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Estimating Population Parameters for the Critically Endangered Bermuda Skink Using Robust Design Capture–Mark–Recapture Modelling

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Estimating Population Parameters for the Critically Endangered Bermuda Skink Using Robust Design Capture–Mark–Recapture Modelling Estimating population parameters for the Critically Endangered Bermuda skink using robust design capture–mark–recapture modelling H ELENA T URNER,RICHARD A. GRIFFITHS M ARK E. OUTERBRIDGE and G ERARDO G ARCIA Abstract Reliably estimating population parameters for survival (Krebs, ; Besbeas et al., ), which are critical highly secretive or rare animals is challenging. We report determinants of population viability (White & Burnham, on the status of the two largest remaining populations of ). Conventionally, marking is used to uniquely identify the Critically Endangered Bermuda skink Plestiodon lon- individuals in successive samples. For lizards, photographic girostris, using a robust design capture–mark–recapture identification using natural markings (Sacchi et al., ), analysis. Skinks were tagged with passive integrated trans- tagging with passive integrated transponders (Germano & ponders on two islands and captured on sampling occa- Williams, ) and individual recognition from DNA sam- sions per year over years. The models provided precise pling (Moore et al., ) have increased the utility and estimates of abundance, capture and survival probabilities application of the capture–mark–recapture approach. and temporary emigration. We estimated skink abundance The Bermuda skink Plestiodon longirostris is the coun- to be ± SE . on Southampton Island and ± SE . try’s only extant endemic reptile (Bacon et al., ). The on Castle Island. The populations do not appear to be stable species primarily feeds on terrestrial and leaf litter arthro- and fluctuated at both sites over the -year period. Although pods such as ants and woodlice (Wingate, ) but also the populations on these two islands appear viable, the on a variety of other food sources such as prickly pear cactus Bermuda skink faces population fluctuations and remains Opuntia sp. and fruits (Wingate, ; Davenport et al., , threatened by increasing anthropogenic activities, invasive ; Edgar et al., ). Unlike many other reptiles, the species and habitat loss. We recommend these two popula- skinks are scavengers with a keen sense of smell that attracts tions for continued monitoring and conservation efforts. them to carrion (Garber, ; Davenport et al., ), and will make use of seasonally abundant food sources such as Keywords Bermuda skink, capture–mark–recapture ana- broken eggs, dead chicks and dropped fish from nesting col- lysis, conservation, Plestiodon longirostris, population moni- onies of the native white-tailed tropicbird Phaethon lepturus toring, reptile, robust design, survival catesbyi and the endemic Bermuda petrel Pterodroma cahow Supplementary material for this article is available at (Garber, ; Edgar et al., ). https://doi.org/./S The skinks were once common throughout the islands of Bermuda but populations have undergone significant de- clines since the s when they were reportedly rarely seen on the mainland because of increased anthropogenic Introduction disturbance, habitat loss and degradation, and the intro- any threatened species are cryptic, elusive and chal- duction of invasive flora and fauna (Davenport et al., ; Mlenging to survey. The development of efficient Glasspool & Outerbridge, ). The species is now re- survey methods to detect them is vitally important for stricted to the edges of rocky coastal habitat and is cate- conservation management. A wide variety of methods gorized as Critically Endangered on the IUCN Red List , have been used in monitoring studies, including capture– (Conyers & Wingate, ), with , individuals mark–recapture techniques to estimate abundance and thought to be left on Bermuda (Edgar et al., ; Turner, ). Recent surveys have confirmed skinks at only sites within nature reserves and offshore islands (Turner, HELENA TURNER (Corresponding author, orcid.org/0000-0002-6067-888X) ), and the continued threats are likely to have a and RICHARD A. GRIFFITHS ( orcid.org/0000-0002-5533-1013) Durrell Institute of Conservation and Ecology, School of Anthropology and major impact on the remaining fragmented and isolated Conservation, University of Kent, Canterbury, UK populations. E-mail [email protected] We used a robust design model to monitor trends in MARK E. OUTERBRIDGE Government of Bermuda, Department of Environment abundance, survival, capture probabilities and temporary ’ and Natural Resources, Flatt s Village, Bermuda emigration of the two largest skink populations on GERARDO GARCIA ( orcid.org/0000-0002-3007-8998) Chester Zoo, Cedar Bermuda. The robust design model of Pollock ()isan House, Chester, UK extension of the Cormack–Jolly–Seber model and has Received July . Revision requested September . Accepted December . First published online September . become increasingly popular as it combines the advantages This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, Downloadeddistribution, from https://www.cambridge.org/core and reproduction in any medium,. IP address: provided 170.106.33.14 the original work, onis 27 properly Sep 2021 cited. at 21:08:44, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/termsOryx, 2021, 55(1), 81–88 © 2019. https://doi.org/10.1017/S0030605318001485 Fauna & Flora International doi:10.1017/S0030605318001485 82 H. Turner et al. of the live-recapture model and the closed-capture models. (M. Outerbridge, , pers. comm.) and because reaching The model and its assumptions are described in detail by the islands in adverse weather was challenging. On both is- Cormack (), Otis et al. (), Seber (, ) and lands we collected data over a -day period per month during Kendall et al. (). The current management plan for May–July of , and , resulting in a total of sam- the Bermuda skink calls for monitoring every – years pling occasions per island and year. Each sampling occasion (Edgar et al., ) but the last capture–mark–recapture sur- consisted of five trap checks per day, with a total trapping veys were undertaken in , on Southampton Island, and time of hours per year per island (Supplementary Table ). the current status of the population was unknown. More fre- We weighed all captured individuals and measured their quent estimates of population parameters will be necessary snout–vent length, tagged unmarked animals and recorded to inform conservation management and future monitoring tags of recaptured ones. All individuals in good health programmes. (excluding gravid females, and juveniles with a snout–vent length , mm or body mass , . g) were tagged with passive integrated transponders ( × . mm, mg, model Study area IDB FDX-B; Trovan, Douglas, Isle of Man) operating at a frequency of . kHz. Tags were inserted subcutaneously This study was undertaken at two sites in Castle Harbour, in either the left or right side of the body with a syringe Bermuda: the . ha Southampton Island and . ha implanter and .-inch -gauge sterile disposable hypo- Castle Island (Fig. ). We chose these two sites because dermic needle. Prior to tagging, the injection site was they are thought to harbour the largest known Bermuda wiped with antiseptic. Immediately after injection, a drop skink populations, are both within protected nature reserves of cyanoacrylate glue was applied over the injection site and are considered the most suitable areas for targeted con- to prevent tag loss and aid wound healing (Germano & servation efforts. The islands are separated by a m wide Williams, ; Gibbons & Andrews, ). Once implanted, water channel and their abiotic factors are similar. Castle the tags were checked using a tag reader that revealed the Island is closer to the main island ( m) and faces more individual’s unique identification code. Even though tagging threats from invasive species and anthropogenic activities, may induce temporary stress (Langkilde & Shine, ), if which have been the main reasons for the skink’s decline inserted properly the tags do not otherwise affect the animals at this location. We surveyed additional sites across Bermuda (Gibbons & Andrews, ; Connette & Semlitsch, ). but sample sizes were too small (, individuals) to provide Once processed, we immediately released individuals at the reliable estimates of abundance. capture site. Methods Statistical analyses Skink capture and marking We compiled capture histories as time series of binary va- lues, with captures coded as and non-captures as , using We adapted methods from Davenport et al. () and used a standard x-matrix format (Otis et al., ; Nichols, ). a consistent survey protocol across the two locations. We Rows represented capture histories of each captured individ- used glass jars (c. × mm, volume . l) as traps, ual and columns represented capture occasions. set up in × m grid networks (skink home ranges are We based the capture–mark–recapture modelling on a ro- c. m ; Davenport et al., ). Traps were mounted at a bust design model (Nichols, ), which assumes population –° angle, with rocks or vegetation placed at the opening closure between secondary sampling occasions or days (i.e. no so skinks could gain access. We used flagging tape to label births, deaths, emigration or immigration during each -day each trap, recorded locations with a handheld GPS and sampling period), but assumes a population open to demo- used dried palmetto Sabal bermudana fronds and small graphic changes between primary sampling occasions or towels to shade the traps. The pitfall traps were baited
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