thermal refuges

Applied Herpetology 6 (2009) 307ndash326 wwwbrillnlah

Thermal properties of artificial refuges and theirimplications for retreat-site selection in lizards

Aude Thierry 1 Marieke Lettink 2 Anne A Besson 1 and Alison Cree 13

1 Department of Zoology University of Otago PO Box 56 Dunedin New Zealand2 Coates Road Birdlings Flat R D 3 Little River New Zealand

3 Corresponding author e-mail alisoncreestonebowotagoacnz

AbstractArtificial retreats or refuges (ARs) provide a useful method for sampling lizards and a possible means ofrestoring habitat to aid population persistence Previous research suggests that preferences for ARs mayvary among species and between different designs To test these ideas further we examined the influenceof thermal and structural characteristics on use of three types of ARs by the nocturnal common gecko(Hoplodactylus maculatus) and diurnal McCannrsquos skink (Oligosoma maccanni) two lizards endemic toNew Zealand The field study confirmed that the three ARs (triple-layered Onduline triple-layered ironsolid concrete) differed in retreat-site temperatures provided during each of three seasons (winter spring andsummer) In their top spaces Onduline ARs were the warmest by day coolest by night and thus displayedthe largest diel variations in temperature In the laboratory common geckos showed a significant preferencefor Onduline whether ARs were exposed to a radiant overhead heat source or not whereas skinks didnot display any preference among the three types of ARs regardless of heating The three types of ARsprovided field temperatures within the thermal preference range of both species (data obtained from theliterature) but only for the top spaces of the ARs and only during summer Onduline was the only ARto consistently provide the temperatures preferred by pregnant females Although this study suggests thatstructural properties alone may be sufficient to explain the preference of geckos for triple-layered Ondulinestacks it does not eliminate the possibility that attractive thermal properties also contribute Long-termstudies are needed to test the effects of artificial refuge supplementation on reptiles and on their predatorsand competitorscopy Koninklijke Brill NV Leiden 2009

Key wordsArtificial retreat gecko Hoplodactylus maculatus Oligosoma maccanni skink temperature thermal char-acteristics

Introduction

Anthropogenic activities continue to degrade and modify natural habitats forwildlife around the world One possible way of reducing the loss is by enhancing

copy Koninklijke Brill NV Leiden 2009 DOI101163157075409X432931

308 A Thierry et al Applied Herpetology 6 (2009) 307ndash326

the environment with artificial retreats (Webb and Shine 2000 Souter et al 2004)This practice is widely used to assist reintroductions or population maintenance forbirds and mammals (Smith and Belthoff 2001 Spring et al 2001) Artificial re-treats are also used as a research instrument for example in characterizing habitatsor assisting in population monitoring (DeGraaf and Yamasaki 1992 Schlesingerand Shine 1994 Spring et al 2001) However to date the design and value of ar-tificial retreats have received only limited attention in reptiles (but see Webb andShine 2000 Lettink and Cree 2007 Arida and Bull 2008)

Reptiles appear to be highly selective when choosing retreat sites evaluatingmultiple aspects of their habitat and making relatively subtle choices among avail-able retreat sites based on their structural and thermal features the presence ofconspecifics andor competitors and the perceived risk of predation (Schlesingerand Shine 1994 Cooper et al 1999 Langkilde and Shine 2004) Temperature isa major factor governing the choice of natural and artificial retreat sites by reptiles(Schlesinger and Shine 1994 Downes and Shine 1998 Shah et al 2004) Selec-tion of a thermally suitable retreat site where animals spend long periods of timemay be especially important for ectotherms because of their temperature-dependentbehavioural and physiological processes (eg locomotion digestion growth ratereproduction Webb and Shine 2000) Geckos and snakes generally choose retreatsites (eg under pavers rocks stones) that provide temperatures within the rangeof their preferred body temperature (Webb and Shine 2000 Kearney 2002) Pre-ferred body temperature (PBT also known as selected body temperature Tsel) isthe temperature chosen by the animal in a laboratory thermal gradient (Rock et al2000) Lizards tend to select rocks or crevices as a function of retreat size widthdepth or exposure (sunshade) all factors that are likely to influence thermal char-acteristics (Webb and Shine 2000 Kearney 2002 Shah et al 2004 Goldsbroughet al 2006)

Two other major factors influencing retreat-site selection in reptiles are socialinteractions and predator avoidance (Downes and Shine 1998 Cooper et al 1999Amo et al 2004 Langkilde and Shine 2004) For example in the velvet gecko(Oedura lesueurii) the dominant larger males occupied the best retreat site that didnot contain the scent of a predator forcing smaller males to use less suitable retreatsites (Downes and Shine 1998 Webb and Shine 2000 Kondo et al 2007) Insome cases the desire to avoid predators may be greater than the need to maximisethermoregulatory opportunities (Downes and Shine 1998 Amo et al 2004)

Our study is a continuation of previous work examining the use of artificial re-treats (hereafter ARs) by two New Zealand lizards the nocturnal common gecko(Hoplodactylus maculatus) and diurnal McCannrsquos skink (Oligosoma maccanniLettink and Cree 2007) Previous research by Lettink and Cree (2007) assessedthe relative use of three types of ARs by lizards living in grazed coastal shrublandon Banks Peninsula (Canterbury New Zealand) In that study ARs consisted ofa triple-layered stack of Onduline sheets a triple-layered stack of corrugated ironsheets and a concrete roofing tile Onduline is a tough lightweight roofing product

A Thierry et al Applied Herpetology 6 (2009) 307ndash326 309

made of natural fibres saturated with bitumen (httpwwwondulinecom) Com-mon geckos which are primarily nocturnal and thigmothermic (Rock et al 2000)displayed a strong preference in the field (P lt 001) for Onduline stacks (81of captures) compared with iron stacks (15) and concrete tiles (4 Lettink andCree 2007) Within the triple-layered ARs geckos favoured the two top layers overthe bottom layer McCannrsquos and common skinks (Oligosoma nigriplantare poly-chroma both diurnal heliotherms) used the three types of ARs without any obviouspreference the small sample size prevented a comparison of preference by skinkswithin layers of the triple-layered ARs The results also highlighted a time-of-yeareffect with significantly reduced use of ARs in winter (P lt 001) by all speciesThe authors suggested that the preference (or lack of preference) for each type ofAR is driven by thermal and structural characteristics of each artificial retreat al-though intraspecific and interspecific social interactions might also play a role AsARs (including those made of Onduline) are increasingly used by herpetologistsparticularly in New Zealand (Lettink 2007ab Wilson et al 2007 M Tocher perscomm to A Cree) obtaining more detailed information on the thermal qualities ofdifferent types of ARs and implications for retreat-site use is important

Here we examine the role of temperature in the choice of three types of ARs bythe common gecko and McCannrsquos skink First we ask how Onduline stacks ironstacks and concrete tiles differ in the retreat site temperatures provided in a field sit-uation Based on their attractiveness for geckos in the field we hypothesized that thelsquotop spacersquo of Onduline stacks would provide the warmest daytime temperaturesespecially in summer (see fig 1 for explanation of lsquospacesrsquo) We predicted that ironstacks would provide temperatures similar to but less stable than those provided byOnduline The concrete tile was predicted to display high thermal inertia compared

Figure 1 Schema showing the set up of the multi-layered artificial retreats and the position of the datalogger (i-button)


with the other two We also predicted that the top spaces of the two multi-layeredARs would be warmer during the day and cooler at night than the middle and bot-tom spaces Second we tested the preference of two species of lizards among thethree ARs in a laboratory setting with and without overhead heating to mimic solarradiation We hypothesised that neither species would have a preference when ARswere unheated but that geckos would prefer Onduline when heated Finally wecombined information from our first question (retreat site temperatures in the field)with available data from other studies on thermal preference in our study speciesWe used this information to answer a third question how well do the three typesof ARs meet the thermal preferences of lizards during summer We hypothesisedthat the top space of Onduline ARs would display temperatures that would remainwithin the lizardsrsquo thermal preference for the greatest period of time We concludeby providing recommendations for the use of ARs in herpetological studies

Materials and methods

Thermal characteristics of ARs in the field

The ARs were of the same design and materials as those used and photographed byLettink and Cree (2007) Briefly they consisted of (1) triple-layered stacks (fig 1)of corrugated Onduline sheets (each 400 times 280 times 25 mm) separated by small spac-ers (1-2 cm lengths of 10 mm circular pine dowel) glued underneath the cornersand centre of each layer (2) triple-layered stacks of corrugated iron sheets (each450 times 230 times 1 mm) with layers spaced as described above and (3) single-layeredconcrete roofing tiles (390 times 320 times 25 mm) with ridges underneath creating smallgaps The size of commercially available sheets and the corrugated nature of thematerial meant that there were slight differences in ground area covered by the ARs(range 0104-0125 m2) Concrete ARs were single-layered because of their weightand cost it is unlikely that they would ever be used as triple-layered structures inthe field We thus compared the three types of AR as used in practical situations byconservation workers

Comparison of the three types of ARs by season Day and night temperatureprofiles within the top layer of each type of AR were compared in each of threeseasons For convenience the study was carried out in Dunedin New Zealand(4551primeS 17032primeE 175 m above sea level) Although this site was 362 km fur-ther south than the field site of Lettink and Cree (2007) relative patterns of dailytemperature change in the ARs are likely to be consistent across regions Groupscontaining the three types of ARs were placed on the top of a sunny north-facinghill in an open area Five such groups were spaced 10 m apart Data loggers(i-buttons DS1922 Maxim Integrated Products) recorded the temperature eachhour (plusmn00625C) during three weeks for each season (winter 20 July-10 August2006 spring 29 September-20 October 2006 and summer 28 December-18 Janu-ary 2007) In the case of the multi-layered ARs (Onduline and iron) one i-button per


AR was placed at a central location on the top of the middle layer (ie within thetop space fig 1) and on top of a corrugation For the concrete AR the i-button wasplaced on the ground (effectively also the top-space for this single-layered retreat)Data loggers were placed in this way to indicate the warmest substrate temperaturesavailable by day for ground-hugging species like skinks geckos which can presstheir dorsal surface to the layer above or hang on upside down (Rock et al 20002002 A Cree pers obs) would have access to even warmer surfaces above

Comparison of the different layers of the multi-layered ARs by season For theOnduline and iron ARs data loggers were centrally placed on the ground on thetop of the ground layer and on the top of the middle layer (in the top space) for fiveARs of each type With 15 data loggers available it was not possible to comparetemperatures simultaneously in all layers for both Onduline and iron ARs so eachAR type was tested during adjacent two-week periods Temperatures were recordedeach hour during winter (22 June-6 July 2006 for Onduline 6-20 July 2006 foriron) spring (1-15 September 2006 for Onduline 15-29 September 2006 for iron)and early summer (1-14 December 2006 for Onduline 14-28 December 2006 foriron) Our interest here was in comparing among layers within an AR type notbetween AR types at different times

Effects of thermal properties on lizard preferences for ARs in the laboratory

Study species and maintenance Both species (Hoplodactylus maculatus andOligosoma maccanni) were studied in laboratory colonies maintained at the Univer-sity of Otago Females were originally collected from Macraes Flat eastern OtagoNew Zealand for other studies (Preest et al 2005 Hare et al 2009) and thenonce pregnancies were completed maintained as described below Among the fivemale common geckos some were born in captivity and some were collected asadults

During routine maintenance common geckos (n = 17 12 females and fivemales 70-81 mm SVL 98-166 g) were housed in Perspex cages (950 times 450 times450 mm two females and one male per cage) containing numerous ceramic tiles(to provide retreat sites) plastic climbing structures water dishes a tray with dampsphagnum moss and an area for basking that was heated to 26-28C McCannrsquosskinks (n = 23 females 57-69 mm SVL 26-47 g) were individually housed in20 l plastic containers Each cage was lined with paper towel and contained a bask-ing site (28plusmn1C inverted terracotta saucer) a water dish a damp sphagnum mossdish and a cold retreat site made of ceramic tiles

For two weeks prior to testing and during the experiment each species washeld in a room at 15C with a 1212 h lightdark cycle which simulated warmspring or autumn conditions and encouraged night-time activity for geckos Heatlamps and UV lights were on for 8 h per day 6 days per week Lizards werefed two times a week once with live locusts (Locusta migratoria) crickets (Teli-ogryllus commodus) or mealworm larvae (Tenebrio molitor) and once with mashed


pears Water was available ad libitum Preference tests ran from 9-17 October 2006(autumn) for common geckos and 17 May-8 June 2006 (spring) for McCannrsquosskinks

Preference among ARs with and without overhead heating Preference trialswere conducted indoors using overhead heat lamps to simulate solar radiation Twocircular test arenas (each 12 m in diameter 025 m high) were placed on the floorof a temperature-controlled room A mixture of top soil potting mix and sand wasused as a substrate One each of the three types of AR were placed equidistantlyseparated by a plastic water dish within each arena Heat lamps (100 W) wereplaced 21 cm above each AR but only one arena had the heat lamps turned on(the heated arena) After 1 h of heating by heat lamps temperatures under eachtype of AR reached and remained at the maxima achieved outdoors during a warmspring day (29 plusmn 1C in the top space for Onduline 28 plusmn 1C in the top space foriron and 25 plusmn 1C for concrete) A video camera was placed 15 m above the arenain a central position In trials with geckos which climb well (unlike skinks) a Per-spex cover with mesh inserts was placed above the ARs and below the heat lampsto prevent them from escaping Lizards were not fed for three days prior to the ex-periment as feeding and digestion can affect preferred body temperature (Cogger1974 Regal 1996)

For common geckos each animal was individually and randomly placed at thecentre of one arena at 1730 h and left undisturbed until the following day at 1700 hat which time its position was recorded by gently raising the various layers of theARs Because geckos are primarily nocturnal checking their position in the after-noon allowed us to assume that we found them in their daytime retreat site (alsochecked by filming see below) Each animal had two randomized trials one withthe heated ARs and another with the non-heated ARs thus each animal effectivelyserved as its own control Each lizard had seven to twelve days between the two tri-als The same process was followed with skinks but because they are diurnal theywere placed at 0830 h and checked at 0800 h the following morning to indicatetheir night-time refuge

Infra-red cameras were used to film movements of both species for 90 min priorto their position check to confirm that they had not moved during that time Skinkmovements were also filmed from 0915 h until 1015 h (likely peak of basking ac-tivity just after the start of the heat lamps) to assess a possible influence of theirbasking site on their subsequent night-time retreat site and also to examine whichAR if any was preferred for basking over those 60 min Cameras were programmedto come on without human disturbance Geckos were not filmed by day as they areless likely to bask openly

After each trial with an individual lizard all the structures (ARs and dishes) fromthe experimental arena were washed with disinfectant (Powerquat Blue biodegrad-able sanitizer) thoroughly rinsed and air-dried in order to remove as much of anypheromonal traces left by the previous lizard as possible The potting substrate wasstirred up between trials to redistribute any potential pheromones


Thermal preference of lizards in comparison with temperatures provided by ARs

Data from several studies examining preferred body temperature (PBT) of geckosand skinks as a function of species sex time-of-day andor season were collated(Rock et al 2000 common gecko males non-pregnant females and pregnant fe-males in summer Hare et al 2009 McCannrsquos skink pregnant females in springpresent study McCannrsquos skink non-pregnant females in summer) All tests weremade with lizards from the Otago region so that thermal preference could be com-pared with temperatures measured in ARs in the field in Dunedin All tests (exceptfor non-pregnant McCannrsquos skinks in summer) were for field-fresh animals ietested within 2 days of capture (non-pregnant McCannrsquos skinks had been captivefor 14 months) Thermal preference was measured by placing lizards in individualraceways on a thermal gradient where substrate temperatures ranged from 12-35CBody temperatures were measured at several times of the day and night using a ther-mocouple inserted into the cloaca

We reanalysed data from the studies cited above as follows For each timepointa set point range was estimated by the bounds of the central 50 of temperaturesselected by lizards (Christian and Weavers 1996) We then determined the pro-portion of time each AR layer remained within the PBT boundaries of animals asa function of season and time-of-day by comparing thermal preferences with thefield temperature profiles for ARs Although the amount of time during which theARs reach the thermal preference of the animals will be specific to a climatic re-gion relative patterns of daily temperature change among AR types are likely to beconsistent across different climates

Statistical analysis

All statistical analyses in this study used the programme STATISTICA 60copyStatSoft Inc A value of P lt 005 was considered significant Data are expressedas mean plusmn 1 SE

The thermal characteristics of ARs in the field were analysed separately for day-time and night-time periods Repeated measures analyses of variance (ANOVA)were run with time-of-day (or night) as the within-subjects variable type of AR(or layer) as the between-subjects factor and temperature as the dependent vari-able Tests for sphericity (Mauchleyrsquos test) were usually rejected so the P valueswere adjusted using the Huynh-Feldt epsilon (Kinnear and Gray 2009) When thebetween-subjects effect of AR (or layer) was significant (indicating a significantdifference in mean temperatures) Fisher LSD post-hoc tests were used to makepair-wise comparisons Additionally we compared mean maximum temperaturesattained at any time of day and mean minimum temperatures attained at any timeof night between different ARs using one-way ANOVAs followed where signifi-cant by Fisher LSD tests

To assess the distribution of lizards among the ARs in laboratory preference testschi-square analysis was used The first test was within each trial (heated and un-


heated) to determine whether use of the three ARs deviated from that predicted bya random distribution The second test was a comparison between heated and un-heated trials to determine whether lizards changed their preference as a function ofheating For skinks the percentage of time spent basking on each AR was comparedusing a non-parametric Friedman test as some variances were equal to zero

A discriminant function analysis was also used for skinks to assess the effect oftime basking on each type of AR on retreat-site choice for the night Data werenormally distributed once transformed by arcsine square root (P gt 005 for theShapiro-Wilkinson and Kolmogorov-Smirnov tests)

Results


Comparison of the three types of ARs by season During all seasons tested meandaytime temperatures in the top space differed significantly among the three typesof AR (between-subjects effect P lt 0008 table 1) Onduline was warmer on av-erage than concrete and also in summer warmer than iron (post hoc tests P lt

0005) The way in which temperatures changed with time also varied significantlyamong the three ARs in each season (P lt 0001 fig 2a) Onduline reached highermean maxima (at any time of day) in the top space than either iron or concrete in allseasons (P lt 002) Differences in mean maxima were especially marked in sum-mer (F212 = 197 P lt 0001) with Onduline reaching temperatures about 6Chigher (306 plusmn 07C) than either iron (245 plusmn 05C) or concrete (249 plusmn 09Cpost hoc tests P lt 0001) Individual temperatures on any day or time point reachedmaxima of 587C for Onduline 437C for iron and 412C for concrete

Regardless of season night-time temperatures in the top space showed a generalreverse of daytime patterns (fig 2b) Type of AR had a significant effect on meantemperatures as well as on the way that temperature changed with time (P lt 0001table 1) Mean minimum temperatures varied significantly among types of ARespecially in summer (F212 = 166 P lt 0001) when the top space of Ondu-line reached lower mean minima (91 plusmn 01C) than either iron (100 plusmn 01C) orconcrete (112 plusmn 04C post hoc tests P lt 005) During winter individual tem-peratures on the coldest nights dropped below freezing (minus6C for Onduline minus4Cfor iron and minus2C for concrete)

Comparison of the different layers of multi-layered ARs by season Here we em-phasise differences within the Onduline retreats (iron sampled over adjacent timeperiods showed broadly similar but less marked effects of layer) Within triple-layered Onduline mean daytime temperatures were always significantly differentamong layers (between-subjects effect P lt 005 table 2) In all seasons the topspace was warmer than the middle space which was warmer than the ground space(post-hoc tests P lt 005) The three layers also differed in the way that temper-ature changed with time (P lt 0001 table 2) At the warmest time-of-day duringsummer mean maxima in the top spaces of Onduline and iron respectively were


Table 1Effect of time (hours) by day and night on temperatures in top spaces of three types of artificialretreats as a function of season (df and P values for within-subjects analyses have been adjusted fornon-sphericity) For post-hoc tests Ond = Onduline and Conc = concrete

Time Season Factor ANOVA Post-hoc LSD Fisher

DayWinter Within-subjects effects

Time F17204 = 1516 P lt 0001Time lowast AR F34204 = 76 P lt 0001

Between-subjects effectsAR F212 = 448 P lt 0001 (Ond + Iron) gt Conc P lt 0001

Spring Within-subjects effectsTime F24291 = 4999 P lt 0001Time lowast AR F48291 = 77 P lt 0001


Summer Within-subjects effectsTime F15183 = 6424 P lt 0001Time lowast AR F31183 = 231 P lt 0001

Between-subjects effectsAR F212 = 149 P lt 0001 Ond gt (Iron + Conc) P lt 0005

NightWinter Within-subjects effects


Between-subjects effectsAR F212 = 399 P lt 0001 (Iron + Conc) gt Ond P lt 0001




Between-subjects effectsAR F212 = 194 P lt 0001 Conc gt Iron gt Ond P lt 005

271C and 225C middle spaces were 216C and 198C and ground spaceswere 177C and 166C By night temperature patterns were reversed The threelayers differed in mean night-time temperature (P lt 0001 for Onduline with thetop layer always being coldest) and in winter and spring in the way that tempera-


(a) Day

(b) Night

Figure 2 (a) Mean (plusmn1 SE) day-time temperatures attained by the top space in each type of artificialretreat (AR) as a function of season and time-of-day Each data point is the mean of five replicateARs for which temperature was measured hourly and averaged over three weeks in winter 2006spring 2006 and summer 2007 (see methods for dates) Each AR type was examined simultaneouslyTime-of-day is in hours of the 24 h clock (b) Mean night-time temperatures obtained for the top spacein each type of AR as a function of season and time-of-night


Table 2Effect of time (hours) by day and night on temperatures in different layers of Onduline artificialretreats as a function of season (df and P values for within-subjects analyses have been adjusted fornon-sphericity)



Time F2241 = 1631 P lt 0001Time lowast Layer F4241 = 269 P lt 0001

Between-subjects effectsLayer F212 = 314 P lt 0001 Top gt Middle gt Ground P lt 0005

Spring Within-subjects effectsTime F16193 = 1799 P lt 0001Time lowast Layer F32193 = 158 P lt 0001


Summer Within-subjects effectsTime F28341 = 2562 P lt 0001Time lowast Layer F57341 = 181 P lt 0001




Between-subjects effectsLayer F212 = 607 P lt 0001 Top lt Middle lt Ground P lt 0001



Summer Within-subjects effectsTime F18215 = 4137 P lt 0001Time lowast Layer F36215 = 045 P = 094


ture changed with time (P lt 0001 for Onduline) At the coolest time of night insummer mean temperatures in the top spaces of Onduline and iron ARs respec-tively were 69C and 83C middle spaces were 82C and 96C and groundspaces were 94C and 108C



When checked at 1700 h after 24 h in the arena common geckos were foundsignificantly more often under the Onduline during both the heated (χ2

1 = 754P lt 001) and non-heated trials (fig 3 χ2

1 = 497 P lt 005 results for ironand concrete were pooled for this and the following test as fewer than five geckoswere found under these ARs) Preference did not change between trials (χ2

1 = 024P gt 005) Filming confirmed that geckos did not move during the 90 minutes priorto the 1700 h check Whether Onduline was heated or unheated most geckos werefound in the top (721 observations) or middle spaces (1221 observations) andrarely in the ground space (221 observations) There was no obvious difference inchoice between male and female geckos

Skinks did not display any preference among the three types of AR whether theARs were heated (χ2

1 = 118 P gt 005) or not (χ21 = 114 P gt 005) Preference

did not change between heated and unheated trials (χ21 = 044 P gt 005) Filming

confirmed that the skinksrsquo location did not vary for the 90 minutes prior to the checkat 0800 h Some skinks (one for the heated trial and two for the non-heated trial)were not included in these results as they spent the night under a water dish Re-

Figure 3 Percentage of the number of common geckos (Hoplodactylus maculatus) and McCan-nrsquos skinks (Oligosoma maccanni) found under each type of artificial retreat during the heated andnon-heated trials (lowastlowast = P lt 001 lowast = P lt 005 ns = P gt 005) As fewer than five geckos werefound under iron and concrete ARs these results were pooled Numbers at the bottom of bars representthe sample size


gardless of heating skinks using Onduline ARs were distributed reasonably evenlyamong layers (717 observations in top space 517 in middle space 517 in groundspace) whereas with iron ARs they mostly used the ground space (1416 observa-tions)

Skinks were very active when heat lamps were on Filming revealed that theyspent much of the first hour of heating exploring the arena and rarely more thanthree minutes at a time basking on the same AR switching from one AR to anotherSkinks did not display a significant basking preference for any particular type ofAR although there was a tendency to spend more time basking on the Onduline(177 plusmn 004) than on iron (69 plusmn 002) or concrete (53 plusmn 002 Friedmantest P = 0057) Only 19 lizards (from a total of 23) were included in this analysisas some videotapes malfunctioned The amount of time each skink spent basking oneach AR did not predict the skinksrsquo choice of night-time retreat site (discriminantfunction analysis Wilk Lambda = 09 P gt 005) During the unheated trial skinksdid climb on the ARs but for much shorter periods of time (typically only for a fewseconds) than in the heated trial and this was therefore not considered as baskingbehaviour


In this section we compare whether the ARs used in the field provided mean temper-atures within the preferred body temperature boundaries for common geckos andMcCannrsquos skinks In the data sets reported here pregnant females of both specieshave uniformly high thermal preferences across the day (figs 4 and 5)

During summer days mean temperatures in the top space of the Ondulinereached or exceeded the thermal preference of common geckos during 8 hday formales and non-pregnant females and 5 hday for pregnant females (fig 4 readingfrom where the temperature profile line crosses the shading for thermal preference)The top space of the iron AR reached the geckosrsquo thermal preference for 6 hdayfor males and 5 hday for non-pregnant females but did not reach the thermal pref-erence of pregnant females The concrete tile reached the thermal preferences ofmales for 75 hday and non-pregnant females for 3 hday Mean temperatures forall of the ARs fell far below the thermal preferences of geckos at night

During summer days mean temperatures in ARs reached or exceeded the ther-mal preference of pregnant female McCannrsquos skinks (recorded in spring) in the topspace of Onduline only (during 4 hday fig 5) Non-pregnant females (long-termcaptives) had more variable and somewhat lower thermal preferences which over-lapped the temperatures provided by the top space of Onduline (for 75 hday) andconcrete (55 hday) but not iron

Discussion

Our field study confirmed that the thermal profiles of the three types of ARs dif-fered As expected Onduline ARs provide the warmest top space temperatures by


Figure 4 Mean (plusmn1 SE) day and night-time temperatures in the top space of each type of artificialretreat (AR) in summer compared with the thermal preference of common geckos (Hoplodactylusmaculatus) Each data point is the mean of five replicate ARs for which temperature was measuredhourly and averaged over three weeks in summer 2007 (same three weeks as in fig 2) The shadedarea represents the preferred body temperature (central 50) of common geckos immediately aftercapture from the wild (recalculated using raw data from Rock et al 2000) Time-of-day is in hours ofthe 24 h clock The horizontal black bar indicates night-time

day especially in summer However they also provided the coldest top space atnight Concrete provided the warmest temperatures at night but the bottom spacesof the multi-layered Onduline and iron stacks provided similar temperatures On-duline showed the largest fluctuations in temperature between day and night of allthe ARs The top space of Onduline ARs reached extreme temperatures far above(58C in summer) or below (minus6C in winter) what a New Zealand lizard is likely tosurvive (Werner and Whitaker 1978 Tocher 1993) Iron ARs did not heat or coolas dramatically as expected whilst heating similarly to the Onduline ARs duringwinter and spring days iron ARs behaved more like the concrete tile at other timesThe concrete tile responded as predicted being the coldest during the day but thewarmest at night regardless of season

Within the triple-layered ARs (Onduline and iron) mean day-time temperaturewas higher from top to bottom regardless of season The night-time pattern wasalways the opposite These results confirm that each space both within an AR andwithin a season is providing significantly different temperatures and different mi-crohabitats giving lizards opportunities to thermoregulate within the same AR


Figure 5 Mean (plusmn1 SE) day and night-time temperatures in the top space of each type of artificialretreat (AR) in summer compared with the thermal preference of McCannrsquos skinks (Oligosoma mac-canni) Each data point is the mean of five replicate ARs for which temperature was measured hourlyand averaged over three weeks in summer 2007 (same three weeks as in fig 2) The shaded arearepresents the preferred body temperature (central 50) of pregnant McCannrsquos skinks measured im-mediately after capture from the wild in spring (Hare et al 2009) and of non-pregnant females froma captive colony in summer (present study) Time-of-day is in hours of the 24 h clock The horizontalblack bar indicates night-time

In the laboratory McCannrsquos skinks used ARs without preference for any partic-ular type whereas common geckos showed a strong preference for the OndulineARs regardless of heating concurring with the field observations of Lettink andCree (2007) This difference in use of ARs between taxa is likely to be a result ofthe different ecology and thermoregulatory habits expected from an heliothermic di-urnal skink versus a primarily thigmothermic and nocturnal gecko Diurnal skinksthermoregulate primarily by direct exposure to solar radiation In contrast com-mon geckos thermoregulate by day by pressing their bodies against the undersideof sun-warmed substrates (Rock et al 2002) and would therefore be expected toshow greater discrimination than skinks in their choice of a diurnal retreat site (Let-tink and Cree 2007) Importantly common geckos in our laboratory tests preferredOnduline whether the ARs were heated or not This suggests that their selectionwas not made solely on the basis of thermal characteristics (or more speculatively


that geckos may be able to anticipate the thermal properties that Onduline will showwhen overhead radiation is available)

Within triple-layered ARs geckos favoured the two uppermost spaces Besidesbeing warmer than the bottom space during the day these spaces have the additionaladvantage of allowing lizards to use crevice-specific defence postures (wedgingtheir body in a crack) in response to predator attacks (Cooper et al 1999 Aridaand Bull 2008) Skinks used the three spaces of the Onduline without any obvi-ous preference but had a tendency to prefer the ground space of the iron Theseresults again concur with field observations by Lettink and Cree (2007) and withobservations in Alexandra (Central Otago) that McCannrsquos skinks shelter at nightunder large rocks between soil-rock interfaces whereas common geckos hide dur-ing the day between rock-rock interfaces (MacAvoy 1976) Another diurnal skinkthe Australian coppertail (Ctenotus taeniolatus) shelters under large rocks withrocky substrates during the day but selects rocks with sandy substrates at night(Goldsbrough et al 2006) Thus selection of substrate type may be of importancewhen using ARs for skink projects

The three AR types exhibited temperatures within the thermal preference rangeof common geckos and McCannrsquos skinks only in the top spaces and only duringsummer Only the Onduline ARs reached the pregnant femalesrsquo thermal preferencePregnant common geckos have higher PBT than the non-reproductive animalswhich probably reflects a requirement for embryonic development (Rock et al2000) although a higher PBT during pregnancy is not yet proven for McCannrsquosskinks Our results suggest that during summer Onduline should be the most attrac-tive AR for both species particularly as lizards can avoid overly warm temperaturesin the top space on the hottest days by moving to layers beneath

Considering that the mean daily maxima of the warmest AR (Onduline) in thefield in Dunedin in July 2006 (winter) was 138C and that the mean daytime ther-mal preference of male common geckos in winter was between 24-26C (Tocher1992) it is unlikely that any of the ARs would reach the lizardsrsquo thermal prefer-ence in winter However common geckos and McCannrsquos skinks are known for theiradaptation to cold climates and are likely to choose to be inactive during winter toavoid hazards of environmental extremes by hiding in deep crevices (MacAvoy1976 Tocher 1993 Tocher and Davison 1996) as do many lizards elsewhere(Kearney 2002) New Zealand lizards are cold-adapted with a critical thermalminimum (temperature below which lizards can barely move) as low as 08C forcommon geckos from Canterbury (Tocher 1992) and slightly warmer for McCan-nrsquos skinks (around 3C A Besson pers obs) The poor use of ARs by lizardsin winter noted by Lettink and Cree (2007) coupled with our observations of ARsreaching minimum temperatures between minus6C and minus2C in winter suggests thatARs are inferior to natural retreats at this time of year because they fail to provideadequate buffering against freezing temperatures

Previous studies have highlighted temperature or the features having an ef-fect on it (eg size width of the rock exposure) as the main factor influencing


reptilesrsquo choice of retreat site (Webb and Shine 1998 Webb and Shine 2000Shah et al 2004) In these Australian studies the broad-headed snake (Hoplo-cephalus bungaroides) the velvet gecko (Oedura lesueurii) and the thick-tailedgecko (Nephrurus milii) all chose retreat sites that would enhance their thermoreg-ulatory opportunities However when predators andor other species of reptiles thatcompete for retreat sites are also present thermoregulation became less of a prioritythan avoiding predators and direct agonistic encounters with competitors (Downesand Shine 1998 Langkilde and Shine 2004) We did not examine the influenceof predators competitors or conspecifics on AR selection but consider these topicsworthy of further attention

Our laboratory preference trial suggests that temperature within ARs may not bethe principal factor influencing choice of an AR site The physical properties of thematerial that ARs are constructed from may also be important Onduline is a tex-tured but soft material compared with the smooth iron or the hard roughness of theconcrete During the filming of the preference trial in the laboratory skinks oftenstruggled to climb on the iron and slipped from it their claws unable to grip Thecorrugated structure and organisation in three layers of the Onduline and iron alsoprovided additional hiding places and possibilities to thermoregulate while the con-crete with only one layer and no corrugated shape did not provide microclimateswithin the AR

The preference for Onduline ARs in the field (but not in the laboratory) couldalso be explained by the presence of food (invertebrates) We observed slaters(wood lice) and slugs in the ground space all year round under the three AR typesbut the Onduline was the only type with small spiders living within the layers inwinter and spring and a large (20 to 30 animals per AR) colony of earwigs duringsummer In coastal Canterbury Onduline ARs were frequently used by endemic redkatipo spiders (Latrodectus katipo Lettink and Patrick 2006) It is unclear whethergeckos and invertebrates are attracted by the same physical properties of the On-duline (temperature moisture physical texture) or whether it is the presence offood that attracts lizards Goldsbrough et al (2003) also referred to the importanceof habitat associations between invertebrates and reptiles under rocks in AustraliaBy combining field observations with carefully-designed laboratory experiments itmay be possible to further untangle the relative influence of the various factors thatinfluence retreat-site selection in lizards

Concluding remarks

Our study suggests that multi-layered Onduline stacks would be more effectivethan iron or concrete ARs for simultaneously attracting both common geckos andMcCannrsquos skinks We therefore recommend this material and design for futureherpetological studies and restoration projects Onduline is inexpensive (approx-imately US$3 per AR Lettink and Cree 2007) available throughout the worldeasy to cut up lightweight has anti-fungal properties and is durable making it a


practical choice for short- and long-term projects alike In comparison iron andconcrete are difficult to cut and carry around Our design could be improved bymaking the top layer slightly larger than the next layer and this layer slightly largerthan the bottom layer hereby reducing the visibility to predators of lizards movingbetween layers (an alternative might be to punch holes between layers althoughthis might reduce the stratification of temperatures) To attract lizards of variousbody sizes gap size could easily be manipulated by using spacers of different sizesReducing the number of entrances could further improve the design as researchelsewhere showed that lizards preferred refuges with one entrance over those withtwo entrances (Cooper et al 1999 Webb and Shine 2000 Arida and Bull 2008)however one would need to keep in mind that changes to entrance size may alsochange the thermal properties In terms of layers three should be a minimum in or-der to provide a wide range of thermal microclimates Neither of our study speciesis obviously attracted to high humidity but the elevated humidity under the groundlayer observed in the field suggests that our design may also provide suitable mi-croclimates for species that require moist environments (eg Neilson et al 2004)

Artificial retreats are a low-disturbance tool for the study and restoration of lizardpopulations As a restoration tool ARs could be used as stepping stones to helpsmall widely-spread populations of lizards interact and disperse and to enhancehabitats and populations of endangered reptiles generally For example Souter etal (2004) showed that the addition of artificial burrows increased the abundanceof endangered pygmy blue tongue lizards (Tiliqua adelaidensis) in southern Aus-tralia and Webb and Shine (2000) strongly suggested that the addition of artificialrocks (concrete pavers) would aid the survival of the broad-headed snake and itsprey the velvet gecko in degraded habitats of south-eastern Australia The additionof ARs may also be useful for re-introductions of threatened species by encourag-ing translocated lizards to remain near their site of release (Burton 2005 Lettink2007a Arida and Bull 2008) However researchers and conservationists need tobe aware of possible unintended consequences of long-term use of ARs includingattraction of illegal collectors or of predators such as feral cats and rodents possi-bly leading to increased predation pressure (Souter et al 2004 Lettink and Cree2007) and to temperature-sensitive life-history changes (eg birth times) that couldbe disadvantageous if ARs were suddenly removed (eg through vandalism) Wealso acknowledge that our study was conducted on species living in cool climateswhere access to preferred body temperature is limited (Rock et al 2002 Hare etal 2009) we therefore recommend further study on species in other countries todetermine the value of ARs made of Onduline in warmer climates

In conclusion untangling the relative importance of the factors driving retreat-site selection and using this information to optimise the design of ARs are steps tounderstanding a speciesrsquo ecology and to improve population management What arenow needed are long-term studies on a wider range of taxa to determine the ultimateeffects of refuge supplementation on reptile assemblages and on their predators andcompetitors


AcknowledgementsWe thank S Boessenkol C Fraser J Germano K Hare C Lagrue and J Oldman for their help in the fieldand these people D Wilson and two anonymous referees for comments that improved the manuscript Forallowing us access to their land we thank F R and B Cunningham For sharing their thermal preferencedata we thank J Rock and J Hare Thanks to the University of Otago Department of Zoology for technicalassistance and to K Miller I Dickson K Garrett and A Armstrong for technical support and help withanimal husbandry This research was undertaken with approval from the Department of Conservation (OT-15086-CAP) the University of Otago Animal Ethics Committee (AEC 4406) and following consultationwith Ngai Tahu

References

Amo L Lopez P Martin J (2004) Trade-offs in the choice of refuges by common wall lizards dothermal costs affect preferences for predator-free refuges Can J Zool 82 897-901

Arida EA Bull CM (2008) Optimising the design of artificial refuges for the Australian skinkEgernia stokesii Appl Herpetol 5 161-172

Burton FJ (2005) Restoring a new wild population of Blue Iguanas (Cyclura lewisi) in the SalinaReserve Grand Cayman Iguana 12 167-174

Christian KA Weavers BW (1996) Thermoregulation of monitor lizards in Australia an evalua-tion of methods in thermal biology Ecol Monogr 66 139-157

Cogger HG (1974) Thermal relations of the Mallee Dragon Amphibolurus fordi (Lacertilia Agami-dae) Aust J Zool 22 319-339

Cooper WE van Wyk JH Mouton P Le FN (1999) Incompletely protective refuges selectionand associated defences by a lizard Cordylus cordylus (Squamata Cordylidae) Ethology 105687-700

DeGraaf RM Yamasaki M (1992) A non-destructive technique to monitor the relative abundanceof terrestrial salamanders Wildlife Soc B 20 260-264

Downes S Shine R (1998) Heat safety or solitude Using habitat selection experiments to identifya lizardrsquos priorities Anim Behav 55 1387-1396

Goldsbrough CL Hochuli DF Shine R (2003) Invertebrate biodiversity under hot rocks habitatuse by the fauna of sandstone outcrops in the Sydney region Biol Conserv 109 85-93

Goldsbrough CL Shine R Hochuli DF (2006) Factors affecting retreat-site selection by copper-tail skinks (Ctenotus taeniolatus) from sandstone outcrops in eastern Australia Austral Ecol 31326-336

Hare JR Holmes KM Wilson JL Cree A (2009) Modelling exposure to selected temperatureduring pregnancy the limitations of squamate viviparity in a cool-climate environment Biol JLinn Soc 96 541-552

Kearney M (2002) Hot rocks and much-too-hot rocks seasonal patterns of retreat-site selection bya nocturnal ectotherm J Therm Biol 27 205-218

Kinnear PR Gray CD (2009) SPSS 16 made simple Psychology Press Hove UKKondo J Downes SJ Keogh SJ (2007) Recent physical encounters affect chemically mediated

retreat-site selection in a gecko Ethology 113 68-75Langkilde T Shine R (2004) Competing for crevices Interspecific conflict influences retreat-site

selection in montane lizards Oecologia 140 684-691Lettink M (2007a) Detectability movements and apparent lack of homing in Hoplodactylus macu-

latus (Reptilia Diplodactylidae) following translocation New Zeal J Ecol 31 111-116Lettink M (2007b) Comparison of two techniques for capturing geckos in rocky habitat Herpetol

Review 38 415-418


Lettink M Cree A (2007) Relative use of three types of artificial retreats by terrestrial lizards ingrazed coastal shrubland New Zealand Appl Herpetol 4 227-243

Lettink M Patrick BH (2006) Use of artificial cover objects for detecting red katipo Latrodectuskatipo Powell (Araneae Theridiidae) New Zeal Entomol 29 99-102

MacAvoy ES (1976) The physiology of lizards from arid regions in central Otago PhD ThesisDepartment of Zoology University of Otago

Neilson K Duganzich D Goetz B Waas JR (2004) Improving search strategies for the crypticNew Zealand striped skink (Oligosoma striatum) through behavioural contrasts with the brownskink (Oligosoma zelandicum) New Zeal J Ecol 28 267-278

Preest M Cree A Tyrrell C (2005) ACTH-induced stress response during pregnancy in aviviparous gecko no observed effect on offspring quality J Exp Zool 304A 823-835

Regal P (1966) Thermophilic response following feeding in certain reptiles Copeia 1966 588-590Rock J Andrews RM Cree A (2000) Effects of reproductive condition season and site on se-

lected temperatures of a viviparous gecko Physiol Biochem Zool 73 344-355Rock J Cree A Andrews RM (2002) The effect of reproductive condition on thermoregulation

in a viviparous gecko from a cool climate J Therm Biol 27 17-27Schlesinger CA Shine R (1994) Selection of diurnal retreat sites by the nocturnal gekkonid lizard

Oedura lesueurii Herpetologica 50 156-163Shah B Shine R Hudson S Kearney M (2004) Experimental analysis of retreat-site selection

by thick-tailed geckos Nephrurus milii Austral Ecol 29 547-552Smith BW Belthoff JR (2001) Burrowing owls and development results of short-distance nest

burrow relocations to minimise constructive impacts J Raptor Res 35 385-391Souter NJ Bull CM Hutchinson MN (2004) Adding burrows to enhance a population of the

endangered pygmy blue tongue lizard Tiliqua adelaidensis Biol Conserv 116 403-408Spring DA Bevers M Kennedy JOS Harley D (2001) Economics of nest-box program for the

conservation of an endangered species a reappraisal Can J Forest Res 31 1992-2003Tocher MD (1992) Paradoxical preferred body temperatures of two allopatric Hoplodactylus mac-

ulatus (Reptilia Gekkonidae) populations from New Zealand New Zeal Nat Sc 19 53-63Tocher MD (1993) Critical minimum body temperatures of Hoplodactylus maculatus (Reptilia

Gekkonidae) from New Zealand New Zeal Nat Sc 20 41-45Tocher MD Davison W (1996) Differential thermal acclimation of metabolic rate in two popula-

tions of the New Zealand common gecko Hoplodactylus maculatus (Reptilia Gekkonidae) J ExpZool 275 8-14

Webb JK Shine R (2000) Paving the way for habitat restoration can artificial rocks restore de-graded habitats of endangered reptiles Biol Conserv 92 93-99

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Accepted 10 March 2009


the environment with artificial retreats (Webb and Shine 2000 Souter et al 2004)This practice is widely used to assist reintroductions or population maintenance forbirds and mammals (Smith and Belthoff 2001 Spring et al 2001) Artificial re-treats are also used as a research instrument for example in characterizing habitatsor assisting in population monitoring (DeGraaf and Yamasaki 1992 Schlesingerand Shine 1994 Spring et al 2001) However to date the design and value of ar-tificial retreats have received only limited attention in reptiles (but see Webb andShine 2000 Lettink and Cree 2007 Arida and Bull 2008)

Reptiles appear to be highly selective when choosing retreat sites evaluatingmultiple aspects of their habitat and making relatively subtle choices among avail-able retreat sites based on their structural and thermal features the presence ofconspecifics andor competitors and the perceived risk of predation (Schlesingerand Shine 1994 Cooper et al 1999 Langkilde and Shine 2004) Temperature isa major factor governing the choice of natural and artificial retreat sites by reptiles(Schlesinger and Shine 1994 Downes and Shine 1998 Shah et al 2004) Selec-tion of a thermally suitable retreat site where animals spend long periods of timemay be especially important for ectotherms because of their temperature-dependentbehavioural and physiological processes (eg locomotion digestion growth ratereproduction Webb and Shine 2000) Geckos and snakes generally choose retreatsites (eg under pavers rocks stones) that provide temperatures within the rangeof their preferred body temperature (Webb and Shine 2000 Kearney 2002) Pre-ferred body temperature (PBT also known as selected body temperature Tsel) isthe temperature chosen by the animal in a laboratory thermal gradient (Rock et al2000) Lizards tend to select rocks or crevices as a function of retreat size widthdepth or exposure (sunshade) all factors that are likely to influence thermal char-acteristics (Webb and Shine 2000 Kearney 2002 Shah et al 2004 Goldsbroughet al 2006)

Two other major factors influencing retreat-site selection in reptiles are socialinteractions and predator avoidance (Downes and Shine 1998 Cooper et al 1999Amo et al 2004 Langkilde and Shine 2004) For example in the velvet gecko(Oedura lesueurii) the dominant larger males occupied the best retreat site that didnot contain the scent of a predator forcing smaller males to use less suitable retreatsites (Downes and Shine 1998 Webb and Shine 2000 Kondo et al 2007) Insome cases the desire to avoid predators may be greater than the need to maximisethermoregulatory opportunities (Downes and Shine 1998 Amo et al 2004)

Our study is a continuation of previous work examining the use of artificial re-treats (hereafter ARs) by two New Zealand lizards the nocturnal common gecko(Hoplodactylus maculatus) and diurnal McCannrsquos skink (Oligosoma maccanniLettink and Cree 2007) Previous research by Lettink and Cree (2007) assessedthe relative use of three types of ARs by lizards living in grazed coastal shrublandon Banks Peninsula (Canterbury New Zealand) In that study ARs consisted ofa triple-layered stack of Onduline sheets a triple-layered stack of corrugated ironsheets and a concrete roofing tile Onduline is a tough lightweight roofing product



































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thermal refuges

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