Submitted 7 April 2016Accepted 15 May 2016Published 9 June 2016

Corresponding authorMiguel A Carreterocarreterocibiouppt

Academic editorJohn Measey

Additional Information andDeclarations can be found onpage 13

DOI 107717peerj2107

Copyright2016 Ferreira et al

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

Does ecophysiology mediate reptileresponses to fire regimes Evidence fromIberian lizardsCatarina C Ferreira12 Xavier Santos2 and Miguel A Carretero2

1Departamento de Biologia Faculdade de Ciecircncias da Universidade do Porto Porto Portugal2CIBIO Research Centre in Biodiversity and Genetic Resources InBIO Universidade do Porto VairatildeoPortugal

ABSTRACTBackground Reptiles are sensitive to habitat disturbance induced by wildfires butspecies frequently show opposing responses Functional causes of such variabilityhave been scarcely explored In the northernmost limit of the Mediterranean biore-gion lizard species of Mediterranean affinity (Psammodromus algirus and Podarcisguadarramae) increase in abundance in burnt areas whereas Atlantic species (Lacertaschreiberi and Podarcis bocagei) decrease Timon lepidus the largest Mediterraneanlizard in the region shows mixed responses depending on the locality and fire historyWe tested whether such interspecific differences are of a functional nature namely ifecophysiological traits may determine lizard response to fire Based on the variation inhabitat structure between burnt and unburnt sites we hypothesise that Mediterraneanspecies which increase density in open habitats promoted by frequent fire regimesshould be more thermophile and suffer lower water losses than Atlantic speciesMethodsWe submitted 6ndash10 adultmales of the five species to standard experiments forassessing preferred body temperatures (Tp) and evaporative water loss rates (EWL) andexamined the variation among species and along time by means of repeated-measuresAN(C)OVAsResults Results only partially supported our initial expectations since the medium-sized P algirus clearly attained higher Tp and lower EWL The two small wall lizards(P bocagei and P guadarramae) displayed low Tp and high EWL while the two largegreen lizards (T lepidus and L schreiberi) displayed intermediate values for bothparametersDiscussion The predicted differences according to the biogeographic affinities withineach pair were not fully confirmed We conclude that ecophysiology may help tounderstand functional reptile responses to fire but other biological traits are also tobe considered

Subjects Biodiversity Conservation Biology EcologyKeywords Reptiles Habitat Functional response Preferred temperatures Water-loss ratesWildfires

INTRODUCTIONWildfire is considered among the environmental disturbances with a major impact onecosystem functioning and composition in many areas of the world (Bond Woodwardamp Midgley 2005) Global climate change (Pintildeol Terradas amp Lloret 1998 McKenzie et al

How to cite this article Ferreira et al (2016) Does ecophysiology mediate reptile responses to fire regimes Evidence from Iberianlizards PeerJ 4e2107 DOI 107717peerj2107

2004 Kasischke amp Turetsky 2006 Westerling et al 2006) and shifts in land-use practices(eg agricultural abandonment and urban sprawlMoreira Rego amp Ferreira 2001Moreiraamp Russo 2007) are considered primary causes for the recent increase of fire frequency andextension Changes in fire regimes are expected to provoke profound effects on thebiodiversity and composition of local communities (McKenzie et al 2004) The increase offire risk and activity in recent decades (Pausas amp Fernaacutendez-Munoz 2012) has attractedconsiderable interest mainly addressed to understanding the environmental drivers andeffects of fire especially in the context of global change (Bowman et al 2009 Flanniganet al 2009 Whitlock et al 2010) In the context of a present shift in fire regimes apressing question is whether we are prepared to manage fire regimes and reduce impactsof fire on many ecosystem components (Pausas amp Keeley 2009) An ecologically-basedframework is crucial in the 21st century conservation scenario (Nimmo et al 2015) inorder to understand how species respond to fire and what is the resistance and resilienceof communities towards this disturbance

The response of species to fire is largely driven by habitat structure (Santos Badiane ampMatos 2016) with some species selecting early or late post-fire stages following a continuumalong vegetation succession (Letnic et al 2004 Santos amp Poquet 2010 Valentine et al2012 Santos Badiane amp Matos 2016) The lsquohabitat accommodationrsquo model of successionproposed by Fox (1982) applied to fire ecology represents a useful framework to helpunderstand and predict the response of animals to fire However field-based studies havefailed to support this model (Driscoll amp Henderson 2008 Lindenmayer et al 2008) sincethe responses of species to fire vary in space and time (Driscoll et al 2012 Nimmo et al2012 Smith Bull amp Driscoll 2013) due to the complexity of biotic and abiotic interactionsbetween vegetation dynamics animal species and climate (Nimmo et al 2014) For thisreason to improve predictive models of fire responses in animal communities detailedecological (functional) information on species is needed (Smith Bull amp Driscoll 2013)

Functional approaches have gained acceptance in community ecology due to the possi-bility of quantification and predictive power (McGill et al 2006) Although such analyseshave rarely been applied to fire ecology (ie traits favoured in burnt areas) some recentstudies highlight its importance for predicting the responses of reptiles to fire (see referencesabove) Reptiles are suitable organisms to examine responses to fire following parallelhabitat-based and functional approaches This is due to their sedentary behaviour depen-dence on environment temperature and strait association with habitat (Huey 1982) Whilereptile responses to fire are often considered to be habitat-mediated such association is notnecessarily direct For instance since fire opens the habitat in the short term many reptilesare expected to benefit from the thermal quality of open areas created by fire (Bury2004) Different species however display opposing responses depending on their habitatpreferences biogeographic affinities and life-history traits (Pastro Dickman amp Letnic 2013Smith Bull amp Driscoll 2013 Ferreira Mateus amp Santos 2016 Santos Badiane amp Matos2016) For example in a mixed reptile community composed of Mediterranean andnon-Mediterranean elements Santos amp Cheylan (2013) detected that repeated-fire regimefavoured reptile assemblages composed of Mediterranean species with short lifespan andinsectivorous habits

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As ectothermic and sedentary animals terrestrial reptiles are directly and locally exposedto environmental variation in temperature and humidity which makes them ideal subjectsfor mechanistic ecological modelling (Kearney amp Porter 2009) Specifically their intrinsicphysiological features may potentially govern the response of different species to fire Thusbody temperature is considered the most important environmental variable affectingperformance of ectotherms including reptiles (Angilletta 2010) heat balance resultingfrom thermal characteristics of the environment (Porter et al 1973 Porter amp Tracy 1983)In particular thermoregulatory reptiles respond to thermal heterogeneity by selectingmicrohabitats with adequate temperatures and modifying their body postures to maximizeheat gain or loss However during these processes reptiles also suffer evaporative water loss(EWL) mainly through the skin but also through respiratory passages and the eyes(Shoemaker amp Nagy 1977Mautz 1982a) Since evaporation increases with temperature atrade-off between thermoregulation and water balance in ectotherms has been suggested(Mautz 1982a) EWL could hence represent a constraint for the activity of ectothermswhen water is not available In this context reptiles exposed to unburnt and burnt habitatsare expected to face opposing environmental conditions Under similar climate regimesunburnt habitats providemore abundant and complex vegetation compared to that in openburnt habitats that in turn are more exposed to extreme temporal variations in temperatureand humidity (Ferreira 2015 data from NW Portugal available from the authors uponrequest) Certainly environmental constraints may preclude reptiles from attaining theirphysiological optima (ie Gvoždiacutek 2002) but under the same conditions some species willbe further from their optima than others (Grbac amp Bauwens 2001) Even if such speciesmay still survive under suboptimal conditions in a complex landscape their fitness will beaffected and demographic repercussions are expected (Castilla Van Damme amp Bauwens1999) Thus we hypothesize that reptile species prevailing in unburnt (forested) habitatswill maintain lower and less variable body temperatures and experience lower water lossrates as vegetation buffers daily variation of humidity and temperature (Ferreira 2015) Incontrast reptiles inhabiting burnt (open) habitats will attain higher but temporally variablebody temperatures and suffer higher evaporative water stress

To test this hypothesis we analysed the community of lacertid lizards inhabitingNorthernPortugal a transition zone betweenAtlantic andMediterranean bioregions wherespecies of different biogeographic affinities coexist Lacertids constitute a guild of diurnalheliothermic and mainly insectivorous lizards highly diversified in habitat use (Arnold1987) which dominate reptile assemblages across the Mediterranean basin (Carretero2004) In syntopy species fromboth biogeographic affinities spatially segregate in a gradientfrom forested to openmicrohabitats within patchy and heterogeneous landscapes (FerreiraŽagar amp Santos in press) Results from systematic monitoring during the last decade inburnt and unburnt areas in Northern Portugal and other areas at the northernmost limitof the Mediterranean bioregion agree with microhabitat segregation at a smaller scale Wedetected opposing responses to fire by different speciesmostly related to their biogeographicaffinity NamelyMediterranean species Psammodromuns algirus and Podarcis guadarramaeincreased in abundance in burnt areas whereas the Atlantic species Lacerta schreiberiand Podarcis bocagei decreased (Santos amp Poquet 2010 Santos amp Cheylan 2013 Ferreira

Ferreira et al (2016) PeerJ DOI 107717peerj2107 321

Mateus amp Santos 2016) TheMediterranean lizardTimon lepidusdisplayedmixed responsesdepending on the population Whereas in the northernmost limit of its distribution it wasfavoured by fire (Santos amp Cheylan 2013) in Mediterranean habitats it prefers long-termunburnt sites suggesting negative short-term responses to fire (Santos Badiane amp Matos2016) Based on this empirical evidence we conducted a comparative experimental studyin order to determine whether Mediterranean and Atlantic species responses to fire arecorrelated to their thermal and hydric physiology Two ecophysiological traits were selectedto represent the general speciesrsquo trends preferred body temperature and evaporative waterloss Specifically we tested whether species favoured by repeated fire regimes would bemore thermophile and achieve lower water loss rates than those negatively affected Inthis case we predict that T lepidus P algirus and P guadarramae species that respondpositively should have higher preferred temperatures and lower evaporative water lossthan L schreiberi and P bocagei species that respond negatively

MATERIALS AND METHODSStudy areaThe Iberian Peninsula encompasses a transition region between the Euro-Siberian andMediterranean biogeographic regions (Metzger et al 2005 Soares amp Brito 2007) These bio-geographic crossroads are known as areas of high diversity of species and habitats (Spector2002) The extensive contact between Mediterranean and Atlantic climates leads to a highbiodiversity of plants and animals due to the co-existence of Atlantic and Mediterraneantypical species in sympatry (Arauacutejo Thuiller amp Pearson 2006 Sillero et al 2009) One ofthese transitional areas is found in Northern Portugal (Soares et al 2005) This is one of theareas in Europe with the highest amount of burnt land wildfire is considered a fundamentalagent of landscape change (Silva et al 2011) Transitional zones affected by intense firehistory provide an opportunity to compare the ecological trends of both types of specieseither in a general conservation context (Kati et al 2004) or more specifically to makepredictions on the effects of wildfires on herpetofauna biodiversity (Hooper et al 2005)

Species samplingThe five lacertid species used in physiological experiments are the reptiles most frequentlyfound in the area (Loureiro et al 2008) These species vary in terms of body size habitatpreferences distribution biogeographic affinities and response to fire (Table 1)

Lizards used in experiments were captured with a noose (Garciacute a-Muntildeoz amp Sillero 2010)in three areas P algirus were captured in Serra da Estrela (4051primeN 753primeW) T lepidusand L schreiberi in Vairatildeo (4132primeN 867primeW) and finally P bocagei and P guadarramaesyntopic in Moledo (4184primeN 887primeW) All the sites are located in Northern Portugal andselected according to the availability of lizards

To exclude effects of reproduction body condition and ontogeny on Tp (Carretero Roigamp Llorente 2005) we only captured 6ndash10 adult males during the peak of the reproductiveseason (May) which were kept in individual cages before the experiments with water andfood provided ad libitum We measured body mass (BM) to the nearest 00001 g of eachlizard with a digital balance and snoutndashvent lengths (SVL) to the nearest 001 mm with

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Table 1 General traits of the five lizard species studiedHabitat distribution and biogeographic affinities after Carretero Galaacuten amp Salvador(2015) Galaacuten (2015) Kaliontzopoulou et al (2011) and Loureiro et al (2008) Fire responses after (Santos amp Cheylan 2013 Santos amp Poquet 2010)and Ferreira Mateus amp Santos (2016)

Species Body size Main habitat Distribution Biogeography Fire response

Timon lepidus Very large Open oak forest big rocks Iberia SW France Mediterranean IncreaseLacerta schreiberi Large Ecotones and riverine forests W Iberia Atlantic DecreasePsammodromus algirus Medium Shrubs Iberia SW France N Africa Mediterranean IncreasePodarcis bocagei Small Dunes grasslands walls rocks NW Iberia Atlantic DecreasePodarcis guadarramae Small Rocks crevices W and central Iberia Mediterranean Increase

a digital calliper After a short period of acclimation (1ndash2 days) to prevent lizards losingbody condition (Brown amp Griffin 2003) we submitted them to temperatures and waterloss experiments in two consecutive days and released them at their capture sites after theexperiments had finished and after being fed and rehydrated

The Institute for the Conservation of Nature and Forest (ICNF Portugal) grantedsampling permit (no 459I2015ICAPT) Experiments followed the ethical guidelines ofUniversity of Porto

Preferred temperaturesPreferred body temperature (Tp body temperature achieved in the absence ofthermoregulatory constraints Huey amp Bennett 1987) provides a reliable representation ofthe overall thermal requirements of a given species while holding some logistic advantagesNamely (1) it correlates directly with several physiological optima (Bauwens et al 1995)(2) its temporal variation is relatively narrow in lacertids which are known to be goodthermoregulators (Huey 1982) (3) it displays phylogenetic signal (Bauwens et al 1995) andremains conservative in conspecific populations under different climate regimes in manylacertid species (ie Diacuteaz Iraeta amp Monasterio 2006) and (4) it can be reliably recorded inthe lab under standardised conditions (Osojnik et al 2013) It is true that at the individuallevel Tp may change as a function of time of the day season feeding activity ontogenyor reproductive status (Castilla Van Damme amp Bauwens 1999) but these biases can beremoved by restricting comparisons to a single class (ie adult males) and time period(ie spring) following a strict experimental protocol (Carretero Roig amp Llorente 2005)

Lizards were individually exposed to a photothermal gradient between 20 and 50 Cpro-duced by a 150-W infrared bulb fixed at one end of the terrarium (1times 03times 04 m) (Veriacutes-simo amp Carretero 2009) The whole experiment was conducted in a room with temperaturemaintained at 22 C to prevent wind and direct sun from affecting the temperaturesin the terrarium while being exposed to natural photoperiod through a window For everyday of experimentation we turned on the bulb 1 h before the lizards were moved from thecages to the terrariums and the first observation was made at 8 h

The whole experiment was conducted between 8 h and 19 h local summer time theperiod of daily activity of the five species At consecutive hourly intervals we measuredthe body temperature of each lizard (precision plusmn 01 C) using a k-thermocouple probeassociated with a digital portable thermometer HIBOK 14 inserted into the animals cloaca

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(Veriacutessimo amp Carretero 2009) This standard procedure (Garciacute a-Muntildeoz amp Carretero 2013Osojnik et al 2013) is a compromise between invasiveness and accuracy since at least thetwo Podarcis sp and P algirus are too small to allocate permanent cloacal probes or toimplant transmitters (Clusella-Trullas et al 2007) and too slender to provide accurateinfrared readings (Carretero 2012) While these latter methods could have been usedwith T lepidus and probably with L schreiberi we preferred to keep the same measuringprocedure for all five species for comparative purposes

Water-loss ratesAlthough reptilian hydric ecophysiology is less studied evaporative water loss (EWL) ratesare known to differ between species from xeric and humid habitats (Mautz 1982b Eynanamp Dmirsquoel 1993 Carneiro et al 2015 Rato amp Carretero 2015) and between phylogeneticallydistant species in the same locality (Garciacute a-Muntildeoz amp Carretero 2013 Osojnik et al 2013)Thismakes EWL potentially informative on the hydric constraints of a speciesrsquo fundamentalniche particularly under restricted water availability (Bowker 1993)

Water-loss experiments were always performed the day after the preferred temperatureexperiments when lizards were kept rehydrated in the terraria We placed the lizards inclosed cylindrical plastic boxes (9 cm diameter 10 cm height) with ventilation holes in thetop and at the bottom Then in groups of five boxes lizards were placed into a biggeropaque sealed chamber (40times 30times 20 cm) in dry conditions guaranteed by silica gel Silicagel (sim100 g) was placed in a bag made of gauze and fixed with tape on the bottom of thechamber lid In the same way 5 g silica gel was placed at the bottom of each box containinga lizard The amount of silica gel used guaranteed a low relative humidity inside of eachbox (20ndash25) The experiment ran from 8 am to 8 pm Conditions inside the chamberwere monitored with a Fluke 971 temperature humidity meter (Fluke Corporation EverettWashington) at hourly intervals to ensure stability around sim24 C and 20ndash30 relativehumidity The environmental temperatures represented the lowest activity temperaturesrecorded for most lacertids in the field (Castilla Van Damme amp Bauwens 1999) to preventlizard stress inside the chambers while still providing relevant EWL rates Every hour thelizards were individually removed from the chamber weighted using an analytical balance(precision plusmn 00001 g CPA model 224S Sartorius) and immediately placed back insidetheir respective boxes in the chamber

Statistical analysesOnce ensured that the distribution of Tp and EWL values did not deviate from normality(ShapirondashWilkrsquos test P gt 005 in all cases) and the sphericity assumption was met(Mauchlyrsquos tests P gt 005) analyses for dependent measures were applied since both Tpand EWLwere recorded for the same individual lizards through timeWe first used analysesof (co)variance with repeated measures (AN(C)OVA-rm) to ascertain variation in Tp as afunction of species and time interval (within- subject factor) In a second step lizardsrsquo SVLand body mass were incorporated as covariates to account for the effect of lizard size andshape (Carretero Roig amp Llorente 2005) When significant post hoc Duncanrsquos tests wereperformed between species pairs to detect eventual significant differences For water loss

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Table 2 Number of adult males tested (n) snout-to-vent length (SVL) preferred body temperature (individual mean of 10 time intervals Tp)body mass (BM) and accumulated water loss (within 12 h EWLt ) for the five lizard species

SVL (mm) Tp( C) BM (g) EWLtSpecies n Meanplusmn SE

MinndashMaxMeanplusmn SEMinndashMax

Meanplusmn SEMinndashMax

Meanplusmn SEMinndashMax

14072plusmn 409 327plusmn 03 697208plusmn 52468 00097plusmn 00012T lepidus 6

13166ndash15817 313ndash334 558682ndash857488 00057ndash001309599plusmn 443 334plusmn 04 235756plusmn 25086 00096plusmn 00012

L schreiberi 87166ndash11145 323ndash353 100750ndash319960 00072ndash001627438plusmn 139 350plusmn 01 115727plusmn 09481 00038plusmn 00006

P algirus 86800ndash8000 345ndash357 73401ndash151519 00020ndash000635404plusmn 121 307plusmn 03 35832plusmn 01919 00299plusmn 00024

P bocagei 104964ndash6054 294ndash325 30369ndash48491 00235ndash004995373plusmn 093 315plusmn 02 30744plusmn 01391 00249plusmn 00028

P guadarramae 94988ndash5857 307ndash322 23594ndash37809 00120ndash00377

experiments we also used AN(C)OVA-rm to determine differences in instantaneouswater loss (EWLi = [(WnminusWn+1)W0] where W is the weight) between species andhour intervals adding lizardsrsquo SVL and body mass as covariates We also calculated theaccumulated water loss for the 11 intervals (EWLa= [(W0minusWn)W0] where W is theweight) and compared it between species using AN(C)OVA also with SVL and body massas covariates The interaction between the mean Tp (calculated from 10 time intervalmeasurements) BM SVL and the total amount of water lost after the 12-hour experiment(EWLt = [(W0minusW11)W0]) was assessed by standard multiple regression between species(average of Tp and EWLt by species) and within species All the analyses were performedin Statistica 12 (Statsoft Tulsa OK USA httpwwwstatsoftcom)

RESULTSThe five lizards species (Table 2) differed in SVL (ANOVA F436= 17655 P lt 10minus6) andbody mass (ANOVA F436= 15126 P lt 10minus6) The post-hoc comparisons (Duncan testsP lt 005) confirmed that the two Podarcis species were shorter and lighter followed byP algirus then L schreiberi and finally Timon lepidus the longest and heaviest species Wealso detected interspecific differences in robustness (ANCOVA on mass with SVL as co-variable F435= 2169 P lt 10minus6) T lepidus being the most robust followed by P bocageiP guadarramae and P algirus and finally by L schreiberi which has the most elongatedbody

Preferred temperaturesWe recorded variation in Tp between species time intervals and time profile by species(interaction) (Tables 2 and 3 Table S1) Essentially P algirus selected higher Tp than allother species (Duncan tests P lt 005) of which L schreiberiT lepidus P gaudarramae andP bocagei selected temperatures in gradually decreasing order Such pattern remained whenSVL and BM were used as covariates (Table 3) While time and timespecies variation were

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Table 3 AN(C)OVA-rm of preferred temperatures (Tp) and evaporative water loss rates (instantaneous EWLi and accumulated EWLi) be-tween the five lizard species for 10 and 11 consecutive hours respectively in the ANCOVA-rmwe used snout-vent length (SVL) and bodymass(BM) as covariables

Tp EWLi EWLa

df F P df F P df F P

ANOVA-rmSpecies 4 36 3742 lt10minus6 4 36 1327 10minus6 4 36 3000 lt10minus6

Time 9 324 542 10minus6 10 36 352 00002 10 360 14150 lt10minus6

Timespecies 36 324 273 10minus6 40 360 167 023 40 360 1907 lt10minus6

ANCOVA-rm (SVL BM)SVL 1 34 017 068 1 34 023 064 1 34 050 049BM 1 34 069 041 1 34 003 086 1 34 023 064Species 4 34 2145 lt10minus6 4 34 648 00005 4 34 973 210minus5

Time 9 306 183 006 10 340 057 084 10 340 079 064TimeSVL 9 306 223 002 10 340 057 083 10 340 014 099TimeBM 9 306 196 004 10 340 036 096 10 340 009 099Timespecies 36 306 153 003 40 340 097 052 40 340 697 lt10minus6

also observed patterns were complex (Fig 1) Only P bocagei displayed a clear bimodalvariation with higher Tp selected in the early morning and late afternoon the other speciesonly showing irregular profiles Finally the significant interaction between time and thecovariables indicated that Tp tended to show stronger temporal fluctuations in small lizards(Table 3)

Water-loss ratesUsing ANOVA-rm we also uncovered significant differences in instantaneous water loss(EWLi) between species and through time with a weak interaction between both factors(Tables 2 and 3) Post-hoc Duncan tests (p lt 005) grouped P algirus and T lepidushaving low rates and both Podarcis species having high rates while L schreberi occupied anintermediate position EWLi also varied along time in all species with both Podarcis speciesdisplaying higher temporal fluctuations (Fig 2) When we added SVL and BM as covariates(ANCOVA-rm) interspecific differences were smoother but still significant while temporaldifferences disappeared (Table 3)

Accumulated water loss by evaporation (EWLa) revealed even more marked differencesbetween the five species (Fig 3) Here two clear groups with no overlap could be distin-guished on one side the larger T lepidus and L schreiberi plus the medium-sized P algirusall with low water loss rates and on the other side the small P guadarramae and P bocageiwithmuch higher water loss rates (Duncan post-hoc tests plt 005) Again after accountingfor SVL and bodymass differences between species remain but differences in time intervalsdid not while the interaction between both factors was also conserved (Table 3) Neitherin EWLi nor EWLa did we observe interactions between factors and covariables

Preferred temperatures vs water loss ratesMean Tp and EWLt were inversely correlated between species while SVL and BM hadno influence on the results (n= 5 rpartialTpminusEWLt =minus099 T =minus1472 P = 004

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Figure 1 Daily variation of the preferred body temperatures (Tp) for five lizard species Median valuesand 095 confidence intervals are displayed

Figure 2 Patterns of instantaneous water loss (EWLi) along a 12-hour experiment for five lizardspecies Median values and 095 confidence intervals are displayed

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Figure 3 Accumulated water loss (EWLa) along a 12-hour experiment for five lizard species Medianvalues and 095 confidence intervals are displayed

rpartial SVLminusEWLt =minus094T =minus270P = 023 rpartial BMminusEWLt = 081T = 141P =039) In contrast within species EWLt was positively correlated with SVL negatively corre-lated with BM but independent from Tp for L schreiberi (n= 5 rpartial TpminusEWLt= ndash062T =minus159 P = 019 rpartial SVLminusEWLt = 084 T = 317 P = 003 rpartial BMminusEWLt =minus083 T =minus298 P = 004) and P algirus (n= 5 rpartial Tp minusEWLt = ndash039 T = 084P = 045 rpartial SVLminusEWLt = 090 T = 402 P = 002 rpartial BMminusEWLt =minus086T =minus338 P = 003)We did not detect significant relationships for the other three species

DISCUSSIONThe environmental differences between burnt and unburnt landscapes highlight the roleof vegetation in the buffering of the natural fluctuations Specifically burnt microhabitatsoften used by lizards undergo larger daily variations of temperature and humidity andalso attain higher temperatures especially in summer (Ferreira 2015) When comparinglizards within the same trophic guild this environmental contrast was expected to benefitMediterranean lizards (compared to Atlantic lizards) from the thermal quality of openhabitats created by fire regimes We only have indirect support for this coming from twoindependent sources of evidence (1) in southern France fire recurrence increased theMediterraneity (sensu Prodon 1993) of the reptile community (Santos amp Cheylan 2013)and (2) in multiple localities reptile species tend to be more common in burnt sitescompared to unburnt ones (Santos amp Poquet 2010 Santos Badiane amp Matos 2016)Although we hypothesised that these opposing responses would be caused by divergentecophysiological features our results only partially met our expectations that speciesfavoured by fire should be more thermophile and economic in water loss Certainly the

Ferreira et al (2016) PeerJ DOI 107717peerj2107 1021

Mediterranean medium-sized P algirus clearly selected for higher temperatures than theremaining species and lost less water than expected for its body size However the differ-ences among the other species seem better explained by alternative factors such as refugeuse life history and body sizeshape rather than by their responses to fire

Thermal and hydric ecophysiology showed signs of a sizeshape-independent trade-offacross species but this should be confirmed by a formal analysis under the comparativemethod framework with an extended species dataset (Bauwens et al 1995 Carneiro et alin press) Within species what we found was the influence of the surfacevolumerelationship (Schmidt-Nielsen 1984) causing slender and smaller lizards to lose morewater by body mass unit Thus in ecophysiological terms species were not arranged in aMediterranean-Atlantic axis While the demographic responses to fire of these five lizardsare mostly related to their biogeographic affinities and global distribution ranges (Sillero etal 2009 Santos amp Poquet 2010 Santos amp Cheylan 2013 Ferreira Mateus amp Santos 2016)the lack of complete concordance with their physiological features suggest a more complexscenario This supports previous claims that the functional approach to predict responsesof reptiles to fire is conceptually accurate but predictively weak (Smith et al 2012 SmithBull amp Driscoll 2013)

Psammodromus algirus is considered a species with a wide ecological valence found fromthe border of Sahara inNorthAfrica tomountain oak forests andother humid environmentsin the border of the Atlantic region in Iberia (Loureiro et al 2008) Notwithstanding thatprevious studies reported high preferred temperatures (Bauwens et al 1995) there is alsoevidence of activity under suboptimal thermal conditions (Carretero amp Llorente 1995) It isalso the only species of the five studied with the body covered by keeled overlapping scales(Arnold 2002) Although this scale arrangement is likely the result from an adaptation forlocomotion in bushy vegetation (matrix climbing Arnold 1987) it apparently providesprotection against water loss acting as an exaptation (Gould amp Vrba 1982) whenenvironmental humidity decreases This may have given the species better conditions tosurvive in burnt areas Although the short-term (one year after the fire) response ofP algirus can be negative in some Mediterranean landscapes recovery has been reportedafter two years since fire has been reported (Santos Badiane amp Matos 2016) Post-fire eggmortality (Smith et al 2012) and life history of the species (Carretero amp Llorente 1997) maybe underlaying reasons for these observed patterns

Both large lizard species undoubtedly take advantage from lower water loss rates dueto their lower surfacevolume relationship (Schmidt-Nielsen 1984) However despite theiropposite biogeographic affinities they only differ slightly in hydric physiology whichmakesit difficult to interpret their responses to fire (Santos amp Cheylan 2013 Ferreira Mateusamp Santos 2016) Instead the variable responses of T lepidus according to the populationstudied and the decrease of L schreiberi in response to fire intensification should be betterinterpreted in terms of habitat use Timon lepidus is more mobile and tends to occupy areasdominated by rocky substrates using big rock holes as refuge (Castilla amp Bauwens 1992)In some localities the species occupies long-unburnt (and structured) habitats (SantosBadiane amp Matos 2016) whereas in others only appears in repeated-burnt ones (Santos ampCheylan 2013) This may be due to shifts in other ecological resources (ie habitat prey)

Ferreira et al (2016) PeerJ DOI 107717peerj2107 1121

but also to different fire ages (Nimmo et al 2014) In contrast L schreberi has small homeranges and uses ecotonal bushy vegetation to thermoregulate forage and hide (Salvador1988) keeping its distribution mostly outside of the range of fire We suggest here that thedivergent responses of both species to fire are likely habitat-mediated while shared thermal(and partly hydric) ecophysiology would result from evolutionary convergence in twolong-term separated lacertid lineages (Arnold Arribas amp Carranza 2007) Interestinglycompetitive exclusion between green (Lacerta sp) and ocellated lizards (Timon sp) at ageographic level is suggested to have shaped the historical biogeography of both groups(Ahmadzadeh et al 2016)

Particular habitat requirements may explain why the two species of wall lizards (Podarcissp) show opposing responses to fire but similar physiological features The geographicranges of P bocagei and P gaudarramae widely overlap geographically and both speciesare frequently found in syntopy (Carretero 2008) However field-work experiencedemonstrated that P guadarramae is the only species found in repeatedly burnt spots(Ferreira Mateus amp Santos 2016) This lizard is more associated to bare rocky substratesthan P bocagei which uses a wider variety of substrates (Kaliontzopoulou Carretero ampLlorente 2010) trend that is accentuated in syntopy (Gomes Carretero amp Kaliontzopoulou2016) Since mean preferred temperatures and water loss rates did not differ we interpretthe dominance of P guadarramae after fire intensification as another result of differenthabitat and refuge use In fact head fattening ofP guadarramaemight confer and advantagewhen rock crevices are used as main refuge (Kaliontzopoulou et al 2012) as expected inburnt areas Nevertheless the accentuated diel variation in preferred temperatures by Pbocagei also suggest sensitivity to midday conditions either thermal or hydric which mightprovide some support for a ecophysiological constrain when compared to P guadarramaeThis aspect should be explored in the future with continuous monitoring of individuallizards (Bowker Wright amp Bowker 2010 Bowker Bowker amp Wright 2013)

Fire is a fundamental driver of ecosystem functioning and composition in the Mediter-ranean basin (Blondel et al 2010) Species that are mostly distributed in this bioregionoccupy fire-prone landscapeswith biota likely resulting froma long evolutionary associationwith fire (Pausas amp Keeley 2009) The effects of fire are observable at multiple scales fromthe landscape (variation in land cover) to the microhabitat (variation in temperature andhumidity ranges) As ectotherms the biological and ecological processes of reptiles aredependent on environmental temperature However heliothermic lizards are able tothermoregulate accurately if habitat complexity provides sufficient thermal heterogeneityfor shuttling and selecting appropriate temperatures (Sears amp Angilletta 2015) Despite thesensitivity of reptiles to modifications in habitat structure (caused by fire) factors such aslife historymicrohabitat preferences and or thermoregulatory behaviourmay have deviatedresults from a pure ecophysiological model Further studies should be addressed tounderstand interactions between fire and other processes in order to more accuratelypredict reptile responses to fire-regimes using an extended species dataset Meanwhilecurrent evidence suggests that ecophysiology plays a functional role in reptile responsesto fire which is likely habitat-mediated (Lindenmayer et al 2008 Santos amp Cheylan 2013Nimmo et al 2014)

Ferreira et al (2016) PeerJ DOI 107717peerj2107 1221

Although this is a first approach to a complex topic ecophysiology already appearsrelevant in anticipating reptile responses to fire even if this needs to be complementedby the analysis of other biological traits Future studies should include more species andmore regions to the analysis not only to obtain better statistical support but also toallow phylogenetic correction in order to exclude the effects of long-term evolutionaryhistory Overall our results already indicate that ecophysiology may provide mechanisticunderstanding for how species occurrence and abundance are spatially distributed atdifferent geographic scales and how they may be modified by human impacts (Sinervo etal 2010 Huey et al 2012 Lara-Reseacutendiz et al 2015 Valenzuela-Ceballos et al 2015)

ACKNOWLEDGEMENTSWe thank D Ferreira for sharing her environmental data from Northern PortugalM Sannolo and T Pinto for field assistance and B Presswell for the linguistic revisionof the manuscript

ADDITIONAL INFORMATION AND DECLARATIONS

FundingMiguel A Carretero is funded by FEDER funds through the Operational Programme forCompetitiveness FactorsmdashCOMPETE and by National Funds through FCT (Foundationfor Science and Technology Portugal) under the UIDBIA500272013 and POCI-01-0145-FEDER-006821 Xavier Santos was supported by a post-doctoral grant (SFRHBPD731762010) from FCT under the Programa Operacional Potencial HumanomdashQuadro deReferecircncia Estrateacutegico Nacional funds from the European Social Fund and PortugueseMinisteacuterio da Educacatildeo e Ciecircncia This study is funded by FCOMP-01-0124-FEDER-008929 PTDCBIA-BEC1012562008 also from FCT The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsFCT UIDBIA500272013 POCI-01-0145-FEDER-006821 SFRHBPD731762010 andFCOMP-01-0124-FEDER-008929 PTDCBIA-BEC1012562008

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Catarina C Ferreira performed the experiments wrote the paper reviewed drafts of thepaperbull Xavier Santos conceived and designed the experiments wrote the paper reviewed draftsof the paperbull Miguel A Carretero conceived and designed the experiments performed theexperiments analyzed the data contributed reagentsmaterialsanalysis tools wrotethe paper prepared figures andor tables reviewed drafts of the paper

Ferreira et al (2016) PeerJ DOI 107717peerj2107 1321

Animal EthicsThe following information was supplied relating to ethical approvals (ie approving bodyand any reference numbers)

Sampling permit was provided by Institute for the Conservation of Nature and Forest -ICNF (Portugal) Permit numbers 4592015CAPT and 5322015CAPT

Data AvailabilityThe following information was supplied regarding data availability

The raw data has been supplied as a Supplemental Dataset

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj2107supplemental-information

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Castilla AM Bauwens D 1992Habitat selection by the lizard Lacerta lepida in aMediterranean oak forest Journal of Herpetology 227ndash30

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Clusella-Trullas S Terblanche JS VanWyk JH Spotila JR 2007 Low repeatabilityof preferred body temperature in four species of Cordylid lizards temporal vari-ation and implications for adaptive significance Evolutionary Ecology 2163ndash79DOI 101007s10682-006-9124-x

Diacuteaz JA Iraeta P Monasterio C 2006 Seasonality provokes a shift of thermal pref-erences in a temperate lizard but altitude does not Journal of Thermal Biology31237ndash242 DOI 101016jjtherbio200510001

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Driscoll DA Smith AL Blight S Maindonald J 2012 Reptile responses to fire and therisk of post-disturbance sampling bias Biological Conservation 211607ndash1625

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Ferreira D 2015 Genetic and morphological impacts of a repeated fire regime onPodarcis guadarramae Master thesis University of Porto

Ferreira D Mateus C Santos X 2016 Responses of reptiles to fire in transition zones aremediated by bioregion affinity of species Biodiversity and Conservation Epub aheadof print May 13 2016

Ferreira D Žagar A Santos X Uncovering the rules of (reptile) species coexistence intransition zones between bioregions Salamandra In Press

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Galaacuten P 2015 Lagartija de bocage ndashPodarcis bocagei In Salvador A Marco A edsEncliclopedia Virtual de los Vertebrados Espantildeoles Madrid Museo Nacional de Cien-cias Naturales Available at httpwwwvertebradosibericosorgreptilespodbochtml(accessed 15 December 2015)

Garciacutea-Muntildeoz E CarreteroMA 2013 Comparative ecophysiology of two sympatriclizards laying the groundwork for mechanistic distribution models Acta Herpeto-logica 8123ndash128 DOI 1013128Acta_Herpetol-13115

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Gomes V CarreteroMA Kaliontzopoulou A 2016 The relevance of morphology forhabitat use and locomotion in two species of wall lizards Acta Oecologica 7087ndash95DOI 101016jactao201512005

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Grbac I Bauwens D 2001 Constraints on temperature regulations in two sympatric Po-darcis lizards during autumn Copeia 2001178ndash186DOI 1016430045-8511(2001)001[0178COTRIT]20CO2

Gvoždiacutek L 2002 To heat or to save time Thermoregulation in the lizards Zootocavivipara (Squamata Lacertidae) in different thermal environments along analtitudinal gradient Canadian Journal of Zoology 80479ndash492 DOI 101139z02-015

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