reptiles, however no conclusive evidence that disease led to declines has been found (Hall et al, 2011). A novel bacteria has been discovered impacting reptiles on Christmas Island (Rose et al., 2017), however its impacts on the Forest Skink are uncertain. Mining and quarrying Habitat loss Likely, past Since the 1890s, land clearing for activities such as phosphate mining, development and road construction has caused the incremental loss of approximately 25 per cent of forest cover on Christmas Island. This clearing left substantially less suitable habitat available for the Christmas Island Forest Skink (Director of National Parks, 2012).

How judged by the Committee in relation to the EPBC Act criteria and regulations

The Christmas Island Forest Skink is assessed by the Committee to be eligible for listing as Extinct under the EPBC Act. A native species is eligible to be included in the Extinct category if there is no reasonable doubt that the last member of the species has died. The Christmas Island Forest Skink was formerly common and abundant in rainforests on all Christmas Island landforms (Cogger and Sadlier, 1981). Declines were first reported in 1998 (Cogger and Sadlier 1999) and understood to be extreme by 2005 (James 2004, Schulz and Barker 2008), only five years before the species was last recorded in the wild (Andrew et al. 2016).

Efforts to establish a captive breeding program for the species from August 2009 failed because only four individuals, three female and one of unidentified sex that did not establish in captivity, could be captured (Andrew et al., 2016). During the 2009 ‘Island Wide Survey’ monitoring program by Christmas Island National Park staff, the species was not recorded at any of the 900 comprehensively distributed sample sites (Director of National Parks, 2012). The species was last seen in August 2010 as part of systematic surveys in the southern section of Egeria Point. Figures 1-3 depict this and other historical locations of the Forest Skink and the Island wide reptile survey effort in 2009 and 2010. Table 1 summarises the survey history and reported declines in the Christmas Island Forest Skink from initial surveys in 1979 until its Extinct listing under the IUCN Red List in 2017.

Emoia nativitatis (Christmas Island Forest Skink) Listing Advice Page 5 of 10 Figure 1. Historical records of the Christmas Island Forest Skink (top map) including the location of last known sightings of the species (bottom map) (Smith et al., 2012).

Emoia nativitatis (Christmas Island Forest Skink) Listing Advice Page 6 of 10 Figure 2. Sites sampled for reptiles on Christmas Island in 2009 and 2010 (Smith et al., 2012).

Figure 3. Survey effort for the Christmas Island Forest Skink at Egeria Point in 2009 and 2010 (Smith et al., 2012).

Emoia nativitatis (Christmas Island Forest Skink) Listing Advice Page 7 of 10 With the extensive surveys and their findings outlined in Table 1 and Figures 1-3, including no detections in the last 10 years, the disappearance of three other reptile species at roughly the same time and spatial pattern (Emery et al. in revision a), and confirmation of the last known individual dying in captivity on 31 May 2014, this assessment concludes there is no reasonable doubt that the last individual has died and the species is eligible for listing as Extinct.

Recommendations The Committee recommends that the list referred to in section 178 of the EPBC Act be amended by including in the list in the Extinct category: Emoia nativitatus.

Threatened Species Scientific Committee

24/09/2020

References cited in the advice

Alcala, A.C. and Brown, W.C. (1967). Population ecology of the tropical scincid lizard, Emoia atrocostata, in the Philippines. Copeia 1967, 596-604.

Andrew, P., Cogger, H., Driscoll, D., Flakus, S., Harlow, P., Maple, D., Misso, M., Pink, C., Retallick, K., Rose, K., Tiernan, B., West, J. and Woinarski, J.C.Z. (2016). Somewhat saved: a captive breeding programme for two endemic Christmas Island lizard species, now extinct in the wild. Oryx: 1-4. doi:10.1017/S0030605316001071.

Beeton, B., Burbidge, A., Grigg, G., Harrison, P., How, R., Humphreys, B., McKenzie, N. and Woinarski, J. (2010). Final Report Christmas Island Expert Working Group to Minister for the Environment. Heritage and the Arts.

Boulenger, G.A. (1887). Reptiles. Proceedings of the Zoological Society London 55, 515-517.

Chapple, D.G., Tingley, R., Mitchell, N.J., Macdonald, S.L., Keogh, J.S., Shea, G.M., Bowles, P., Cox, N.A. and Woinarski, J.C (2019). The Action Plan for Australian Lizards and Snakes 2017. CSIRO Publishing.

Cogger, H. and Sadlier, R. (1981). The terrestrial reptiles of Christmas Island, Indian Ocean. Unpublished report to Australian National Parks & Wildlife Service, Canberra (Australian Museum, Sydney).

Cogger, H. and Sadlier, R. (1999). The terrestrial reptiles of Christmas Island: a reappraisal of their status. Unpublished report to Parks Australia, Canberra (Australian Museum, Sydney).

Cogger, H. and Woinarski, J. (2017). Emoia nativitatis. The IUCN Red List of Threatened Species 2017: Downloaded on 08 April 2020.

Cogger, H.G., Sadlier, R. and Cameron, E. (1983) The Terrestrial Reptiles of Australia’s Island Territories. Australian National Parks and Wildlife Service, Canberra, Australia.

Emoia nativitatis (Christmas Island Forest Skink) Listing Advice Page 8 of 10 Director of National Parks (2008). Christmas Island Biodiversity Monitoring Program: December 2003 to April 2007. Report to the Department of Finance and Deregulation from the Director of National Parks.

Director of National Parks (2012). Dry Season Reptile Monitoring, Christmas Island National Park Natural Resources Management Team.

Donnellan, S., Armstrong, K. and Potter, S. (2011). Christmas Island National Park centipede genetics. Report to Parks Australia, Canberra (South Australian Museum, Adelaide).

Emery, J. P., Mitchell, N. J., Cogger, H., Agius, J., Andrew, P., Detto, T., Driscoll, D.A., Flakus, S., Green, P., Harlow, P., McFadden, M., Pink, C, Retallick, K., Rose, K., Sleeth, M., Tiernan, B., Valentine, L.E. and Woinarski, J.Z. (in revision a). The lost lizards of Christmas Island: a retrospective assessment of factors driving the collapse of a native reptile community. Conservation Science and Practice

Emery, J. P., Valentine, L. E., Hitchen, Y., & Mitchell, N. J (in revision b). Survival of an Extinct in the Wild skink from Christmas Island is reduced by an invasive centipede: implications for future reintroductions. Biological Invasions

Hall, J., Rose, K., Spratt, D., Harlow, P., Donahoe, S., Andrew, P., Field, H., DeJong, C., Smith, C., and Hyatt, A (2011). Assessment of reptile and mammal disease prevalence on Christmas Island. Report to Parks Australia. Australian Registry of Wildlife Health, Taronga Conservation Society Australia, Sydney, Australia.

Harper, G. A., & Bunbury, N (2015). Invasive rats on tropical islands: their population biology and impacts on native species. Global Ecology and Conservation, 3:607-627.

James, D.J. (2004). Christmas Island biodiversity monitoring programme. Third Quarterly Report April-June 2004. Parks Australia North, Christmas Island, Australia.

James, D.J. (2007). Christmas Island Biodiversity Monitoring Programme: Summary Report, December 2003 to April 2006. Report to Department of Finance and Deregulation, and Department of the Environment , Water, Heritage and the Arts for Parks Australia North, Christmas Island Biodiversity Monitoring Programme, March 2007.

Rose, K., Agius, J., Hall, J., Thompson, P., Eden, J.S., Srivastava, M., Tiernan, B., Jenkins, C. and Phalen, D., 2017. Emergent multisystemic Enterococcus infection threatens endangered Christmas Island reptile populations. PloS one, 12(7), p.e0181240.

Rumpff, H. (1992). Distribution, population structure and ecological behaviour of the introduced south-east Asian wolf snake (Lycodon aulicus capucinus) on Christmas Island, Indian Ocean. Report to Australian National Parks and Wildlife Service, Canberra.

Schulz, M. and Barker, C. (2008). A terrestrial reptile survey of Christmas Island, May-June 2008. Consultancy report for Parks Australia North, Christmas Island.

Emoia nativitatis (Christmas Island Forest Skink) Listing Advice Page 9 of 10 Sleeth, M. (2017) Home range ecology and microhabitat use of the invasive wolf snake (Lycodon capucinus) of Christmas Island. Honours thesis, Deakin University.

Smith, M.J., Cogger, H., Tiernan, B., Maple, D., Boland, C., Napier, F., Detto, T. and Smith, P. (2012). An oceanic island reptile community under threat: The decline of reptiles on Christmas Island, Indian Ocean. Herpetological Conservation and Biology 7(2), 206–218.

Threatened Species Scientific Committee (TSSC). (2014). Conservation Advice for the Christmas Island Forest Skink Emoia nativitatis.

Tidemann, C.R. (1989). Survey of the terrestrial mammals on Christmas Island (Indian Ocean). Forestry Department, Australian National University.

Emoia nativitatis (Christmas Island Forest Skink) Listing Advice Page 10 of 10