Sand lizard Lacerta agilis reintroductions in southern England

Int. Zoo Yb. (2017) 51: 1–10DOI:10.1111/izy.12155

Outcomes and lessons from a quarter of a centuryof Sand lizard Lacerta agilis reintroductions insouthern England

T. WOODFINE1,2, M. WILKIE1, R. GARDNER1,2, P. EDGAR3, N. MOULTON4 &P. RIORDAN1

1Marwell Wildlife, Colden Common, Winchester SO21 1JH, United Kingdom,2BiologicalSciences, Faculty of Natural and Environmental Sciences, University of Southampton, LifeSciences Building 85, Highfield Campus, Southampton SO17 1BJ, United Kingdom,3NaturalEngland, 2nd Floor, Cromwell House, 15 Andover Road, Winchester, Hampshire SO237BT, United Kingdom, and 4Amphibian & Reptile Conservation Trust, 665A ChristchurchRoad, Boscombe, Bournemouth, Dorset BH1 4AP, United KingdomE-mail: [email protected]

Despite occurring widely across Europe and Asia, theSand lizard Lacerta agilis is threatened in the north-western part of its range and had disappeared frommuch of its former habitat in England and Wales priorto concerted conservation action. A breeding popula-tion established at Marwell Zoo, UK, contributed tothe re-establishment of 26 populations of Sand lizardsat heathland and coastal dune sites across southernEngland as part of a wider multi-stakeholder responseto reverse the decline of the species. Knowledge aboutthe biology of Sand lizards was accrued during theprocess, which helped to refine the management of thebreeding population that was maintained in a naturalis-tic setting within the indigenous range of the species.These successes were underpinned by coordinated col-laborative actions and long-term institutional commit-ments against a backdrop of considerable change inthe statutory framework governing Sand lizard conser-vation. The management of this project was not with-out cost or risk, including protection of valuablefounder stock, incomplete knowledge about the healthand disease status of Sand lizards, intrinsic constraintsof limited founder representation, and the challenges ofmonitoring this elusive species post release.

Key-words: adaptation; breeding; heathland;reintroduction; sand lizard; species conservation.

INTRODUCTION

Species reintroductions are a significantconservation tool for many taxa (Fischer &Lindenmayer, 2000; Soorae, 2016), thoughsuch initiatives are often technically and

logistically challenging. Understanding theoutcomes and experiences of concertedreintroduction efforts is essential for practi-tioners to plan or refine methodologies(Sutherland et al., 2004; Seddon et al.,2007). Here, we report on a quarter of acentury of captive breeding and reintroduc-tion of Sand lizards Lacerta agilis in thesouth of England, sharing knowledge aboutthe biology of the species accrued duringthis period, and summarizing the challengesand effectiveness of this long-term initia-tive. The project carried out at MarwellZoo in Hampshire, UK, contributed to there-establishment of Sand lizards at 26 loca-tions, and is an example of reintroductionfrom a small captive founder populationmaintained in naturalistic conditions withinthe indigenous range of the species. Thiswas one of a number of parallel and coordi-nated projects that contributed to successivenational action plans to stabilize andreverse the decline of the Sand lizard in theUK.

SAND LIZARDS IN THE UK

There are ten recognized subspecies ofSand lizard found throughout Europe and

Int. Zoo Yb. (2017) 51: 1–10 © 2017 The Zoological Society of London

SAND LIZARD REINTRODUCTIONS IN SOUTHERN ENGLAND 1

across Asia. While the species is patchilydistributed in places, its range stretchesfrom the United Kingdom in the west,through Europe and Central Asia to north-western Mongolia in the east (Agasyanet al., 2010). The nominotypical subspeciesLacerta agilis agilis occurs in central andwestern Europe including the now frag-mented populations in England and Wales(Cox & Temple, 2009; Andres et al.,2014). The wide distribution of the speciesmeans that it is categorized globally asLeast Concern in The IUCN Red List ofThreatened Species (Agasyan et al., 2010),but has declined sharply in north-west Eur-ope and is therefore considered endangeredin this part of its range (Edgar & Bird,2006). Hence, the Sand lizard is includedin Appendix II of the Berne Convention onthe Conservation of European Wildlife andNatural Habitats, in Annex IV of the EUHabitats Directive (92/43/EEC: CouncilDirective, 1992), and is a protected speciesin most of the countries where it is found(Edgar & Bird, 2006).

In the UK, Sand lizards occur on dryheathland and coastal dune systems withsufficient vegetation structure for foragingand shelter, and areas of open sand for egglaying (House & Spellerberg, 1983; Corbett& Moulton, 1998; Blanke & Fearnley,2015; Spellerberg & House, unpubl.). Thespecies suffered catastrophic declines fol-lowing habitat loss, degradation and frag-mentation as a result of housing andindustrial developments, conversion ofheathland to conifer plantations, scrubencroachment, livestock and human distur-bance, and fires (mainly caused by arson)(Corbett & Tamarind, 1979; House &Spellerberg, 1983; Edgar, 2002; Moultonet al., 2011). By the late 1980s and early1990s, this had resulted in the disappear-ance of Sand lizards from north and westWales and nine English counties. Wherethe species remained extant, populations arethought to have reduced by over 90% bywhich time the majority of the UK’s Sandlizards were confined to the fragmentedDorset heathlands (Corbett & Moulton,

1998). The Sand lizard became the subjectof a national Species Recovery Programmebetween 1994 and 1997 (Corbett & Moul-ton, 1998), and a subsequent SpeciesAction Plan led jointly by the statutory nat-ure conservation agencies in England andWales, and the Amphibian and ReptileConservation (ARC) Trust (formerly theHerpetological Conservation Trust), Bour-nemouth, UK, with contributions fromother non-governmental partners.

MANAGEMENT OF SAND LIZARDS

Breeding and reintroduction of Sand lizardswas one of several interventions that soughtto stabilize and enhance the status of thespecies in England and Wales (Edgar &Bird, 2006; ARC, 2016). Initiated and sup-ported by the British Herpetological SocietyConservation Committee (BHSCC), abreeding facility was established at MarwellZoo in 1989 (Edgar, 1990); one of a num-ber of vivaria set up for this purpose as partof a wider Sand lizard breeding programmepioneered by BHSCC and ARC Trust. Theinitial aim of the Marwell facility was tore-establish Sand lizards in the nearby NewForest, but the initiative was continued toproduce reintroduction stock for heathlandand coastal dune sites throughout the southof England.A 12 m 9 5 m Sand lizard vivarium

was created using heathland soil and plantsrescued from Canford Heath in Dorset, UK,prior to the construction of a housing estate.The sheltered, south-facing aspect, variedtopography, vegetation cover (predomi-nantly Heather Calluna vulgaris) and areasof open sand were designed to replicate dryheathland features favoured by Sand lizards(Plate 1). This habitat was created over afoundation layer of bricks and other build-ing rubble to help drainage and provideplentiful hibernation cavities. It was thencontained within boundaries of transparentacrylic sheets extending 0�4 m above and0�3 m below ground, and held in place bya timber frame. An overhang was createdalong the top of the vivarium walls to


2 REINTRODUCTIONS AND OTHER CONSERVATION TRANSLOCATIONS

prevent lizards climbing out while deterringencroachment by rodents that might enterthe area. However, the entire vivarium andimmediate surroundings were enclosedwithin a wider structure of small-gauge wir-emesh and nylon netting for protectionagainst rodent and avian predators whileallowing invertebrates, the natural prey ofSand lizards, to enter freely and colonizethe habitat.

The vivarium was populated with Sandlizards rescued from heathland sites in Dor-set either prior to the habitat being lost todevelopment or following catastrophic fires,some of which were started accidentally ornaturally occurring, but mainly caused byarson. A simple husbandry routine was fol-lowed. From March to September, the Sandlizards were fed during the middle of theday with gut-loaded Black field cricketsGryllus bimaculatus occasionally dustedwith a vitamin and mineral powder (mostrecently Nutrobal for Reptiles) to supple-ment the natural diet. During periods of lit-tle or no rainfall, vegetation was sprayedwith a fine mist of collected rainwater repli-cating natural precipitation and providingopportunities for the Sand lizards to drink.The visibility of Sand lizards while

drinking made it possible to count the ani-mals regularly and undertake observationsof body condition.The borders of the vivarium were kept

clear of vegetation from March to June toensure areas of open sand remained avail-able for egg laying and the reproductivestatus of female Sand lizards was closelymonitored from mid-May to mid-July.Depending on conditions at the time, egglaying occurred from late May, peaking inJune and sometimes extending into July.Eggs were removed from the vivarium withclutches incubated in tubs of vermiculite.Emerging hatchlings were then transferredto outdoor, vegetated rearing tanks wherethey received a daily diet of micro-crickets(Black field crickets) and were providedwith water as per the adults. Following aperiod of a month to 6 weeks and precau-tionary health screening, juvenile lizardswere collected and transported for release atdesignated sites.The breeding population of Sand lizards

hibernated naturally in the vivarium duringthe winter months. During this time exces-sive vegetation was removed from thevivarium and any maintenance and repairsto the enclosure were undertaken.

Plate 1. Male Sand lizard Lacerta agilis in the breeding enclosure at Marwell Zoo, UK. Rachel Gardner, Mar-well Wildlife.



BREEDING AND BIOLOGY

In total, 61 Sand lizards were transferred tothe breeding vivarium at various intervalsduring the 25 year duration of the project.This founder representation began with agroup of seven adults [2.5 (♂.♀)] in 1989,although there was in inauspicious start tothe project because of encroachment by ratsRattus norvegicus and only two hatchlingssurvived for release. Following some modi-fications to improve protection of the vivar-ium, an additional nine adult Sand lizards(3.6) were introduced in 1990 and therewere immediate improvements in hatchlingsurvival with 43 juveniles released thatyear. In 1991, a further 14 adult femaleSand lizards were added to the breedingpopulation, resulting in the release of 180juvenile lizards at the end of the summer.Unfortunately, residual weaknesses in theoriginal structure of the vivarium wereagain exploited by rats in 1992 and most ofthe gravid female Sand lizards were lost topredation. Far more robust reinforcementand protection of the vivarium was under-taken in response and, with the exceptionof five surviving male Sand lizards, a newfounder population was effectively createdin 1994 with a group of 22 animals (2.20).Further lizards, rescued from degradedheathland sites, arrived in 1996 (2.0), 2000(3.3) and 2001 (1.0). Apart from isolatedcases of rodents entering the area throughbreaks in the enclosure netting, the protec-tion of the vivarium proved adequate forthe next two decades and no further lossesto predation were recorded.

Around 20 Sand lizards were typicallyhoused in the vivarium each year(max = 30) with a mean of 2�5 females permale (max = 6, min = 0�7). This resultedin a mean density of 0�32 Sand lizards perm2 (max = 0�5 m�2, min = 0�13 m�2).With a mean 0�8 (� 0�3) clutches perfemale, there were some years in which notall females reproduced, but in favourableconditions double clutches were possible. Amean 7�4 eggs were laid per female(max = 17�8, min = 1�8). Eighty-seven per

cent (� 13�1) of eggs hatched and 89%(� 9�2) of hatchlings survived until releaseage (4–6 weeks). These intuitively high fig-ures are likely reflections of protection andhusbandry interventions, albeit data on wildSand lizards for comparison are lacking.Mean weight of newly hatched Sand

lizards was 0�67 g (� 0�13, n = 50) with amean snout to vent length of 28�58 mm(� 1�85, n = 50). Young lizards increasedtheir weight by up to 30% during the firstmonth, with those maintained at low density(5 m�2) growing at faster rates than theircounterparts kept at double this densityregardless of food supply not being a limit-ing factor (Isaacs, 2009; Kain, 2010).Aggression between juvenile Sand lizardswas significantly lower when kept at lowdensity (Isaacs, 2009; Kain, 2010), with thecost of additional energy expended by ani-mals maintained at high density the likelycause of observed differences in growth rate.Wide variations in the weights and snout

to vent lengths measured in adult male andfemale Sand lizards reflected continuousgrowth with age. Contrary to expectation,weights of female Sand lizards (mean =15�7 g � 3�7, n = 38) were often greaterthan of males (mean = 12�27 � 3�25 g,n = 25). This may have been an artefact ofage, reproductive status, the provision ofabundant supplementary food designed tokeep female Sand lizards in optimal bodycondition during the breeding season, andthe competitive energy expenditure ofmales kept at high density. However, therewas little difference in snout to vent lengthof adult male (72�42 � 23�61 mm, n = 25)versus adult female Sand lizards (73�24 �6�00 mm, n = 38).As reported by Fearnley (2009), sightings

of Sand lizards in this closed environmentwere influenced by sex, reproductive stageand weather. The probability of detectingmales was greater before mating whenobservations were strongly associated withweather and time of day, compared withlater in the season when they were mostoften seen at solar radiation values of



between 300 and 700 W m�2. The proba-bility of detecting females was greater aftermating when surface ground temperaturewas between 17�5 and 27�5°C, comparedwith earlier in the season when they wereoften seen basking within an optimum levelof ultraviolet light (UV index between 2�00and 5�00). Further variations in detection offemale Sand lizards occurred during andafter egg laying.

Sand lizards arriving at Marwell weresubject to health screening and a period ofquarantine before joining the breeding pop-ulation. Similarly, health-screening proto-cols were adopted to mitigate risk ofpathogenic disease transmission to wildSand lizard and other reptile populationsduring releases (Lloyd & Sainsbury, 2003;Molenaar et al., 2008). Because of the diffi-culties of practically, safely and humanelytesting small and fragile juvenile Sandlizards, oral and cloacal swabs, and faecalsamples were taken from adult Sand lizardsto assess the health status of the populationas a whole. Aerobic and anaerobic culturesisolated Escherichia coli, Klebsiella oxy-toca, Pasteurella multocida, Serratia mar-cescens, Staphylococcus sp andStreptococcus sp in some years, but perhapssurprisingly there were no positive tests foreither Salmonella or Campylobacter. Partic-ular caution was exercised following a posi-tive test for Serratia marcescens as theonly common finding in the post-mortemtesting of four juvenile Sand lizards thatdied in quick succession in 2005 (Molenaar& Sainsbury, 2009). However, this speciesof bacteria proved to be present in wildSand lizard populations in Dorset and,therefore, was not considered a significantrisk (Sainsbury, 2012).

OUTCOMES OF REINTRODUCTIONS

During 25 years of captive breeding in anaturalistic environment, the project con-tributed 1892 Sand lizards for release at 21reintroduction sites across the south of Eng-land (Fig. 1). Animals were released inmore than one location within five of the

reintroduction sites and so contributed tothe attempted re-establishment of 27 dis-creet populations (Plate 2). This included758 juvenile Sand lizards released betweenfive locations in the New Forest between1990 and 1994 representing 91% of thereintroduction stock for that area and com-pleting the original aim of the project.Overall, the majority of Sand lizard releaselocations were heathland habitats in thecounties of Dorset (10), Hampshire (10,including those in the New Forest), Surrey(2) and West Sussex (1), with the remain-der coastal dune systems in Devon (1),Dorset (1), West Sussex (2) and Kent (1).With juvenile Sand lizards from Marwelljoining other captive-bred stock, a mean144 (� 64) Sand lizards were released perlocation (max = 306, min = 13).Surveys carried out by ARC Trust con-

firmed the continued presence of Sandlizards at 21 of the release locations during2016, at two locations in 2015 and at threeother locations in 2014. Hence, all but oneof the 27 reintroduction initiatives havebeen assessed within the last 3 years withapparently successful outcomes. Theremaining release location was last evalu-ated in 2000 and thought to have failedbecause of fire (suspected arson).Based on the period elapsed between the

year of last release at a given location andthe most recent survey confirming theirpresence, seven Sand lizard populations hadbecome re-established for over 20 years;the longest dating back to the beginning ofthe project with animals being detected26 years after founders were reintroduced.Nine Sand lizard populations had becomeestablished for between one and two dec-ades while a further ten Sand lizard popula-tions were at earlier stages of re-establishment of between 2 and 9 years.

DISCUSSION

Given the precarious status of the Sandlizard in southern England by the late1980s and early 1990s, captive breedingand reintroduction were seen as a necessity



(Corbett & Moulton, 1998). Common tothese sorts of interventions, the successesreported here have not come without riskand cost (IUCN/SSC, 2013). In this case,loss of valuable founder animals to rat pre-dation was a major setback during the earlystages of the project and physically protect-ing the population was a considerableundertaking. Similarly, biosecurity measuresand health screening of animals arriving forbreeding and of those departing for release

(Lloyd & Sainsbury, 2003; Molenaar et al.,2008) required substantial effort whilejudgements on these matters were hamperedby lack of information on the infectious-disease status of wild Sand lizards untilvery recently (Molenaar & Sainsbury,2010; Sainsbury, 2012) and even then, thisknowledge is limited.However, there were theoretical benefits

accruing from this approach to captivebreeding of Sand lizards. Use of transplanted

Fig. 1. Sand lizard Lacerta agilis reintroduction sites across the south of England (circles) and the location ofMarwell Zoo (black dot) in Hampshire, UK. Contains OS data © Crown Copyright and database right (2016).

Plate 2. Sand lizard Lacerta agilis release site on the dry heathland of Woolmer Forest in Hampshire, UK.Tim Woodfine, Marwell Wildlife.



habitat within the indigenous and climaticrange of the species, and allowing naturalprocesses, such as hibernation, foraging forprey and typical social interactions, weredesigned to minimize mismatch with theevolved biology of the species and retainadaptive traits that may otherwise be lostover time (Frankham, 2008; Bijlsma &Loeschcke, 2012; Schulte-Hostedde & Mas-tromonaco, 2015). Similarly, juvenile Sandlizards spent a relatively short period of timein captivity, being released within severalweeks of hatching and thereafter beingexposed to natural selection at the recipientsite. Protection of the breeding populationfrom predation and disturbance, plus the arti-ficial incubation of eggs and supplementaryfeeding, were designed to enhance produc-tivity, hatch rates and survival of juveniles topoint of release. This helped to produce thenumbers of Sand lizards needed for releasebut with unknown consequences of relaxingthe selection pressures (Lahti et al., 2009;Christie et al., 2012) on young Sand lizardsduring this critical phase of their develop-ment and on subsequent generations.

The Sand lizard reintroduction strategyfollowed an original recommendation torelease cohorts of 50 juveniles (Moulton &Corbett, 1999), and more recently 80 juve-niles (Berglind et al., 2015), per year dur-ing three consecutive years, taking placeany time between mid-April and earlySeptember (Plate 3). Evaluating the out-comes of releases is reliant on evidence(sightings of live animals or recently shedskin) that the species persists post release.However, population estimates and, there-fore, trends in the status of the species at agiven location have not been establishedbecause of the cost and logistical challengesof detecting these often elusive animals.Even with improved understanding ofdetection probability (Fearnley, 2009), coin-ciding site visits with conditions favourablefor seeing Sand lizards on sufficient occa-sions remains difficult. With this in minduse of indices of Sand lizard abundance,such as egg-burrow counts per unit areaover time, are now being assessed, while

advances in cost-effective micro-scale track-ing technology could improve understand-ing of post-release dispersal and habitatselection (Brady & Phillips, 2012), andthereby help to focus monitoring efforts.Despite the challenges of monitoring rein-

troduced populations, recent records of Sandlizard sightings at 26 out of 27 locations pro-vide some indication of successful outcomes.However, intrinsic pressures on small popu-lations, such as founder effect, inbreedingand genetic drift (Olsson et al., 1996; Frank-ham et al., 2010), continue to jeopardize thelong-term viability of reintroduced Sandlizards. While we lack much of the biologi-cal and environmental data needed to predictthe probability of persistence, moleculartechniques (Russell, 2012a,b) can provideinsights into genetic variation found withinisolated populations. Unless numbers ofSand lizards at a given site have becomelarge enough to achieve a long-term viablepopulation and evolutionary adaptation(Franklin, 1980; Frankham et al., 2014),genetic augmentation and metapopulationmanagement will become an important com-ponent of the next phase of conservationintervention for this species in southern Eng-land. Indeed, questions about how distribu-tion and phenotypic traits of Sand lizardsmay be positively or negatively affected by awarming climate (Urban et al., 2014;Ljungstr€om et al., 2015) place furtheremphasis on plasticity and genetic adapta-tion of isolated populations.The inability of Sand lizards to naturally

recolonize suitable habitats or movebetween fragmented patches means thattheir dispersal will continue to depend onhuman-mediated connectivity for the fore-seeable future. Captive breeding may con-tinue to have a role in supplying the largenumbers of Sand lizards needed to re-estab-lish the species (Berglind et al., 2015)where they became extinct, but with theinherent genetic limitations of small captivefounder populations and potential distrac-tion from allocating resources to achievingfavourable conservation status for existingwild populations. In contrast, wild to wild



translocation offers a lower-cost option forgenetic augmentation and metapopulationmanagement with access to the full spec-trum of available genetic variation. How-ever, these operations may be impracticaland there are questions about the robustnessof potential donor populations to highlevels of offtake. In either case, risks of dis-ease transmission need to be mitigated.Regardless, ongoing restoration and man-agement of heathland and coastal dune sitesremains essential because viability of Sandlizard populations will ultimately depend onthe size and quality of habitat.

Even for small-bodied species with shortgeneration lengths, the period of timeneeded to re-establish a reintroduced popu-lation can be considerable and difficult todetermine from the outset. A long-termstrategy with accompanying financial andinstitutional commitments is thereforeneeded. This has fortunately been the casefor the Sand lizard in the south of Englandduring the last quarter of a century, albeitagainst a backdrop of considerable statutorychange and cessation of governmental fund-ing contributions in more recent years.

The last two decades of this reintroductionprogramme have seen substantial changes in

the structure and function of the UK’s statu-tory agencies responsible for wildlife conser-vation resulting from policies of successivegovernments and requirements of devolution.During this period, the original Sand lizardSpecies Recovery Programme informed andwas superseded by the UK BiodiversityAction Plan (UK BAP), with specific inter-ventions for the Sand lizard eventually com-bined with those for the Smooth snakeCoronella austriaca in a rare reptile SpeciesAction Plan (ARC, 2009). Since then UKBAP has in turn been replaced by the UKPost-2010 Biodiversity Framework (JNCC &Defra, 2012). In England, this is now deliv-ered through a landscape-scale strategy forwildlife conservation and ecosystem services(Defra, 2011) allied to the Convention onBiological Diversity Strategic Plan for Biodi-versity 2011–2020 and the achievement of theAichi Targets (CBD, 2010). The Sand lizardis listed alongside other priority species inSection 41 of the Natural Environment andRural Communities Act, 2006, and linkedwith Lowland Heathland and Coastal SandDune priority habitats. There will be inevita-ble uncertainty about approaches to Sandlizard conservation in the coming yearsbecause of the UK’s exit from the European

Plate 3. Juvenile Sand lizards Lacerta agilis in Woolmer Forest, Hampshire, UK, following release. TimWoodfine, Marwell Wildlife.



Union; how this will affect status of EuropeanProtected Species in this country, and how therole and resourcing of Natural England andother statutory agencies will be shaped areunpredictable.

The Sand lizard vivarium at Marwell Zoohas in the meantime provided an opportunityto enhance understanding of the reproductivebiology, morphology, behaviour and healthof this species in a naturalistic setting, assummarized here. As part of parallel andcoordinated long-term efforts, the projectmade a significant contribution to the re-establishment of Sand lizard populationsacross the south of England.

ACKNOWLEDGEMENTSOur thanks to all our colleagues at the Amphibian andReptile Conservation Trust, The British HerpetologicalSociety, Natural England and Marwell Wildlife forsupporting this project throughout the years, and toTania Gilbert, Will Justice, Heidi Mitchell and twoanonymous reviewers for their helpful comments onthe manuscript.

PRODUCT MENTIONED IN THE TEXTNutrobal for reptiles: vitamin/mineral supplementspecifically formulated for insectivorous reptiles andbirds, manufactured by VETARK Professional, POBox 60, Winchester SO23 9XN, UK.

REFERENCESAGASYAN, A., AVCI, A., TUNIYEV, B., LYMBERAKIS, P.,ANDR�EN, C., COGALNICEANU, D., WILKINSON, J., ANAN-

JEVA, N., €UZ€UM, N., ORLOV, N., PODLOUCKY, R.,TUNIYEV, S., KAYA, U., CRNOBRNJA ISAILOVIC, J.,VOGRIN, M., CORTI, C., P�EREZ MELLADO, V., S�A-SOUSA,P., CHEYLAN, M., PLEGUEZUELOS, J., KYEK, M., WESTER-

STR€OM, A., NETTMANN, H. K., BORCZYK, B., STERIJOVSKI,B. & SCHMIDT, B. (2010): Lacerta agilis. In The IUCNRed List of Threatened Species. Gland, Switzerland,and Cambridge, UK: International Union for Conserva-tion of Nature. Available at https://doi.org/10.2305/IUCN.UK.2010-4.RLTS.T157288A5071439.en (ac-cessed 16 May 2016).ANDRES, C., FRANKE, F., BLEIDORN, C., BERNHARD, D. &SCHLEGEL, M. (2014): Phylogenetic analysis of the Lac-erta agilis subspecies complex. Systematics and Biodi-versity 12: 1–12.ARC (2009): Rare reptile (sand lizard and smoothsnake) (revised) species action plan. Bournemouth:Amphibian and Reptile Conservation Trust.ARC (2016): Sand lizard species recovery programmepartnership: captive breeding and translocation planfor England, 2016. ARC research report. Bourne-mouth: Amphibian and Reptile Conservation Trust.

BERGLIND, S.-A., GULLBERG, A. & OLSSON, M. (2015):Atgardsprogram for sandodla, 2014–2017. Stockholm:Naturvardsverket.BIJLSMA, R. & LOESCHCKE, V. (2012): Genetic erosionimpedes adaptive responses to stressful environments.Evolutionary Applications 5: 117–129.BLANKE, I. & FEARNLEY, H. (2015): The sand lizard:between light and shadow. Bielefeld: Laurenti-Verlag.BRADY, L. D. & PHILLIPS, M. (2012): Developing a‘habitat suitability index’ for reptiles. ARC researchreport 112/06. Bournemouth: Amphibian and ReptileConservation Trust.CBD (2010): Strategic plan for biodiversity 2011–2020 and the Aichi targets: “living in harmony withnature”. Montreal, QC: Secretariat of the Conventionon Biological Diversity.CHRISTIE, M., MARINE, M., FRENCH, R. & BLOUIN, M.(2012): Genetic adaptation to captivity can occur in asingle generation. Proceedings of the National Acad-emy of Sciences of the United States of America 109:238–242.CORBETT, K. & MOULTON, N. (1998): Sand lizard spe-cies recovery programme (1994–1997). Peterborough:English Nature.CORBETT, K. & TAMARIND, D. (1979): Conservation ofthe sand lizard, Lacerta agilis, by habitat management.British Journal of Herpetology 5: 799–823.COUNCIL DIRECTIVE (1992): Council Directive 92/43/EEC of 21 May 1992 on the conservation of naturalhabitats and of wild fauna and flora. Official Journalof the European Communities 22 July 1992: L206/7–L206/50. Available at http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:31992L0043&from=ENCOX, N. A. & TEMPLE, H. J. (2009): European Red Listof reptiles. Luxembourg: Office for Official Publicationof the European Communities.DEFRA (2011): Biodiversity 2020: a strategy for Eng-land’s wildlife and ecosystem services. London:Department of Environment, Food & Rural Affairs.EDGAR, P. (1990): A captive breeding and release pro-gramme for sand lizards and natterjack toads at Mar-well Zoological Park: an appeal for sponsorship.British Herpetological Society Bulletin 31: 3–10.EDGAR, P. (2002): The effects of public access onamphibians and reptiles. An assessment of the poten-tial effects of increased public access due to the intro-duction of the countryside rights of way act 2000.Bangor: The Countryside Council for Wales, The Her-petological Conservation Trust.EDGAR, P. & BIRD, D. (2006): Action plan for the con-servation of the sand lizard (Lacerta agilis) in north-west Europe. In Convention on the conservation ofEuropean wildlife and natural habitats. Standing com-mittee 26th meeting, Strasbourg, 27–30 November2006. Report T-PVS/Inf (2006) 18. Strasbourg: Coun-cil of Europe. Available at https://wcd.coe.int/com.instranet.InstraServlet?command=com.instranet.CmdBlobGet&InstranetImage=1304260&SecMode=1&DocId=1437092&Usage=2



https://doi.org/10.2305/IUCN.UK.2010-4.RLTS.T157288A5071439.en

https://doi.org/10.2305/IUCN.UK.2010-4.RLTS.T157288A5071439.en

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FEARNLEY, H. (2009): Towards the ecology and conser-vation of sand lizard (Lacerta agilis) populations insouthern England. PhD thesis, University ofSouthampton, UK.FISCHER, J. & LINDENMAYER, D. B. (2000): An assess-ment of the published results of animals relocations.Biological Conservation 96: 1–11.FRANKHAM, R. (2008): Genetic adaptation to captivityin species conservation programs. Molecular Ecology17: 325–333.FRANKHAM, R., BALLOU, J. & BRISCOE, D. (2010): Intro-duction to conservation genetics (2nd edn). Cam-bridge: Cambridge University Press.FRANKHAM, R., BRADSHAW, C. J. A. & BROOK, B. W.(2014): Genetics in conservation management: revisedrecommendations for the 50/500 rules, Red List criteriaand population viability analyses. Biological Conserva-tion 170: 56–63.FRANKLIN, I. R. (1980): Evolutionary change in smallpopulations. In Conservation biology: an evolutionaryecological perspective: 135–149. Soul�e, M. E. & Wil-cox, B. A. (Eds). Sunderland, MA: Sinauer.HOUSE, S. M. & SPELLERBERG, I. F. (1983): Ecologyand conservation of the sand lizard (Lacerta agilis L.)habitat in southern England. Journal of Applied Ecol-ogy 20: 417–437.ISAACS, S. (2009): The effects of feeding regime on thegrowth and development of captive-bred juvenile sandlizards (Lacerta agilis). MSc thesis, University ofSouthampton, UK.IUCN/SSC (2013): Guidelines for reintroductions andother conservation translocations: version 1.0. Gland,Switzerland: International Union for Conservation ofNature Species Survival Commission.JNCC & DEFRA (2012): UK post-2010 biodiversityframework. July 2012. Peterborough: Joint NatureConservation Committee. Available at http://jncc.defra.gov.uk/page-6189 (accessed August 2016).KAIN, S. (2010): Effects of population density ongrowth, development and behaviour of juvenile cap-tive-bred sand lizard populations. MSc thesis, Univer-sity of Southampton, UK.LAHTI, D., JOHNSON, N., AJIE, B., OTTO, S., HENDRY, A.,BLUMSTEIN, D., COSS, R., DONOHUE, K. & FOSTER, S.(2009): Relaxed selection in the wild. Trends in Ecol-ogy and Evolution 24: 487–496.LJUNGSTR€OM, G., WAPSTRA, E. & OLSSON, M. (2015):Sand lizard (Lacerta agilis) phenology in a warmingworld. BMC Evolutionary Biology 15: Art. 206.LLOYD, C. & SAINSBURY, A. (2003): Disease risk analy-sis for the sand lizard (Lacerta agilis agilis) reintro-duction. London: The Zoological Society of Londonand Natural England.MOLENAAR, F. & SAINSBURY, A. (2009): Disease riskanalysis of the sand lizard (Lacerta agilis) reintroduc-tion programme: screening of free-living sand lizardsfor Serratia marcescens and other possible pathogens,2009. London: The Zoological Society of London,Institute of Zoology.MOLENAAR, F. & SAINSBURY, A. (2010): Disease risk analy-sis for the sand lizard (Lacerta agilis) reintroduction

programme: hazard identification in free-living sandlizards in Wareham (Dorset), 2009. London: The Zoologi-cal Society of London, Institute of Zoology.MOLENAAR, F., SAINSBURY, A. & MARSCHANG, R.(2008): Disease risk analysis for the sand lizard(Lacerta agilis) reintroduction programme: hazardidentification in free-living sand lizards. London: TheZoological Society of London, Institute of Zoology.MOULTON, N. & CORBETT, K. (1999): The sand lizardconservation handbook. Peterborough: English Nature.MOULTON, N., WILKINSON, J., DAVIS, C., FOSTER, J. &HOWE, L. (2011): Sand lizard translocation in the UK.In Global re-introduction perspectives: 2011. Morecase studies from around the globe: 116–119. Soorae,P. S. (Ed.). Gland, and Switzerland: IUCN/SSC Re-introduction Specialist Group, and Abu Dhabi, UAE:Environment Agency-Abu Dhabi.OLSSON, M., GULLBERG, A. & TEGELSTR€OM, H. (1996):Malformed offspring, sibling matings, and selectionagainst inbreeding in the sand lizard (Lacerta agilis).Journal of Evolutionary Biology 9: 229–242.RUSSELL, L. (2012a): The conservation and landscapegenetics of the sand lizard Lacerta agilis. PhD thesis,University of Sussex, UK.RUSSELL, L. (2012b): Investigating the viability of smalland isolated amphibian and reptile populations. ARCresearch report 12/03. Bournemouth: Amphibian andReptile Conservation Trust.SAINSBURY, T. (2012): Disease risk management andpost-release health surveillance of the sand lizardLacerta agilis agilis re-introduction programme 2011/2012. London: The Zoological Society of London,Institute of Zoology.SCHULTE-HOSTEDDE, A. I. & MASTROMONACO, G. F. (2015):Integrating evolution in the management of captive zoopopulations. Evolutionary Applications 8: 413–422.SEDDON, P. J., ARMSTRONG, D. P. & MALONEY, R. F.(2007): Developing the science of reintroduction biol-ogy. Conservation Biology 21: 303–312.SOORAE, P. S. (2016): Global re-introduction perspectives:2016 case studies from around the globe. Gland, Switzer-land: IUCN/SSC Re-introduction Specialist Group, andAbu Dhabi, UAE: Environment Agency-Abu Dhabi.SPELLERBERG, I. F. & HOUSE, S. M. (Unpublished): Ananalysis of the sand lizard (Lacerta agilis L.) habitat insouthern England. A programme of Research financedby The Natural Environment Research Council, Swin-don, UK, 1980.SUTHERLAND, W. J., PULLIN, A. S., DOLMAN, P. M. &KNIGHT, T. M. (2004): The need for evidence-based con-servation. Trends in Ecology & Evolution 19: 305–308.URBAN, M. C., RICHARDSON, J. L. & FREIDENFELDS, N.A. (2014): Plasticity and genetic adaptation mediateamphibian and reptile responses to climate change.Evolutionary Applications 7: 88–103.

Manuscript submitted 23 September 2016;revised 26 January 2017; accepted 13 Feb-ruary 2017



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Sand lizard Lacerta agilis reintroductions in southern England

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