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Research ArticleClimate-Related Variation in Body Dimensions withinFour Lacertid Species
Stanislav Volynchik
The Steinhardt Museum of Natural History and National Research Center Department of ZoologyFaculty of Life Sciences Tel Aviv University 6997801 Tel Aviv Israel
Correspondence should be addressed to Stanislav Volynchik stanislav volynchikyahoocom
Received 17 December 2013 Revised 9 April 2014 Accepted 15 April 2014 Published 19 May 2014
Academic Editor Michel Laurin
Copyright copy 2014 Stanislav VolynchikThis is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited
A close relationship between habitat and external morphology is widespread among many animals including reptiles HereI studied the relationship between abiotic environmental conditions and body size of four lacertid species (Phoenicolacertalaevis Ophisops elegans Acanthodactylus boskianus and Mesalina guttulata) occurring in Israel I examined the effect of averageannual temperature and average annual precipitation on body and limb dimensions using linear statistical models Temperature-and precipitation-related geographic clines in body size showed the same trend among all species Females displayed strongerphenotypic response to temperature gradient than conspecific males suggesting a sex-specific effect of natural selection Snout-vent length (SVL) was negatively correlated with temperature supporting Bergmannrsquos rule inO elegans and in female P laevis andA boskianus but not inM guttulataPrecipitationwas positively related to SVL inO elegans andM guttulata and in femaleP laevisand A boskianusThe relative extremity lengths especially hind limb segments generally increase towards hot and dry locationsfollowing Allenrsquos rule Among the Mediterranean region species (P laevis O elegans) the morphological-environmental link withtemperature was stronger than in desert dwellers (A boskianus M guttulata) for which precipitation was the major determinantof spatial variation
1 Introduction
Latitudinal variation in corporeal dimensions has often beenexplained as a response to temperature gradients which arestrong predictors of animalsrsquo external morphology Zoogeo-graphic principles such as Bergmannrsquos and Allenrsquos rules inclassical (thermal) interpretation express the relationshipbetween body size or shape and environmental temperature[1] Therefore the most renowned and generally acceptedexplanation for these rules is based on the heat-conservationhypothesis [2ndash4] reduced surface area-to-volume ratio pro-vides better heat retention in order to reduce body heat lossat low temperatures (Bergmannrsquos rule) Bergmann [5] statedthat in cooler climates large-bodied endotherms with a lowbody surface area to body volume ratio (ie a greater thermalinertia) typically retain body heat better than smaller onesSimilar principles contributing to reduce heat loss underlieAllenrsquos rule [6] which predicted that animals living in colderenvironments tend to have shorter protruding body partssuch as ears tails and limbs Furthermore several authors
[7 8] have shown that the geographical intraspecific variationin corporeal dimensions of homeotherms has been relatedto either ambient temperature or moisture or both On thewhole there is evidence showing the link between phenotypicplasticity and food availability that is the ldquoresource rulerdquo [9ndash11] depending in turn on a complex of climatic (mainlywater- and temperature-related) parameters Yom-Tov andNix [12] concluded that in some Australian mammals pre-cipitation which mostly contributes to primary productionin hot and dry habitats is often better correlated with bodysize than is temperatureTherefore food resources constitutethe major factor determining body size variation RecentlyPincheira-Donoso and Meiri [13] based on an interconti-nental dataset (65 reptile species from Israel Argentinaand Chile) found that for both Israeli and South Americansquamates the resource rule is better predictor of body sizethan temperature
Multiple studies have noted that many tetrapods showsize-latitude gradients Clines in body dimensions havebeen well documented among many mammals reptiles and
Hindawi Publishing CorporationInternational Journal of ZoologyVolume 2014 Article ID 795387 14 pageshttpdxdoiorg1011552014795387
2 International Journal of Zoology
amphibians [14ndash16] In reptiles even earlier investigations[9] based on species assemblages have revealed that ingeneral they do not exhibit noticeable latitudinal trendsalthough some snake taxa show a weak gradient Howeverthe appearance of spatial trends in body size for ectotherms[2] including vertebrates [17ndash19] is still disputed [13 20ndash23]In recent years many studies have tested Bergmannrsquos rule forvarious ectotherm taxa and have found a wide range of pat-terns depicting the connection between body size and envi-ronmental gradient [16 18 24ndash27] Atkinson and Sibly [28]andCruz et al [29] have claimed that some ectotherms followBergmannrsquos rule whereas for other species the oppositepattern is true [30 31] Ashton and Feldman [17] found thatturtles follow Bergmannrsquos rule whereas squamates contrast itCruz et al [29] demonstrated a strong negative temperature-body size gradient among Liolaemus lizard species reflectinga profound effect of thermal inertia at higher latitudes oraltitudes in accordance with Bergmannrsquos rule HoweverPincheira-Donoso et al [20 32] within the same lineage butbased on an enlarged sample size failed to find statisticalsupport for Bergmannrsquos clines and claiming that in theseanimals the evolution of larger bodies in colder areas isdisadvantageous they suggested that it applied exclusivelyto endotherms It is possible that the spatial trends in bodydimensions are influenced by a complex set of both abiotic(eg seasonality and temperature) and biotic (eg intra-and interspecific competition) factors and their interactions[17 18 33] and that no single mechanism can explain them
However to my knowledge some important issuesremain obscure For instance tests of intraspecific body sizeor shape patterns in squamates accounting for gender-specificaspects are scarce because the papers often provide data forthe pooledmale and female samples Taking into account thatreptiles are often sexually dimorphic ([34 35] see also theresults) it is possible that conclusions of some ecogeographicstudies may suffer from biased sampling In this contextmy primary goal is to compare the sexes in respect totheir relationship with climate variables A nonphylogeneticapproachwas used here to test themain hypothesis thatmalesand females facing different thermal and metabolic demandsfollow different patterns in their phenotypic responses toenvironmental gradient Further I evaluate the combinedeffect of temperature and precipitation on body dimensionswithin all the species studied Finally I also focus on species-specific peculiarities in the appearance of environmentallyrelated phenotypic variation Diurnal lizards including arid-zone dwellers bask in large amounts of time especially in themorning hours (personal observations) Under this scenarioI hypothesize that in the desertM guttulata andA boskianuswhich are affected by exposure to extreme daily temperaturefluctuations a smaller size is likely to be preferable Small-bodied individuals may have better heating and cooling abil-ities heating faster after the cold nights and can thus remainactive for longer periods It is generally accepted [36 37] thattemperature is the most important factor influencing lizardsrsquoactivities and that thermal demands play an important role inhabitat selection by reptiles In thewild lizards apply a varietyof strategies to achieve their preferred body temperatureThermoregulation is realized behaviourally through shuttling
between warm and cold sites [38] as well as physiologicallyby altering peripheral blood flow and modifying heart rates[39 40] In addition some species apply ventilatory heat loss[41 42] via evaporation through their mouth or cloaca
In arid areas where the present study mainly took placerainfall as well as temperature is an important factor inanimal ecology including determining food availability andthus also growth rate [11] The dispute over which geographiccomponent determines body sizemostmakes an examinationof the respective influence of temperature- and water-relatedvariables on morphological features timely In the presentstudy I used a range of linear measurements and ratios infour oviparous lizard species in order to determine the corre-lation between morphology temperature and precipitationI examined environmentally induced phenotypic variabil-ity and the validity of ecomorphological patterns such asBergmannrsquos and Allenrsquos rules in four Middle-Eastern wide-ranging lacertid lizards Phoenicolacerta laevis Ophisopselegans Acanthodactylus boskianus andMesalina guttulata
Acanthodactylus and Mesalina species are mainly desertinhabitants while the Phoenicolacerta and Ophisops speciesmostly inhabit theMediterranean region (amoremesic area)In Israel these species occur along pronounced temperatureand rainfall gradients ([43] and see below) which makesthis region a convenient model for examining intraspecificecomorphological variation Thus in Israel mean annualrainfall ranges from sim1000mm in the north to 25mm in thesouth There is a negative north-south gradient in ambienttemperature with annual averages of about 15∘C and 25∘C inthe north and south respectively Another strong climaticfeature is a U-shaped westeast temperature gradient fromthe temperate Mediterranean coast to the colder centralmountain range and the very hot Jordan Valley in the east(Figure 1)The daily and annual temperature fluctuations alsodiffer greatly across Israel
Israel which has a wide range of climates and landscapesincluding mountain regions coastal plains humid valleysrocky deserts and sand dunes is a hotspot of reptile speciesrichness [44] Environmental temperatures (eg extremeannualdiurnal values) and rainfall intensity (Figures 1(a) and1(b)) are markedly different across the distribution ranges ofboth desert and the Mediterranean region species Hencethe appearance of morphological variation in ectothermsis expected to be adjusted by species-specific ecologicalinteractions leading to interspecific differences in body size(or shape) gradient In this context I expect a different linkbetween both abiotic predictors and bodylimb proportionswithin ecologically different lizard species For example tem-perature may be a stronger ecological determinant of body orextremities size variation for P laevis and O elegans living incooler environments than for the desert A boskianus andMguttulata The present study is the first including analyses ofboth Bergmannrsquos and Allenrsquos rules to investigate a functionalconnection between abiotic habitat conditions and the exter-nalmorphology of theMiddle East lacertid lizards it also dis-cusses the functional link between corporeal measurementsand geographic variables The findings are expected to con-tribute to our understanding of the potential importance ofabiotic components as sources of morphological intraspecific
International Journal of Zoology 3
Temperature (∘C)75ndash119119ndash146146ndash161161ndash173173ndash185185ndash196196ndash207207ndash217217ndash228228ndash2424ndash252
3534
33
33
32
31
30
29
28
Egypt
Israel
Mediterranean Sea
Sinai Peninsula
Acanthodactylus boskianus (136ndash235)Mesalina guttulata (136ndash241)Ophisops elegans (90ndash200)Phoenicolacerta laeis (126ndash208)
GulfofSuez
Gulf of
Aqaba
0 15 30 60 90 120
gt252
(km)
(a)
3534
33
33
32
31
30
29
28
Egypt
Israel
Mediterranean Sea
Sinai Peninsula
GulfofSuez
Gulf of
Aqaba
0 15 30 60 90 120
0ndash1010ndash5050ndash100100ndash150150ndash200200ndash250250ndash300300ndash400400ndash500500ndash650650ndash800
(4ndash381)(18ndash525)
(121ndash907)(318ndash780)
Precipitation (mm)
Acanthodactylus boskianus
Mesalina guttulata
Ophisops elegans
Phoenicolacerta laeis
lt800
(km)
(b)
Figure 1 Climatic maps of the studied areas (excluding Turkish localities) (a) Average annual temperature and (b) average annual precipi-tation The ranges of temperature and precipitation for each species are given in brackets
variability in ectothermic vertebrates whose metabolic ratesand life history are greatly affected by environments
2 Material and Methods
21 Samples and Site Locations The observed specimenswere adult males and females of four lizard species (morethan 100 individuals per species) with large geographicranges I measured 679 preserved specimens of four lacertidspecies in the Natural History Museum of the Departmentof Zoology Faculty of Life Sciences Tel Aviv University(TAUM)The specimens had been collected between 1941 and2012 mostly 866 from Israel but some 71 from Egypt (theSinai Peninsula) and 20 specimens from Turkey
The following specimens were collected Phoenicolacertalaevis 104 specimens were collected from Mt Hermon theGolan Heights the Galilee the foothills of Judea and thecoastal plain (Israel) Ophisops elegans 127 specimens werecollected from Israel (Mt Hermon the Golan Heights theGalilee the Judean foothills and the northern and centralNegev) and 20 specimens from Turkey Acanthodactylusboskianus 164 specimens were collected from Israel (theArsquorava Valley and the northern central and southern Negev)and 50 specimens from Egypt (northern Sinai Sinai moun-tains and the western Sinai coastal plain)Mesalina guttulata193 specimens were collected from Israel (the Judean Hillsthe Judean Desert Dead Sea area and the northern centraland southern Negev) and 21 specimens from Egypt (thenorthern Sinai and Sinai mountains)
22 Study Species Phoenicolacerta laevis (Gray 1838) is amedium-sized lizard SVL up to 77mm (according to ourrecords) generally distributed in the Mediterranean land-scape from Turkey to Israel and Jordan This fairly adaptablespecies is found in relatively humid biotopes such as tem-perate forests valleys Mediterranean-type shrub vegetationcultivated fields and gardens ([45 46] pers obs) It is foundfrom 200m below sea level up to 2200m above sea level(TAUM records)
Ophisops elegans (Menetries 1832) is a small slenderlizard The largest specimen in our sample has a SVL of59mm It occurs in open arid plains of the Mediterraneanregion and Central Asia and was found in sparse forestsvegetated rocky hillsides and wadis [46ndash48] Its verticaldistribution ranges from 240m below sea level to 2000mabove sea level (TAUM records)
Acanthodactylus boskianus (Daudin 1802) is a medium-sized lizard with adults up to 88mm SVL It is widespreadin desert and semidesert areas of the Saharo-Arabian regionfrom northern Africa through the eastern Mediterraneanand the Arabian Peninsula to Iraq It inhabits rather hardsubstrate and occupies a wide range of sandy and gravelhabitats It was collected from400mbelow sea level to 1300mabove sea level [46 48 49]
Mesalina guttulata (Lichtenstein 1823) is a rather smallslender lizard with a maximum SVL of 57mm It is widelydistributed in North Africa and south-west Asia It usuallyinhabits desert and semidesert regions with various terrains
4 International Journal of Zoology
prefers hard substrate and scattered rocks and avoids sanddunes [46ndash48] It is found from 350m below sea level to2000m above sea level (TAUM records)
23MorphologicalMeasurements For each specimen Imea-sured the following snout-vent length (SVL) humerus length(HmL) distance from axilla to apex of elbow forearmlength (FaL) distance from elbow apex to apex of wristfemur length (FeL) distance from groin to apex of kneeand tibia length (TbL) distance from apex of knee to heelFrom these total fore limb length (FLL) and total hindlimb length (HLL) which were obtained as the sums ofthe corresponding segment lengths (ie HmL + FaL andFeL + TbL) as well as the limbs-body ratios (HmLSVLFaLSVL FeLSVL TbLSVL) were calculated Tail lengthwas not included in the analysis because many individualshad broken or regenerated tails For each specimen I alsorecorded collection data (region and locality with geographiccoordinates and elevation) as well as bodyweight (119872) whichwas taken shortly after capture to the nearest 01 g Sex wasdetermined by tail base shape and hemipenis eversion or indoubtful cases by dissection Measurements were made witha digital caliper (Mitutoyo CD-610158401015840CX) to the nearest 001mmexcept for SVL which was measured to the nearest 05mmusing a millimeter ruler I could not record all measurementsfrom each specimen due to the bad preservation conditionsof some reptiles so the sample sizes vary among features(Table 1) All measurements were made by the author
24 Meteorological Data The climate elements consideredwere average annual temperature and average annual precip-itation within the natural locations of the animals Spatiallyinterpolated climate data [50] for the 1950ndash2000 period ongrids with spatial resolution of 30 arc-second (often referredto as 1-km spatial resolution) were taken from httpwwwworldclimorg and imported into a GIS application
25 Data Analyses I applied one-way ANOVAwith multipletesting corrections (Duncanrsquos multiple range test MRT) toexamine the presence of sexual size dimorphism (SSD) inbody and limbdimensions in all species studied I used simpleordinary least squares (OLS) regression model treating tem-perature and precipitation as continuous predictors to assessthe relationship between abiotic environmental componentsand morphological traits In this analysis the examinedsamples suppose a great dispersion of the data that cannotbe addressed with log-transformations In fact both bodysize ranges within the samples and the sample sizes acrossthe observed locations vary among the species Howeverprior to analyses the data were tested for normality (Shapiro-Wilkrsquos test) and homogeneity of variances (Levenersquos test)As argued in the Introduction testing the possible presenceof intraspecific clines requires that sexual size dimorphismwithin the species studied to be taken into account Inview of these considerations relationships between abioticvariables and the measurementsratios were tested for eachsex separately I also controlled for the effect of temperatureand precipitation on limb length (for each sex separately) byMANCOVA using SVL as a covariate In this analysis both
abiotic factors treated separately as categorical predictors andtotal fore limb length (FLL) and total hind limb length (HLL)as dependent variablesMultiple ordinary least squares (OLS)regression analysis using SVL as a dependent variable andtreating climatic factors as predictors was applied to examinethe combined effect of temperature and precipitation on bodysizeHere in order to produce amoremeaningful index of theobserved effects the slope coefficients were transformed intostandardized ldquobetardquo coefficients (120573) All statistical analyseswere done using Statistica 8 (StatSoft Inc USA)
3 Results
31 Sexual Dimorphism Summary data of basicmorphologi-cal features for males and females of each species are given inTable 1 Simple intersexual comparisons (one-way ANOVA)of the lizardsrsquo external morphology indicate that male Oelegans andA boskianus are significantly (119875 lt 00001) longerand heavier than females (Table 1) In M guttulata femalesare longer but not heavier than males In P laevis malesare marginally nonsignificantly heavier than females but notlonger
Moreover there is a pronounced sexual dimorphism (119875 lt00001) in extremity length Within all the species studied inabsolute terms (mm) HmL FaL FeL and TbL in males weremuch greater (from 73 to 136) than those in conspecificfemales Assessing the ratios of fore and hind limbsrsquo segmentsrelative to SVL (ie HmLSVL FaLSVL FeLSVL andTbLSVL) made very little difference (data not shown)
32 Environment-Related Variation
P laevis The studied locations are characterized by a highlysignificant correlation between latitude and both temperature(119903 = minus0607 119875 lt 00001) and precipitation (119903 = 0879119875 lt 00001) and between temperature and precipitationsas well (119903 = minus0732 119875 lt 00001) Considering body sizegradient the scatter plots shown in Figure 2 indicate thatalthough the individuals exhibit a notable dispersion (it isalso true for other species studied) the major trends becomeevident Male SVL does not vary significantly in relation toclimate (temperature OLS slope plusmn SE = minus025 plusmn 045 119903 =minus0081 119875 = 0585 precipitation slope = minus0001 plusmn 0006119903 = minus0032 119875 = 0827) whereas females are greatly affectedby it growing significantly heavier and longer (Figures 2(a)and 2(b)) in cool and wet habitats (temperature slope =minus147 plusmn 031 119903 = minus0543 119875 lt 00001 precipitation slope =001 plusmn 0004 119903 = 0369 119875 = 0005) Continuous sampling(Table 2) revealed a stronger effect of climate on corporealproportions than on absolute sizes Analysis of latitudinalvariability in body proportions showed a significant relation-ship between temperature and relative extremities length Inboth sexes relatively larger limbs are associated with hothabitats among females the recorded temperature-relatedcorrelation was highly significant for these morphologicalvariables The influence of precipitation was less obviousalthough in females it was still significant for all ratios Inmales only HmLSVL varied in relation to precipitationWith SVL as a covariate however a MANCOVA indicates a
International Journal of Zoology 5
Table 1 Morphological characteristics of lizard species studied and their intersexual comparisons (one-way ANOVA with multiple testingcorrections Duncanrsquos multiple range test MRT)
Species Features Range Mean plusmn SD nDDCC
119875 119865
DD CC DD CC
Phoenicolacertalaevis
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
25ndash105505ndash7753ndash9
59ndash932762ndash1184875ndash13
3ndash11450ndash76
522ndash73459ndash7877ndash10585ndash114
585 plusmn 191
6353 plusmn 665699 plusmn 079
761 plusmn 077
966 plusmn 103
1104 plusmn 102
513 plusmn 194
6297 plusmn 601
634 plusmn 047
696 plusmn 046
878 plusmn 063
987 plusmn 062
485648564756475647564756
0059065400001000010000100001
3620202636284927405101
Ophisops elegans
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
09ndash4240ndash59445ndash61478ndash67253ndash872715ndash1053
12ndash3540ndash53539ndash54423ndash62252-747646ndash922
25 plusmn 072
4807 plusmn 427
53 plusmn 04
582 plusmn 05
722 plusmn 071
9 plusmn 081
198 plusmn 051
4647 plusmn 344
466 plusmn 035
515 plusmn 041
629 plusmn 057
778 plusmn 063
856285628461846184618461
lt000010016lt00001lt00001lt00001lt00001
23225859838732069119538
Acanthodactylusboskianus
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
17ndash13852ndash8852ndash918592ndash992845ndash1338108ndash164
3ndash12150ndash805462ndash7358ndash84883ndash122810ndash1454
699 plusmn 215
659 plusmn 646
69 plusmn 075
796 plusmn 079
112 plusmn 104
1377 plusmn 119
535 plusmn 163
6111 plusmn 583
626 plusmn 056
712 plusmn 062
981 plusmn 075
1212 plusmn 087
121931219311385113851148511485
lt00001lt00001lt00001lt00001lt00001lt00001
37233131433365571086211606
Mesalinaguttulata
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
08ndash640ndash57413ndash5945ndash624595ndash82717ndash967
116ndash3740ndash5639ndash5442ndash56557ndash776664ndash88
204 plusmn 063
4561 plusmn 301
5 plusmn 031
534 plusmn 03
707 plusmn 046
839 plusmn 045
201 plusmn 056
469 plusmn 373
462 plusmn 029
495 plusmn 03
652 plusmn 041
763 plusmn 044
98791199511895118951189511895
07480005lt00001lt00001lt00001lt00001
01078078228409796115251
80
76
72
68
64
60
56
52
4814 15 16 17 18 19 20 21
SVL
(mm
)
Average annual temperature (∘C)
(a)
80
76
72
68
64
60
56
52
48
SVL
(mm
)
300 350 400 450 500 800550 600 650 700 750
Average annual precipitation (mm)
(b)
Figure 2 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Phoenicolacerta laevissolid line with circles males dashed line with triangles females
statistically significant effect of temperature on both FLL andHLL in females (Table 3) The results of multiple regressionwith SVL as a response (Table 4) indicate that the body size-environment link is more obvious in respect to temperaturethan to precipitation Thus in females SVL is much moreaffected by the former variable 119875 = 00009 120573 = minus061 plusmn 017than by the latter 119875 = 0588 120573 = minus009 plusmn 017
O elegans Examination of the environmental relationshipacross the observed area of thismostlyMediterranean species
demonstrates a highly significant correlation between latitudeand both temperature (119903 = minus0801 119875 lt 00001) and pre-cipitation (119903 = 0433 119875 lt 00001) Temperature is negativelycorrelated with precipitation (119903 = minus0388 119875 lt 00001)Snout-vent lengths (Figures 3(a) and 3(b)) of both sexesincrease with temperature (males slope = minus072 plusmn 018 119903 =minus0402 119875 = 00001 females slope = minus049plusmn014 119903 = minus0408119875 = 0001) and with precipitation (males slope = 0007 plusmn0001 119903 = 0395 119875 = 00002 females slope = 0005 plusmn 0001119903 = 0374 119875 = 0002)
6 International Journal of Zoology
Table 2 Climate-morphology relationship between average annual temperature (AAT)average annual precipitation (AAP) and bodymeasurementsratios (regression analysis with temperature and precipitation as the predictors and features as the responses) Positivecorrelation (+) and negative correlation (minus) single sign significant difference (119875 lt 005) and double sign highly significant difference (119875 lt00001)
FeaturesPhoenicolacerta laevis Ophisops elegans Acanthodactylus boskianus Mesalina guttulata
AAT AAP AAT AAP AAT AAP AAT AAPDD CC DD CC DD CC DD CC DD CC DD CC DD CC DD CC
M minus + minus + + + +SVL minusminus + minus minus + + minus + + +HmL minus minus + ++FaL minus minus + + +FeL minus minus ++ +TbL minus minus + +HmLSVL + ++ minus minus + minus minus +FaLSVL + ++ minus + minusminus minus +FeLSVL + ++ minusminus + + + minus minus + minus minus
TbLSVL + ++ minus + minus minus + minus minus
Table 3 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Phoenicolacerta laevis with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
77
88
052111
079152
145149
243333
02140199
00280004
Covariate(SVL)
FLLHLL
11
11
73211275
23494734
20171707
71641038
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
033276
404766
093371
12321679
03410062
lt0001lt0001
Error FLLHLL
3737
4646
036074
033045
Precipitation FLLHLL
88
88
047099
064150
126130
187327
02940275
00880005
Covariate(SVL)
FLLHLL
11
11
71081208
21624677
19131582
62751017
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
030296
493798
081388
14331738
03740056
lt0001lt0001
Error FLLHLL
3636
4646
037076
034045
Table 4 The effect of climate variables on snout-vent length (SVL) Results of multiple regression with SVL as a dependent variable andclimatic factors as predictors
Effect of temperature Effect of precipitation120573 plusmn SE 119905 119875 120573 plusmn SE 119905 119875
Phoenicolacertalaevis
DD minus021 plusmn 021 minus098 0328 minus018 plusmn 021 minus085 0399CC minus0615 plusmn 017 minus351 00009 minus009 plusmn 017 minus054 0588
Ophisops elegansDD minus027 plusmn 011 minus251 0013 026 plusmn 011 238 0019CC minus032 plusmn 012 minus266 0009 025 plusmn 012 208 0041
Acanthodactylusboskianus
DD minus003 plusmn 009 minus034 0727 0136 plusmn 009 137 0207CC minus013 plusmn 011 minus115 0251 021 plusmn 011 minus177 0079
Mesalina guttulata DD minus003 plusmn 009 minus041 068 021 plusmn 009 236 0019CC minus014 plusmn 009 minus151 0134 033 plusmn 009 339 0001
International Journal of Zoology 7
SVL
(mm
)
Average annual temperature (∘C)
60
56
52
48
44
40
8 10 12 14 16 18 20
(a)
SVL
(mm
)
60
56
52
48
44
40
100 200 300 400 500 700 800600 900
Average annual precipitation (mm)
(b)
Figure 3 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Ophisops elegans solidline with circles males dashed line with triangles females
The corporeal ratios and especially lengths (Table 2)are noticeably influenced by the local climate conditionsRegression analysis indicates that the sexes generally followsimilar trends in their corporal dimensions and becomesignificantly larger at higher latitudes By analogy with SVLappendages were positively correlated with precipitation andwere negatively correlated with temperature In additionin both sexes the longer femora may be associated withincreased precipitation However after accounting for SVLa MANCOVA reveals a nonsignificant effect of both abi-otic predictors on limb size (Table 5) Multiple regressiondemonstrates the equivalency of two climate influences intheir relationships with SVL (Table 4) Furthermore malesand females in general did not differ from one another intheir responses to either temperature (120573 = minus027plusmn011 versus120573 = minus032 plusmn 012) or precipitation (120573 = 026 plusmn 011 versus120573 = 025 plusmn 012) gradient
A boskianus In the desert habitats of this species temperaturewas uncorrelated with latitude (119903 = minus0082 119875 = 0247)across the observed geographic range There is however apronounced latitudinal precipitation gradient (119903 = 0815119875 lt 00001) and a negative relationship between annualaverages of temperature and precipitation 119903 = minus0367 119875 lt00001 In this lizard the sexes differ in respect to theirenvironmental-morphological connection (Figures 4(a) and4(b)) The SVL of males did not correlate consistently withtemperature (slope = minus021 plusmn 029 119903 = minus0067 119875 = 0485)and precipitation (slope = 001 plusmn 0008 119903 = 0134 119875 =0160) whereas the SVL of females varied in relation to thesevariables slope = minus081 plusmn 034 119903 = minus0243 119875 = 0021 andslope = 002 plusmn 0007 119903 = 0280 119875 = 0007 for temperatureand precipitation respectively
Corporeal measurements (Table 2) showed a close rela-tionship with rainfall in both sexes and increased precip-itation is correlated to shorter extremities relative to SVLDespite the fact that the appendages tend to lengthen relativeto their SVL with rise in temperature this abiotic component
would seem to affect only hind limb segments (FeL and TbL)The MANCOVA results (Table 6) also suggest that withinboth sexes the temperature gradient significantly contributesonly to HLL variation Precipitation had a significant effecton hind extremity in both sexes furthermore within males itinfluenced the variation in FLL as well Analysis of combinedeffect of environmental variables when both temperature andprecipitation were regressed against SVL (Table 4) revealsthe role of moisture as a major predictor of intraspecificvariability Moreover males and females were similar in thistrend 120573 = minus003 plusmn 009 (temperature) 120573 = 0136 plusmn 009(precipitation) for males and 120573 = 013 plusmn 011 versus 120573 =021 plusmn 011 for females respectively
M guttulata The studied geographic range of this desertlacertid is characterized by a highly significant correlationbetween latitude and both temperature (119903 = 0657 119875 lt00001) and precipitation (119903 = 0682 119875 lt 00001) whereastemperature was uncorrelated with precipitation (119903 = 0030119875 = 0654) In both sexes SVL (Figures 5(a) and 5(b))increased along a rainfall gradient slope = 0006 plusmn 0002 119903 =0215 119875 = 0018 for males slope = 001 plusmn 0004 119903 = 0317119875 = 0001 for females Continuous sampling also revealed aninsignificant relationship between temperature and SVL inthis species Regression analysis (Table 2) indicated an impor-tant role of precipitation in the creation of clines in body andlimb dimensions Moreover spatial changes of both climaticcomponents may induce some allometric shifts in latitudinalspace Thus temperature rise has led to the appearance oflonger (relative to SVL) extremities among females Thisobservation was confirmed by MANCOVA a significantassociation was observed between either FLL or HLLandtemperature as well as between HLL and precipitation Inmales this approach however indicates a nonsignificanteffect of both climatic variables on limb dimensions (Table 7)
Similarly to other desert dwellers (A boskianus) in thisspecies too precipitation level is a stronger ecological deter-minant of body length (Table 4) than temperature gradient
8 International Journal of Zoology
Table 5 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Ophisops elegans with SVL as a covariate
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
1717
1616
012048
026071
081121
140147
06720278
01860155
Covariate(SVL)
FLLHLL
11
11
25225696
5291525
16331432
28643183
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
101138
251265
651347
1359552
00130067
00010023
Error FLLHLL
6565
4242
015039
018047
Precipitation FLLHLL
2323
1717
013056
024064
083156
129130
06730086
02430241
Covariate(SVL)
FLLHLL
11
11
21864902
5341481
14061366
28222971
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
123201
263305
796559
1393612
00060021
00010018
Error FLLHLL
5959
4141
015035
018049
14 16 18 20 22 24
SVL
(mm
)
Average annual temperature (∘C)
85
80
75
70
65
60
55
50
(a)
SVL
(mm
)
85
80
75
70
65
60
55
50
0 50 150 200100 250 300
Average annual precipitation (mm)
(b)
Figure 4 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Acanthodactylusboskianus solid line with circles males dashed line with triangles females
119875 = 0019 120573 = 021plusmn009 versus119875 = 0680 120573 = minus003plusmn009for males 119875 = 0001 120573 = 033 plusmn 009 versus 119875 = 0134120573 = minus014 plusmn 009 for females respectively
4 Discussion
Despite the inability of ectotherms to produce significantmetabolic heat the interaction between body size and heatbalance based on a set of behavioural anatomical andphysiological mechanisms [51] that contribute to fitnessmight explain the peculiarity of ecological drivers in sizeclines among these animalsThe relationship between habitatconditions and morphological variables (body tail or limbdimensions) and consequent shifts in phenology due toclimate change have been observed across a wide range ofreptile taxa [52ndash54] It is possible that in diurnal squamates
environmental conditions may favour selection for smaller-sized individuals [55] which due to the ability to achievemore accurate adjustment of their body temperature havebetter thermoregulatory capacities [56] and thus display highactivity levels In terrestrial ectotherms thermoregulation isrealized behaviourally by habitat selection and daily activitypattern [57] while at the same time morphological special-ization may also essentially facilitate it [55] For exampleShine and Madsen [58] pointed out that for relatively smallreptile species behavioural thermoregulation seems to bemore important especially in conditions of high diurnalthermal heterogeneity In this context desert reptiles inhab-iting warmer regions with lower thermoregulatory costs mayadjust their body temperature mainly behaviourally andthus invest less in adjustment of either body size or shapein relation to ambient temperature Despite the great data
International Journal of Zoology 9
Table 6 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Acanthodactylus boskianus with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
3535
2828
089151
053131
141191
125175
01180012
02390040
Covariate(SVL)
FLLHLL
11
11
60441731
34366125
95262186
80188176
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
203445
4952911
320562
11563885
00780021
0001lt0001
Error FLLHLL
6565
5151
063079
042074
Precipitation FLLHLL
3333
3131
086151
046116
178186
101171
00230016
04810049
Covariate(SVL)
FLLHLL
11
11
64151792
23944222
13182201
51436151
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
161422
7043482
332518
15145073
00730026
lt0001lt0001
Error FLLHLL
6767
4848
048081
046068
14 16 18 20 22 24
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
Average annual temperature (∘C)
(a)
0 50 150 200100 250 300 350 400 450 500 550
Average annual precipitation (mm)
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
(b)
Figure 5The relationship between SVL and (a) average annual temperature and (b) average annual precipitation inMesalina guttulata solidline with circles males dashed line with triangles females
dispersion (as shown in the scatter plots) it was foundthat among the two ldquodesertrdquo species studied (M guttulataand A boskianus) only females of the latter were smallerin hot temperatures whereas in both sexes of the formeras well as in A boskianus males SVL did not correlatewith temperature In the Mediterranean region P laevisand O elegans inhabit cooler climates than the desert Aboskianus and M guttulata In these environments largergravid reptiles in addition to the buffering effects of thebehavioural thermoregulation supplied by the mother [5960] can provide greater temperature stability during thepreoviposition period Volynchik [19] however found that alarge-bodied local viper (Vipera palaestinae) with a Mediter-ranean distribution pattern does not follow Bergmannrsquos ruleor its converse At the same time the most ldquocold-lovingrdquolizard (O elegans) in my own sample obeyed Bergmannrsquos
rule growing larger in cooler environments On the otherhand in desert habitats this pattern of greater thermal inertiaseems to be less important and the behavioural componentof thermoregulation becomes paramount
The impact of ambient temperature on external mor-phology is also significant in respect to relative extremitylengths different degrees of intraspecific variability in limbproportions supporting Allenrsquos rule were observed in all thespecies studied The present findings indicate that temper-ature decrease across the observed habitats could lead toreduction in size of extremity segments relative to bodylength thus constituting a compensatory adaptation to eithercooler or hotter areas I noted an allometric shift in humerusforearm femur and tibia lengths relative to SVL along atemperature gradient among P laevis A similar relationshipbetween average annual temperature and corporeal ratioswas
10 International Journal of Zoology
Table 7 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) inMesalina guttulata with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
2525
2424
021045
024054
156143
181191
00650110
00290019
Covariate(SVL)
FLLHLL
11
11
20084405
9872011
14751407
72797114
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
4501082
8922073
33113455
65837331
lt0001lt0001
lt0001lt0001
Error FLLHLL
9191
6969
013031
013028
Precipitation FLLHLL
2828
2525
019041
022056
142129
162211
01070181
00590008
Covariate(SVL)
FLLHLL
11
11
19504181
9631908
14091307
68667094
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
356901
8021918
25752817
57177133
lt0001lt0001
lt0001lt0001
Error FLLHLL
8888
6868
013032
014026
noted in females of M guttulata Among A boskianus totalhind limb length significantly correlated with both thermalregime and rainfall gradient Hence both Mediterraneanand desert reptiles follow a similar pattern in their bodyshape variation and may benefit from various morphologicalmodifications matched to habitat range
Body temperature changes affect reptile ecology [61]becoming more important to ectotherms living in coolerenvironments which complicate attaining proper body tem-perature [58 62] In support of this my results show the asso-ciation between biogeographic origins of the species exam-ined and their relationship with environmental variables Oninterspecific comparison the most pronounced distinctionswere noted in phenotypic responses to the temperature gra-dient between Mediterranean and desert inhabitants whilethe between-species differences for precipitation-related vari-ation were weaker As expected both Mediterranean regionspecies (P laevis O elegans) display significantly strongerresponses to temperature than desert dwellers (A boskianusM guttulata) Apparently the cooler locations of the formerforce them to exhibit more consistent morphological vari-ability in respect to temperature changes whereas for desertspecies such habitat-morphology connection seems to be lessimportant It is highly likely that the speciesrsquo sensitivity tothe environment is associated not only with their ecologicaldifferentiation but also with body size ranges within thesample Thus this might be one possible explanation for thedifferent albeit relatively minor responses to temperaturebetween ecologically similar species (ie P laevis versus Oelegans andA boskianus versusM guttulata) that were notedhere In the examined samples L laevis owing to its greatermeasurement ranges than O elegans has a higher potentialfor more consistent matching of its body dimensions to theobserved temperature gradient The same is true for the twodesert lizardsA boskianus due to its extended body and limb
ranges in comparison with M guttulata displays a strongermorphological-environmental link
The examination of gender-specific habitat-morphologyinteractions revealed that within three of the four species (Plaevis A boskianus and M guttulata) sensitivity to the envi-ronment is coupledwith sex Considering the effect of climatevariables on SVL the findings demonstrate that females ingeneral show a more consistent link between temperatureand bodylimb measurements than males while the effectof precipitation on external characters was similar for bothsexes Moreover in P laevis SVL was significantly morestrongly correlated with the temperature gradient in femalesthan in malesThese observations indicate the sex-associatedeffect of natural selection pointing to different thermal andmetabolic demands inmales and femalesThus it is likely thatin females the increased body size in colder environmentsis associated with reproduction-induced requirements Thispattern suggests that females due to increased thermalrequirements particularly during vitellogenesis [63] aremore able to generate a range of suitable morphologicalmodifications for maintenance of optimal body temperaturein local environments Overall my findings indicate thatalthough females show amore consistent correlation betweenSVL and a temperature gradient than males the body shapechanges involving both body and limb dimensions arerather preliminary in explaining the observed intersexualdivergence in the habitat-morphology relationship
Environmental conditions within the nest experiencedduring early ontogenesis especially temperature and mois-ture of substrate can significantly affect development andgrowth trajectories of individuals in oviparous reptiles [64ndash68] As observed in many species either posthatching phe-notype or offspring fitness are closely associated with thermalregime [63 69ndash71] In both the laboratory and in naturalnests [64] temperature is traditionally considered to be animportant environmental determinant of reptile size while
International Journal of Zoology 11
the effect of water-related factors is more complex Severalrecent studies have tested the effect of substrate moistureduring incubation of eggs on a diverse range of reptile speciesSignificant effects are found in certain species [66 68 72 73]but not in others [74ndash76] that may reflect either differentwater permeability of the eggshell or interspecific variationin the water content of eggs [77] On the other hand theappearance of morphological variation along a precipitationgradient which in desert lizards is even more evident thanthe temperature-related variability can be considered as aresponse to the local habitats In reptiles food availabilitystrongly affects growth trajectories and is one of the possibledeterminants of body size and shape [78ndash80] Overall inarid regions where vegetation and arthropod fauna aredetermined primarily by precipitation [11] wetter localitiesprovide better food resources to lizards at the populationlevel The present findings suggest that among desert speciesthe possible spatial differences in prey availability and thusin nutrition levels may lead to morphometric differentiationbetween specimens inhabiting dry or wet sites Howeverdetailed studies on possible dietary variation linked tolocal environments are necessary to answer the question ofwhether the habitat conditions which are dependent on pre-cipitation have an effect on body dimensions in these lizards
A nonphylogenetic approach suggests that lizard speciestend to exhibit strong morphological specialization in rela-tion to their habitat [53 81] Variation in body charactersrelated to locomotion which in turn is associated withsubstrate pattern has been observed across many lizard taxa[54 82ndash84] Unfortunately based on available datasets Icould not evaluate whether the shift in substrate usage isassociated with limb proportion changes and so a rationalexplanation for the effect of vegetation on limb lengthsthrough its dependence upon hydrothermal regime remainsto be determined My findings show that generally theexamined species indicate a uniform pattern in extremitiessize variation fore and especially hind limb lengths werepositively correlated with temperature and negatively withprecipitation The results indicate that ecological adaptationto abiotic factors is a powerful source of extremity sizevariation which is under the effect of natural selection Inlizards the morphology-performance relationships suggestthat ground-dwelling species from open landscapes shouldpossess relatively long limb segments to their body length[53] This body shape pattern increases stride length provid-ing better sprinting abilities [85 86] Furthermore shorterextremities may facilitate the locomotion in highly vegetatedareas where long limbs may be disadvantageous [53] In thiscontextmyfindings suggest that various body shape patternssuch as relatively shortlong limbs or their segments whichare suited to the environmental requirements may reflect anadaptation to either dense or sparse vegetation resulting fromdifferent rainfall intensities across the distribution range
Finally given the potential importance of habitats forlimb size variation lizardsmay also use their protruding bodyparts as additional (together with body surface area) heatexchangers In these reptiles for optimal balance betweenheat gain and heat loss isometric size changes to a certainextent are a ldquotwo-edged swordrdquo inwhich high thermal inertia
of large bodies is accompanied by slow heating rates and viceversa In this respect among desert dwellers relatively longextremities and small size enhance heat exchange and seemto be a morphological adaptation for effective thermoreg-ulation In desert areas large daily fluctuations of temper-ature force the ectotherms to quickly respond to changingconditions and rapidly reach the necessary metabolic ratesfor locomotor activity Long-limbed individuals which havean increased surface area-to-volume ratio may enhancetheir heating and cooling abilities through more effectiveinteractions between the body and either solar radiationor surface temperature gradient Hence a consistent linkbetween environmental variables and limb lengths can alsobe explained by their importance for maintenance of optimalbody temperature in local environments As shown above thefact that the extremity size-environment link is more obviousin respect to hind limbs than to fore ones reinforces thishypothesis relatively large hind limbs having an increasedheat exchange capacity are much more powerful tool foreffective thermoregulation than small fore extremities
In summary the lacertid lizards I studied generallyfollowed the ecogeographic rules of Bergmann and AllenIn addition the findings indicate both intersexual and inter-specific differences in the habitat-morphology relationshipwhich can be considered within the framework of theirfunctional connectionMydata provide evidence that femalestend to show stronger relationships between climate vari-ables and body dimensions than males In desert speciestemperature has a smaller effect than rainfall on lizardphenotypes Under a constant dry climate water availabilityseems to be the most important abiotic factor in reptileecology In this respect due to the strong association betweenprecipitation and productivity my findings could also beinterpreted as evidence for the hypothesis that different bodysize patterns are linked to the spatial variation in primaryproduction that is the ldquoresource rulerdquo In the Mediterraneanregion lizards the thermal regime is apparently the maindriving force of morphological variability The present studysuggests a complex link between environmental variablesand morphological characters within lacertid species Thephysical conditions such as temperature and precipitationgradient were shown to be able to significantly affect bothbody and limb dimensions and thus as a powerful sourceof variation they play an important role in lizard mor-phology However general statements about the habitat-morphology relationships and their potential importance formaintenance of optimal body temperature in reptiles arehard to make due to the enormous diversity of variationsin body composition and physiology across species sexesand even individuals and the difficulty in evaluating enoughmechanisms in enough species Consequently additionalfield and experimental studies testing both body size andshape variations and their relationships with environmentalvariables especially at the intraspecific level and accountingfor sex-specific aspects are needed to help determine whetherthe observed patterns are common across species and to whatextent they are important for effective thermoregulation
12 International Journal of Zoology
Conflict of Interests
The author declares that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The author would like to thank Shai Meiri for his helpfulcomments on earlier drafts of the paper The author thanksErezMaza for assistancewith data preparationAnat Feldmanfor provision of the GIS-compatible temperature data andNaomi Paz for linguistic editing The author also thanks theIsrael Ministry of Science Culture and Sport for supportingthe National Collections of Natural History at Tel AvivUniversity as a biodiversity environment and agricultureresearch knowledge centre
References
[1] E Mayr Animal Species and Evolution Harvard UniversityPress Cambridge Mass USA 1963
[2] C Ray ldquoThe application of Bergmannrsquos and Allenrsquos rules to thepoikilothermsrdquo Journal of Morphology vol 106 pp 85ndash1081960
[3] TM Blackburn K J Gaston andN Loder ldquoGeographic gradi-ents in body size a clarification of Bergmannrsquos rulerdquo Diversityand Distributions vol 5 no 4 pp 165ndash174 1999
[4] K J Gaston and TM Blackburn Pattern and Process inMacro-ecology Blackwell Malden Mass USA 2000
[5] C Bergmann ldquoUber die verhaltnisse der warmeokonomie derthiere zu ihrer grosserdquo Gottinger Studien vol 3 pp 595ndash7081847
[6] J A Allen ldquoThe influence of physical conditions in the genesisof speciesrdquo Radical Review vol 1 pp 108ndash140 1877
[7] F C James ldquoGeographic size variation in birds and its relation-ship with climaterdquo Ecology vol 51 pp 365ndash390 1970
[8] C D Burnett ldquoGeographic and climatic correlates of morpho-logical variation inEptesicus fuscusrdquo Journal ofMammalogy vol64 no 3 pp 437ndash444 1983
[9] C C Lindsey ldquoBody sizes of poikilotherm vertebrates at differ-ent latitudesrdquo Evolution vol 20 pp 456ndash465 1966
[10] M L Rosenzweig ldquoThe strategy of body size in mammaliancarnivoresrdquo American Midland Naturalist vol 80 pp 299ndash3151968
[11] Y Yom-Tov and E Geffen ldquoGeographic variation in body sizethe effects of ambient temperature and precipitationrdquoOecologiavol 148 no 2 pp 213ndash218 2006
[12] Y Yom-Tov and H Nix ldquoClimatological correlates for body sizeof five species of Australian mammalsrdquo Biological Journal of theLinnean Society vol 29 no 4 pp 245ndash262 1986
[13] D Pincheira-Donoso and SMeiri ldquoAn intercontinental analysisof climate-driven body size clines in reptiles no support forpatterns no signals of processesrdquo Evolutionary Biology vol 40no 4 pp 562ndash578 2013
[14] K G Ashton M C Tracy and A de Queiroz ldquoIs Bergmannrsquosrule valid for mammalsrdquoThe American Naturalist vol 156 no4 pp 390ndash415 2000
[15] S Meiri and T Dayan ldquoOn the validity of Bergmannrsquos rulerdquoJournal of Biogeography vol 30 no 3 pp 331ndash351 2003
[16] K G Ashton ldquoSensitivity of intraspecific latitudinal clines ofbody size for tetrapods to sampling latitude and body sizerdquoIntegrative and Comparative Biology vol 44 no 6 pp 403ndash4122004
[17] K G Ashton and C R Feldman ldquoBergmannrsquos rule in nonavianreptiles turtles follow it lizards and snakes reverse itrdquoEvolutionvol 57 no 5 pp 1151ndash1163 2003
[18] M A Olalla-Tarraga M A Rodrıguez and B A HawkinsldquoBroad-scale patterns of body size in squamate reptiles ofEurope and North Americardquo Journal of Biogeography vol 33no 5 pp 781ndash793 2006
[19] S Volynchik ldquoMorphological variability in Vipera palaesti-nae along an environmental gradientrdquo Asian HerpetologicalResearch vol 3 pp 227ndash239 2012
[20] D Pincheira-Donoso D J Hodgson and T Tregenza ldquoTheevolution of body size under environmental gradients inectothermswhy shouldBergmannrsquos rule apply to lizardsrdquoBMCEvolutionary Biology vol 8 no 1 article 68 2008
[21] R C Stillwell ldquoAre latitudinal clines in body size adaptiverdquoOikos vol 119 no 9 pp 1387ndash1390 2010
[22] S Meiri ldquoBergmannrsquos rulemdashwhatrsquos in a namerdquo Global Ecologyand Biogeography vol 20 no 1 pp 203ndash207 2011
[23] D Pincheira-Donoso ldquoPredictable variation of range-sizesacross an extreme environmental gradient in a lizard adaptiveradiation evolutionary and ecological inferencesrdquo PLoS ONEvol 6 no 12 Article ID e28942 2011
[24] K G Ashton ldquoDo amphibians follow Bergmannrsquos rulerdquo Cana-dian Journal of Zoology vol 80 no 4 pp 708ndash716 2002
[25] M J Angilletta Jr T D Steury andMW Sears ldquoTemperaturegrowth rate and body size in ectotherms fitting pieces of a life-history puzzlerdquo Integrative and Comparative Biology vol 44 no6 pp 498ndash509 2004
[26] C E Oufiero G E A Gartner S C Adolph and T GarlandldquoLatitudinal and climatic variation in body size and dorsalscale counts in Sceloporus lizards a phylogenetic perspectiverdquoEvolution vol 65 no 12 pp 3590ndash3607 2011
[27] S Meiri ldquoEvolution and ecology of lizard body sizesrdquo GlobalEcology and Biogeography vol 17 no 6 pp 724ndash734 2008
[28] D Atkinson and RM Sibly ldquoWhy are organisms usually biggerin colder environments Making sense of a life history puzzlerdquoTrends in Ecology amp Evolution vol 12 pp 235ndash239 1997
[29] F B Cruz L A Fitzgerald R E Espinoza and J A Schulte IIldquoThe importance of phylogenetic scale in tests of Bergmannrsquosand Rapoportrsquos rules lessons from a clade of South Americanlizardsrdquo Journal of Evolutionary Biology vol 18 no 6 pp 1559ndash1574 2005
[30] T AMousseau ldquoEctotherms follow the converse to BergmannrsquosRulerdquo Evolution vol 51 pp 630ndash632 1997
[31] R N Reed ldquoInterspecific patterns of species richness geo-graphic range size and body size among NewWorld venomoussnakesrdquo Ecography vol 26 no 1 pp 107ndash117 2003
[32] D Pincheira-Donoso T Tregenza and D J Hodgson ldquoBodysize evolution in South American Liolaemus lizards of theboulengeri clade a contrasting reassessmentrdquo Journal of Evolu-tionary Biology vol 20 no 5 pp 2067ndash2071 2007
[33] M J Angilletta P H Niewiarowski A E Dunham A Leacheand W P Porter ldquoBergmannrsquos clines in ectotherms illustratinga life-historical perspective with sceloporine lizardsrdquoTheAmer-ican Naturalist vol 164 pp E168ndashE183 2004
[34] M Andersson Sexual Selection Princeton University PressPrinceton NJ USA 1994
International Journal of Zoology 13
[35] F Brana ldquoSexual dimorphism in lacertid lizards male headincrease vs female abdomen increaserdquo Oikos vol 75 pp 511ndash523 1996
[36] E R Pianka ldquoLizard species density in the Kalahari desertrdquoEcology vol 52 pp 1024ndash1029 1971
[37] E R Pianka ldquoSome intercontinental comparisons of desertlizardsrdquoNational Geographic Research vol 1 no 4 pp 490ndash5041985
[38] B H Brattstrom ldquoSocial and thermoregulatory behavior of thebearded dragon Amphibolurus barbatusrdquo Copeia vol 3 pp484ndash497 1971
[39] G C Grigg and F Seebacher ldquoField test of a paradigm hyster-esis of heart rate in thermoregulation by a free-ranging lizard(Pogona barbata)rdquo Proceedings of the Royal Society B BiologicalSciences vol 266 no 1425 pp 1291ndash1297 1999
[40] F Seebacher and C E Franklin ldquoControl of heart rate duringthermoregulation in the heliothermic lizard Pogona barbataimportance of cholinergic and adrenergic mechanismsrdquo TheJournal of Experimental Biology vol 204 no 24 pp 4361ndash43662001
[41] G J Tattersall and R M Gerlach ldquoHypoxia progressivelylowers thermal gaping thresholds in bearded dragons Pogonavitticepsrdquo The Journal of Experimental Biology vol 208 no 17pp 3321ndash3330 2005
[42] D F DeNardo T E Zubal and T C M Hoffman ldquoCloacalevaporative cooling a previously undescribedmeans of increas-ing evaporative water loss at higher temperatures in a desertectotherm theGilamonsterHeloderma suspectumrdquoThe Journalof Experimental Biology vol 207 no 6 pp 945ndash953 2004
[43] S Jaffe ldquoClimate of Israelrdquo inTheZoogeography of Israel Y Yom-Tov and E Tchernov Eds pp 79ndash92 Dr W Junk PublishersDordrecht The Netherlands 1988
[44] U Roll L Stone and S Meiri ldquoHot-spot facts and artifacts-questioning Israelrsquos great biodiversityrdquo Israel Journal of Ecologyand Evolution vol 55 no 3 pp 263ndash279 2009
[45] W Bischoff and J F Schmidtler ldquoNew data on the distributionmorphology and habitat choice of the Lacerta laevis-kulzericomplexrdquo Natura Croatica vol 8 no 3 pp 211ndash222 1999
[46] A Disi D Modry P Necas and L Rifai Amphibians andReptiles of the Hashemite Kingdom of Jordan An Atlas and FieldGuide Edit Chimaira Frankfurt Germany 2001
[47] A Bouskila and P Amitai Handbook of Amphibians andReptiles of Israel Keter Publishing House Jerusalem Israel2001 (Hebrew)
[48] A Bar and G Haimovitch A Field Guide to Reptiles andAmphibians of Israel Pazbar LTD Herzliya Israel 2012
[49] Y L Werner ldquoGeographic sympatry of Acanthodactylus opheo-durus with A boskianus in the Levantrdquo Zoology in the MiddleEast vol 1 pp 92ndash95 1986
[50] R J Hijmans S E Cameron J L Parra P G Jones and AJarvis ldquoVery high resolution interpolated climate surfaces forglobal land areasrdquo International Journal of Climatology vol 25no 15 pp 1965ndash1978 2005
[51] R B Huey ldquoTemperature physiology and the ecology ofreptilesrdquo inBiology of the Reptilia CGans and FH Pough Edsvol 12 of Physiology (C) pp 25ndash91 Academic Press New YorkNY USA 1982
[52] D J Irschick and J B Losos ldquoDo lizards avoid habitats inwhich performance is submaximal The relationship betweensprinting capabilities and structural habitat use in Caribbeananolesrdquo The American Naturalist vol 154 no 3 pp 293ndash3051999
[53] B Vanhooydonck and R Van Damme ldquoEvolutionary relation-ships between body shape and habitat use in lacertid lizardsrdquoEvolutionary Ecology Research vol 1 no 7 pp 785ndash805 1999
[54] J Melville and R Swain ldquoEvolutionary relationships betweenmorphology performance and habitat openness in the lizardgenus Niveoscincus (Scincidae Lygosominae)rdquo Biological Jour-nal of the Linnean Society vol 70 no 4 pp 667ndash683 2000
[55] R B Huey and M Slatkin ldquoCost and benefits of lizard thermo-regulationrdquo The Quarterly Review of Biology vol 51 no 3 pp363ndash384 1976
[56] R D Stevenson ldquoBody size and limits to the daily range of bodytemperature in terrestrial ectothermsrdquoTheAmericanNaturalistvol 125 pp 102ndash117 1985
[57] B W Grant ldquoTrade-offs in activity time and physiologicalperformance for thermoregulating desert lizards Sceloporusmerriamirdquo Ecology vol 71 no 6 pp 2323ndash2333 1990
[58] R Shine and T Madsen ldquoIs thermoregulation unimportant tomost reptiles An example using water pythons (Liasis fuscus)in tropical AustraliardquoPhysiological Zoology vol 69 pp 252ndash2691996
[59] R Shine ldquoReptilian viviparity in cold climates testing theassumptions of an evolutionary hypothesisrdquo Oecologia vol 57no 3 pp 397ndash405 1983
[60] C R Peterson A R Gibson andM E Dorcas ldquoSnake thermalecology the causes and consequences of body temperaturevariationrdquo in Snakes Ecology and Behavior R A Seigel and J TCollins Eds pp 241ndash314 McGraw-Hill New York NY USA1993
[61] R B Huey and J G Kingsolver ldquoEvolution of thermal sensitiv-ity of ectotherm performancerdquo Trends in Ecology and Evolutionvol 4 no 5 pp 131ndash135 1989
[62] J A Dıaz D Bauwens and B Asensio ldquoA comparative studyof the relation between heating rates and ambient temperaturesin lacertid lizardsrdquo Physiological Zoology vol 69 pp 1359ndash13831996
[63] D C Deeming ldquoPost-hatching phenotypic effects of incubationin reptilesrdquo in Reptilian Incubation Environment Evolutionand Behaviour D C Deeming Ed pp 229ndash251 NottinghamUniversity Press Nottingham UK 2004
[64] R Shine M J Elphick and P S Harlow ldquoThe influence ofnatural incubation environments on the phenotypic traits ofhatchling lizardrdquo Ecology vol 78 pp 2559ndash2568 1997
[65] T Flatt R Shine P A Borges-Landaez and S J DownesldquoPhenotypic variation in an oviparousmontane lizard (Bassianaduperreyi) the effects of thermal and hydric incubation envi-ronmentsrdquo Biological Journal of the Linnean Society vol 74 no3 pp 339ndash350 2001
[66] R Shine and M J Elphick ldquoThe effect of short-term weatherfluctuations on temperatures inside lizard nests and on thephenotypic traits of hatchling lizardsrdquo Biological Journal of theLinnean Society vol 72 no 4 pp 555ndash565 2001
[67] O Lourdais R Shine X Bonnet M Guillon and G NaulleauldquoClimate affects embryonic development in a viviparous snakeVipera aspisrdquo Oikos vol 104 no 3 pp 551ndash560 2004
[68] V Delmas X Bonnet M Girondot and A-C Prevot-JulliardldquoVarying hydric conditions during incubation influence eggwater exchange and hatchling phenotype in the red-eared sliderturtlerdquo Physiological and Biochemical Zoology vol 81 no 3 pp345ndash355 2008
[69] X-F Yan X-L Tang F Yue et al ldquoInfluence of ambient temper-ature onmaternal thermoregulation and neonate phenotypes in
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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International Journal of
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International Journal of
Microbiology
2 International Journal of Zoology
amphibians [14ndash16] In reptiles even earlier investigations[9] based on species assemblages have revealed that ingeneral they do not exhibit noticeable latitudinal trendsalthough some snake taxa show a weak gradient Howeverthe appearance of spatial trends in body size for ectotherms[2] including vertebrates [17ndash19] is still disputed [13 20ndash23]In recent years many studies have tested Bergmannrsquos rule forvarious ectotherm taxa and have found a wide range of pat-terns depicting the connection between body size and envi-ronmental gradient [16 18 24ndash27] Atkinson and Sibly [28]andCruz et al [29] have claimed that some ectotherms followBergmannrsquos rule whereas for other species the oppositepattern is true [30 31] Ashton and Feldman [17] found thatturtles follow Bergmannrsquos rule whereas squamates contrast itCruz et al [29] demonstrated a strong negative temperature-body size gradient among Liolaemus lizard species reflectinga profound effect of thermal inertia at higher latitudes oraltitudes in accordance with Bergmannrsquos rule HoweverPincheira-Donoso et al [20 32] within the same lineage butbased on an enlarged sample size failed to find statisticalsupport for Bergmannrsquos clines and claiming that in theseanimals the evolution of larger bodies in colder areas isdisadvantageous they suggested that it applied exclusivelyto endotherms It is possible that the spatial trends in bodydimensions are influenced by a complex set of both abiotic(eg seasonality and temperature) and biotic (eg intra-and interspecific competition) factors and their interactions[17 18 33] and that no single mechanism can explain them
However to my knowledge some important issuesremain obscure For instance tests of intraspecific body sizeor shape patterns in squamates accounting for gender-specificaspects are scarce because the papers often provide data forthe pooledmale and female samples Taking into account thatreptiles are often sexually dimorphic ([34 35] see also theresults) it is possible that conclusions of some ecogeographicstudies may suffer from biased sampling In this contextmy primary goal is to compare the sexes in respect totheir relationship with climate variables A nonphylogeneticapproachwas used here to test themain hypothesis thatmalesand females facing different thermal and metabolic demandsfollow different patterns in their phenotypic responses toenvironmental gradient Further I evaluate the combinedeffect of temperature and precipitation on body dimensionswithin all the species studied Finally I also focus on species-specific peculiarities in the appearance of environmentallyrelated phenotypic variation Diurnal lizards including arid-zone dwellers bask in large amounts of time especially in themorning hours (personal observations) Under this scenarioI hypothesize that in the desertM guttulata andA boskianuswhich are affected by exposure to extreme daily temperaturefluctuations a smaller size is likely to be preferable Small-bodied individuals may have better heating and cooling abil-ities heating faster after the cold nights and can thus remainactive for longer periods It is generally accepted [36 37] thattemperature is the most important factor influencing lizardsrsquoactivities and that thermal demands play an important role inhabitat selection by reptiles In thewild lizards apply a varietyof strategies to achieve their preferred body temperatureThermoregulation is realized behaviourally through shuttling
between warm and cold sites [38] as well as physiologicallyby altering peripheral blood flow and modifying heart rates[39 40] In addition some species apply ventilatory heat loss[41 42] via evaporation through their mouth or cloaca
In arid areas where the present study mainly took placerainfall as well as temperature is an important factor inanimal ecology including determining food availability andthus also growth rate [11] The dispute over which geographiccomponent determines body sizemostmakes an examinationof the respective influence of temperature- and water-relatedvariables on morphological features timely In the presentstudy I used a range of linear measurements and ratios infour oviparous lizard species in order to determine the corre-lation between morphology temperature and precipitationI examined environmentally induced phenotypic variabil-ity and the validity of ecomorphological patterns such asBergmannrsquos and Allenrsquos rules in four Middle-Eastern wide-ranging lacertid lizards Phoenicolacerta laevis Ophisopselegans Acanthodactylus boskianus andMesalina guttulata
Acanthodactylus and Mesalina species are mainly desertinhabitants while the Phoenicolacerta and Ophisops speciesmostly inhabit theMediterranean region (amoremesic area)In Israel these species occur along pronounced temperatureand rainfall gradients ([43] and see below) which makesthis region a convenient model for examining intraspecificecomorphological variation Thus in Israel mean annualrainfall ranges from sim1000mm in the north to 25mm in thesouth There is a negative north-south gradient in ambienttemperature with annual averages of about 15∘C and 25∘C inthe north and south respectively Another strong climaticfeature is a U-shaped westeast temperature gradient fromthe temperate Mediterranean coast to the colder centralmountain range and the very hot Jordan Valley in the east(Figure 1)The daily and annual temperature fluctuations alsodiffer greatly across Israel
Israel which has a wide range of climates and landscapesincluding mountain regions coastal plains humid valleysrocky deserts and sand dunes is a hotspot of reptile speciesrichness [44] Environmental temperatures (eg extremeannualdiurnal values) and rainfall intensity (Figures 1(a) and1(b)) are markedly different across the distribution ranges ofboth desert and the Mediterranean region species Hencethe appearance of morphological variation in ectothermsis expected to be adjusted by species-specific ecologicalinteractions leading to interspecific differences in body size(or shape) gradient In this context I expect a different linkbetween both abiotic predictors and bodylimb proportionswithin ecologically different lizard species For example tem-perature may be a stronger ecological determinant of body orextremities size variation for P laevis and O elegans living incooler environments than for the desert A boskianus andMguttulata The present study is the first including analyses ofboth Bergmannrsquos and Allenrsquos rules to investigate a functionalconnection between abiotic habitat conditions and the exter-nalmorphology of theMiddle East lacertid lizards it also dis-cusses the functional link between corporeal measurementsand geographic variables The findings are expected to con-tribute to our understanding of the potential importance ofabiotic components as sources of morphological intraspecific
International Journal of Zoology 3
Temperature (∘C)75ndash119119ndash146146ndash161161ndash173173ndash185185ndash196196ndash207207ndash217217ndash228228ndash2424ndash252
3534
33
33
32
31
30
29
28
Egypt
Israel
Mediterranean Sea
Sinai Peninsula
Acanthodactylus boskianus (136ndash235)Mesalina guttulata (136ndash241)Ophisops elegans (90ndash200)Phoenicolacerta laeis (126ndash208)
GulfofSuez
Gulf of
Aqaba
0 15 30 60 90 120
gt252
(km)
(a)
3534
33
33
32
31
30
29
28
Egypt
Israel
Mediterranean Sea
Sinai Peninsula
GulfofSuez
Gulf of
Aqaba
0 15 30 60 90 120
0ndash1010ndash5050ndash100100ndash150150ndash200200ndash250250ndash300300ndash400400ndash500500ndash650650ndash800
(4ndash381)(18ndash525)
(121ndash907)(318ndash780)
Precipitation (mm)
Acanthodactylus boskianus
Mesalina guttulata
Ophisops elegans
Phoenicolacerta laeis
lt800
(km)
(b)
Figure 1 Climatic maps of the studied areas (excluding Turkish localities) (a) Average annual temperature and (b) average annual precipi-tation The ranges of temperature and precipitation for each species are given in brackets
variability in ectothermic vertebrates whose metabolic ratesand life history are greatly affected by environments
2 Material and Methods
21 Samples and Site Locations The observed specimenswere adult males and females of four lizard species (morethan 100 individuals per species) with large geographicranges I measured 679 preserved specimens of four lacertidspecies in the Natural History Museum of the Departmentof Zoology Faculty of Life Sciences Tel Aviv University(TAUM)The specimens had been collected between 1941 and2012 mostly 866 from Israel but some 71 from Egypt (theSinai Peninsula) and 20 specimens from Turkey
The following specimens were collected Phoenicolacertalaevis 104 specimens were collected from Mt Hermon theGolan Heights the Galilee the foothills of Judea and thecoastal plain (Israel) Ophisops elegans 127 specimens werecollected from Israel (Mt Hermon the Golan Heights theGalilee the Judean foothills and the northern and centralNegev) and 20 specimens from Turkey Acanthodactylusboskianus 164 specimens were collected from Israel (theArsquorava Valley and the northern central and southern Negev)and 50 specimens from Egypt (northern Sinai Sinai moun-tains and the western Sinai coastal plain)Mesalina guttulata193 specimens were collected from Israel (the Judean Hillsthe Judean Desert Dead Sea area and the northern centraland southern Negev) and 21 specimens from Egypt (thenorthern Sinai and Sinai mountains)
22 Study Species Phoenicolacerta laevis (Gray 1838) is amedium-sized lizard SVL up to 77mm (according to ourrecords) generally distributed in the Mediterranean land-scape from Turkey to Israel and Jordan This fairly adaptablespecies is found in relatively humid biotopes such as tem-perate forests valleys Mediterranean-type shrub vegetationcultivated fields and gardens ([45 46] pers obs) It is foundfrom 200m below sea level up to 2200m above sea level(TAUM records)
Ophisops elegans (Menetries 1832) is a small slenderlizard The largest specimen in our sample has a SVL of59mm It occurs in open arid plains of the Mediterraneanregion and Central Asia and was found in sparse forestsvegetated rocky hillsides and wadis [46ndash48] Its verticaldistribution ranges from 240m below sea level to 2000mabove sea level (TAUM records)
Acanthodactylus boskianus (Daudin 1802) is a medium-sized lizard with adults up to 88mm SVL It is widespreadin desert and semidesert areas of the Saharo-Arabian regionfrom northern Africa through the eastern Mediterraneanand the Arabian Peninsula to Iraq It inhabits rather hardsubstrate and occupies a wide range of sandy and gravelhabitats It was collected from400mbelow sea level to 1300mabove sea level [46 48 49]
Mesalina guttulata (Lichtenstein 1823) is a rather smallslender lizard with a maximum SVL of 57mm It is widelydistributed in North Africa and south-west Asia It usuallyinhabits desert and semidesert regions with various terrains
4 International Journal of Zoology
prefers hard substrate and scattered rocks and avoids sanddunes [46ndash48] It is found from 350m below sea level to2000m above sea level (TAUM records)
23MorphologicalMeasurements For each specimen Imea-sured the following snout-vent length (SVL) humerus length(HmL) distance from axilla to apex of elbow forearmlength (FaL) distance from elbow apex to apex of wristfemur length (FeL) distance from groin to apex of kneeand tibia length (TbL) distance from apex of knee to heelFrom these total fore limb length (FLL) and total hindlimb length (HLL) which were obtained as the sums ofthe corresponding segment lengths (ie HmL + FaL andFeL + TbL) as well as the limbs-body ratios (HmLSVLFaLSVL FeLSVL TbLSVL) were calculated Tail lengthwas not included in the analysis because many individualshad broken or regenerated tails For each specimen I alsorecorded collection data (region and locality with geographiccoordinates and elevation) as well as bodyweight (119872) whichwas taken shortly after capture to the nearest 01 g Sex wasdetermined by tail base shape and hemipenis eversion or indoubtful cases by dissection Measurements were made witha digital caliper (Mitutoyo CD-610158401015840CX) to the nearest 001mmexcept for SVL which was measured to the nearest 05mmusing a millimeter ruler I could not record all measurementsfrom each specimen due to the bad preservation conditionsof some reptiles so the sample sizes vary among features(Table 1) All measurements were made by the author
24 Meteorological Data The climate elements consideredwere average annual temperature and average annual precip-itation within the natural locations of the animals Spatiallyinterpolated climate data [50] for the 1950ndash2000 period ongrids with spatial resolution of 30 arc-second (often referredto as 1-km spatial resolution) were taken from httpwwwworldclimorg and imported into a GIS application
25 Data Analyses I applied one-way ANOVAwith multipletesting corrections (Duncanrsquos multiple range test MRT) toexamine the presence of sexual size dimorphism (SSD) inbody and limbdimensions in all species studied I used simpleordinary least squares (OLS) regression model treating tem-perature and precipitation as continuous predictors to assessthe relationship between abiotic environmental componentsand morphological traits In this analysis the examinedsamples suppose a great dispersion of the data that cannotbe addressed with log-transformations In fact both bodysize ranges within the samples and the sample sizes acrossthe observed locations vary among the species Howeverprior to analyses the data were tested for normality (Shapiro-Wilkrsquos test) and homogeneity of variances (Levenersquos test)As argued in the Introduction testing the possible presenceof intraspecific clines requires that sexual size dimorphismwithin the species studied to be taken into account Inview of these considerations relationships between abioticvariables and the measurementsratios were tested for eachsex separately I also controlled for the effect of temperatureand precipitation on limb length (for each sex separately) byMANCOVA using SVL as a covariate In this analysis both
abiotic factors treated separately as categorical predictors andtotal fore limb length (FLL) and total hind limb length (HLL)as dependent variablesMultiple ordinary least squares (OLS)regression analysis using SVL as a dependent variable andtreating climatic factors as predictors was applied to examinethe combined effect of temperature and precipitation on bodysizeHere in order to produce amoremeaningful index of theobserved effects the slope coefficients were transformed intostandardized ldquobetardquo coefficients (120573) All statistical analyseswere done using Statistica 8 (StatSoft Inc USA)
3 Results
31 Sexual Dimorphism Summary data of basicmorphologi-cal features for males and females of each species are given inTable 1 Simple intersexual comparisons (one-way ANOVA)of the lizardsrsquo external morphology indicate that male Oelegans andA boskianus are significantly (119875 lt 00001) longerand heavier than females (Table 1) In M guttulata femalesare longer but not heavier than males In P laevis malesare marginally nonsignificantly heavier than females but notlonger
Moreover there is a pronounced sexual dimorphism (119875 lt00001) in extremity length Within all the species studied inabsolute terms (mm) HmL FaL FeL and TbL in males weremuch greater (from 73 to 136) than those in conspecificfemales Assessing the ratios of fore and hind limbsrsquo segmentsrelative to SVL (ie HmLSVL FaLSVL FeLSVL andTbLSVL) made very little difference (data not shown)
32 Environment-Related Variation
P laevis The studied locations are characterized by a highlysignificant correlation between latitude and both temperature(119903 = minus0607 119875 lt 00001) and precipitation (119903 = 0879119875 lt 00001) and between temperature and precipitationsas well (119903 = minus0732 119875 lt 00001) Considering body sizegradient the scatter plots shown in Figure 2 indicate thatalthough the individuals exhibit a notable dispersion (it isalso true for other species studied) the major trends becomeevident Male SVL does not vary significantly in relation toclimate (temperature OLS slope plusmn SE = minus025 plusmn 045 119903 =minus0081 119875 = 0585 precipitation slope = minus0001 plusmn 0006119903 = minus0032 119875 = 0827) whereas females are greatly affectedby it growing significantly heavier and longer (Figures 2(a)and 2(b)) in cool and wet habitats (temperature slope =minus147 plusmn 031 119903 = minus0543 119875 lt 00001 precipitation slope =001 plusmn 0004 119903 = 0369 119875 = 0005) Continuous sampling(Table 2) revealed a stronger effect of climate on corporealproportions than on absolute sizes Analysis of latitudinalvariability in body proportions showed a significant relation-ship between temperature and relative extremities length Inboth sexes relatively larger limbs are associated with hothabitats among females the recorded temperature-relatedcorrelation was highly significant for these morphologicalvariables The influence of precipitation was less obviousalthough in females it was still significant for all ratios Inmales only HmLSVL varied in relation to precipitationWith SVL as a covariate however a MANCOVA indicates a
International Journal of Zoology 5
Table 1 Morphological characteristics of lizard species studied and their intersexual comparisons (one-way ANOVA with multiple testingcorrections Duncanrsquos multiple range test MRT)
Species Features Range Mean plusmn SD nDDCC
119875 119865
DD CC DD CC
Phoenicolacertalaevis
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
25ndash105505ndash7753ndash9
59ndash932762ndash1184875ndash13
3ndash11450ndash76
522ndash73459ndash7877ndash10585ndash114
585 plusmn 191
6353 plusmn 665699 plusmn 079
761 plusmn 077
966 plusmn 103
1104 plusmn 102
513 plusmn 194
6297 plusmn 601
634 plusmn 047
696 plusmn 046
878 plusmn 063
987 plusmn 062
485648564756475647564756
0059065400001000010000100001
3620202636284927405101
Ophisops elegans
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
09ndash4240ndash59445ndash61478ndash67253ndash872715ndash1053
12ndash3540ndash53539ndash54423ndash62252-747646ndash922
25 plusmn 072
4807 plusmn 427
53 plusmn 04
582 plusmn 05
722 plusmn 071
9 plusmn 081
198 plusmn 051
4647 plusmn 344
466 plusmn 035
515 plusmn 041
629 plusmn 057
778 plusmn 063
856285628461846184618461
lt000010016lt00001lt00001lt00001lt00001
23225859838732069119538
Acanthodactylusboskianus
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
17ndash13852ndash8852ndash918592ndash992845ndash1338108ndash164
3ndash12150ndash805462ndash7358ndash84883ndash122810ndash1454
699 plusmn 215
659 plusmn 646
69 plusmn 075
796 plusmn 079
112 plusmn 104
1377 plusmn 119
535 plusmn 163
6111 plusmn 583
626 plusmn 056
712 plusmn 062
981 plusmn 075
1212 plusmn 087
121931219311385113851148511485
lt00001lt00001lt00001lt00001lt00001lt00001
37233131433365571086211606
Mesalinaguttulata
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
08ndash640ndash57413ndash5945ndash624595ndash82717ndash967
116ndash3740ndash5639ndash5442ndash56557ndash776664ndash88
204 plusmn 063
4561 plusmn 301
5 plusmn 031
534 plusmn 03
707 plusmn 046
839 plusmn 045
201 plusmn 056
469 plusmn 373
462 plusmn 029
495 plusmn 03
652 plusmn 041
763 plusmn 044
98791199511895118951189511895
07480005lt00001lt00001lt00001lt00001
01078078228409796115251
80
76
72
68
64
60
56
52
4814 15 16 17 18 19 20 21
SVL
(mm
)
Average annual temperature (∘C)
(a)
80
76
72
68
64
60
56
52
48
SVL
(mm
)
300 350 400 450 500 800550 600 650 700 750
Average annual precipitation (mm)
(b)
Figure 2 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Phoenicolacerta laevissolid line with circles males dashed line with triangles females
statistically significant effect of temperature on both FLL andHLL in females (Table 3) The results of multiple regressionwith SVL as a response (Table 4) indicate that the body size-environment link is more obvious in respect to temperaturethan to precipitation Thus in females SVL is much moreaffected by the former variable 119875 = 00009 120573 = minus061 plusmn 017than by the latter 119875 = 0588 120573 = minus009 plusmn 017
O elegans Examination of the environmental relationshipacross the observed area of thismostlyMediterranean species
demonstrates a highly significant correlation between latitudeand both temperature (119903 = minus0801 119875 lt 00001) and pre-cipitation (119903 = 0433 119875 lt 00001) Temperature is negativelycorrelated with precipitation (119903 = minus0388 119875 lt 00001)Snout-vent lengths (Figures 3(a) and 3(b)) of both sexesincrease with temperature (males slope = minus072 plusmn 018 119903 =minus0402 119875 = 00001 females slope = minus049plusmn014 119903 = minus0408119875 = 0001) and with precipitation (males slope = 0007 plusmn0001 119903 = 0395 119875 = 00002 females slope = 0005 plusmn 0001119903 = 0374 119875 = 0002)
6 International Journal of Zoology
Table 2 Climate-morphology relationship between average annual temperature (AAT)average annual precipitation (AAP) and bodymeasurementsratios (regression analysis with temperature and precipitation as the predictors and features as the responses) Positivecorrelation (+) and negative correlation (minus) single sign significant difference (119875 lt 005) and double sign highly significant difference (119875 lt00001)
FeaturesPhoenicolacerta laevis Ophisops elegans Acanthodactylus boskianus Mesalina guttulata
AAT AAP AAT AAP AAT AAP AAT AAPDD CC DD CC DD CC DD CC DD CC DD CC DD CC DD CC
M minus + minus + + + +SVL minusminus + minus minus + + minus + + +HmL minus minus + ++FaL minus minus + + +FeL minus minus ++ +TbL minus minus + +HmLSVL + ++ minus minus + minus minus +FaLSVL + ++ minus + minusminus minus +FeLSVL + ++ minusminus + + + minus minus + minus minus
TbLSVL + ++ minus + minus minus + minus minus
Table 3 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Phoenicolacerta laevis with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
77
88
052111
079152
145149
243333
02140199
00280004
Covariate(SVL)
FLLHLL
11
11
73211275
23494734
20171707
71641038
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
033276
404766
093371
12321679
03410062
lt0001lt0001
Error FLLHLL
3737
4646
036074
033045
Precipitation FLLHLL
88
88
047099
064150
126130
187327
02940275
00880005
Covariate(SVL)
FLLHLL
11
11
71081208
21624677
19131582
62751017
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
030296
493798
081388
14331738
03740056
lt0001lt0001
Error FLLHLL
3636
4646
037076
034045
Table 4 The effect of climate variables on snout-vent length (SVL) Results of multiple regression with SVL as a dependent variable andclimatic factors as predictors
Effect of temperature Effect of precipitation120573 plusmn SE 119905 119875 120573 plusmn SE 119905 119875
Phoenicolacertalaevis
DD minus021 plusmn 021 minus098 0328 minus018 plusmn 021 minus085 0399CC minus0615 plusmn 017 minus351 00009 minus009 plusmn 017 minus054 0588
Ophisops elegansDD minus027 plusmn 011 minus251 0013 026 plusmn 011 238 0019CC minus032 plusmn 012 minus266 0009 025 plusmn 012 208 0041
Acanthodactylusboskianus
DD minus003 plusmn 009 minus034 0727 0136 plusmn 009 137 0207CC minus013 plusmn 011 minus115 0251 021 plusmn 011 minus177 0079
Mesalina guttulata DD minus003 plusmn 009 minus041 068 021 plusmn 009 236 0019CC minus014 plusmn 009 minus151 0134 033 plusmn 009 339 0001
International Journal of Zoology 7
SVL
(mm
)
Average annual temperature (∘C)
60
56
52
48
44
40
8 10 12 14 16 18 20
(a)
SVL
(mm
)
60
56
52
48
44
40
100 200 300 400 500 700 800600 900
Average annual precipitation (mm)
(b)
Figure 3 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Ophisops elegans solidline with circles males dashed line with triangles females
The corporeal ratios and especially lengths (Table 2)are noticeably influenced by the local climate conditionsRegression analysis indicates that the sexes generally followsimilar trends in their corporal dimensions and becomesignificantly larger at higher latitudes By analogy with SVLappendages were positively correlated with precipitation andwere negatively correlated with temperature In additionin both sexes the longer femora may be associated withincreased precipitation However after accounting for SVLa MANCOVA reveals a nonsignificant effect of both abi-otic predictors on limb size (Table 5) Multiple regressiondemonstrates the equivalency of two climate influences intheir relationships with SVL (Table 4) Furthermore malesand females in general did not differ from one another intheir responses to either temperature (120573 = minus027plusmn011 versus120573 = minus032 plusmn 012) or precipitation (120573 = 026 plusmn 011 versus120573 = 025 plusmn 012) gradient
A boskianus In the desert habitats of this species temperaturewas uncorrelated with latitude (119903 = minus0082 119875 = 0247)across the observed geographic range There is however apronounced latitudinal precipitation gradient (119903 = 0815119875 lt 00001) and a negative relationship between annualaverages of temperature and precipitation 119903 = minus0367 119875 lt00001 In this lizard the sexes differ in respect to theirenvironmental-morphological connection (Figures 4(a) and4(b)) The SVL of males did not correlate consistently withtemperature (slope = minus021 plusmn 029 119903 = minus0067 119875 = 0485)and precipitation (slope = 001 plusmn 0008 119903 = 0134 119875 =0160) whereas the SVL of females varied in relation to thesevariables slope = minus081 plusmn 034 119903 = minus0243 119875 = 0021 andslope = 002 plusmn 0007 119903 = 0280 119875 = 0007 for temperatureand precipitation respectively
Corporeal measurements (Table 2) showed a close rela-tionship with rainfall in both sexes and increased precip-itation is correlated to shorter extremities relative to SVLDespite the fact that the appendages tend to lengthen relativeto their SVL with rise in temperature this abiotic component
would seem to affect only hind limb segments (FeL and TbL)The MANCOVA results (Table 6) also suggest that withinboth sexes the temperature gradient significantly contributesonly to HLL variation Precipitation had a significant effecton hind extremity in both sexes furthermore within males itinfluenced the variation in FLL as well Analysis of combinedeffect of environmental variables when both temperature andprecipitation were regressed against SVL (Table 4) revealsthe role of moisture as a major predictor of intraspecificvariability Moreover males and females were similar in thistrend 120573 = minus003 plusmn 009 (temperature) 120573 = 0136 plusmn 009(precipitation) for males and 120573 = 013 plusmn 011 versus 120573 =021 plusmn 011 for females respectively
M guttulata The studied geographic range of this desertlacertid is characterized by a highly significant correlationbetween latitude and both temperature (119903 = 0657 119875 lt00001) and precipitation (119903 = 0682 119875 lt 00001) whereastemperature was uncorrelated with precipitation (119903 = 0030119875 = 0654) In both sexes SVL (Figures 5(a) and 5(b))increased along a rainfall gradient slope = 0006 plusmn 0002 119903 =0215 119875 = 0018 for males slope = 001 plusmn 0004 119903 = 0317119875 = 0001 for females Continuous sampling also revealed aninsignificant relationship between temperature and SVL inthis species Regression analysis (Table 2) indicated an impor-tant role of precipitation in the creation of clines in body andlimb dimensions Moreover spatial changes of both climaticcomponents may induce some allometric shifts in latitudinalspace Thus temperature rise has led to the appearance oflonger (relative to SVL) extremities among females Thisobservation was confirmed by MANCOVA a significantassociation was observed between either FLL or HLLandtemperature as well as between HLL and precipitation Inmales this approach however indicates a nonsignificanteffect of both climatic variables on limb dimensions (Table 7)
Similarly to other desert dwellers (A boskianus) in thisspecies too precipitation level is a stronger ecological deter-minant of body length (Table 4) than temperature gradient
8 International Journal of Zoology
Table 5 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Ophisops elegans with SVL as a covariate
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
1717
1616
012048
026071
081121
140147
06720278
01860155
Covariate(SVL)
FLLHLL
11
11
25225696
5291525
16331432
28643183
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
101138
251265
651347
1359552
00130067
00010023
Error FLLHLL
6565
4242
015039
018047
Precipitation FLLHLL
2323
1717
013056
024064
083156
129130
06730086
02430241
Covariate(SVL)
FLLHLL
11
11
21864902
5341481
14061366
28222971
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
123201
263305
796559
1393612
00060021
00010018
Error FLLHLL
5959
4141
015035
018049
14 16 18 20 22 24
SVL
(mm
)
Average annual temperature (∘C)
85
80
75
70
65
60
55
50
(a)
SVL
(mm
)
85
80
75
70
65
60
55
50
0 50 150 200100 250 300
Average annual precipitation (mm)
(b)
Figure 4 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Acanthodactylusboskianus solid line with circles males dashed line with triangles females
119875 = 0019 120573 = 021plusmn009 versus119875 = 0680 120573 = minus003plusmn009for males 119875 = 0001 120573 = 033 plusmn 009 versus 119875 = 0134120573 = minus014 plusmn 009 for females respectively
4 Discussion
Despite the inability of ectotherms to produce significantmetabolic heat the interaction between body size and heatbalance based on a set of behavioural anatomical andphysiological mechanisms [51] that contribute to fitnessmight explain the peculiarity of ecological drivers in sizeclines among these animalsThe relationship between habitatconditions and morphological variables (body tail or limbdimensions) and consequent shifts in phenology due toclimate change have been observed across a wide range ofreptile taxa [52ndash54] It is possible that in diurnal squamates
environmental conditions may favour selection for smaller-sized individuals [55] which due to the ability to achievemore accurate adjustment of their body temperature havebetter thermoregulatory capacities [56] and thus display highactivity levels In terrestrial ectotherms thermoregulation isrealized behaviourally by habitat selection and daily activitypattern [57] while at the same time morphological special-ization may also essentially facilitate it [55] For exampleShine and Madsen [58] pointed out that for relatively smallreptile species behavioural thermoregulation seems to bemore important especially in conditions of high diurnalthermal heterogeneity In this context desert reptiles inhab-iting warmer regions with lower thermoregulatory costs mayadjust their body temperature mainly behaviourally andthus invest less in adjustment of either body size or shapein relation to ambient temperature Despite the great data
International Journal of Zoology 9
Table 6 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Acanthodactylus boskianus with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
3535
2828
089151
053131
141191
125175
01180012
02390040
Covariate(SVL)
FLLHLL
11
11
60441731
34366125
95262186
80188176
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
203445
4952911
320562
11563885
00780021
0001lt0001
Error FLLHLL
6565
5151
063079
042074
Precipitation FLLHLL
3333
3131
086151
046116
178186
101171
00230016
04810049
Covariate(SVL)
FLLHLL
11
11
64151792
23944222
13182201
51436151
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
161422
7043482
332518
15145073
00730026
lt0001lt0001
Error FLLHLL
6767
4848
048081
046068
14 16 18 20 22 24
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
Average annual temperature (∘C)
(a)
0 50 150 200100 250 300 350 400 450 500 550
Average annual precipitation (mm)
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
(b)
Figure 5The relationship between SVL and (a) average annual temperature and (b) average annual precipitation inMesalina guttulata solidline with circles males dashed line with triangles females
dispersion (as shown in the scatter plots) it was foundthat among the two ldquodesertrdquo species studied (M guttulataand A boskianus) only females of the latter were smallerin hot temperatures whereas in both sexes of the formeras well as in A boskianus males SVL did not correlatewith temperature In the Mediterranean region P laevisand O elegans inhabit cooler climates than the desert Aboskianus and M guttulata In these environments largergravid reptiles in addition to the buffering effects of thebehavioural thermoregulation supplied by the mother [5960] can provide greater temperature stability during thepreoviposition period Volynchik [19] however found that alarge-bodied local viper (Vipera palaestinae) with a Mediter-ranean distribution pattern does not follow Bergmannrsquos ruleor its converse At the same time the most ldquocold-lovingrdquolizard (O elegans) in my own sample obeyed Bergmannrsquos
rule growing larger in cooler environments On the otherhand in desert habitats this pattern of greater thermal inertiaseems to be less important and the behavioural componentof thermoregulation becomes paramount
The impact of ambient temperature on external mor-phology is also significant in respect to relative extremitylengths different degrees of intraspecific variability in limbproportions supporting Allenrsquos rule were observed in all thespecies studied The present findings indicate that temper-ature decrease across the observed habitats could lead toreduction in size of extremity segments relative to bodylength thus constituting a compensatory adaptation to eithercooler or hotter areas I noted an allometric shift in humerusforearm femur and tibia lengths relative to SVL along atemperature gradient among P laevis A similar relationshipbetween average annual temperature and corporeal ratioswas
10 International Journal of Zoology
Table 7 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) inMesalina guttulata with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
2525
2424
021045
024054
156143
181191
00650110
00290019
Covariate(SVL)
FLLHLL
11
11
20084405
9872011
14751407
72797114
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
4501082
8922073
33113455
65837331
lt0001lt0001
lt0001lt0001
Error FLLHLL
9191
6969
013031
013028
Precipitation FLLHLL
2828
2525
019041
022056
142129
162211
01070181
00590008
Covariate(SVL)
FLLHLL
11
11
19504181
9631908
14091307
68667094
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
356901
8021918
25752817
57177133
lt0001lt0001
lt0001lt0001
Error FLLHLL
8888
6868
013032
014026
noted in females of M guttulata Among A boskianus totalhind limb length significantly correlated with both thermalregime and rainfall gradient Hence both Mediterraneanand desert reptiles follow a similar pattern in their bodyshape variation and may benefit from various morphologicalmodifications matched to habitat range
Body temperature changes affect reptile ecology [61]becoming more important to ectotherms living in coolerenvironments which complicate attaining proper body tem-perature [58 62] In support of this my results show the asso-ciation between biogeographic origins of the species exam-ined and their relationship with environmental variables Oninterspecific comparison the most pronounced distinctionswere noted in phenotypic responses to the temperature gra-dient between Mediterranean and desert inhabitants whilethe between-species differences for precipitation-related vari-ation were weaker As expected both Mediterranean regionspecies (P laevis O elegans) display significantly strongerresponses to temperature than desert dwellers (A boskianusM guttulata) Apparently the cooler locations of the formerforce them to exhibit more consistent morphological vari-ability in respect to temperature changes whereas for desertspecies such habitat-morphology connection seems to be lessimportant It is highly likely that the speciesrsquo sensitivity tothe environment is associated not only with their ecologicaldifferentiation but also with body size ranges within thesample Thus this might be one possible explanation for thedifferent albeit relatively minor responses to temperaturebetween ecologically similar species (ie P laevis versus Oelegans andA boskianus versusM guttulata) that were notedhere In the examined samples L laevis owing to its greatermeasurement ranges than O elegans has a higher potentialfor more consistent matching of its body dimensions to theobserved temperature gradient The same is true for the twodesert lizardsA boskianus due to its extended body and limb
ranges in comparison with M guttulata displays a strongermorphological-environmental link
The examination of gender-specific habitat-morphologyinteractions revealed that within three of the four species (Plaevis A boskianus and M guttulata) sensitivity to the envi-ronment is coupledwith sex Considering the effect of climatevariables on SVL the findings demonstrate that females ingeneral show a more consistent link between temperatureand bodylimb measurements than males while the effectof precipitation on external characters was similar for bothsexes Moreover in P laevis SVL was significantly morestrongly correlated with the temperature gradient in femalesthan in malesThese observations indicate the sex-associatedeffect of natural selection pointing to different thermal andmetabolic demands inmales and femalesThus it is likely thatin females the increased body size in colder environmentsis associated with reproduction-induced requirements Thispattern suggests that females due to increased thermalrequirements particularly during vitellogenesis [63] aremore able to generate a range of suitable morphologicalmodifications for maintenance of optimal body temperaturein local environments Overall my findings indicate thatalthough females show amore consistent correlation betweenSVL and a temperature gradient than males the body shapechanges involving both body and limb dimensions arerather preliminary in explaining the observed intersexualdivergence in the habitat-morphology relationship
Environmental conditions within the nest experiencedduring early ontogenesis especially temperature and mois-ture of substrate can significantly affect development andgrowth trajectories of individuals in oviparous reptiles [64ndash68] As observed in many species either posthatching phe-notype or offspring fitness are closely associated with thermalregime [63 69ndash71] In both the laboratory and in naturalnests [64] temperature is traditionally considered to be animportant environmental determinant of reptile size while
International Journal of Zoology 11
the effect of water-related factors is more complex Severalrecent studies have tested the effect of substrate moistureduring incubation of eggs on a diverse range of reptile speciesSignificant effects are found in certain species [66 68 72 73]but not in others [74ndash76] that may reflect either differentwater permeability of the eggshell or interspecific variationin the water content of eggs [77] On the other hand theappearance of morphological variation along a precipitationgradient which in desert lizards is even more evident thanthe temperature-related variability can be considered as aresponse to the local habitats In reptiles food availabilitystrongly affects growth trajectories and is one of the possibledeterminants of body size and shape [78ndash80] Overall inarid regions where vegetation and arthropod fauna aredetermined primarily by precipitation [11] wetter localitiesprovide better food resources to lizards at the populationlevel The present findings suggest that among desert speciesthe possible spatial differences in prey availability and thusin nutrition levels may lead to morphometric differentiationbetween specimens inhabiting dry or wet sites Howeverdetailed studies on possible dietary variation linked tolocal environments are necessary to answer the question ofwhether the habitat conditions which are dependent on pre-cipitation have an effect on body dimensions in these lizards
A nonphylogenetic approach suggests that lizard speciestend to exhibit strong morphological specialization in rela-tion to their habitat [53 81] Variation in body charactersrelated to locomotion which in turn is associated withsubstrate pattern has been observed across many lizard taxa[54 82ndash84] Unfortunately based on available datasets Icould not evaluate whether the shift in substrate usage isassociated with limb proportion changes and so a rationalexplanation for the effect of vegetation on limb lengthsthrough its dependence upon hydrothermal regime remainsto be determined My findings show that generally theexamined species indicate a uniform pattern in extremitiessize variation fore and especially hind limb lengths werepositively correlated with temperature and negatively withprecipitation The results indicate that ecological adaptationto abiotic factors is a powerful source of extremity sizevariation which is under the effect of natural selection Inlizards the morphology-performance relationships suggestthat ground-dwelling species from open landscapes shouldpossess relatively long limb segments to their body length[53] This body shape pattern increases stride length provid-ing better sprinting abilities [85 86] Furthermore shorterextremities may facilitate the locomotion in highly vegetatedareas where long limbs may be disadvantageous [53] In thiscontextmyfindings suggest that various body shape patternssuch as relatively shortlong limbs or their segments whichare suited to the environmental requirements may reflect anadaptation to either dense or sparse vegetation resulting fromdifferent rainfall intensities across the distribution range
Finally given the potential importance of habitats forlimb size variation lizardsmay also use their protruding bodyparts as additional (together with body surface area) heatexchangers In these reptiles for optimal balance betweenheat gain and heat loss isometric size changes to a certainextent are a ldquotwo-edged swordrdquo inwhich high thermal inertia
of large bodies is accompanied by slow heating rates and viceversa In this respect among desert dwellers relatively longextremities and small size enhance heat exchange and seemto be a morphological adaptation for effective thermoreg-ulation In desert areas large daily fluctuations of temper-ature force the ectotherms to quickly respond to changingconditions and rapidly reach the necessary metabolic ratesfor locomotor activity Long-limbed individuals which havean increased surface area-to-volume ratio may enhancetheir heating and cooling abilities through more effectiveinteractions between the body and either solar radiationor surface temperature gradient Hence a consistent linkbetween environmental variables and limb lengths can alsobe explained by their importance for maintenance of optimalbody temperature in local environments As shown above thefact that the extremity size-environment link is more obviousin respect to hind limbs than to fore ones reinforces thishypothesis relatively large hind limbs having an increasedheat exchange capacity are much more powerful tool foreffective thermoregulation than small fore extremities
In summary the lacertid lizards I studied generallyfollowed the ecogeographic rules of Bergmann and AllenIn addition the findings indicate both intersexual and inter-specific differences in the habitat-morphology relationshipwhich can be considered within the framework of theirfunctional connectionMydata provide evidence that femalestend to show stronger relationships between climate vari-ables and body dimensions than males In desert speciestemperature has a smaller effect than rainfall on lizardphenotypes Under a constant dry climate water availabilityseems to be the most important abiotic factor in reptileecology In this respect due to the strong association betweenprecipitation and productivity my findings could also beinterpreted as evidence for the hypothesis that different bodysize patterns are linked to the spatial variation in primaryproduction that is the ldquoresource rulerdquo In the Mediterraneanregion lizards the thermal regime is apparently the maindriving force of morphological variability The present studysuggests a complex link between environmental variablesand morphological characters within lacertid species Thephysical conditions such as temperature and precipitationgradient were shown to be able to significantly affect bothbody and limb dimensions and thus as a powerful sourceof variation they play an important role in lizard mor-phology However general statements about the habitat-morphology relationships and their potential importance formaintenance of optimal body temperature in reptiles arehard to make due to the enormous diversity of variationsin body composition and physiology across species sexesand even individuals and the difficulty in evaluating enoughmechanisms in enough species Consequently additionalfield and experimental studies testing both body size andshape variations and their relationships with environmentalvariables especially at the intraspecific level and accountingfor sex-specific aspects are needed to help determine whetherthe observed patterns are common across species and to whatextent they are important for effective thermoregulation
12 International Journal of Zoology
Conflict of Interests
The author declares that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The author would like to thank Shai Meiri for his helpfulcomments on earlier drafts of the paper The author thanksErezMaza for assistancewith data preparationAnat Feldmanfor provision of the GIS-compatible temperature data andNaomi Paz for linguistic editing The author also thanks theIsrael Ministry of Science Culture and Sport for supportingthe National Collections of Natural History at Tel AvivUniversity as a biodiversity environment and agricultureresearch knowledge centre
References
[1] E Mayr Animal Species and Evolution Harvard UniversityPress Cambridge Mass USA 1963
[2] C Ray ldquoThe application of Bergmannrsquos and Allenrsquos rules to thepoikilothermsrdquo Journal of Morphology vol 106 pp 85ndash1081960
[3] TM Blackburn K J Gaston andN Loder ldquoGeographic gradi-ents in body size a clarification of Bergmannrsquos rulerdquo Diversityand Distributions vol 5 no 4 pp 165ndash174 1999
[4] K J Gaston and TM Blackburn Pattern and Process inMacro-ecology Blackwell Malden Mass USA 2000
[5] C Bergmann ldquoUber die verhaltnisse der warmeokonomie derthiere zu ihrer grosserdquo Gottinger Studien vol 3 pp 595ndash7081847
[6] J A Allen ldquoThe influence of physical conditions in the genesisof speciesrdquo Radical Review vol 1 pp 108ndash140 1877
[7] F C James ldquoGeographic size variation in birds and its relation-ship with climaterdquo Ecology vol 51 pp 365ndash390 1970
[8] C D Burnett ldquoGeographic and climatic correlates of morpho-logical variation inEptesicus fuscusrdquo Journal ofMammalogy vol64 no 3 pp 437ndash444 1983
[9] C C Lindsey ldquoBody sizes of poikilotherm vertebrates at differ-ent latitudesrdquo Evolution vol 20 pp 456ndash465 1966
[10] M L Rosenzweig ldquoThe strategy of body size in mammaliancarnivoresrdquo American Midland Naturalist vol 80 pp 299ndash3151968
[11] Y Yom-Tov and E Geffen ldquoGeographic variation in body sizethe effects of ambient temperature and precipitationrdquoOecologiavol 148 no 2 pp 213ndash218 2006
[12] Y Yom-Tov and H Nix ldquoClimatological correlates for body sizeof five species of Australian mammalsrdquo Biological Journal of theLinnean Society vol 29 no 4 pp 245ndash262 1986
[13] D Pincheira-Donoso and SMeiri ldquoAn intercontinental analysisof climate-driven body size clines in reptiles no support forpatterns no signals of processesrdquo Evolutionary Biology vol 40no 4 pp 562ndash578 2013
[14] K G Ashton M C Tracy and A de Queiroz ldquoIs Bergmannrsquosrule valid for mammalsrdquoThe American Naturalist vol 156 no4 pp 390ndash415 2000
[15] S Meiri and T Dayan ldquoOn the validity of Bergmannrsquos rulerdquoJournal of Biogeography vol 30 no 3 pp 331ndash351 2003
[16] K G Ashton ldquoSensitivity of intraspecific latitudinal clines ofbody size for tetrapods to sampling latitude and body sizerdquoIntegrative and Comparative Biology vol 44 no 6 pp 403ndash4122004
[17] K G Ashton and C R Feldman ldquoBergmannrsquos rule in nonavianreptiles turtles follow it lizards and snakes reverse itrdquoEvolutionvol 57 no 5 pp 1151ndash1163 2003
[18] M A Olalla-Tarraga M A Rodrıguez and B A HawkinsldquoBroad-scale patterns of body size in squamate reptiles ofEurope and North Americardquo Journal of Biogeography vol 33no 5 pp 781ndash793 2006
[19] S Volynchik ldquoMorphological variability in Vipera palaesti-nae along an environmental gradientrdquo Asian HerpetologicalResearch vol 3 pp 227ndash239 2012
[20] D Pincheira-Donoso D J Hodgson and T Tregenza ldquoTheevolution of body size under environmental gradients inectothermswhy shouldBergmannrsquos rule apply to lizardsrdquoBMCEvolutionary Biology vol 8 no 1 article 68 2008
[21] R C Stillwell ldquoAre latitudinal clines in body size adaptiverdquoOikos vol 119 no 9 pp 1387ndash1390 2010
[22] S Meiri ldquoBergmannrsquos rulemdashwhatrsquos in a namerdquo Global Ecologyand Biogeography vol 20 no 1 pp 203ndash207 2011
[23] D Pincheira-Donoso ldquoPredictable variation of range-sizesacross an extreme environmental gradient in a lizard adaptiveradiation evolutionary and ecological inferencesrdquo PLoS ONEvol 6 no 12 Article ID e28942 2011
[24] K G Ashton ldquoDo amphibians follow Bergmannrsquos rulerdquo Cana-dian Journal of Zoology vol 80 no 4 pp 708ndash716 2002
[25] M J Angilletta Jr T D Steury andMW Sears ldquoTemperaturegrowth rate and body size in ectotherms fitting pieces of a life-history puzzlerdquo Integrative and Comparative Biology vol 44 no6 pp 498ndash509 2004
[26] C E Oufiero G E A Gartner S C Adolph and T GarlandldquoLatitudinal and climatic variation in body size and dorsalscale counts in Sceloporus lizards a phylogenetic perspectiverdquoEvolution vol 65 no 12 pp 3590ndash3607 2011
[27] S Meiri ldquoEvolution and ecology of lizard body sizesrdquo GlobalEcology and Biogeography vol 17 no 6 pp 724ndash734 2008
[28] D Atkinson and RM Sibly ldquoWhy are organisms usually biggerin colder environments Making sense of a life history puzzlerdquoTrends in Ecology amp Evolution vol 12 pp 235ndash239 1997
[29] F B Cruz L A Fitzgerald R E Espinoza and J A Schulte IIldquoThe importance of phylogenetic scale in tests of Bergmannrsquosand Rapoportrsquos rules lessons from a clade of South Americanlizardsrdquo Journal of Evolutionary Biology vol 18 no 6 pp 1559ndash1574 2005
[30] T AMousseau ldquoEctotherms follow the converse to BergmannrsquosRulerdquo Evolution vol 51 pp 630ndash632 1997
[31] R N Reed ldquoInterspecific patterns of species richness geo-graphic range size and body size among NewWorld venomoussnakesrdquo Ecography vol 26 no 1 pp 107ndash117 2003
[32] D Pincheira-Donoso T Tregenza and D J Hodgson ldquoBodysize evolution in South American Liolaemus lizards of theboulengeri clade a contrasting reassessmentrdquo Journal of Evolu-tionary Biology vol 20 no 5 pp 2067ndash2071 2007
[33] M J Angilletta P H Niewiarowski A E Dunham A Leacheand W P Porter ldquoBergmannrsquos clines in ectotherms illustratinga life-historical perspective with sceloporine lizardsrdquoTheAmer-ican Naturalist vol 164 pp E168ndashE183 2004
[34] M Andersson Sexual Selection Princeton University PressPrinceton NJ USA 1994
International Journal of Zoology 13
[35] F Brana ldquoSexual dimorphism in lacertid lizards male headincrease vs female abdomen increaserdquo Oikos vol 75 pp 511ndash523 1996
[36] E R Pianka ldquoLizard species density in the Kalahari desertrdquoEcology vol 52 pp 1024ndash1029 1971
[37] E R Pianka ldquoSome intercontinental comparisons of desertlizardsrdquoNational Geographic Research vol 1 no 4 pp 490ndash5041985
[38] B H Brattstrom ldquoSocial and thermoregulatory behavior of thebearded dragon Amphibolurus barbatusrdquo Copeia vol 3 pp484ndash497 1971
[39] G C Grigg and F Seebacher ldquoField test of a paradigm hyster-esis of heart rate in thermoregulation by a free-ranging lizard(Pogona barbata)rdquo Proceedings of the Royal Society B BiologicalSciences vol 266 no 1425 pp 1291ndash1297 1999
[40] F Seebacher and C E Franklin ldquoControl of heart rate duringthermoregulation in the heliothermic lizard Pogona barbataimportance of cholinergic and adrenergic mechanismsrdquo TheJournal of Experimental Biology vol 204 no 24 pp 4361ndash43662001
[41] G J Tattersall and R M Gerlach ldquoHypoxia progressivelylowers thermal gaping thresholds in bearded dragons Pogonavitticepsrdquo The Journal of Experimental Biology vol 208 no 17pp 3321ndash3330 2005
[42] D F DeNardo T E Zubal and T C M Hoffman ldquoCloacalevaporative cooling a previously undescribedmeans of increas-ing evaporative water loss at higher temperatures in a desertectotherm theGilamonsterHeloderma suspectumrdquoThe Journalof Experimental Biology vol 207 no 6 pp 945ndash953 2004
[43] S Jaffe ldquoClimate of Israelrdquo inTheZoogeography of Israel Y Yom-Tov and E Tchernov Eds pp 79ndash92 Dr W Junk PublishersDordrecht The Netherlands 1988
[44] U Roll L Stone and S Meiri ldquoHot-spot facts and artifacts-questioning Israelrsquos great biodiversityrdquo Israel Journal of Ecologyand Evolution vol 55 no 3 pp 263ndash279 2009
[45] W Bischoff and J F Schmidtler ldquoNew data on the distributionmorphology and habitat choice of the Lacerta laevis-kulzericomplexrdquo Natura Croatica vol 8 no 3 pp 211ndash222 1999
[46] A Disi D Modry P Necas and L Rifai Amphibians andReptiles of the Hashemite Kingdom of Jordan An Atlas and FieldGuide Edit Chimaira Frankfurt Germany 2001
[47] A Bouskila and P Amitai Handbook of Amphibians andReptiles of Israel Keter Publishing House Jerusalem Israel2001 (Hebrew)
[48] A Bar and G Haimovitch A Field Guide to Reptiles andAmphibians of Israel Pazbar LTD Herzliya Israel 2012
[49] Y L Werner ldquoGeographic sympatry of Acanthodactylus opheo-durus with A boskianus in the Levantrdquo Zoology in the MiddleEast vol 1 pp 92ndash95 1986
[50] R J Hijmans S E Cameron J L Parra P G Jones and AJarvis ldquoVery high resolution interpolated climate surfaces forglobal land areasrdquo International Journal of Climatology vol 25no 15 pp 1965ndash1978 2005
[51] R B Huey ldquoTemperature physiology and the ecology ofreptilesrdquo inBiology of the Reptilia CGans and FH Pough Edsvol 12 of Physiology (C) pp 25ndash91 Academic Press New YorkNY USA 1982
[52] D J Irschick and J B Losos ldquoDo lizards avoid habitats inwhich performance is submaximal The relationship betweensprinting capabilities and structural habitat use in Caribbeananolesrdquo The American Naturalist vol 154 no 3 pp 293ndash3051999
[53] B Vanhooydonck and R Van Damme ldquoEvolutionary relation-ships between body shape and habitat use in lacertid lizardsrdquoEvolutionary Ecology Research vol 1 no 7 pp 785ndash805 1999
[54] J Melville and R Swain ldquoEvolutionary relationships betweenmorphology performance and habitat openness in the lizardgenus Niveoscincus (Scincidae Lygosominae)rdquo Biological Jour-nal of the Linnean Society vol 70 no 4 pp 667ndash683 2000
[55] R B Huey and M Slatkin ldquoCost and benefits of lizard thermo-regulationrdquo The Quarterly Review of Biology vol 51 no 3 pp363ndash384 1976
[56] R D Stevenson ldquoBody size and limits to the daily range of bodytemperature in terrestrial ectothermsrdquoTheAmericanNaturalistvol 125 pp 102ndash117 1985
[57] B W Grant ldquoTrade-offs in activity time and physiologicalperformance for thermoregulating desert lizards Sceloporusmerriamirdquo Ecology vol 71 no 6 pp 2323ndash2333 1990
[58] R Shine and T Madsen ldquoIs thermoregulation unimportant tomost reptiles An example using water pythons (Liasis fuscus)in tropical AustraliardquoPhysiological Zoology vol 69 pp 252ndash2691996
[59] R Shine ldquoReptilian viviparity in cold climates testing theassumptions of an evolutionary hypothesisrdquo Oecologia vol 57no 3 pp 397ndash405 1983
[60] C R Peterson A R Gibson andM E Dorcas ldquoSnake thermalecology the causes and consequences of body temperaturevariationrdquo in Snakes Ecology and Behavior R A Seigel and J TCollins Eds pp 241ndash314 McGraw-Hill New York NY USA1993
[61] R B Huey and J G Kingsolver ldquoEvolution of thermal sensitiv-ity of ectotherm performancerdquo Trends in Ecology and Evolutionvol 4 no 5 pp 131ndash135 1989
[62] J A Dıaz D Bauwens and B Asensio ldquoA comparative studyof the relation between heating rates and ambient temperaturesin lacertid lizardsrdquo Physiological Zoology vol 69 pp 1359ndash13831996
[63] D C Deeming ldquoPost-hatching phenotypic effects of incubationin reptilesrdquo in Reptilian Incubation Environment Evolutionand Behaviour D C Deeming Ed pp 229ndash251 NottinghamUniversity Press Nottingham UK 2004
[64] R Shine M J Elphick and P S Harlow ldquoThe influence ofnatural incubation environments on the phenotypic traits ofhatchling lizardrdquo Ecology vol 78 pp 2559ndash2568 1997
[65] T Flatt R Shine P A Borges-Landaez and S J DownesldquoPhenotypic variation in an oviparousmontane lizard (Bassianaduperreyi) the effects of thermal and hydric incubation envi-ronmentsrdquo Biological Journal of the Linnean Society vol 74 no3 pp 339ndash350 2001
[66] R Shine and M J Elphick ldquoThe effect of short-term weatherfluctuations on temperatures inside lizard nests and on thephenotypic traits of hatchling lizardsrdquo Biological Journal of theLinnean Society vol 72 no 4 pp 555ndash565 2001
[67] O Lourdais R Shine X Bonnet M Guillon and G NaulleauldquoClimate affects embryonic development in a viviparous snakeVipera aspisrdquo Oikos vol 104 no 3 pp 551ndash560 2004
[68] V Delmas X Bonnet M Girondot and A-C Prevot-JulliardldquoVarying hydric conditions during incubation influence eggwater exchange and hatchling phenotype in the red-eared sliderturtlerdquo Physiological and Biochemical Zoology vol 81 no 3 pp345ndash355 2008
[69] X-F Yan X-L Tang F Yue et al ldquoInfluence of ambient temper-ature onmaternal thermoregulation and neonate phenotypes in
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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International Journal of
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Zoology
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ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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International Journal of
Microbiology
International Journal of Zoology 3
Temperature (∘C)75ndash119119ndash146146ndash161161ndash173173ndash185185ndash196196ndash207207ndash217217ndash228228ndash2424ndash252
3534
33
33
32
31
30
29
28
Egypt
Israel
Mediterranean Sea
Sinai Peninsula
Acanthodactylus boskianus (136ndash235)Mesalina guttulata (136ndash241)Ophisops elegans (90ndash200)Phoenicolacerta laeis (126ndash208)
GulfofSuez
Gulf of
Aqaba
0 15 30 60 90 120
gt252
(km)
(a)
3534
33
33
32
31
30
29
28
Egypt
Israel
Mediterranean Sea
Sinai Peninsula
GulfofSuez
Gulf of
Aqaba
0 15 30 60 90 120
0ndash1010ndash5050ndash100100ndash150150ndash200200ndash250250ndash300300ndash400400ndash500500ndash650650ndash800
(4ndash381)(18ndash525)
(121ndash907)(318ndash780)
Precipitation (mm)
Acanthodactylus boskianus
Mesalina guttulata
Ophisops elegans
Phoenicolacerta laeis
lt800
(km)
(b)
Figure 1 Climatic maps of the studied areas (excluding Turkish localities) (a) Average annual temperature and (b) average annual precipi-tation The ranges of temperature and precipitation for each species are given in brackets
variability in ectothermic vertebrates whose metabolic ratesand life history are greatly affected by environments
2 Material and Methods
21 Samples and Site Locations The observed specimenswere adult males and females of four lizard species (morethan 100 individuals per species) with large geographicranges I measured 679 preserved specimens of four lacertidspecies in the Natural History Museum of the Departmentof Zoology Faculty of Life Sciences Tel Aviv University(TAUM)The specimens had been collected between 1941 and2012 mostly 866 from Israel but some 71 from Egypt (theSinai Peninsula) and 20 specimens from Turkey
The following specimens were collected Phoenicolacertalaevis 104 specimens were collected from Mt Hermon theGolan Heights the Galilee the foothills of Judea and thecoastal plain (Israel) Ophisops elegans 127 specimens werecollected from Israel (Mt Hermon the Golan Heights theGalilee the Judean foothills and the northern and centralNegev) and 20 specimens from Turkey Acanthodactylusboskianus 164 specimens were collected from Israel (theArsquorava Valley and the northern central and southern Negev)and 50 specimens from Egypt (northern Sinai Sinai moun-tains and the western Sinai coastal plain)Mesalina guttulata193 specimens were collected from Israel (the Judean Hillsthe Judean Desert Dead Sea area and the northern centraland southern Negev) and 21 specimens from Egypt (thenorthern Sinai and Sinai mountains)
22 Study Species Phoenicolacerta laevis (Gray 1838) is amedium-sized lizard SVL up to 77mm (according to ourrecords) generally distributed in the Mediterranean land-scape from Turkey to Israel and Jordan This fairly adaptablespecies is found in relatively humid biotopes such as tem-perate forests valleys Mediterranean-type shrub vegetationcultivated fields and gardens ([45 46] pers obs) It is foundfrom 200m below sea level up to 2200m above sea level(TAUM records)
Ophisops elegans (Menetries 1832) is a small slenderlizard The largest specimen in our sample has a SVL of59mm It occurs in open arid plains of the Mediterraneanregion and Central Asia and was found in sparse forestsvegetated rocky hillsides and wadis [46ndash48] Its verticaldistribution ranges from 240m below sea level to 2000mabove sea level (TAUM records)
Acanthodactylus boskianus (Daudin 1802) is a medium-sized lizard with adults up to 88mm SVL It is widespreadin desert and semidesert areas of the Saharo-Arabian regionfrom northern Africa through the eastern Mediterraneanand the Arabian Peninsula to Iraq It inhabits rather hardsubstrate and occupies a wide range of sandy and gravelhabitats It was collected from400mbelow sea level to 1300mabove sea level [46 48 49]
Mesalina guttulata (Lichtenstein 1823) is a rather smallslender lizard with a maximum SVL of 57mm It is widelydistributed in North Africa and south-west Asia It usuallyinhabits desert and semidesert regions with various terrains
4 International Journal of Zoology
prefers hard substrate and scattered rocks and avoids sanddunes [46ndash48] It is found from 350m below sea level to2000m above sea level (TAUM records)
23MorphologicalMeasurements For each specimen Imea-sured the following snout-vent length (SVL) humerus length(HmL) distance from axilla to apex of elbow forearmlength (FaL) distance from elbow apex to apex of wristfemur length (FeL) distance from groin to apex of kneeand tibia length (TbL) distance from apex of knee to heelFrom these total fore limb length (FLL) and total hindlimb length (HLL) which were obtained as the sums ofthe corresponding segment lengths (ie HmL + FaL andFeL + TbL) as well as the limbs-body ratios (HmLSVLFaLSVL FeLSVL TbLSVL) were calculated Tail lengthwas not included in the analysis because many individualshad broken or regenerated tails For each specimen I alsorecorded collection data (region and locality with geographiccoordinates and elevation) as well as bodyweight (119872) whichwas taken shortly after capture to the nearest 01 g Sex wasdetermined by tail base shape and hemipenis eversion or indoubtful cases by dissection Measurements were made witha digital caliper (Mitutoyo CD-610158401015840CX) to the nearest 001mmexcept for SVL which was measured to the nearest 05mmusing a millimeter ruler I could not record all measurementsfrom each specimen due to the bad preservation conditionsof some reptiles so the sample sizes vary among features(Table 1) All measurements were made by the author
24 Meteorological Data The climate elements consideredwere average annual temperature and average annual precip-itation within the natural locations of the animals Spatiallyinterpolated climate data [50] for the 1950ndash2000 period ongrids with spatial resolution of 30 arc-second (often referredto as 1-km spatial resolution) were taken from httpwwwworldclimorg and imported into a GIS application
25 Data Analyses I applied one-way ANOVAwith multipletesting corrections (Duncanrsquos multiple range test MRT) toexamine the presence of sexual size dimorphism (SSD) inbody and limbdimensions in all species studied I used simpleordinary least squares (OLS) regression model treating tem-perature and precipitation as continuous predictors to assessthe relationship between abiotic environmental componentsand morphological traits In this analysis the examinedsamples suppose a great dispersion of the data that cannotbe addressed with log-transformations In fact both bodysize ranges within the samples and the sample sizes acrossthe observed locations vary among the species Howeverprior to analyses the data were tested for normality (Shapiro-Wilkrsquos test) and homogeneity of variances (Levenersquos test)As argued in the Introduction testing the possible presenceof intraspecific clines requires that sexual size dimorphismwithin the species studied to be taken into account Inview of these considerations relationships between abioticvariables and the measurementsratios were tested for eachsex separately I also controlled for the effect of temperatureand precipitation on limb length (for each sex separately) byMANCOVA using SVL as a covariate In this analysis both
abiotic factors treated separately as categorical predictors andtotal fore limb length (FLL) and total hind limb length (HLL)as dependent variablesMultiple ordinary least squares (OLS)regression analysis using SVL as a dependent variable andtreating climatic factors as predictors was applied to examinethe combined effect of temperature and precipitation on bodysizeHere in order to produce amoremeaningful index of theobserved effects the slope coefficients were transformed intostandardized ldquobetardquo coefficients (120573) All statistical analyseswere done using Statistica 8 (StatSoft Inc USA)
3 Results
31 Sexual Dimorphism Summary data of basicmorphologi-cal features for males and females of each species are given inTable 1 Simple intersexual comparisons (one-way ANOVA)of the lizardsrsquo external morphology indicate that male Oelegans andA boskianus are significantly (119875 lt 00001) longerand heavier than females (Table 1) In M guttulata femalesare longer but not heavier than males In P laevis malesare marginally nonsignificantly heavier than females but notlonger
Moreover there is a pronounced sexual dimorphism (119875 lt00001) in extremity length Within all the species studied inabsolute terms (mm) HmL FaL FeL and TbL in males weremuch greater (from 73 to 136) than those in conspecificfemales Assessing the ratios of fore and hind limbsrsquo segmentsrelative to SVL (ie HmLSVL FaLSVL FeLSVL andTbLSVL) made very little difference (data not shown)
32 Environment-Related Variation
P laevis The studied locations are characterized by a highlysignificant correlation between latitude and both temperature(119903 = minus0607 119875 lt 00001) and precipitation (119903 = 0879119875 lt 00001) and between temperature and precipitationsas well (119903 = minus0732 119875 lt 00001) Considering body sizegradient the scatter plots shown in Figure 2 indicate thatalthough the individuals exhibit a notable dispersion (it isalso true for other species studied) the major trends becomeevident Male SVL does not vary significantly in relation toclimate (temperature OLS slope plusmn SE = minus025 plusmn 045 119903 =minus0081 119875 = 0585 precipitation slope = minus0001 plusmn 0006119903 = minus0032 119875 = 0827) whereas females are greatly affectedby it growing significantly heavier and longer (Figures 2(a)and 2(b)) in cool and wet habitats (temperature slope =minus147 plusmn 031 119903 = minus0543 119875 lt 00001 precipitation slope =001 plusmn 0004 119903 = 0369 119875 = 0005) Continuous sampling(Table 2) revealed a stronger effect of climate on corporealproportions than on absolute sizes Analysis of latitudinalvariability in body proportions showed a significant relation-ship between temperature and relative extremities length Inboth sexes relatively larger limbs are associated with hothabitats among females the recorded temperature-relatedcorrelation was highly significant for these morphologicalvariables The influence of precipitation was less obviousalthough in females it was still significant for all ratios Inmales only HmLSVL varied in relation to precipitationWith SVL as a covariate however a MANCOVA indicates a
International Journal of Zoology 5
Table 1 Morphological characteristics of lizard species studied and their intersexual comparisons (one-way ANOVA with multiple testingcorrections Duncanrsquos multiple range test MRT)
Species Features Range Mean plusmn SD nDDCC
119875 119865
DD CC DD CC
Phoenicolacertalaevis
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
25ndash105505ndash7753ndash9
59ndash932762ndash1184875ndash13
3ndash11450ndash76
522ndash73459ndash7877ndash10585ndash114
585 plusmn 191
6353 plusmn 665699 plusmn 079
761 plusmn 077
966 plusmn 103
1104 plusmn 102
513 plusmn 194
6297 plusmn 601
634 plusmn 047
696 plusmn 046
878 plusmn 063
987 plusmn 062
485648564756475647564756
0059065400001000010000100001
3620202636284927405101
Ophisops elegans
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
09ndash4240ndash59445ndash61478ndash67253ndash872715ndash1053
12ndash3540ndash53539ndash54423ndash62252-747646ndash922
25 plusmn 072
4807 plusmn 427
53 plusmn 04
582 plusmn 05
722 plusmn 071
9 plusmn 081
198 plusmn 051
4647 plusmn 344
466 plusmn 035
515 plusmn 041
629 plusmn 057
778 plusmn 063
856285628461846184618461
lt000010016lt00001lt00001lt00001lt00001
23225859838732069119538
Acanthodactylusboskianus
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
17ndash13852ndash8852ndash918592ndash992845ndash1338108ndash164
3ndash12150ndash805462ndash7358ndash84883ndash122810ndash1454
699 plusmn 215
659 plusmn 646
69 plusmn 075
796 plusmn 079
112 plusmn 104
1377 plusmn 119
535 plusmn 163
6111 plusmn 583
626 plusmn 056
712 plusmn 062
981 plusmn 075
1212 plusmn 087
121931219311385113851148511485
lt00001lt00001lt00001lt00001lt00001lt00001
37233131433365571086211606
Mesalinaguttulata
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
08ndash640ndash57413ndash5945ndash624595ndash82717ndash967
116ndash3740ndash5639ndash5442ndash56557ndash776664ndash88
204 plusmn 063
4561 plusmn 301
5 plusmn 031
534 plusmn 03
707 plusmn 046
839 plusmn 045
201 plusmn 056
469 plusmn 373
462 plusmn 029
495 plusmn 03
652 plusmn 041
763 plusmn 044
98791199511895118951189511895
07480005lt00001lt00001lt00001lt00001
01078078228409796115251
80
76
72
68
64
60
56
52
4814 15 16 17 18 19 20 21
SVL
(mm
)
Average annual temperature (∘C)
(a)
80
76
72
68
64
60
56
52
48
SVL
(mm
)
300 350 400 450 500 800550 600 650 700 750
Average annual precipitation (mm)
(b)
Figure 2 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Phoenicolacerta laevissolid line with circles males dashed line with triangles females
statistically significant effect of temperature on both FLL andHLL in females (Table 3) The results of multiple regressionwith SVL as a response (Table 4) indicate that the body size-environment link is more obvious in respect to temperaturethan to precipitation Thus in females SVL is much moreaffected by the former variable 119875 = 00009 120573 = minus061 plusmn 017than by the latter 119875 = 0588 120573 = minus009 plusmn 017
O elegans Examination of the environmental relationshipacross the observed area of thismostlyMediterranean species
demonstrates a highly significant correlation between latitudeand both temperature (119903 = minus0801 119875 lt 00001) and pre-cipitation (119903 = 0433 119875 lt 00001) Temperature is negativelycorrelated with precipitation (119903 = minus0388 119875 lt 00001)Snout-vent lengths (Figures 3(a) and 3(b)) of both sexesincrease with temperature (males slope = minus072 plusmn 018 119903 =minus0402 119875 = 00001 females slope = minus049plusmn014 119903 = minus0408119875 = 0001) and with precipitation (males slope = 0007 plusmn0001 119903 = 0395 119875 = 00002 females slope = 0005 plusmn 0001119903 = 0374 119875 = 0002)
6 International Journal of Zoology
Table 2 Climate-morphology relationship between average annual temperature (AAT)average annual precipitation (AAP) and bodymeasurementsratios (regression analysis with temperature and precipitation as the predictors and features as the responses) Positivecorrelation (+) and negative correlation (minus) single sign significant difference (119875 lt 005) and double sign highly significant difference (119875 lt00001)
FeaturesPhoenicolacerta laevis Ophisops elegans Acanthodactylus boskianus Mesalina guttulata
AAT AAP AAT AAP AAT AAP AAT AAPDD CC DD CC DD CC DD CC DD CC DD CC DD CC DD CC
M minus + minus + + + +SVL minusminus + minus minus + + minus + + +HmL minus minus + ++FaL minus minus + + +FeL minus minus ++ +TbL minus minus + +HmLSVL + ++ minus minus + minus minus +FaLSVL + ++ minus + minusminus minus +FeLSVL + ++ minusminus + + + minus minus + minus minus
TbLSVL + ++ minus + minus minus + minus minus
Table 3 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Phoenicolacerta laevis with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
77
88
052111
079152
145149
243333
02140199
00280004
Covariate(SVL)
FLLHLL
11
11
73211275
23494734
20171707
71641038
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
033276
404766
093371
12321679
03410062
lt0001lt0001
Error FLLHLL
3737
4646
036074
033045
Precipitation FLLHLL
88
88
047099
064150
126130
187327
02940275
00880005
Covariate(SVL)
FLLHLL
11
11
71081208
21624677
19131582
62751017
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
030296
493798
081388
14331738
03740056
lt0001lt0001
Error FLLHLL
3636
4646
037076
034045
Table 4 The effect of climate variables on snout-vent length (SVL) Results of multiple regression with SVL as a dependent variable andclimatic factors as predictors
Effect of temperature Effect of precipitation120573 plusmn SE 119905 119875 120573 plusmn SE 119905 119875
Phoenicolacertalaevis
DD minus021 plusmn 021 minus098 0328 minus018 plusmn 021 minus085 0399CC minus0615 plusmn 017 minus351 00009 minus009 plusmn 017 minus054 0588
Ophisops elegansDD minus027 plusmn 011 minus251 0013 026 plusmn 011 238 0019CC minus032 plusmn 012 minus266 0009 025 plusmn 012 208 0041
Acanthodactylusboskianus
DD minus003 plusmn 009 minus034 0727 0136 plusmn 009 137 0207CC minus013 plusmn 011 minus115 0251 021 plusmn 011 minus177 0079
Mesalina guttulata DD minus003 plusmn 009 minus041 068 021 plusmn 009 236 0019CC minus014 plusmn 009 minus151 0134 033 plusmn 009 339 0001
International Journal of Zoology 7
SVL
(mm
)
Average annual temperature (∘C)
60
56
52
48
44
40
8 10 12 14 16 18 20
(a)
SVL
(mm
)
60
56
52
48
44
40
100 200 300 400 500 700 800600 900
Average annual precipitation (mm)
(b)
Figure 3 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Ophisops elegans solidline with circles males dashed line with triangles females
The corporeal ratios and especially lengths (Table 2)are noticeably influenced by the local climate conditionsRegression analysis indicates that the sexes generally followsimilar trends in their corporal dimensions and becomesignificantly larger at higher latitudes By analogy with SVLappendages were positively correlated with precipitation andwere negatively correlated with temperature In additionin both sexes the longer femora may be associated withincreased precipitation However after accounting for SVLa MANCOVA reveals a nonsignificant effect of both abi-otic predictors on limb size (Table 5) Multiple regressiondemonstrates the equivalency of two climate influences intheir relationships with SVL (Table 4) Furthermore malesand females in general did not differ from one another intheir responses to either temperature (120573 = minus027plusmn011 versus120573 = minus032 plusmn 012) or precipitation (120573 = 026 plusmn 011 versus120573 = 025 plusmn 012) gradient
A boskianus In the desert habitats of this species temperaturewas uncorrelated with latitude (119903 = minus0082 119875 = 0247)across the observed geographic range There is however apronounced latitudinal precipitation gradient (119903 = 0815119875 lt 00001) and a negative relationship between annualaverages of temperature and precipitation 119903 = minus0367 119875 lt00001 In this lizard the sexes differ in respect to theirenvironmental-morphological connection (Figures 4(a) and4(b)) The SVL of males did not correlate consistently withtemperature (slope = minus021 plusmn 029 119903 = minus0067 119875 = 0485)and precipitation (slope = 001 plusmn 0008 119903 = 0134 119875 =0160) whereas the SVL of females varied in relation to thesevariables slope = minus081 plusmn 034 119903 = minus0243 119875 = 0021 andslope = 002 plusmn 0007 119903 = 0280 119875 = 0007 for temperatureand precipitation respectively
Corporeal measurements (Table 2) showed a close rela-tionship with rainfall in both sexes and increased precip-itation is correlated to shorter extremities relative to SVLDespite the fact that the appendages tend to lengthen relativeto their SVL with rise in temperature this abiotic component
would seem to affect only hind limb segments (FeL and TbL)The MANCOVA results (Table 6) also suggest that withinboth sexes the temperature gradient significantly contributesonly to HLL variation Precipitation had a significant effecton hind extremity in both sexes furthermore within males itinfluenced the variation in FLL as well Analysis of combinedeffect of environmental variables when both temperature andprecipitation were regressed against SVL (Table 4) revealsthe role of moisture as a major predictor of intraspecificvariability Moreover males and females were similar in thistrend 120573 = minus003 plusmn 009 (temperature) 120573 = 0136 plusmn 009(precipitation) for males and 120573 = 013 plusmn 011 versus 120573 =021 plusmn 011 for females respectively
M guttulata The studied geographic range of this desertlacertid is characterized by a highly significant correlationbetween latitude and both temperature (119903 = 0657 119875 lt00001) and precipitation (119903 = 0682 119875 lt 00001) whereastemperature was uncorrelated with precipitation (119903 = 0030119875 = 0654) In both sexes SVL (Figures 5(a) and 5(b))increased along a rainfall gradient slope = 0006 plusmn 0002 119903 =0215 119875 = 0018 for males slope = 001 plusmn 0004 119903 = 0317119875 = 0001 for females Continuous sampling also revealed aninsignificant relationship between temperature and SVL inthis species Regression analysis (Table 2) indicated an impor-tant role of precipitation in the creation of clines in body andlimb dimensions Moreover spatial changes of both climaticcomponents may induce some allometric shifts in latitudinalspace Thus temperature rise has led to the appearance oflonger (relative to SVL) extremities among females Thisobservation was confirmed by MANCOVA a significantassociation was observed between either FLL or HLLandtemperature as well as between HLL and precipitation Inmales this approach however indicates a nonsignificanteffect of both climatic variables on limb dimensions (Table 7)
Similarly to other desert dwellers (A boskianus) in thisspecies too precipitation level is a stronger ecological deter-minant of body length (Table 4) than temperature gradient
8 International Journal of Zoology
Table 5 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Ophisops elegans with SVL as a covariate
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
1717
1616
012048
026071
081121
140147
06720278
01860155
Covariate(SVL)
FLLHLL
11
11
25225696
5291525
16331432
28643183
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
101138
251265
651347
1359552
00130067
00010023
Error FLLHLL
6565
4242
015039
018047
Precipitation FLLHLL
2323
1717
013056
024064
083156
129130
06730086
02430241
Covariate(SVL)
FLLHLL
11
11
21864902
5341481
14061366
28222971
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
123201
263305
796559
1393612
00060021
00010018
Error FLLHLL
5959
4141
015035
018049
14 16 18 20 22 24
SVL
(mm
)
Average annual temperature (∘C)
85
80
75
70
65
60
55
50
(a)
SVL
(mm
)
85
80
75
70
65
60
55
50
0 50 150 200100 250 300
Average annual precipitation (mm)
(b)
Figure 4 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Acanthodactylusboskianus solid line with circles males dashed line with triangles females
119875 = 0019 120573 = 021plusmn009 versus119875 = 0680 120573 = minus003plusmn009for males 119875 = 0001 120573 = 033 plusmn 009 versus 119875 = 0134120573 = minus014 plusmn 009 for females respectively
4 Discussion
Despite the inability of ectotherms to produce significantmetabolic heat the interaction between body size and heatbalance based on a set of behavioural anatomical andphysiological mechanisms [51] that contribute to fitnessmight explain the peculiarity of ecological drivers in sizeclines among these animalsThe relationship between habitatconditions and morphological variables (body tail or limbdimensions) and consequent shifts in phenology due toclimate change have been observed across a wide range ofreptile taxa [52ndash54] It is possible that in diurnal squamates
environmental conditions may favour selection for smaller-sized individuals [55] which due to the ability to achievemore accurate adjustment of their body temperature havebetter thermoregulatory capacities [56] and thus display highactivity levels In terrestrial ectotherms thermoregulation isrealized behaviourally by habitat selection and daily activitypattern [57] while at the same time morphological special-ization may also essentially facilitate it [55] For exampleShine and Madsen [58] pointed out that for relatively smallreptile species behavioural thermoregulation seems to bemore important especially in conditions of high diurnalthermal heterogeneity In this context desert reptiles inhab-iting warmer regions with lower thermoregulatory costs mayadjust their body temperature mainly behaviourally andthus invest less in adjustment of either body size or shapein relation to ambient temperature Despite the great data
International Journal of Zoology 9
Table 6 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Acanthodactylus boskianus with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
3535
2828
089151
053131
141191
125175
01180012
02390040
Covariate(SVL)
FLLHLL
11
11
60441731
34366125
95262186
80188176
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
203445
4952911
320562
11563885
00780021
0001lt0001
Error FLLHLL
6565
5151
063079
042074
Precipitation FLLHLL
3333
3131
086151
046116
178186
101171
00230016
04810049
Covariate(SVL)
FLLHLL
11
11
64151792
23944222
13182201
51436151
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
161422
7043482
332518
15145073
00730026
lt0001lt0001
Error FLLHLL
6767
4848
048081
046068
14 16 18 20 22 24
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
Average annual temperature (∘C)
(a)
0 50 150 200100 250 300 350 400 450 500 550
Average annual precipitation (mm)
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
(b)
Figure 5The relationship between SVL and (a) average annual temperature and (b) average annual precipitation inMesalina guttulata solidline with circles males dashed line with triangles females
dispersion (as shown in the scatter plots) it was foundthat among the two ldquodesertrdquo species studied (M guttulataand A boskianus) only females of the latter were smallerin hot temperatures whereas in both sexes of the formeras well as in A boskianus males SVL did not correlatewith temperature In the Mediterranean region P laevisand O elegans inhabit cooler climates than the desert Aboskianus and M guttulata In these environments largergravid reptiles in addition to the buffering effects of thebehavioural thermoregulation supplied by the mother [5960] can provide greater temperature stability during thepreoviposition period Volynchik [19] however found that alarge-bodied local viper (Vipera palaestinae) with a Mediter-ranean distribution pattern does not follow Bergmannrsquos ruleor its converse At the same time the most ldquocold-lovingrdquolizard (O elegans) in my own sample obeyed Bergmannrsquos
rule growing larger in cooler environments On the otherhand in desert habitats this pattern of greater thermal inertiaseems to be less important and the behavioural componentof thermoregulation becomes paramount
The impact of ambient temperature on external mor-phology is also significant in respect to relative extremitylengths different degrees of intraspecific variability in limbproportions supporting Allenrsquos rule were observed in all thespecies studied The present findings indicate that temper-ature decrease across the observed habitats could lead toreduction in size of extremity segments relative to bodylength thus constituting a compensatory adaptation to eithercooler or hotter areas I noted an allometric shift in humerusforearm femur and tibia lengths relative to SVL along atemperature gradient among P laevis A similar relationshipbetween average annual temperature and corporeal ratioswas
10 International Journal of Zoology
Table 7 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) inMesalina guttulata with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
2525
2424
021045
024054
156143
181191
00650110
00290019
Covariate(SVL)
FLLHLL
11
11
20084405
9872011
14751407
72797114
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
4501082
8922073
33113455
65837331
lt0001lt0001
lt0001lt0001
Error FLLHLL
9191
6969
013031
013028
Precipitation FLLHLL
2828
2525
019041
022056
142129
162211
01070181
00590008
Covariate(SVL)
FLLHLL
11
11
19504181
9631908
14091307
68667094
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
356901
8021918
25752817
57177133
lt0001lt0001
lt0001lt0001
Error FLLHLL
8888
6868
013032
014026
noted in females of M guttulata Among A boskianus totalhind limb length significantly correlated with both thermalregime and rainfall gradient Hence both Mediterraneanand desert reptiles follow a similar pattern in their bodyshape variation and may benefit from various morphologicalmodifications matched to habitat range
Body temperature changes affect reptile ecology [61]becoming more important to ectotherms living in coolerenvironments which complicate attaining proper body tem-perature [58 62] In support of this my results show the asso-ciation between biogeographic origins of the species exam-ined and their relationship with environmental variables Oninterspecific comparison the most pronounced distinctionswere noted in phenotypic responses to the temperature gra-dient between Mediterranean and desert inhabitants whilethe between-species differences for precipitation-related vari-ation were weaker As expected both Mediterranean regionspecies (P laevis O elegans) display significantly strongerresponses to temperature than desert dwellers (A boskianusM guttulata) Apparently the cooler locations of the formerforce them to exhibit more consistent morphological vari-ability in respect to temperature changes whereas for desertspecies such habitat-morphology connection seems to be lessimportant It is highly likely that the speciesrsquo sensitivity tothe environment is associated not only with their ecologicaldifferentiation but also with body size ranges within thesample Thus this might be one possible explanation for thedifferent albeit relatively minor responses to temperaturebetween ecologically similar species (ie P laevis versus Oelegans andA boskianus versusM guttulata) that were notedhere In the examined samples L laevis owing to its greatermeasurement ranges than O elegans has a higher potentialfor more consistent matching of its body dimensions to theobserved temperature gradient The same is true for the twodesert lizardsA boskianus due to its extended body and limb
ranges in comparison with M guttulata displays a strongermorphological-environmental link
The examination of gender-specific habitat-morphologyinteractions revealed that within three of the four species (Plaevis A boskianus and M guttulata) sensitivity to the envi-ronment is coupledwith sex Considering the effect of climatevariables on SVL the findings demonstrate that females ingeneral show a more consistent link between temperatureand bodylimb measurements than males while the effectof precipitation on external characters was similar for bothsexes Moreover in P laevis SVL was significantly morestrongly correlated with the temperature gradient in femalesthan in malesThese observations indicate the sex-associatedeffect of natural selection pointing to different thermal andmetabolic demands inmales and femalesThus it is likely thatin females the increased body size in colder environmentsis associated with reproduction-induced requirements Thispattern suggests that females due to increased thermalrequirements particularly during vitellogenesis [63] aremore able to generate a range of suitable morphologicalmodifications for maintenance of optimal body temperaturein local environments Overall my findings indicate thatalthough females show amore consistent correlation betweenSVL and a temperature gradient than males the body shapechanges involving both body and limb dimensions arerather preliminary in explaining the observed intersexualdivergence in the habitat-morphology relationship
Environmental conditions within the nest experiencedduring early ontogenesis especially temperature and mois-ture of substrate can significantly affect development andgrowth trajectories of individuals in oviparous reptiles [64ndash68] As observed in many species either posthatching phe-notype or offspring fitness are closely associated with thermalregime [63 69ndash71] In both the laboratory and in naturalnests [64] temperature is traditionally considered to be animportant environmental determinant of reptile size while
International Journal of Zoology 11
the effect of water-related factors is more complex Severalrecent studies have tested the effect of substrate moistureduring incubation of eggs on a diverse range of reptile speciesSignificant effects are found in certain species [66 68 72 73]but not in others [74ndash76] that may reflect either differentwater permeability of the eggshell or interspecific variationin the water content of eggs [77] On the other hand theappearance of morphological variation along a precipitationgradient which in desert lizards is even more evident thanthe temperature-related variability can be considered as aresponse to the local habitats In reptiles food availabilitystrongly affects growth trajectories and is one of the possibledeterminants of body size and shape [78ndash80] Overall inarid regions where vegetation and arthropod fauna aredetermined primarily by precipitation [11] wetter localitiesprovide better food resources to lizards at the populationlevel The present findings suggest that among desert speciesthe possible spatial differences in prey availability and thusin nutrition levels may lead to morphometric differentiationbetween specimens inhabiting dry or wet sites Howeverdetailed studies on possible dietary variation linked tolocal environments are necessary to answer the question ofwhether the habitat conditions which are dependent on pre-cipitation have an effect on body dimensions in these lizards
A nonphylogenetic approach suggests that lizard speciestend to exhibit strong morphological specialization in rela-tion to their habitat [53 81] Variation in body charactersrelated to locomotion which in turn is associated withsubstrate pattern has been observed across many lizard taxa[54 82ndash84] Unfortunately based on available datasets Icould not evaluate whether the shift in substrate usage isassociated with limb proportion changes and so a rationalexplanation for the effect of vegetation on limb lengthsthrough its dependence upon hydrothermal regime remainsto be determined My findings show that generally theexamined species indicate a uniform pattern in extremitiessize variation fore and especially hind limb lengths werepositively correlated with temperature and negatively withprecipitation The results indicate that ecological adaptationto abiotic factors is a powerful source of extremity sizevariation which is under the effect of natural selection Inlizards the morphology-performance relationships suggestthat ground-dwelling species from open landscapes shouldpossess relatively long limb segments to their body length[53] This body shape pattern increases stride length provid-ing better sprinting abilities [85 86] Furthermore shorterextremities may facilitate the locomotion in highly vegetatedareas where long limbs may be disadvantageous [53] In thiscontextmyfindings suggest that various body shape patternssuch as relatively shortlong limbs or their segments whichare suited to the environmental requirements may reflect anadaptation to either dense or sparse vegetation resulting fromdifferent rainfall intensities across the distribution range
Finally given the potential importance of habitats forlimb size variation lizardsmay also use their protruding bodyparts as additional (together with body surface area) heatexchangers In these reptiles for optimal balance betweenheat gain and heat loss isometric size changes to a certainextent are a ldquotwo-edged swordrdquo inwhich high thermal inertia
of large bodies is accompanied by slow heating rates and viceversa In this respect among desert dwellers relatively longextremities and small size enhance heat exchange and seemto be a morphological adaptation for effective thermoreg-ulation In desert areas large daily fluctuations of temper-ature force the ectotherms to quickly respond to changingconditions and rapidly reach the necessary metabolic ratesfor locomotor activity Long-limbed individuals which havean increased surface area-to-volume ratio may enhancetheir heating and cooling abilities through more effectiveinteractions between the body and either solar radiationor surface temperature gradient Hence a consistent linkbetween environmental variables and limb lengths can alsobe explained by their importance for maintenance of optimalbody temperature in local environments As shown above thefact that the extremity size-environment link is more obviousin respect to hind limbs than to fore ones reinforces thishypothesis relatively large hind limbs having an increasedheat exchange capacity are much more powerful tool foreffective thermoregulation than small fore extremities
In summary the lacertid lizards I studied generallyfollowed the ecogeographic rules of Bergmann and AllenIn addition the findings indicate both intersexual and inter-specific differences in the habitat-morphology relationshipwhich can be considered within the framework of theirfunctional connectionMydata provide evidence that femalestend to show stronger relationships between climate vari-ables and body dimensions than males In desert speciestemperature has a smaller effect than rainfall on lizardphenotypes Under a constant dry climate water availabilityseems to be the most important abiotic factor in reptileecology In this respect due to the strong association betweenprecipitation and productivity my findings could also beinterpreted as evidence for the hypothesis that different bodysize patterns are linked to the spatial variation in primaryproduction that is the ldquoresource rulerdquo In the Mediterraneanregion lizards the thermal regime is apparently the maindriving force of morphological variability The present studysuggests a complex link between environmental variablesand morphological characters within lacertid species Thephysical conditions such as temperature and precipitationgradient were shown to be able to significantly affect bothbody and limb dimensions and thus as a powerful sourceof variation they play an important role in lizard mor-phology However general statements about the habitat-morphology relationships and their potential importance formaintenance of optimal body temperature in reptiles arehard to make due to the enormous diversity of variationsin body composition and physiology across species sexesand even individuals and the difficulty in evaluating enoughmechanisms in enough species Consequently additionalfield and experimental studies testing both body size andshape variations and their relationships with environmentalvariables especially at the intraspecific level and accountingfor sex-specific aspects are needed to help determine whetherthe observed patterns are common across species and to whatextent they are important for effective thermoregulation
12 International Journal of Zoology
Conflict of Interests
The author declares that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The author would like to thank Shai Meiri for his helpfulcomments on earlier drafts of the paper The author thanksErezMaza for assistancewith data preparationAnat Feldmanfor provision of the GIS-compatible temperature data andNaomi Paz for linguistic editing The author also thanks theIsrael Ministry of Science Culture and Sport for supportingthe National Collections of Natural History at Tel AvivUniversity as a biodiversity environment and agricultureresearch knowledge centre
References
[1] E Mayr Animal Species and Evolution Harvard UniversityPress Cambridge Mass USA 1963
[2] C Ray ldquoThe application of Bergmannrsquos and Allenrsquos rules to thepoikilothermsrdquo Journal of Morphology vol 106 pp 85ndash1081960
[3] TM Blackburn K J Gaston andN Loder ldquoGeographic gradi-ents in body size a clarification of Bergmannrsquos rulerdquo Diversityand Distributions vol 5 no 4 pp 165ndash174 1999
[4] K J Gaston and TM Blackburn Pattern and Process inMacro-ecology Blackwell Malden Mass USA 2000
[5] C Bergmann ldquoUber die verhaltnisse der warmeokonomie derthiere zu ihrer grosserdquo Gottinger Studien vol 3 pp 595ndash7081847
[6] J A Allen ldquoThe influence of physical conditions in the genesisof speciesrdquo Radical Review vol 1 pp 108ndash140 1877
[7] F C James ldquoGeographic size variation in birds and its relation-ship with climaterdquo Ecology vol 51 pp 365ndash390 1970
[8] C D Burnett ldquoGeographic and climatic correlates of morpho-logical variation inEptesicus fuscusrdquo Journal ofMammalogy vol64 no 3 pp 437ndash444 1983
[9] C C Lindsey ldquoBody sizes of poikilotherm vertebrates at differ-ent latitudesrdquo Evolution vol 20 pp 456ndash465 1966
[10] M L Rosenzweig ldquoThe strategy of body size in mammaliancarnivoresrdquo American Midland Naturalist vol 80 pp 299ndash3151968
[11] Y Yom-Tov and E Geffen ldquoGeographic variation in body sizethe effects of ambient temperature and precipitationrdquoOecologiavol 148 no 2 pp 213ndash218 2006
[12] Y Yom-Tov and H Nix ldquoClimatological correlates for body sizeof five species of Australian mammalsrdquo Biological Journal of theLinnean Society vol 29 no 4 pp 245ndash262 1986
[13] D Pincheira-Donoso and SMeiri ldquoAn intercontinental analysisof climate-driven body size clines in reptiles no support forpatterns no signals of processesrdquo Evolutionary Biology vol 40no 4 pp 562ndash578 2013
[14] K G Ashton M C Tracy and A de Queiroz ldquoIs Bergmannrsquosrule valid for mammalsrdquoThe American Naturalist vol 156 no4 pp 390ndash415 2000
[15] S Meiri and T Dayan ldquoOn the validity of Bergmannrsquos rulerdquoJournal of Biogeography vol 30 no 3 pp 331ndash351 2003
[16] K G Ashton ldquoSensitivity of intraspecific latitudinal clines ofbody size for tetrapods to sampling latitude and body sizerdquoIntegrative and Comparative Biology vol 44 no 6 pp 403ndash4122004
[17] K G Ashton and C R Feldman ldquoBergmannrsquos rule in nonavianreptiles turtles follow it lizards and snakes reverse itrdquoEvolutionvol 57 no 5 pp 1151ndash1163 2003
[18] M A Olalla-Tarraga M A Rodrıguez and B A HawkinsldquoBroad-scale patterns of body size in squamate reptiles ofEurope and North Americardquo Journal of Biogeography vol 33no 5 pp 781ndash793 2006
[19] S Volynchik ldquoMorphological variability in Vipera palaesti-nae along an environmental gradientrdquo Asian HerpetologicalResearch vol 3 pp 227ndash239 2012
[20] D Pincheira-Donoso D J Hodgson and T Tregenza ldquoTheevolution of body size under environmental gradients inectothermswhy shouldBergmannrsquos rule apply to lizardsrdquoBMCEvolutionary Biology vol 8 no 1 article 68 2008
[21] R C Stillwell ldquoAre latitudinal clines in body size adaptiverdquoOikos vol 119 no 9 pp 1387ndash1390 2010
[22] S Meiri ldquoBergmannrsquos rulemdashwhatrsquos in a namerdquo Global Ecologyand Biogeography vol 20 no 1 pp 203ndash207 2011
[23] D Pincheira-Donoso ldquoPredictable variation of range-sizesacross an extreme environmental gradient in a lizard adaptiveradiation evolutionary and ecological inferencesrdquo PLoS ONEvol 6 no 12 Article ID e28942 2011
[24] K G Ashton ldquoDo amphibians follow Bergmannrsquos rulerdquo Cana-dian Journal of Zoology vol 80 no 4 pp 708ndash716 2002
[25] M J Angilletta Jr T D Steury andMW Sears ldquoTemperaturegrowth rate and body size in ectotherms fitting pieces of a life-history puzzlerdquo Integrative and Comparative Biology vol 44 no6 pp 498ndash509 2004
[26] C E Oufiero G E A Gartner S C Adolph and T GarlandldquoLatitudinal and climatic variation in body size and dorsalscale counts in Sceloporus lizards a phylogenetic perspectiverdquoEvolution vol 65 no 12 pp 3590ndash3607 2011
[27] S Meiri ldquoEvolution and ecology of lizard body sizesrdquo GlobalEcology and Biogeography vol 17 no 6 pp 724ndash734 2008
[28] D Atkinson and RM Sibly ldquoWhy are organisms usually biggerin colder environments Making sense of a life history puzzlerdquoTrends in Ecology amp Evolution vol 12 pp 235ndash239 1997
[29] F B Cruz L A Fitzgerald R E Espinoza and J A Schulte IIldquoThe importance of phylogenetic scale in tests of Bergmannrsquosand Rapoportrsquos rules lessons from a clade of South Americanlizardsrdquo Journal of Evolutionary Biology vol 18 no 6 pp 1559ndash1574 2005
[30] T AMousseau ldquoEctotherms follow the converse to BergmannrsquosRulerdquo Evolution vol 51 pp 630ndash632 1997
[31] R N Reed ldquoInterspecific patterns of species richness geo-graphic range size and body size among NewWorld venomoussnakesrdquo Ecography vol 26 no 1 pp 107ndash117 2003
[32] D Pincheira-Donoso T Tregenza and D J Hodgson ldquoBodysize evolution in South American Liolaemus lizards of theboulengeri clade a contrasting reassessmentrdquo Journal of Evolu-tionary Biology vol 20 no 5 pp 2067ndash2071 2007
[33] M J Angilletta P H Niewiarowski A E Dunham A Leacheand W P Porter ldquoBergmannrsquos clines in ectotherms illustratinga life-historical perspective with sceloporine lizardsrdquoTheAmer-ican Naturalist vol 164 pp E168ndashE183 2004
[34] M Andersson Sexual Selection Princeton University PressPrinceton NJ USA 1994
International Journal of Zoology 13
[35] F Brana ldquoSexual dimorphism in lacertid lizards male headincrease vs female abdomen increaserdquo Oikos vol 75 pp 511ndash523 1996
[36] E R Pianka ldquoLizard species density in the Kalahari desertrdquoEcology vol 52 pp 1024ndash1029 1971
[37] E R Pianka ldquoSome intercontinental comparisons of desertlizardsrdquoNational Geographic Research vol 1 no 4 pp 490ndash5041985
[38] B H Brattstrom ldquoSocial and thermoregulatory behavior of thebearded dragon Amphibolurus barbatusrdquo Copeia vol 3 pp484ndash497 1971
[39] G C Grigg and F Seebacher ldquoField test of a paradigm hyster-esis of heart rate in thermoregulation by a free-ranging lizard(Pogona barbata)rdquo Proceedings of the Royal Society B BiologicalSciences vol 266 no 1425 pp 1291ndash1297 1999
[40] F Seebacher and C E Franklin ldquoControl of heart rate duringthermoregulation in the heliothermic lizard Pogona barbataimportance of cholinergic and adrenergic mechanismsrdquo TheJournal of Experimental Biology vol 204 no 24 pp 4361ndash43662001
[41] G J Tattersall and R M Gerlach ldquoHypoxia progressivelylowers thermal gaping thresholds in bearded dragons Pogonavitticepsrdquo The Journal of Experimental Biology vol 208 no 17pp 3321ndash3330 2005
[42] D F DeNardo T E Zubal and T C M Hoffman ldquoCloacalevaporative cooling a previously undescribedmeans of increas-ing evaporative water loss at higher temperatures in a desertectotherm theGilamonsterHeloderma suspectumrdquoThe Journalof Experimental Biology vol 207 no 6 pp 945ndash953 2004
[43] S Jaffe ldquoClimate of Israelrdquo inTheZoogeography of Israel Y Yom-Tov and E Tchernov Eds pp 79ndash92 Dr W Junk PublishersDordrecht The Netherlands 1988
[44] U Roll L Stone and S Meiri ldquoHot-spot facts and artifacts-questioning Israelrsquos great biodiversityrdquo Israel Journal of Ecologyand Evolution vol 55 no 3 pp 263ndash279 2009
[45] W Bischoff and J F Schmidtler ldquoNew data on the distributionmorphology and habitat choice of the Lacerta laevis-kulzericomplexrdquo Natura Croatica vol 8 no 3 pp 211ndash222 1999
[46] A Disi D Modry P Necas and L Rifai Amphibians andReptiles of the Hashemite Kingdom of Jordan An Atlas and FieldGuide Edit Chimaira Frankfurt Germany 2001
[47] A Bouskila and P Amitai Handbook of Amphibians andReptiles of Israel Keter Publishing House Jerusalem Israel2001 (Hebrew)
[48] A Bar and G Haimovitch A Field Guide to Reptiles andAmphibians of Israel Pazbar LTD Herzliya Israel 2012
[49] Y L Werner ldquoGeographic sympatry of Acanthodactylus opheo-durus with A boskianus in the Levantrdquo Zoology in the MiddleEast vol 1 pp 92ndash95 1986
[50] R J Hijmans S E Cameron J L Parra P G Jones and AJarvis ldquoVery high resolution interpolated climate surfaces forglobal land areasrdquo International Journal of Climatology vol 25no 15 pp 1965ndash1978 2005
[51] R B Huey ldquoTemperature physiology and the ecology ofreptilesrdquo inBiology of the Reptilia CGans and FH Pough Edsvol 12 of Physiology (C) pp 25ndash91 Academic Press New YorkNY USA 1982
[52] D J Irschick and J B Losos ldquoDo lizards avoid habitats inwhich performance is submaximal The relationship betweensprinting capabilities and structural habitat use in Caribbeananolesrdquo The American Naturalist vol 154 no 3 pp 293ndash3051999
[53] B Vanhooydonck and R Van Damme ldquoEvolutionary relation-ships between body shape and habitat use in lacertid lizardsrdquoEvolutionary Ecology Research vol 1 no 7 pp 785ndash805 1999
[54] J Melville and R Swain ldquoEvolutionary relationships betweenmorphology performance and habitat openness in the lizardgenus Niveoscincus (Scincidae Lygosominae)rdquo Biological Jour-nal of the Linnean Society vol 70 no 4 pp 667ndash683 2000
[55] R B Huey and M Slatkin ldquoCost and benefits of lizard thermo-regulationrdquo The Quarterly Review of Biology vol 51 no 3 pp363ndash384 1976
[56] R D Stevenson ldquoBody size and limits to the daily range of bodytemperature in terrestrial ectothermsrdquoTheAmericanNaturalistvol 125 pp 102ndash117 1985
[57] B W Grant ldquoTrade-offs in activity time and physiologicalperformance for thermoregulating desert lizards Sceloporusmerriamirdquo Ecology vol 71 no 6 pp 2323ndash2333 1990
[58] R Shine and T Madsen ldquoIs thermoregulation unimportant tomost reptiles An example using water pythons (Liasis fuscus)in tropical AustraliardquoPhysiological Zoology vol 69 pp 252ndash2691996
[59] R Shine ldquoReptilian viviparity in cold climates testing theassumptions of an evolutionary hypothesisrdquo Oecologia vol 57no 3 pp 397ndash405 1983
[60] C R Peterson A R Gibson andM E Dorcas ldquoSnake thermalecology the causes and consequences of body temperaturevariationrdquo in Snakes Ecology and Behavior R A Seigel and J TCollins Eds pp 241ndash314 McGraw-Hill New York NY USA1993
[61] R B Huey and J G Kingsolver ldquoEvolution of thermal sensitiv-ity of ectotherm performancerdquo Trends in Ecology and Evolutionvol 4 no 5 pp 131ndash135 1989
[62] J A Dıaz D Bauwens and B Asensio ldquoA comparative studyof the relation between heating rates and ambient temperaturesin lacertid lizardsrdquo Physiological Zoology vol 69 pp 1359ndash13831996
[63] D C Deeming ldquoPost-hatching phenotypic effects of incubationin reptilesrdquo in Reptilian Incubation Environment Evolutionand Behaviour D C Deeming Ed pp 229ndash251 NottinghamUniversity Press Nottingham UK 2004
[64] R Shine M J Elphick and P S Harlow ldquoThe influence ofnatural incubation environments on the phenotypic traits ofhatchling lizardrdquo Ecology vol 78 pp 2559ndash2568 1997
[65] T Flatt R Shine P A Borges-Landaez and S J DownesldquoPhenotypic variation in an oviparousmontane lizard (Bassianaduperreyi) the effects of thermal and hydric incubation envi-ronmentsrdquo Biological Journal of the Linnean Society vol 74 no3 pp 339ndash350 2001
[66] R Shine and M J Elphick ldquoThe effect of short-term weatherfluctuations on temperatures inside lizard nests and on thephenotypic traits of hatchling lizardsrdquo Biological Journal of theLinnean Society vol 72 no 4 pp 555ndash565 2001
[67] O Lourdais R Shine X Bonnet M Guillon and G NaulleauldquoClimate affects embryonic development in a viviparous snakeVipera aspisrdquo Oikos vol 104 no 3 pp 551ndash560 2004
[68] V Delmas X Bonnet M Girondot and A-C Prevot-JulliardldquoVarying hydric conditions during incubation influence eggwater exchange and hatchling phenotype in the red-eared sliderturtlerdquo Physiological and Biochemical Zoology vol 81 no 3 pp345ndash355 2008
[69] X-F Yan X-L Tang F Yue et al ldquoInfluence of ambient temper-ature onmaternal thermoregulation and neonate phenotypes in
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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International Journal of
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Zoology
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International Journal of
Microbiology
4 International Journal of Zoology
prefers hard substrate and scattered rocks and avoids sanddunes [46ndash48] It is found from 350m below sea level to2000m above sea level (TAUM records)
23MorphologicalMeasurements For each specimen Imea-sured the following snout-vent length (SVL) humerus length(HmL) distance from axilla to apex of elbow forearmlength (FaL) distance from elbow apex to apex of wristfemur length (FeL) distance from groin to apex of kneeand tibia length (TbL) distance from apex of knee to heelFrom these total fore limb length (FLL) and total hindlimb length (HLL) which were obtained as the sums ofthe corresponding segment lengths (ie HmL + FaL andFeL + TbL) as well as the limbs-body ratios (HmLSVLFaLSVL FeLSVL TbLSVL) were calculated Tail lengthwas not included in the analysis because many individualshad broken or regenerated tails For each specimen I alsorecorded collection data (region and locality with geographiccoordinates and elevation) as well as bodyweight (119872) whichwas taken shortly after capture to the nearest 01 g Sex wasdetermined by tail base shape and hemipenis eversion or indoubtful cases by dissection Measurements were made witha digital caliper (Mitutoyo CD-610158401015840CX) to the nearest 001mmexcept for SVL which was measured to the nearest 05mmusing a millimeter ruler I could not record all measurementsfrom each specimen due to the bad preservation conditionsof some reptiles so the sample sizes vary among features(Table 1) All measurements were made by the author
24 Meteorological Data The climate elements consideredwere average annual temperature and average annual precip-itation within the natural locations of the animals Spatiallyinterpolated climate data [50] for the 1950ndash2000 period ongrids with spatial resolution of 30 arc-second (often referredto as 1-km spatial resolution) were taken from httpwwwworldclimorg and imported into a GIS application
25 Data Analyses I applied one-way ANOVAwith multipletesting corrections (Duncanrsquos multiple range test MRT) toexamine the presence of sexual size dimorphism (SSD) inbody and limbdimensions in all species studied I used simpleordinary least squares (OLS) regression model treating tem-perature and precipitation as continuous predictors to assessthe relationship between abiotic environmental componentsand morphological traits In this analysis the examinedsamples suppose a great dispersion of the data that cannotbe addressed with log-transformations In fact both bodysize ranges within the samples and the sample sizes acrossthe observed locations vary among the species Howeverprior to analyses the data were tested for normality (Shapiro-Wilkrsquos test) and homogeneity of variances (Levenersquos test)As argued in the Introduction testing the possible presenceof intraspecific clines requires that sexual size dimorphismwithin the species studied to be taken into account Inview of these considerations relationships between abioticvariables and the measurementsratios were tested for eachsex separately I also controlled for the effect of temperatureand precipitation on limb length (for each sex separately) byMANCOVA using SVL as a covariate In this analysis both
abiotic factors treated separately as categorical predictors andtotal fore limb length (FLL) and total hind limb length (HLL)as dependent variablesMultiple ordinary least squares (OLS)regression analysis using SVL as a dependent variable andtreating climatic factors as predictors was applied to examinethe combined effect of temperature and precipitation on bodysizeHere in order to produce amoremeaningful index of theobserved effects the slope coefficients were transformed intostandardized ldquobetardquo coefficients (120573) All statistical analyseswere done using Statistica 8 (StatSoft Inc USA)
3 Results
31 Sexual Dimorphism Summary data of basicmorphologi-cal features for males and females of each species are given inTable 1 Simple intersexual comparisons (one-way ANOVA)of the lizardsrsquo external morphology indicate that male Oelegans andA boskianus are significantly (119875 lt 00001) longerand heavier than females (Table 1) In M guttulata femalesare longer but not heavier than males In P laevis malesare marginally nonsignificantly heavier than females but notlonger
Moreover there is a pronounced sexual dimorphism (119875 lt00001) in extremity length Within all the species studied inabsolute terms (mm) HmL FaL FeL and TbL in males weremuch greater (from 73 to 136) than those in conspecificfemales Assessing the ratios of fore and hind limbsrsquo segmentsrelative to SVL (ie HmLSVL FaLSVL FeLSVL andTbLSVL) made very little difference (data not shown)
32 Environment-Related Variation
P laevis The studied locations are characterized by a highlysignificant correlation between latitude and both temperature(119903 = minus0607 119875 lt 00001) and precipitation (119903 = 0879119875 lt 00001) and between temperature and precipitationsas well (119903 = minus0732 119875 lt 00001) Considering body sizegradient the scatter plots shown in Figure 2 indicate thatalthough the individuals exhibit a notable dispersion (it isalso true for other species studied) the major trends becomeevident Male SVL does not vary significantly in relation toclimate (temperature OLS slope plusmn SE = minus025 plusmn 045 119903 =minus0081 119875 = 0585 precipitation slope = minus0001 plusmn 0006119903 = minus0032 119875 = 0827) whereas females are greatly affectedby it growing significantly heavier and longer (Figures 2(a)and 2(b)) in cool and wet habitats (temperature slope =minus147 plusmn 031 119903 = minus0543 119875 lt 00001 precipitation slope =001 plusmn 0004 119903 = 0369 119875 = 0005) Continuous sampling(Table 2) revealed a stronger effect of climate on corporealproportions than on absolute sizes Analysis of latitudinalvariability in body proportions showed a significant relation-ship between temperature and relative extremities length Inboth sexes relatively larger limbs are associated with hothabitats among females the recorded temperature-relatedcorrelation was highly significant for these morphologicalvariables The influence of precipitation was less obviousalthough in females it was still significant for all ratios Inmales only HmLSVL varied in relation to precipitationWith SVL as a covariate however a MANCOVA indicates a
International Journal of Zoology 5
Table 1 Morphological characteristics of lizard species studied and their intersexual comparisons (one-way ANOVA with multiple testingcorrections Duncanrsquos multiple range test MRT)
Species Features Range Mean plusmn SD nDDCC
119875 119865
DD CC DD CC
Phoenicolacertalaevis
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
25ndash105505ndash7753ndash9
59ndash932762ndash1184875ndash13
3ndash11450ndash76
522ndash73459ndash7877ndash10585ndash114
585 plusmn 191
6353 plusmn 665699 plusmn 079
761 plusmn 077
966 plusmn 103
1104 plusmn 102
513 plusmn 194
6297 plusmn 601
634 plusmn 047
696 plusmn 046
878 plusmn 063
987 plusmn 062
485648564756475647564756
0059065400001000010000100001
3620202636284927405101
Ophisops elegans
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
09ndash4240ndash59445ndash61478ndash67253ndash872715ndash1053
12ndash3540ndash53539ndash54423ndash62252-747646ndash922
25 plusmn 072
4807 plusmn 427
53 plusmn 04
582 plusmn 05
722 plusmn 071
9 plusmn 081
198 plusmn 051
4647 plusmn 344
466 plusmn 035
515 plusmn 041
629 plusmn 057
778 plusmn 063
856285628461846184618461
lt000010016lt00001lt00001lt00001lt00001
23225859838732069119538
Acanthodactylusboskianus
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
17ndash13852ndash8852ndash918592ndash992845ndash1338108ndash164
3ndash12150ndash805462ndash7358ndash84883ndash122810ndash1454
699 plusmn 215
659 plusmn 646
69 plusmn 075
796 plusmn 079
112 plusmn 104
1377 plusmn 119
535 plusmn 163
6111 plusmn 583
626 plusmn 056
712 plusmn 062
981 plusmn 075
1212 plusmn 087
121931219311385113851148511485
lt00001lt00001lt00001lt00001lt00001lt00001
37233131433365571086211606
Mesalinaguttulata
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
08ndash640ndash57413ndash5945ndash624595ndash82717ndash967
116ndash3740ndash5639ndash5442ndash56557ndash776664ndash88
204 plusmn 063
4561 plusmn 301
5 plusmn 031
534 plusmn 03
707 plusmn 046
839 plusmn 045
201 plusmn 056
469 plusmn 373
462 plusmn 029
495 plusmn 03
652 plusmn 041
763 plusmn 044
98791199511895118951189511895
07480005lt00001lt00001lt00001lt00001
01078078228409796115251
80
76
72
68
64
60
56
52
4814 15 16 17 18 19 20 21
SVL
(mm
)
Average annual temperature (∘C)
(a)
80
76
72
68
64
60
56
52
48
SVL
(mm
)
300 350 400 450 500 800550 600 650 700 750
Average annual precipitation (mm)
(b)
Figure 2 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Phoenicolacerta laevissolid line with circles males dashed line with triangles females
statistically significant effect of temperature on both FLL andHLL in females (Table 3) The results of multiple regressionwith SVL as a response (Table 4) indicate that the body size-environment link is more obvious in respect to temperaturethan to precipitation Thus in females SVL is much moreaffected by the former variable 119875 = 00009 120573 = minus061 plusmn 017than by the latter 119875 = 0588 120573 = minus009 plusmn 017
O elegans Examination of the environmental relationshipacross the observed area of thismostlyMediterranean species
demonstrates a highly significant correlation between latitudeand both temperature (119903 = minus0801 119875 lt 00001) and pre-cipitation (119903 = 0433 119875 lt 00001) Temperature is negativelycorrelated with precipitation (119903 = minus0388 119875 lt 00001)Snout-vent lengths (Figures 3(a) and 3(b)) of both sexesincrease with temperature (males slope = minus072 plusmn 018 119903 =minus0402 119875 = 00001 females slope = minus049plusmn014 119903 = minus0408119875 = 0001) and with precipitation (males slope = 0007 plusmn0001 119903 = 0395 119875 = 00002 females slope = 0005 plusmn 0001119903 = 0374 119875 = 0002)
6 International Journal of Zoology
Table 2 Climate-morphology relationship between average annual temperature (AAT)average annual precipitation (AAP) and bodymeasurementsratios (regression analysis with temperature and precipitation as the predictors and features as the responses) Positivecorrelation (+) and negative correlation (minus) single sign significant difference (119875 lt 005) and double sign highly significant difference (119875 lt00001)
FeaturesPhoenicolacerta laevis Ophisops elegans Acanthodactylus boskianus Mesalina guttulata
AAT AAP AAT AAP AAT AAP AAT AAPDD CC DD CC DD CC DD CC DD CC DD CC DD CC DD CC
M minus + minus + + + +SVL minusminus + minus minus + + minus + + +HmL minus minus + ++FaL minus minus + + +FeL minus minus ++ +TbL minus minus + +HmLSVL + ++ minus minus + minus minus +FaLSVL + ++ minus + minusminus minus +FeLSVL + ++ minusminus + + + minus minus + minus minus
TbLSVL + ++ minus + minus minus + minus minus
Table 3 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Phoenicolacerta laevis with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
77
88
052111
079152
145149
243333
02140199
00280004
Covariate(SVL)
FLLHLL
11
11
73211275
23494734
20171707
71641038
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
033276
404766
093371
12321679
03410062
lt0001lt0001
Error FLLHLL
3737
4646
036074
033045
Precipitation FLLHLL
88
88
047099
064150
126130
187327
02940275
00880005
Covariate(SVL)
FLLHLL
11
11
71081208
21624677
19131582
62751017
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
030296
493798
081388
14331738
03740056
lt0001lt0001
Error FLLHLL
3636
4646
037076
034045
Table 4 The effect of climate variables on snout-vent length (SVL) Results of multiple regression with SVL as a dependent variable andclimatic factors as predictors
Effect of temperature Effect of precipitation120573 plusmn SE 119905 119875 120573 plusmn SE 119905 119875
Phoenicolacertalaevis
DD minus021 plusmn 021 minus098 0328 minus018 plusmn 021 minus085 0399CC minus0615 plusmn 017 minus351 00009 minus009 plusmn 017 minus054 0588
Ophisops elegansDD minus027 plusmn 011 minus251 0013 026 plusmn 011 238 0019CC minus032 plusmn 012 minus266 0009 025 plusmn 012 208 0041
Acanthodactylusboskianus
DD minus003 plusmn 009 minus034 0727 0136 plusmn 009 137 0207CC minus013 plusmn 011 minus115 0251 021 plusmn 011 minus177 0079
Mesalina guttulata DD minus003 plusmn 009 minus041 068 021 plusmn 009 236 0019CC minus014 plusmn 009 minus151 0134 033 plusmn 009 339 0001
International Journal of Zoology 7
SVL
(mm
)
Average annual temperature (∘C)
60
56
52
48
44
40
8 10 12 14 16 18 20
(a)
SVL
(mm
)
60
56
52
48
44
40
100 200 300 400 500 700 800600 900
Average annual precipitation (mm)
(b)
Figure 3 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Ophisops elegans solidline with circles males dashed line with triangles females
The corporeal ratios and especially lengths (Table 2)are noticeably influenced by the local climate conditionsRegression analysis indicates that the sexes generally followsimilar trends in their corporal dimensions and becomesignificantly larger at higher latitudes By analogy with SVLappendages were positively correlated with precipitation andwere negatively correlated with temperature In additionin both sexes the longer femora may be associated withincreased precipitation However after accounting for SVLa MANCOVA reveals a nonsignificant effect of both abi-otic predictors on limb size (Table 5) Multiple regressiondemonstrates the equivalency of two climate influences intheir relationships with SVL (Table 4) Furthermore malesand females in general did not differ from one another intheir responses to either temperature (120573 = minus027plusmn011 versus120573 = minus032 plusmn 012) or precipitation (120573 = 026 plusmn 011 versus120573 = 025 plusmn 012) gradient
A boskianus In the desert habitats of this species temperaturewas uncorrelated with latitude (119903 = minus0082 119875 = 0247)across the observed geographic range There is however apronounced latitudinal precipitation gradient (119903 = 0815119875 lt 00001) and a negative relationship between annualaverages of temperature and precipitation 119903 = minus0367 119875 lt00001 In this lizard the sexes differ in respect to theirenvironmental-morphological connection (Figures 4(a) and4(b)) The SVL of males did not correlate consistently withtemperature (slope = minus021 plusmn 029 119903 = minus0067 119875 = 0485)and precipitation (slope = 001 plusmn 0008 119903 = 0134 119875 =0160) whereas the SVL of females varied in relation to thesevariables slope = minus081 plusmn 034 119903 = minus0243 119875 = 0021 andslope = 002 plusmn 0007 119903 = 0280 119875 = 0007 for temperatureand precipitation respectively
Corporeal measurements (Table 2) showed a close rela-tionship with rainfall in both sexes and increased precip-itation is correlated to shorter extremities relative to SVLDespite the fact that the appendages tend to lengthen relativeto their SVL with rise in temperature this abiotic component
would seem to affect only hind limb segments (FeL and TbL)The MANCOVA results (Table 6) also suggest that withinboth sexes the temperature gradient significantly contributesonly to HLL variation Precipitation had a significant effecton hind extremity in both sexes furthermore within males itinfluenced the variation in FLL as well Analysis of combinedeffect of environmental variables when both temperature andprecipitation were regressed against SVL (Table 4) revealsthe role of moisture as a major predictor of intraspecificvariability Moreover males and females were similar in thistrend 120573 = minus003 plusmn 009 (temperature) 120573 = 0136 plusmn 009(precipitation) for males and 120573 = 013 plusmn 011 versus 120573 =021 plusmn 011 for females respectively
M guttulata The studied geographic range of this desertlacertid is characterized by a highly significant correlationbetween latitude and both temperature (119903 = 0657 119875 lt00001) and precipitation (119903 = 0682 119875 lt 00001) whereastemperature was uncorrelated with precipitation (119903 = 0030119875 = 0654) In both sexes SVL (Figures 5(a) and 5(b))increased along a rainfall gradient slope = 0006 plusmn 0002 119903 =0215 119875 = 0018 for males slope = 001 plusmn 0004 119903 = 0317119875 = 0001 for females Continuous sampling also revealed aninsignificant relationship between temperature and SVL inthis species Regression analysis (Table 2) indicated an impor-tant role of precipitation in the creation of clines in body andlimb dimensions Moreover spatial changes of both climaticcomponents may induce some allometric shifts in latitudinalspace Thus temperature rise has led to the appearance oflonger (relative to SVL) extremities among females Thisobservation was confirmed by MANCOVA a significantassociation was observed between either FLL or HLLandtemperature as well as between HLL and precipitation Inmales this approach however indicates a nonsignificanteffect of both climatic variables on limb dimensions (Table 7)
Similarly to other desert dwellers (A boskianus) in thisspecies too precipitation level is a stronger ecological deter-minant of body length (Table 4) than temperature gradient
8 International Journal of Zoology
Table 5 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Ophisops elegans with SVL as a covariate
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
1717
1616
012048
026071
081121
140147
06720278
01860155
Covariate(SVL)
FLLHLL
11
11
25225696
5291525
16331432
28643183
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
101138
251265
651347
1359552
00130067
00010023
Error FLLHLL
6565
4242
015039
018047
Precipitation FLLHLL
2323
1717
013056
024064
083156
129130
06730086
02430241
Covariate(SVL)
FLLHLL
11
11
21864902
5341481
14061366
28222971
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
123201
263305
796559
1393612
00060021
00010018
Error FLLHLL
5959
4141
015035
018049
14 16 18 20 22 24
SVL
(mm
)
Average annual temperature (∘C)
85
80
75
70
65
60
55
50
(a)
SVL
(mm
)
85
80
75
70
65
60
55
50
0 50 150 200100 250 300
Average annual precipitation (mm)
(b)
Figure 4 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Acanthodactylusboskianus solid line with circles males dashed line with triangles females
119875 = 0019 120573 = 021plusmn009 versus119875 = 0680 120573 = minus003plusmn009for males 119875 = 0001 120573 = 033 plusmn 009 versus 119875 = 0134120573 = minus014 plusmn 009 for females respectively
4 Discussion
Despite the inability of ectotherms to produce significantmetabolic heat the interaction between body size and heatbalance based on a set of behavioural anatomical andphysiological mechanisms [51] that contribute to fitnessmight explain the peculiarity of ecological drivers in sizeclines among these animalsThe relationship between habitatconditions and morphological variables (body tail or limbdimensions) and consequent shifts in phenology due toclimate change have been observed across a wide range ofreptile taxa [52ndash54] It is possible that in diurnal squamates
environmental conditions may favour selection for smaller-sized individuals [55] which due to the ability to achievemore accurate adjustment of their body temperature havebetter thermoregulatory capacities [56] and thus display highactivity levels In terrestrial ectotherms thermoregulation isrealized behaviourally by habitat selection and daily activitypattern [57] while at the same time morphological special-ization may also essentially facilitate it [55] For exampleShine and Madsen [58] pointed out that for relatively smallreptile species behavioural thermoregulation seems to bemore important especially in conditions of high diurnalthermal heterogeneity In this context desert reptiles inhab-iting warmer regions with lower thermoregulatory costs mayadjust their body temperature mainly behaviourally andthus invest less in adjustment of either body size or shapein relation to ambient temperature Despite the great data
International Journal of Zoology 9
Table 6 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Acanthodactylus boskianus with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
3535
2828
089151
053131
141191
125175
01180012
02390040
Covariate(SVL)
FLLHLL
11
11
60441731
34366125
95262186
80188176
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
203445
4952911
320562
11563885
00780021
0001lt0001
Error FLLHLL
6565
5151
063079
042074
Precipitation FLLHLL
3333
3131
086151
046116
178186
101171
00230016
04810049
Covariate(SVL)
FLLHLL
11
11
64151792
23944222
13182201
51436151
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
161422
7043482
332518
15145073
00730026
lt0001lt0001
Error FLLHLL
6767
4848
048081
046068
14 16 18 20 22 24
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
Average annual temperature (∘C)
(a)
0 50 150 200100 250 300 350 400 450 500 550
Average annual precipitation (mm)
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
(b)
Figure 5The relationship between SVL and (a) average annual temperature and (b) average annual precipitation inMesalina guttulata solidline with circles males dashed line with triangles females
dispersion (as shown in the scatter plots) it was foundthat among the two ldquodesertrdquo species studied (M guttulataand A boskianus) only females of the latter were smallerin hot temperatures whereas in both sexes of the formeras well as in A boskianus males SVL did not correlatewith temperature In the Mediterranean region P laevisand O elegans inhabit cooler climates than the desert Aboskianus and M guttulata In these environments largergravid reptiles in addition to the buffering effects of thebehavioural thermoregulation supplied by the mother [5960] can provide greater temperature stability during thepreoviposition period Volynchik [19] however found that alarge-bodied local viper (Vipera palaestinae) with a Mediter-ranean distribution pattern does not follow Bergmannrsquos ruleor its converse At the same time the most ldquocold-lovingrdquolizard (O elegans) in my own sample obeyed Bergmannrsquos
rule growing larger in cooler environments On the otherhand in desert habitats this pattern of greater thermal inertiaseems to be less important and the behavioural componentof thermoregulation becomes paramount
The impact of ambient temperature on external mor-phology is also significant in respect to relative extremitylengths different degrees of intraspecific variability in limbproportions supporting Allenrsquos rule were observed in all thespecies studied The present findings indicate that temper-ature decrease across the observed habitats could lead toreduction in size of extremity segments relative to bodylength thus constituting a compensatory adaptation to eithercooler or hotter areas I noted an allometric shift in humerusforearm femur and tibia lengths relative to SVL along atemperature gradient among P laevis A similar relationshipbetween average annual temperature and corporeal ratioswas
10 International Journal of Zoology
Table 7 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) inMesalina guttulata with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
2525
2424
021045
024054
156143
181191
00650110
00290019
Covariate(SVL)
FLLHLL
11
11
20084405
9872011
14751407
72797114
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
4501082
8922073
33113455
65837331
lt0001lt0001
lt0001lt0001
Error FLLHLL
9191
6969
013031
013028
Precipitation FLLHLL
2828
2525
019041
022056
142129
162211
01070181
00590008
Covariate(SVL)
FLLHLL
11
11
19504181
9631908
14091307
68667094
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
356901
8021918
25752817
57177133
lt0001lt0001
lt0001lt0001
Error FLLHLL
8888
6868
013032
014026
noted in females of M guttulata Among A boskianus totalhind limb length significantly correlated with both thermalregime and rainfall gradient Hence both Mediterraneanand desert reptiles follow a similar pattern in their bodyshape variation and may benefit from various morphologicalmodifications matched to habitat range
Body temperature changes affect reptile ecology [61]becoming more important to ectotherms living in coolerenvironments which complicate attaining proper body tem-perature [58 62] In support of this my results show the asso-ciation between biogeographic origins of the species exam-ined and their relationship with environmental variables Oninterspecific comparison the most pronounced distinctionswere noted in phenotypic responses to the temperature gra-dient between Mediterranean and desert inhabitants whilethe between-species differences for precipitation-related vari-ation were weaker As expected both Mediterranean regionspecies (P laevis O elegans) display significantly strongerresponses to temperature than desert dwellers (A boskianusM guttulata) Apparently the cooler locations of the formerforce them to exhibit more consistent morphological vari-ability in respect to temperature changes whereas for desertspecies such habitat-morphology connection seems to be lessimportant It is highly likely that the speciesrsquo sensitivity tothe environment is associated not only with their ecologicaldifferentiation but also with body size ranges within thesample Thus this might be one possible explanation for thedifferent albeit relatively minor responses to temperaturebetween ecologically similar species (ie P laevis versus Oelegans andA boskianus versusM guttulata) that were notedhere In the examined samples L laevis owing to its greatermeasurement ranges than O elegans has a higher potentialfor more consistent matching of its body dimensions to theobserved temperature gradient The same is true for the twodesert lizardsA boskianus due to its extended body and limb
ranges in comparison with M guttulata displays a strongermorphological-environmental link
The examination of gender-specific habitat-morphologyinteractions revealed that within three of the four species (Plaevis A boskianus and M guttulata) sensitivity to the envi-ronment is coupledwith sex Considering the effect of climatevariables on SVL the findings demonstrate that females ingeneral show a more consistent link between temperatureand bodylimb measurements than males while the effectof precipitation on external characters was similar for bothsexes Moreover in P laevis SVL was significantly morestrongly correlated with the temperature gradient in femalesthan in malesThese observations indicate the sex-associatedeffect of natural selection pointing to different thermal andmetabolic demands inmales and femalesThus it is likely thatin females the increased body size in colder environmentsis associated with reproduction-induced requirements Thispattern suggests that females due to increased thermalrequirements particularly during vitellogenesis [63] aremore able to generate a range of suitable morphologicalmodifications for maintenance of optimal body temperaturein local environments Overall my findings indicate thatalthough females show amore consistent correlation betweenSVL and a temperature gradient than males the body shapechanges involving both body and limb dimensions arerather preliminary in explaining the observed intersexualdivergence in the habitat-morphology relationship
Environmental conditions within the nest experiencedduring early ontogenesis especially temperature and mois-ture of substrate can significantly affect development andgrowth trajectories of individuals in oviparous reptiles [64ndash68] As observed in many species either posthatching phe-notype or offspring fitness are closely associated with thermalregime [63 69ndash71] In both the laboratory and in naturalnests [64] temperature is traditionally considered to be animportant environmental determinant of reptile size while
International Journal of Zoology 11
the effect of water-related factors is more complex Severalrecent studies have tested the effect of substrate moistureduring incubation of eggs on a diverse range of reptile speciesSignificant effects are found in certain species [66 68 72 73]but not in others [74ndash76] that may reflect either differentwater permeability of the eggshell or interspecific variationin the water content of eggs [77] On the other hand theappearance of morphological variation along a precipitationgradient which in desert lizards is even more evident thanthe temperature-related variability can be considered as aresponse to the local habitats In reptiles food availabilitystrongly affects growth trajectories and is one of the possibledeterminants of body size and shape [78ndash80] Overall inarid regions where vegetation and arthropod fauna aredetermined primarily by precipitation [11] wetter localitiesprovide better food resources to lizards at the populationlevel The present findings suggest that among desert speciesthe possible spatial differences in prey availability and thusin nutrition levels may lead to morphometric differentiationbetween specimens inhabiting dry or wet sites Howeverdetailed studies on possible dietary variation linked tolocal environments are necessary to answer the question ofwhether the habitat conditions which are dependent on pre-cipitation have an effect on body dimensions in these lizards
A nonphylogenetic approach suggests that lizard speciestend to exhibit strong morphological specialization in rela-tion to their habitat [53 81] Variation in body charactersrelated to locomotion which in turn is associated withsubstrate pattern has been observed across many lizard taxa[54 82ndash84] Unfortunately based on available datasets Icould not evaluate whether the shift in substrate usage isassociated with limb proportion changes and so a rationalexplanation for the effect of vegetation on limb lengthsthrough its dependence upon hydrothermal regime remainsto be determined My findings show that generally theexamined species indicate a uniform pattern in extremitiessize variation fore and especially hind limb lengths werepositively correlated with temperature and negatively withprecipitation The results indicate that ecological adaptationto abiotic factors is a powerful source of extremity sizevariation which is under the effect of natural selection Inlizards the morphology-performance relationships suggestthat ground-dwelling species from open landscapes shouldpossess relatively long limb segments to their body length[53] This body shape pattern increases stride length provid-ing better sprinting abilities [85 86] Furthermore shorterextremities may facilitate the locomotion in highly vegetatedareas where long limbs may be disadvantageous [53] In thiscontextmyfindings suggest that various body shape patternssuch as relatively shortlong limbs or their segments whichare suited to the environmental requirements may reflect anadaptation to either dense or sparse vegetation resulting fromdifferent rainfall intensities across the distribution range
Finally given the potential importance of habitats forlimb size variation lizardsmay also use their protruding bodyparts as additional (together with body surface area) heatexchangers In these reptiles for optimal balance betweenheat gain and heat loss isometric size changes to a certainextent are a ldquotwo-edged swordrdquo inwhich high thermal inertia
of large bodies is accompanied by slow heating rates and viceversa In this respect among desert dwellers relatively longextremities and small size enhance heat exchange and seemto be a morphological adaptation for effective thermoreg-ulation In desert areas large daily fluctuations of temper-ature force the ectotherms to quickly respond to changingconditions and rapidly reach the necessary metabolic ratesfor locomotor activity Long-limbed individuals which havean increased surface area-to-volume ratio may enhancetheir heating and cooling abilities through more effectiveinteractions between the body and either solar radiationor surface temperature gradient Hence a consistent linkbetween environmental variables and limb lengths can alsobe explained by their importance for maintenance of optimalbody temperature in local environments As shown above thefact that the extremity size-environment link is more obviousin respect to hind limbs than to fore ones reinforces thishypothesis relatively large hind limbs having an increasedheat exchange capacity are much more powerful tool foreffective thermoregulation than small fore extremities
In summary the lacertid lizards I studied generallyfollowed the ecogeographic rules of Bergmann and AllenIn addition the findings indicate both intersexual and inter-specific differences in the habitat-morphology relationshipwhich can be considered within the framework of theirfunctional connectionMydata provide evidence that femalestend to show stronger relationships between climate vari-ables and body dimensions than males In desert speciestemperature has a smaller effect than rainfall on lizardphenotypes Under a constant dry climate water availabilityseems to be the most important abiotic factor in reptileecology In this respect due to the strong association betweenprecipitation and productivity my findings could also beinterpreted as evidence for the hypothesis that different bodysize patterns are linked to the spatial variation in primaryproduction that is the ldquoresource rulerdquo In the Mediterraneanregion lizards the thermal regime is apparently the maindriving force of morphological variability The present studysuggests a complex link between environmental variablesand morphological characters within lacertid species Thephysical conditions such as temperature and precipitationgradient were shown to be able to significantly affect bothbody and limb dimensions and thus as a powerful sourceof variation they play an important role in lizard mor-phology However general statements about the habitat-morphology relationships and their potential importance formaintenance of optimal body temperature in reptiles arehard to make due to the enormous diversity of variationsin body composition and physiology across species sexesand even individuals and the difficulty in evaluating enoughmechanisms in enough species Consequently additionalfield and experimental studies testing both body size andshape variations and their relationships with environmentalvariables especially at the intraspecific level and accountingfor sex-specific aspects are needed to help determine whetherthe observed patterns are common across species and to whatextent they are important for effective thermoregulation
12 International Journal of Zoology
Conflict of Interests
The author declares that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The author would like to thank Shai Meiri for his helpfulcomments on earlier drafts of the paper The author thanksErezMaza for assistancewith data preparationAnat Feldmanfor provision of the GIS-compatible temperature data andNaomi Paz for linguistic editing The author also thanks theIsrael Ministry of Science Culture and Sport for supportingthe National Collections of Natural History at Tel AvivUniversity as a biodiversity environment and agricultureresearch knowledge centre
References
[1] E Mayr Animal Species and Evolution Harvard UniversityPress Cambridge Mass USA 1963
[2] C Ray ldquoThe application of Bergmannrsquos and Allenrsquos rules to thepoikilothermsrdquo Journal of Morphology vol 106 pp 85ndash1081960
[3] TM Blackburn K J Gaston andN Loder ldquoGeographic gradi-ents in body size a clarification of Bergmannrsquos rulerdquo Diversityand Distributions vol 5 no 4 pp 165ndash174 1999
[4] K J Gaston and TM Blackburn Pattern and Process inMacro-ecology Blackwell Malden Mass USA 2000
[5] C Bergmann ldquoUber die verhaltnisse der warmeokonomie derthiere zu ihrer grosserdquo Gottinger Studien vol 3 pp 595ndash7081847
[6] J A Allen ldquoThe influence of physical conditions in the genesisof speciesrdquo Radical Review vol 1 pp 108ndash140 1877
[7] F C James ldquoGeographic size variation in birds and its relation-ship with climaterdquo Ecology vol 51 pp 365ndash390 1970
[8] C D Burnett ldquoGeographic and climatic correlates of morpho-logical variation inEptesicus fuscusrdquo Journal ofMammalogy vol64 no 3 pp 437ndash444 1983
[9] C C Lindsey ldquoBody sizes of poikilotherm vertebrates at differ-ent latitudesrdquo Evolution vol 20 pp 456ndash465 1966
[10] M L Rosenzweig ldquoThe strategy of body size in mammaliancarnivoresrdquo American Midland Naturalist vol 80 pp 299ndash3151968
[11] Y Yom-Tov and E Geffen ldquoGeographic variation in body sizethe effects of ambient temperature and precipitationrdquoOecologiavol 148 no 2 pp 213ndash218 2006
[12] Y Yom-Tov and H Nix ldquoClimatological correlates for body sizeof five species of Australian mammalsrdquo Biological Journal of theLinnean Society vol 29 no 4 pp 245ndash262 1986
[13] D Pincheira-Donoso and SMeiri ldquoAn intercontinental analysisof climate-driven body size clines in reptiles no support forpatterns no signals of processesrdquo Evolutionary Biology vol 40no 4 pp 562ndash578 2013
[14] K G Ashton M C Tracy and A de Queiroz ldquoIs Bergmannrsquosrule valid for mammalsrdquoThe American Naturalist vol 156 no4 pp 390ndash415 2000
[15] S Meiri and T Dayan ldquoOn the validity of Bergmannrsquos rulerdquoJournal of Biogeography vol 30 no 3 pp 331ndash351 2003
[16] K G Ashton ldquoSensitivity of intraspecific latitudinal clines ofbody size for tetrapods to sampling latitude and body sizerdquoIntegrative and Comparative Biology vol 44 no 6 pp 403ndash4122004
[17] K G Ashton and C R Feldman ldquoBergmannrsquos rule in nonavianreptiles turtles follow it lizards and snakes reverse itrdquoEvolutionvol 57 no 5 pp 1151ndash1163 2003
[18] M A Olalla-Tarraga M A Rodrıguez and B A HawkinsldquoBroad-scale patterns of body size in squamate reptiles ofEurope and North Americardquo Journal of Biogeography vol 33no 5 pp 781ndash793 2006
[19] S Volynchik ldquoMorphological variability in Vipera palaesti-nae along an environmental gradientrdquo Asian HerpetologicalResearch vol 3 pp 227ndash239 2012
[20] D Pincheira-Donoso D J Hodgson and T Tregenza ldquoTheevolution of body size under environmental gradients inectothermswhy shouldBergmannrsquos rule apply to lizardsrdquoBMCEvolutionary Biology vol 8 no 1 article 68 2008
[21] R C Stillwell ldquoAre latitudinal clines in body size adaptiverdquoOikos vol 119 no 9 pp 1387ndash1390 2010
[22] S Meiri ldquoBergmannrsquos rulemdashwhatrsquos in a namerdquo Global Ecologyand Biogeography vol 20 no 1 pp 203ndash207 2011
[23] D Pincheira-Donoso ldquoPredictable variation of range-sizesacross an extreme environmental gradient in a lizard adaptiveradiation evolutionary and ecological inferencesrdquo PLoS ONEvol 6 no 12 Article ID e28942 2011
[24] K G Ashton ldquoDo amphibians follow Bergmannrsquos rulerdquo Cana-dian Journal of Zoology vol 80 no 4 pp 708ndash716 2002
[25] M J Angilletta Jr T D Steury andMW Sears ldquoTemperaturegrowth rate and body size in ectotherms fitting pieces of a life-history puzzlerdquo Integrative and Comparative Biology vol 44 no6 pp 498ndash509 2004
[26] C E Oufiero G E A Gartner S C Adolph and T GarlandldquoLatitudinal and climatic variation in body size and dorsalscale counts in Sceloporus lizards a phylogenetic perspectiverdquoEvolution vol 65 no 12 pp 3590ndash3607 2011
[27] S Meiri ldquoEvolution and ecology of lizard body sizesrdquo GlobalEcology and Biogeography vol 17 no 6 pp 724ndash734 2008
[28] D Atkinson and RM Sibly ldquoWhy are organisms usually biggerin colder environments Making sense of a life history puzzlerdquoTrends in Ecology amp Evolution vol 12 pp 235ndash239 1997
[29] F B Cruz L A Fitzgerald R E Espinoza and J A Schulte IIldquoThe importance of phylogenetic scale in tests of Bergmannrsquosand Rapoportrsquos rules lessons from a clade of South Americanlizardsrdquo Journal of Evolutionary Biology vol 18 no 6 pp 1559ndash1574 2005
[30] T AMousseau ldquoEctotherms follow the converse to BergmannrsquosRulerdquo Evolution vol 51 pp 630ndash632 1997
[31] R N Reed ldquoInterspecific patterns of species richness geo-graphic range size and body size among NewWorld venomoussnakesrdquo Ecography vol 26 no 1 pp 107ndash117 2003
[32] D Pincheira-Donoso T Tregenza and D J Hodgson ldquoBodysize evolution in South American Liolaemus lizards of theboulengeri clade a contrasting reassessmentrdquo Journal of Evolu-tionary Biology vol 20 no 5 pp 2067ndash2071 2007
[33] M J Angilletta P H Niewiarowski A E Dunham A Leacheand W P Porter ldquoBergmannrsquos clines in ectotherms illustratinga life-historical perspective with sceloporine lizardsrdquoTheAmer-ican Naturalist vol 164 pp E168ndashE183 2004
[34] M Andersson Sexual Selection Princeton University PressPrinceton NJ USA 1994
International Journal of Zoology 13
[35] F Brana ldquoSexual dimorphism in lacertid lizards male headincrease vs female abdomen increaserdquo Oikos vol 75 pp 511ndash523 1996
[36] E R Pianka ldquoLizard species density in the Kalahari desertrdquoEcology vol 52 pp 1024ndash1029 1971
[37] E R Pianka ldquoSome intercontinental comparisons of desertlizardsrdquoNational Geographic Research vol 1 no 4 pp 490ndash5041985
[38] B H Brattstrom ldquoSocial and thermoregulatory behavior of thebearded dragon Amphibolurus barbatusrdquo Copeia vol 3 pp484ndash497 1971
[39] G C Grigg and F Seebacher ldquoField test of a paradigm hyster-esis of heart rate in thermoregulation by a free-ranging lizard(Pogona barbata)rdquo Proceedings of the Royal Society B BiologicalSciences vol 266 no 1425 pp 1291ndash1297 1999
[40] F Seebacher and C E Franklin ldquoControl of heart rate duringthermoregulation in the heliothermic lizard Pogona barbataimportance of cholinergic and adrenergic mechanismsrdquo TheJournal of Experimental Biology vol 204 no 24 pp 4361ndash43662001
[41] G J Tattersall and R M Gerlach ldquoHypoxia progressivelylowers thermal gaping thresholds in bearded dragons Pogonavitticepsrdquo The Journal of Experimental Biology vol 208 no 17pp 3321ndash3330 2005
[42] D F DeNardo T E Zubal and T C M Hoffman ldquoCloacalevaporative cooling a previously undescribedmeans of increas-ing evaporative water loss at higher temperatures in a desertectotherm theGilamonsterHeloderma suspectumrdquoThe Journalof Experimental Biology vol 207 no 6 pp 945ndash953 2004
[43] S Jaffe ldquoClimate of Israelrdquo inTheZoogeography of Israel Y Yom-Tov and E Tchernov Eds pp 79ndash92 Dr W Junk PublishersDordrecht The Netherlands 1988
[44] U Roll L Stone and S Meiri ldquoHot-spot facts and artifacts-questioning Israelrsquos great biodiversityrdquo Israel Journal of Ecologyand Evolution vol 55 no 3 pp 263ndash279 2009
[45] W Bischoff and J F Schmidtler ldquoNew data on the distributionmorphology and habitat choice of the Lacerta laevis-kulzericomplexrdquo Natura Croatica vol 8 no 3 pp 211ndash222 1999
[46] A Disi D Modry P Necas and L Rifai Amphibians andReptiles of the Hashemite Kingdom of Jordan An Atlas and FieldGuide Edit Chimaira Frankfurt Germany 2001
[47] A Bouskila and P Amitai Handbook of Amphibians andReptiles of Israel Keter Publishing House Jerusalem Israel2001 (Hebrew)
[48] A Bar and G Haimovitch A Field Guide to Reptiles andAmphibians of Israel Pazbar LTD Herzliya Israel 2012
[49] Y L Werner ldquoGeographic sympatry of Acanthodactylus opheo-durus with A boskianus in the Levantrdquo Zoology in the MiddleEast vol 1 pp 92ndash95 1986
[50] R J Hijmans S E Cameron J L Parra P G Jones and AJarvis ldquoVery high resolution interpolated climate surfaces forglobal land areasrdquo International Journal of Climatology vol 25no 15 pp 1965ndash1978 2005
[51] R B Huey ldquoTemperature physiology and the ecology ofreptilesrdquo inBiology of the Reptilia CGans and FH Pough Edsvol 12 of Physiology (C) pp 25ndash91 Academic Press New YorkNY USA 1982
[52] D J Irschick and J B Losos ldquoDo lizards avoid habitats inwhich performance is submaximal The relationship betweensprinting capabilities and structural habitat use in Caribbeananolesrdquo The American Naturalist vol 154 no 3 pp 293ndash3051999
[53] B Vanhooydonck and R Van Damme ldquoEvolutionary relation-ships between body shape and habitat use in lacertid lizardsrdquoEvolutionary Ecology Research vol 1 no 7 pp 785ndash805 1999
[54] J Melville and R Swain ldquoEvolutionary relationships betweenmorphology performance and habitat openness in the lizardgenus Niveoscincus (Scincidae Lygosominae)rdquo Biological Jour-nal of the Linnean Society vol 70 no 4 pp 667ndash683 2000
[55] R B Huey and M Slatkin ldquoCost and benefits of lizard thermo-regulationrdquo The Quarterly Review of Biology vol 51 no 3 pp363ndash384 1976
[56] R D Stevenson ldquoBody size and limits to the daily range of bodytemperature in terrestrial ectothermsrdquoTheAmericanNaturalistvol 125 pp 102ndash117 1985
[57] B W Grant ldquoTrade-offs in activity time and physiologicalperformance for thermoregulating desert lizards Sceloporusmerriamirdquo Ecology vol 71 no 6 pp 2323ndash2333 1990
[58] R Shine and T Madsen ldquoIs thermoregulation unimportant tomost reptiles An example using water pythons (Liasis fuscus)in tropical AustraliardquoPhysiological Zoology vol 69 pp 252ndash2691996
[59] R Shine ldquoReptilian viviparity in cold climates testing theassumptions of an evolutionary hypothesisrdquo Oecologia vol 57no 3 pp 397ndash405 1983
[60] C R Peterson A R Gibson andM E Dorcas ldquoSnake thermalecology the causes and consequences of body temperaturevariationrdquo in Snakes Ecology and Behavior R A Seigel and J TCollins Eds pp 241ndash314 McGraw-Hill New York NY USA1993
[61] R B Huey and J G Kingsolver ldquoEvolution of thermal sensitiv-ity of ectotherm performancerdquo Trends in Ecology and Evolutionvol 4 no 5 pp 131ndash135 1989
[62] J A Dıaz D Bauwens and B Asensio ldquoA comparative studyof the relation between heating rates and ambient temperaturesin lacertid lizardsrdquo Physiological Zoology vol 69 pp 1359ndash13831996
[63] D C Deeming ldquoPost-hatching phenotypic effects of incubationin reptilesrdquo in Reptilian Incubation Environment Evolutionand Behaviour D C Deeming Ed pp 229ndash251 NottinghamUniversity Press Nottingham UK 2004
[64] R Shine M J Elphick and P S Harlow ldquoThe influence ofnatural incubation environments on the phenotypic traits ofhatchling lizardrdquo Ecology vol 78 pp 2559ndash2568 1997
[65] T Flatt R Shine P A Borges-Landaez and S J DownesldquoPhenotypic variation in an oviparousmontane lizard (Bassianaduperreyi) the effects of thermal and hydric incubation envi-ronmentsrdquo Biological Journal of the Linnean Society vol 74 no3 pp 339ndash350 2001
[66] R Shine and M J Elphick ldquoThe effect of short-term weatherfluctuations on temperatures inside lizard nests and on thephenotypic traits of hatchling lizardsrdquo Biological Journal of theLinnean Society vol 72 no 4 pp 555ndash565 2001
[67] O Lourdais R Shine X Bonnet M Guillon and G NaulleauldquoClimate affects embryonic development in a viviparous snakeVipera aspisrdquo Oikos vol 104 no 3 pp 551ndash560 2004
[68] V Delmas X Bonnet M Girondot and A-C Prevot-JulliardldquoVarying hydric conditions during incubation influence eggwater exchange and hatchling phenotype in the red-eared sliderturtlerdquo Physiological and Biochemical Zoology vol 81 no 3 pp345ndash355 2008
[69] X-F Yan X-L Tang F Yue et al ldquoInfluence of ambient temper-ature onmaternal thermoregulation and neonate phenotypes in
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
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International Journal of Zoology 5
Table 1 Morphological characteristics of lizard species studied and their intersexual comparisons (one-way ANOVA with multiple testingcorrections Duncanrsquos multiple range test MRT)
Species Features Range Mean plusmn SD nDDCC
119875 119865
DD CC DD CC
Phoenicolacertalaevis
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
25ndash105505ndash7753ndash9
59ndash932762ndash1184875ndash13
3ndash11450ndash76
522ndash73459ndash7877ndash10585ndash114
585 plusmn 191
6353 plusmn 665699 plusmn 079
761 plusmn 077
966 plusmn 103
1104 plusmn 102
513 plusmn 194
6297 plusmn 601
634 plusmn 047
696 plusmn 046
878 plusmn 063
987 plusmn 062
485648564756475647564756
0059065400001000010000100001
3620202636284927405101
Ophisops elegans
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
09ndash4240ndash59445ndash61478ndash67253ndash872715ndash1053
12ndash3540ndash53539ndash54423ndash62252-747646ndash922
25 plusmn 072
4807 plusmn 427
53 plusmn 04
582 plusmn 05
722 plusmn 071
9 plusmn 081
198 plusmn 051
4647 plusmn 344
466 plusmn 035
515 plusmn 041
629 plusmn 057
778 plusmn 063
856285628461846184618461
lt000010016lt00001lt00001lt00001lt00001
23225859838732069119538
Acanthodactylusboskianus
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
17ndash13852ndash8852ndash918592ndash992845ndash1338108ndash164
3ndash12150ndash805462ndash7358ndash84883ndash122810ndash1454
699 plusmn 215
659 plusmn 646
69 plusmn 075
796 plusmn 079
112 plusmn 104
1377 plusmn 119
535 plusmn 163
6111 plusmn 583
626 plusmn 056
712 plusmn 062
981 plusmn 075
1212 plusmn 087
121931219311385113851148511485
lt00001lt00001lt00001lt00001lt00001lt00001
37233131433365571086211606
Mesalinaguttulata
M (g)SVL (mm)HmL (mm)FaL (mm)FeL (mm)TbL (mm)
08ndash640ndash57413ndash5945ndash624595ndash82717ndash967
116ndash3740ndash5639ndash5442ndash56557ndash776664ndash88
204 plusmn 063
4561 plusmn 301
5 plusmn 031
534 plusmn 03
707 plusmn 046
839 plusmn 045
201 plusmn 056
469 plusmn 373
462 plusmn 029
495 plusmn 03
652 plusmn 041
763 plusmn 044
98791199511895118951189511895
07480005lt00001lt00001lt00001lt00001
01078078228409796115251
80
76
72
68
64
60
56
52
4814 15 16 17 18 19 20 21
SVL
(mm
)
Average annual temperature (∘C)
(a)
80
76
72
68
64
60
56
52
48
SVL
(mm
)
300 350 400 450 500 800550 600 650 700 750
Average annual precipitation (mm)
(b)
Figure 2 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Phoenicolacerta laevissolid line with circles males dashed line with triangles females
statistically significant effect of temperature on both FLL andHLL in females (Table 3) The results of multiple regressionwith SVL as a response (Table 4) indicate that the body size-environment link is more obvious in respect to temperaturethan to precipitation Thus in females SVL is much moreaffected by the former variable 119875 = 00009 120573 = minus061 plusmn 017than by the latter 119875 = 0588 120573 = minus009 plusmn 017
O elegans Examination of the environmental relationshipacross the observed area of thismostlyMediterranean species
demonstrates a highly significant correlation between latitudeand both temperature (119903 = minus0801 119875 lt 00001) and pre-cipitation (119903 = 0433 119875 lt 00001) Temperature is negativelycorrelated with precipitation (119903 = minus0388 119875 lt 00001)Snout-vent lengths (Figures 3(a) and 3(b)) of both sexesincrease with temperature (males slope = minus072 plusmn 018 119903 =minus0402 119875 = 00001 females slope = minus049plusmn014 119903 = minus0408119875 = 0001) and with precipitation (males slope = 0007 plusmn0001 119903 = 0395 119875 = 00002 females slope = 0005 plusmn 0001119903 = 0374 119875 = 0002)
6 International Journal of Zoology
Table 2 Climate-morphology relationship between average annual temperature (AAT)average annual precipitation (AAP) and bodymeasurementsratios (regression analysis with temperature and precipitation as the predictors and features as the responses) Positivecorrelation (+) and negative correlation (minus) single sign significant difference (119875 lt 005) and double sign highly significant difference (119875 lt00001)
FeaturesPhoenicolacerta laevis Ophisops elegans Acanthodactylus boskianus Mesalina guttulata
AAT AAP AAT AAP AAT AAP AAT AAPDD CC DD CC DD CC DD CC DD CC DD CC DD CC DD CC
M minus + minus + + + +SVL minusminus + minus minus + + minus + + +HmL minus minus + ++FaL minus minus + + +FeL minus minus ++ +TbL minus minus + +HmLSVL + ++ minus minus + minus minus +FaLSVL + ++ minus + minusminus minus +FeLSVL + ++ minusminus + + + minus minus + minus minus
TbLSVL + ++ minus + minus minus + minus minus
Table 3 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Phoenicolacerta laevis with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
77
88
052111
079152
145149
243333
02140199
00280004
Covariate(SVL)
FLLHLL
11
11
73211275
23494734
20171707
71641038
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
033276
404766
093371
12321679
03410062
lt0001lt0001
Error FLLHLL
3737
4646
036074
033045
Precipitation FLLHLL
88
88
047099
064150
126130
187327
02940275
00880005
Covariate(SVL)
FLLHLL
11
11
71081208
21624677
19131582
62751017
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
030296
493798
081388
14331738
03740056
lt0001lt0001
Error FLLHLL
3636
4646
037076
034045
Table 4 The effect of climate variables on snout-vent length (SVL) Results of multiple regression with SVL as a dependent variable andclimatic factors as predictors
Effect of temperature Effect of precipitation120573 plusmn SE 119905 119875 120573 plusmn SE 119905 119875
Phoenicolacertalaevis
DD minus021 plusmn 021 minus098 0328 minus018 plusmn 021 minus085 0399CC minus0615 plusmn 017 minus351 00009 minus009 plusmn 017 minus054 0588
Ophisops elegansDD minus027 plusmn 011 minus251 0013 026 plusmn 011 238 0019CC minus032 plusmn 012 minus266 0009 025 plusmn 012 208 0041
Acanthodactylusboskianus
DD minus003 plusmn 009 minus034 0727 0136 plusmn 009 137 0207CC minus013 plusmn 011 minus115 0251 021 plusmn 011 minus177 0079
Mesalina guttulata DD minus003 plusmn 009 minus041 068 021 plusmn 009 236 0019CC minus014 plusmn 009 minus151 0134 033 plusmn 009 339 0001
International Journal of Zoology 7
SVL
(mm
)
Average annual temperature (∘C)
60
56
52
48
44
40
8 10 12 14 16 18 20
(a)
SVL
(mm
)
60
56
52
48
44
40
100 200 300 400 500 700 800600 900
Average annual precipitation (mm)
(b)
Figure 3 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Ophisops elegans solidline with circles males dashed line with triangles females
The corporeal ratios and especially lengths (Table 2)are noticeably influenced by the local climate conditionsRegression analysis indicates that the sexes generally followsimilar trends in their corporal dimensions and becomesignificantly larger at higher latitudes By analogy with SVLappendages were positively correlated with precipitation andwere negatively correlated with temperature In additionin both sexes the longer femora may be associated withincreased precipitation However after accounting for SVLa MANCOVA reveals a nonsignificant effect of both abi-otic predictors on limb size (Table 5) Multiple regressiondemonstrates the equivalency of two climate influences intheir relationships with SVL (Table 4) Furthermore malesand females in general did not differ from one another intheir responses to either temperature (120573 = minus027plusmn011 versus120573 = minus032 plusmn 012) or precipitation (120573 = 026 plusmn 011 versus120573 = 025 plusmn 012) gradient
A boskianus In the desert habitats of this species temperaturewas uncorrelated with latitude (119903 = minus0082 119875 = 0247)across the observed geographic range There is however apronounced latitudinal precipitation gradient (119903 = 0815119875 lt 00001) and a negative relationship between annualaverages of temperature and precipitation 119903 = minus0367 119875 lt00001 In this lizard the sexes differ in respect to theirenvironmental-morphological connection (Figures 4(a) and4(b)) The SVL of males did not correlate consistently withtemperature (slope = minus021 plusmn 029 119903 = minus0067 119875 = 0485)and precipitation (slope = 001 plusmn 0008 119903 = 0134 119875 =0160) whereas the SVL of females varied in relation to thesevariables slope = minus081 plusmn 034 119903 = minus0243 119875 = 0021 andslope = 002 plusmn 0007 119903 = 0280 119875 = 0007 for temperatureand precipitation respectively
Corporeal measurements (Table 2) showed a close rela-tionship with rainfall in both sexes and increased precip-itation is correlated to shorter extremities relative to SVLDespite the fact that the appendages tend to lengthen relativeto their SVL with rise in temperature this abiotic component
would seem to affect only hind limb segments (FeL and TbL)The MANCOVA results (Table 6) also suggest that withinboth sexes the temperature gradient significantly contributesonly to HLL variation Precipitation had a significant effecton hind extremity in both sexes furthermore within males itinfluenced the variation in FLL as well Analysis of combinedeffect of environmental variables when both temperature andprecipitation were regressed against SVL (Table 4) revealsthe role of moisture as a major predictor of intraspecificvariability Moreover males and females were similar in thistrend 120573 = minus003 plusmn 009 (temperature) 120573 = 0136 plusmn 009(precipitation) for males and 120573 = 013 plusmn 011 versus 120573 =021 plusmn 011 for females respectively
M guttulata The studied geographic range of this desertlacertid is characterized by a highly significant correlationbetween latitude and both temperature (119903 = 0657 119875 lt00001) and precipitation (119903 = 0682 119875 lt 00001) whereastemperature was uncorrelated with precipitation (119903 = 0030119875 = 0654) In both sexes SVL (Figures 5(a) and 5(b))increased along a rainfall gradient slope = 0006 plusmn 0002 119903 =0215 119875 = 0018 for males slope = 001 plusmn 0004 119903 = 0317119875 = 0001 for females Continuous sampling also revealed aninsignificant relationship between temperature and SVL inthis species Regression analysis (Table 2) indicated an impor-tant role of precipitation in the creation of clines in body andlimb dimensions Moreover spatial changes of both climaticcomponents may induce some allometric shifts in latitudinalspace Thus temperature rise has led to the appearance oflonger (relative to SVL) extremities among females Thisobservation was confirmed by MANCOVA a significantassociation was observed between either FLL or HLLandtemperature as well as between HLL and precipitation Inmales this approach however indicates a nonsignificanteffect of both climatic variables on limb dimensions (Table 7)
Similarly to other desert dwellers (A boskianus) in thisspecies too precipitation level is a stronger ecological deter-minant of body length (Table 4) than temperature gradient
8 International Journal of Zoology
Table 5 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Ophisops elegans with SVL as a covariate
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
1717
1616
012048
026071
081121
140147
06720278
01860155
Covariate(SVL)
FLLHLL
11
11
25225696
5291525
16331432
28643183
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
101138
251265
651347
1359552
00130067
00010023
Error FLLHLL
6565
4242
015039
018047
Precipitation FLLHLL
2323
1717
013056
024064
083156
129130
06730086
02430241
Covariate(SVL)
FLLHLL
11
11
21864902
5341481
14061366
28222971
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
123201
263305
796559
1393612
00060021
00010018
Error FLLHLL
5959
4141
015035
018049
14 16 18 20 22 24
SVL
(mm
)
Average annual temperature (∘C)
85
80
75
70
65
60
55
50
(a)
SVL
(mm
)
85
80
75
70
65
60
55
50
0 50 150 200100 250 300
Average annual precipitation (mm)
(b)
Figure 4 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Acanthodactylusboskianus solid line with circles males dashed line with triangles females
119875 = 0019 120573 = 021plusmn009 versus119875 = 0680 120573 = minus003plusmn009for males 119875 = 0001 120573 = 033 plusmn 009 versus 119875 = 0134120573 = minus014 plusmn 009 for females respectively
4 Discussion
Despite the inability of ectotherms to produce significantmetabolic heat the interaction between body size and heatbalance based on a set of behavioural anatomical andphysiological mechanisms [51] that contribute to fitnessmight explain the peculiarity of ecological drivers in sizeclines among these animalsThe relationship between habitatconditions and morphological variables (body tail or limbdimensions) and consequent shifts in phenology due toclimate change have been observed across a wide range ofreptile taxa [52ndash54] It is possible that in diurnal squamates
environmental conditions may favour selection for smaller-sized individuals [55] which due to the ability to achievemore accurate adjustment of their body temperature havebetter thermoregulatory capacities [56] and thus display highactivity levels In terrestrial ectotherms thermoregulation isrealized behaviourally by habitat selection and daily activitypattern [57] while at the same time morphological special-ization may also essentially facilitate it [55] For exampleShine and Madsen [58] pointed out that for relatively smallreptile species behavioural thermoregulation seems to bemore important especially in conditions of high diurnalthermal heterogeneity In this context desert reptiles inhab-iting warmer regions with lower thermoregulatory costs mayadjust their body temperature mainly behaviourally andthus invest less in adjustment of either body size or shapein relation to ambient temperature Despite the great data
International Journal of Zoology 9
Table 6 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Acanthodactylus boskianus with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
3535
2828
089151
053131
141191
125175
01180012
02390040
Covariate(SVL)
FLLHLL
11
11
60441731
34366125
95262186
80188176
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
203445
4952911
320562
11563885
00780021
0001lt0001
Error FLLHLL
6565
5151
063079
042074
Precipitation FLLHLL
3333
3131
086151
046116
178186
101171
00230016
04810049
Covariate(SVL)
FLLHLL
11
11
64151792
23944222
13182201
51436151
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
161422
7043482
332518
15145073
00730026
lt0001lt0001
Error FLLHLL
6767
4848
048081
046068
14 16 18 20 22 24
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
Average annual temperature (∘C)
(a)
0 50 150 200100 250 300 350 400 450 500 550
Average annual precipitation (mm)
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
(b)
Figure 5The relationship between SVL and (a) average annual temperature and (b) average annual precipitation inMesalina guttulata solidline with circles males dashed line with triangles females
dispersion (as shown in the scatter plots) it was foundthat among the two ldquodesertrdquo species studied (M guttulataand A boskianus) only females of the latter were smallerin hot temperatures whereas in both sexes of the formeras well as in A boskianus males SVL did not correlatewith temperature In the Mediterranean region P laevisand O elegans inhabit cooler climates than the desert Aboskianus and M guttulata In these environments largergravid reptiles in addition to the buffering effects of thebehavioural thermoregulation supplied by the mother [5960] can provide greater temperature stability during thepreoviposition period Volynchik [19] however found that alarge-bodied local viper (Vipera palaestinae) with a Mediter-ranean distribution pattern does not follow Bergmannrsquos ruleor its converse At the same time the most ldquocold-lovingrdquolizard (O elegans) in my own sample obeyed Bergmannrsquos
rule growing larger in cooler environments On the otherhand in desert habitats this pattern of greater thermal inertiaseems to be less important and the behavioural componentof thermoregulation becomes paramount
The impact of ambient temperature on external mor-phology is also significant in respect to relative extremitylengths different degrees of intraspecific variability in limbproportions supporting Allenrsquos rule were observed in all thespecies studied The present findings indicate that temper-ature decrease across the observed habitats could lead toreduction in size of extremity segments relative to bodylength thus constituting a compensatory adaptation to eithercooler or hotter areas I noted an allometric shift in humerusforearm femur and tibia lengths relative to SVL along atemperature gradient among P laevis A similar relationshipbetween average annual temperature and corporeal ratioswas
10 International Journal of Zoology
Table 7 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) inMesalina guttulata with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
2525
2424
021045
024054
156143
181191
00650110
00290019
Covariate(SVL)
FLLHLL
11
11
20084405
9872011
14751407
72797114
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
4501082
8922073
33113455
65837331
lt0001lt0001
lt0001lt0001
Error FLLHLL
9191
6969
013031
013028
Precipitation FLLHLL
2828
2525
019041
022056
142129
162211
01070181
00590008
Covariate(SVL)
FLLHLL
11
11
19504181
9631908
14091307
68667094
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
356901
8021918
25752817
57177133
lt0001lt0001
lt0001lt0001
Error FLLHLL
8888
6868
013032
014026
noted in females of M guttulata Among A boskianus totalhind limb length significantly correlated with both thermalregime and rainfall gradient Hence both Mediterraneanand desert reptiles follow a similar pattern in their bodyshape variation and may benefit from various morphologicalmodifications matched to habitat range
Body temperature changes affect reptile ecology [61]becoming more important to ectotherms living in coolerenvironments which complicate attaining proper body tem-perature [58 62] In support of this my results show the asso-ciation between biogeographic origins of the species exam-ined and their relationship with environmental variables Oninterspecific comparison the most pronounced distinctionswere noted in phenotypic responses to the temperature gra-dient between Mediterranean and desert inhabitants whilethe between-species differences for precipitation-related vari-ation were weaker As expected both Mediterranean regionspecies (P laevis O elegans) display significantly strongerresponses to temperature than desert dwellers (A boskianusM guttulata) Apparently the cooler locations of the formerforce them to exhibit more consistent morphological vari-ability in respect to temperature changes whereas for desertspecies such habitat-morphology connection seems to be lessimportant It is highly likely that the speciesrsquo sensitivity tothe environment is associated not only with their ecologicaldifferentiation but also with body size ranges within thesample Thus this might be one possible explanation for thedifferent albeit relatively minor responses to temperaturebetween ecologically similar species (ie P laevis versus Oelegans andA boskianus versusM guttulata) that were notedhere In the examined samples L laevis owing to its greatermeasurement ranges than O elegans has a higher potentialfor more consistent matching of its body dimensions to theobserved temperature gradient The same is true for the twodesert lizardsA boskianus due to its extended body and limb
ranges in comparison with M guttulata displays a strongermorphological-environmental link
The examination of gender-specific habitat-morphologyinteractions revealed that within three of the four species (Plaevis A boskianus and M guttulata) sensitivity to the envi-ronment is coupledwith sex Considering the effect of climatevariables on SVL the findings demonstrate that females ingeneral show a more consistent link between temperatureand bodylimb measurements than males while the effectof precipitation on external characters was similar for bothsexes Moreover in P laevis SVL was significantly morestrongly correlated with the temperature gradient in femalesthan in malesThese observations indicate the sex-associatedeffect of natural selection pointing to different thermal andmetabolic demands inmales and femalesThus it is likely thatin females the increased body size in colder environmentsis associated with reproduction-induced requirements Thispattern suggests that females due to increased thermalrequirements particularly during vitellogenesis [63] aremore able to generate a range of suitable morphologicalmodifications for maintenance of optimal body temperaturein local environments Overall my findings indicate thatalthough females show amore consistent correlation betweenSVL and a temperature gradient than males the body shapechanges involving both body and limb dimensions arerather preliminary in explaining the observed intersexualdivergence in the habitat-morphology relationship
Environmental conditions within the nest experiencedduring early ontogenesis especially temperature and mois-ture of substrate can significantly affect development andgrowth trajectories of individuals in oviparous reptiles [64ndash68] As observed in many species either posthatching phe-notype or offspring fitness are closely associated with thermalregime [63 69ndash71] In both the laboratory and in naturalnests [64] temperature is traditionally considered to be animportant environmental determinant of reptile size while
International Journal of Zoology 11
the effect of water-related factors is more complex Severalrecent studies have tested the effect of substrate moistureduring incubation of eggs on a diverse range of reptile speciesSignificant effects are found in certain species [66 68 72 73]but not in others [74ndash76] that may reflect either differentwater permeability of the eggshell or interspecific variationin the water content of eggs [77] On the other hand theappearance of morphological variation along a precipitationgradient which in desert lizards is even more evident thanthe temperature-related variability can be considered as aresponse to the local habitats In reptiles food availabilitystrongly affects growth trajectories and is one of the possibledeterminants of body size and shape [78ndash80] Overall inarid regions where vegetation and arthropod fauna aredetermined primarily by precipitation [11] wetter localitiesprovide better food resources to lizards at the populationlevel The present findings suggest that among desert speciesthe possible spatial differences in prey availability and thusin nutrition levels may lead to morphometric differentiationbetween specimens inhabiting dry or wet sites Howeverdetailed studies on possible dietary variation linked tolocal environments are necessary to answer the question ofwhether the habitat conditions which are dependent on pre-cipitation have an effect on body dimensions in these lizards
A nonphylogenetic approach suggests that lizard speciestend to exhibit strong morphological specialization in rela-tion to their habitat [53 81] Variation in body charactersrelated to locomotion which in turn is associated withsubstrate pattern has been observed across many lizard taxa[54 82ndash84] Unfortunately based on available datasets Icould not evaluate whether the shift in substrate usage isassociated with limb proportion changes and so a rationalexplanation for the effect of vegetation on limb lengthsthrough its dependence upon hydrothermal regime remainsto be determined My findings show that generally theexamined species indicate a uniform pattern in extremitiessize variation fore and especially hind limb lengths werepositively correlated with temperature and negatively withprecipitation The results indicate that ecological adaptationto abiotic factors is a powerful source of extremity sizevariation which is under the effect of natural selection Inlizards the morphology-performance relationships suggestthat ground-dwelling species from open landscapes shouldpossess relatively long limb segments to their body length[53] This body shape pattern increases stride length provid-ing better sprinting abilities [85 86] Furthermore shorterextremities may facilitate the locomotion in highly vegetatedareas where long limbs may be disadvantageous [53] In thiscontextmyfindings suggest that various body shape patternssuch as relatively shortlong limbs or their segments whichare suited to the environmental requirements may reflect anadaptation to either dense or sparse vegetation resulting fromdifferent rainfall intensities across the distribution range
Finally given the potential importance of habitats forlimb size variation lizardsmay also use their protruding bodyparts as additional (together with body surface area) heatexchangers In these reptiles for optimal balance betweenheat gain and heat loss isometric size changes to a certainextent are a ldquotwo-edged swordrdquo inwhich high thermal inertia
of large bodies is accompanied by slow heating rates and viceversa In this respect among desert dwellers relatively longextremities and small size enhance heat exchange and seemto be a morphological adaptation for effective thermoreg-ulation In desert areas large daily fluctuations of temper-ature force the ectotherms to quickly respond to changingconditions and rapidly reach the necessary metabolic ratesfor locomotor activity Long-limbed individuals which havean increased surface area-to-volume ratio may enhancetheir heating and cooling abilities through more effectiveinteractions between the body and either solar radiationor surface temperature gradient Hence a consistent linkbetween environmental variables and limb lengths can alsobe explained by their importance for maintenance of optimalbody temperature in local environments As shown above thefact that the extremity size-environment link is more obviousin respect to hind limbs than to fore ones reinforces thishypothesis relatively large hind limbs having an increasedheat exchange capacity are much more powerful tool foreffective thermoregulation than small fore extremities
In summary the lacertid lizards I studied generallyfollowed the ecogeographic rules of Bergmann and AllenIn addition the findings indicate both intersexual and inter-specific differences in the habitat-morphology relationshipwhich can be considered within the framework of theirfunctional connectionMydata provide evidence that femalestend to show stronger relationships between climate vari-ables and body dimensions than males In desert speciestemperature has a smaller effect than rainfall on lizardphenotypes Under a constant dry climate water availabilityseems to be the most important abiotic factor in reptileecology In this respect due to the strong association betweenprecipitation and productivity my findings could also beinterpreted as evidence for the hypothesis that different bodysize patterns are linked to the spatial variation in primaryproduction that is the ldquoresource rulerdquo In the Mediterraneanregion lizards the thermal regime is apparently the maindriving force of morphological variability The present studysuggests a complex link between environmental variablesand morphological characters within lacertid species Thephysical conditions such as temperature and precipitationgradient were shown to be able to significantly affect bothbody and limb dimensions and thus as a powerful sourceof variation they play an important role in lizard mor-phology However general statements about the habitat-morphology relationships and their potential importance formaintenance of optimal body temperature in reptiles arehard to make due to the enormous diversity of variationsin body composition and physiology across species sexesand even individuals and the difficulty in evaluating enoughmechanisms in enough species Consequently additionalfield and experimental studies testing both body size andshape variations and their relationships with environmentalvariables especially at the intraspecific level and accountingfor sex-specific aspects are needed to help determine whetherthe observed patterns are common across species and to whatextent they are important for effective thermoregulation
12 International Journal of Zoology
Conflict of Interests
The author declares that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The author would like to thank Shai Meiri for his helpfulcomments on earlier drafts of the paper The author thanksErezMaza for assistancewith data preparationAnat Feldmanfor provision of the GIS-compatible temperature data andNaomi Paz for linguistic editing The author also thanks theIsrael Ministry of Science Culture and Sport for supportingthe National Collections of Natural History at Tel AvivUniversity as a biodiversity environment and agricultureresearch knowledge centre
References
[1] E Mayr Animal Species and Evolution Harvard UniversityPress Cambridge Mass USA 1963
[2] C Ray ldquoThe application of Bergmannrsquos and Allenrsquos rules to thepoikilothermsrdquo Journal of Morphology vol 106 pp 85ndash1081960
[3] TM Blackburn K J Gaston andN Loder ldquoGeographic gradi-ents in body size a clarification of Bergmannrsquos rulerdquo Diversityand Distributions vol 5 no 4 pp 165ndash174 1999
[4] K J Gaston and TM Blackburn Pattern and Process inMacro-ecology Blackwell Malden Mass USA 2000
[5] C Bergmann ldquoUber die verhaltnisse der warmeokonomie derthiere zu ihrer grosserdquo Gottinger Studien vol 3 pp 595ndash7081847
[6] J A Allen ldquoThe influence of physical conditions in the genesisof speciesrdquo Radical Review vol 1 pp 108ndash140 1877
[7] F C James ldquoGeographic size variation in birds and its relation-ship with climaterdquo Ecology vol 51 pp 365ndash390 1970
[8] C D Burnett ldquoGeographic and climatic correlates of morpho-logical variation inEptesicus fuscusrdquo Journal ofMammalogy vol64 no 3 pp 437ndash444 1983
[9] C C Lindsey ldquoBody sizes of poikilotherm vertebrates at differ-ent latitudesrdquo Evolution vol 20 pp 456ndash465 1966
[10] M L Rosenzweig ldquoThe strategy of body size in mammaliancarnivoresrdquo American Midland Naturalist vol 80 pp 299ndash3151968
[11] Y Yom-Tov and E Geffen ldquoGeographic variation in body sizethe effects of ambient temperature and precipitationrdquoOecologiavol 148 no 2 pp 213ndash218 2006
[12] Y Yom-Tov and H Nix ldquoClimatological correlates for body sizeof five species of Australian mammalsrdquo Biological Journal of theLinnean Society vol 29 no 4 pp 245ndash262 1986
[13] D Pincheira-Donoso and SMeiri ldquoAn intercontinental analysisof climate-driven body size clines in reptiles no support forpatterns no signals of processesrdquo Evolutionary Biology vol 40no 4 pp 562ndash578 2013
[14] K G Ashton M C Tracy and A de Queiroz ldquoIs Bergmannrsquosrule valid for mammalsrdquoThe American Naturalist vol 156 no4 pp 390ndash415 2000
[15] S Meiri and T Dayan ldquoOn the validity of Bergmannrsquos rulerdquoJournal of Biogeography vol 30 no 3 pp 331ndash351 2003
[16] K G Ashton ldquoSensitivity of intraspecific latitudinal clines ofbody size for tetrapods to sampling latitude and body sizerdquoIntegrative and Comparative Biology vol 44 no 6 pp 403ndash4122004
[17] K G Ashton and C R Feldman ldquoBergmannrsquos rule in nonavianreptiles turtles follow it lizards and snakes reverse itrdquoEvolutionvol 57 no 5 pp 1151ndash1163 2003
[18] M A Olalla-Tarraga M A Rodrıguez and B A HawkinsldquoBroad-scale patterns of body size in squamate reptiles ofEurope and North Americardquo Journal of Biogeography vol 33no 5 pp 781ndash793 2006
[19] S Volynchik ldquoMorphological variability in Vipera palaesti-nae along an environmental gradientrdquo Asian HerpetologicalResearch vol 3 pp 227ndash239 2012
[20] D Pincheira-Donoso D J Hodgson and T Tregenza ldquoTheevolution of body size under environmental gradients inectothermswhy shouldBergmannrsquos rule apply to lizardsrdquoBMCEvolutionary Biology vol 8 no 1 article 68 2008
[21] R C Stillwell ldquoAre latitudinal clines in body size adaptiverdquoOikos vol 119 no 9 pp 1387ndash1390 2010
[22] S Meiri ldquoBergmannrsquos rulemdashwhatrsquos in a namerdquo Global Ecologyand Biogeography vol 20 no 1 pp 203ndash207 2011
[23] D Pincheira-Donoso ldquoPredictable variation of range-sizesacross an extreme environmental gradient in a lizard adaptiveradiation evolutionary and ecological inferencesrdquo PLoS ONEvol 6 no 12 Article ID e28942 2011
[24] K G Ashton ldquoDo amphibians follow Bergmannrsquos rulerdquo Cana-dian Journal of Zoology vol 80 no 4 pp 708ndash716 2002
[25] M J Angilletta Jr T D Steury andMW Sears ldquoTemperaturegrowth rate and body size in ectotherms fitting pieces of a life-history puzzlerdquo Integrative and Comparative Biology vol 44 no6 pp 498ndash509 2004
[26] C E Oufiero G E A Gartner S C Adolph and T GarlandldquoLatitudinal and climatic variation in body size and dorsalscale counts in Sceloporus lizards a phylogenetic perspectiverdquoEvolution vol 65 no 12 pp 3590ndash3607 2011
[27] S Meiri ldquoEvolution and ecology of lizard body sizesrdquo GlobalEcology and Biogeography vol 17 no 6 pp 724ndash734 2008
[28] D Atkinson and RM Sibly ldquoWhy are organisms usually biggerin colder environments Making sense of a life history puzzlerdquoTrends in Ecology amp Evolution vol 12 pp 235ndash239 1997
[29] F B Cruz L A Fitzgerald R E Espinoza and J A Schulte IIldquoThe importance of phylogenetic scale in tests of Bergmannrsquosand Rapoportrsquos rules lessons from a clade of South Americanlizardsrdquo Journal of Evolutionary Biology vol 18 no 6 pp 1559ndash1574 2005
[30] T AMousseau ldquoEctotherms follow the converse to BergmannrsquosRulerdquo Evolution vol 51 pp 630ndash632 1997
[31] R N Reed ldquoInterspecific patterns of species richness geo-graphic range size and body size among NewWorld venomoussnakesrdquo Ecography vol 26 no 1 pp 107ndash117 2003
[32] D Pincheira-Donoso T Tregenza and D J Hodgson ldquoBodysize evolution in South American Liolaemus lizards of theboulengeri clade a contrasting reassessmentrdquo Journal of Evolu-tionary Biology vol 20 no 5 pp 2067ndash2071 2007
[33] M J Angilletta P H Niewiarowski A E Dunham A Leacheand W P Porter ldquoBergmannrsquos clines in ectotherms illustratinga life-historical perspective with sceloporine lizardsrdquoTheAmer-ican Naturalist vol 164 pp E168ndashE183 2004
[34] M Andersson Sexual Selection Princeton University PressPrinceton NJ USA 1994
International Journal of Zoology 13
[35] F Brana ldquoSexual dimorphism in lacertid lizards male headincrease vs female abdomen increaserdquo Oikos vol 75 pp 511ndash523 1996
[36] E R Pianka ldquoLizard species density in the Kalahari desertrdquoEcology vol 52 pp 1024ndash1029 1971
[37] E R Pianka ldquoSome intercontinental comparisons of desertlizardsrdquoNational Geographic Research vol 1 no 4 pp 490ndash5041985
[38] B H Brattstrom ldquoSocial and thermoregulatory behavior of thebearded dragon Amphibolurus barbatusrdquo Copeia vol 3 pp484ndash497 1971
[39] G C Grigg and F Seebacher ldquoField test of a paradigm hyster-esis of heart rate in thermoregulation by a free-ranging lizard(Pogona barbata)rdquo Proceedings of the Royal Society B BiologicalSciences vol 266 no 1425 pp 1291ndash1297 1999
[40] F Seebacher and C E Franklin ldquoControl of heart rate duringthermoregulation in the heliothermic lizard Pogona barbataimportance of cholinergic and adrenergic mechanismsrdquo TheJournal of Experimental Biology vol 204 no 24 pp 4361ndash43662001
[41] G J Tattersall and R M Gerlach ldquoHypoxia progressivelylowers thermal gaping thresholds in bearded dragons Pogonavitticepsrdquo The Journal of Experimental Biology vol 208 no 17pp 3321ndash3330 2005
[42] D F DeNardo T E Zubal and T C M Hoffman ldquoCloacalevaporative cooling a previously undescribedmeans of increas-ing evaporative water loss at higher temperatures in a desertectotherm theGilamonsterHeloderma suspectumrdquoThe Journalof Experimental Biology vol 207 no 6 pp 945ndash953 2004
[43] S Jaffe ldquoClimate of Israelrdquo inTheZoogeography of Israel Y Yom-Tov and E Tchernov Eds pp 79ndash92 Dr W Junk PublishersDordrecht The Netherlands 1988
[44] U Roll L Stone and S Meiri ldquoHot-spot facts and artifacts-questioning Israelrsquos great biodiversityrdquo Israel Journal of Ecologyand Evolution vol 55 no 3 pp 263ndash279 2009
[45] W Bischoff and J F Schmidtler ldquoNew data on the distributionmorphology and habitat choice of the Lacerta laevis-kulzericomplexrdquo Natura Croatica vol 8 no 3 pp 211ndash222 1999
[46] A Disi D Modry P Necas and L Rifai Amphibians andReptiles of the Hashemite Kingdom of Jordan An Atlas and FieldGuide Edit Chimaira Frankfurt Germany 2001
[47] A Bouskila and P Amitai Handbook of Amphibians andReptiles of Israel Keter Publishing House Jerusalem Israel2001 (Hebrew)
[48] A Bar and G Haimovitch A Field Guide to Reptiles andAmphibians of Israel Pazbar LTD Herzliya Israel 2012
[49] Y L Werner ldquoGeographic sympatry of Acanthodactylus opheo-durus with A boskianus in the Levantrdquo Zoology in the MiddleEast vol 1 pp 92ndash95 1986
[50] R J Hijmans S E Cameron J L Parra P G Jones and AJarvis ldquoVery high resolution interpolated climate surfaces forglobal land areasrdquo International Journal of Climatology vol 25no 15 pp 1965ndash1978 2005
[51] R B Huey ldquoTemperature physiology and the ecology ofreptilesrdquo inBiology of the Reptilia CGans and FH Pough Edsvol 12 of Physiology (C) pp 25ndash91 Academic Press New YorkNY USA 1982
[52] D J Irschick and J B Losos ldquoDo lizards avoid habitats inwhich performance is submaximal The relationship betweensprinting capabilities and structural habitat use in Caribbeananolesrdquo The American Naturalist vol 154 no 3 pp 293ndash3051999
[53] B Vanhooydonck and R Van Damme ldquoEvolutionary relation-ships between body shape and habitat use in lacertid lizardsrdquoEvolutionary Ecology Research vol 1 no 7 pp 785ndash805 1999
[54] J Melville and R Swain ldquoEvolutionary relationships betweenmorphology performance and habitat openness in the lizardgenus Niveoscincus (Scincidae Lygosominae)rdquo Biological Jour-nal of the Linnean Society vol 70 no 4 pp 667ndash683 2000
[55] R B Huey and M Slatkin ldquoCost and benefits of lizard thermo-regulationrdquo The Quarterly Review of Biology vol 51 no 3 pp363ndash384 1976
[56] R D Stevenson ldquoBody size and limits to the daily range of bodytemperature in terrestrial ectothermsrdquoTheAmericanNaturalistvol 125 pp 102ndash117 1985
[57] B W Grant ldquoTrade-offs in activity time and physiologicalperformance for thermoregulating desert lizards Sceloporusmerriamirdquo Ecology vol 71 no 6 pp 2323ndash2333 1990
[58] R Shine and T Madsen ldquoIs thermoregulation unimportant tomost reptiles An example using water pythons (Liasis fuscus)in tropical AustraliardquoPhysiological Zoology vol 69 pp 252ndash2691996
[59] R Shine ldquoReptilian viviparity in cold climates testing theassumptions of an evolutionary hypothesisrdquo Oecologia vol 57no 3 pp 397ndash405 1983
[60] C R Peterson A R Gibson andM E Dorcas ldquoSnake thermalecology the causes and consequences of body temperaturevariationrdquo in Snakes Ecology and Behavior R A Seigel and J TCollins Eds pp 241ndash314 McGraw-Hill New York NY USA1993
[61] R B Huey and J G Kingsolver ldquoEvolution of thermal sensitiv-ity of ectotherm performancerdquo Trends in Ecology and Evolutionvol 4 no 5 pp 131ndash135 1989
[62] J A Dıaz D Bauwens and B Asensio ldquoA comparative studyof the relation between heating rates and ambient temperaturesin lacertid lizardsrdquo Physiological Zoology vol 69 pp 1359ndash13831996
[63] D C Deeming ldquoPost-hatching phenotypic effects of incubationin reptilesrdquo in Reptilian Incubation Environment Evolutionand Behaviour D C Deeming Ed pp 229ndash251 NottinghamUniversity Press Nottingham UK 2004
[64] R Shine M J Elphick and P S Harlow ldquoThe influence ofnatural incubation environments on the phenotypic traits ofhatchling lizardrdquo Ecology vol 78 pp 2559ndash2568 1997
[65] T Flatt R Shine P A Borges-Landaez and S J DownesldquoPhenotypic variation in an oviparousmontane lizard (Bassianaduperreyi) the effects of thermal and hydric incubation envi-ronmentsrdquo Biological Journal of the Linnean Society vol 74 no3 pp 339ndash350 2001
[66] R Shine and M J Elphick ldquoThe effect of short-term weatherfluctuations on temperatures inside lizard nests and on thephenotypic traits of hatchling lizardsrdquo Biological Journal of theLinnean Society vol 72 no 4 pp 555ndash565 2001
[67] O Lourdais R Shine X Bonnet M Guillon and G NaulleauldquoClimate affects embryonic development in a viviparous snakeVipera aspisrdquo Oikos vol 104 no 3 pp 551ndash560 2004
[68] V Delmas X Bonnet M Girondot and A-C Prevot-JulliardldquoVarying hydric conditions during incubation influence eggwater exchange and hatchling phenotype in the red-eared sliderturtlerdquo Physiological and Biochemical Zoology vol 81 no 3 pp345ndash355 2008
[69] X-F Yan X-L Tang F Yue et al ldquoInfluence of ambient temper-ature onmaternal thermoregulation and neonate phenotypes in
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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International Journal of
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Zoology
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International Journal of
Microbiology
6 International Journal of Zoology
Table 2 Climate-morphology relationship between average annual temperature (AAT)average annual precipitation (AAP) and bodymeasurementsratios (regression analysis with temperature and precipitation as the predictors and features as the responses) Positivecorrelation (+) and negative correlation (minus) single sign significant difference (119875 lt 005) and double sign highly significant difference (119875 lt00001)
FeaturesPhoenicolacerta laevis Ophisops elegans Acanthodactylus boskianus Mesalina guttulata
AAT AAP AAT AAP AAT AAP AAT AAPDD CC DD CC DD CC DD CC DD CC DD CC DD CC DD CC
M minus + minus + + + +SVL minusminus + minus minus + + minus + + +HmL minus minus + ++FaL minus minus + + +FeL minus minus ++ +TbL minus minus + +HmLSVL + ++ minus minus + minus minus +FaLSVL + ++ minus + minusminus minus +FeLSVL + ++ minusminus + + + minus minus + minus minus
TbLSVL + ++ minus + minus minus + minus minus
Table 3 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Phoenicolacerta laevis with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
77
88
052111
079152
145149
243333
02140199
00280004
Covariate(SVL)
FLLHLL
11
11
73211275
23494734
20171707
71641038
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
033276
404766
093371
12321679
03410062
lt0001lt0001
Error FLLHLL
3737
4646
036074
033045
Precipitation FLLHLL
88
88
047099
064150
126130
187327
02940275
00880005
Covariate(SVL)
FLLHLL
11
11
71081208
21624677
19131582
62751017
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
030296
493798
081388
14331738
03740056
lt0001lt0001
Error FLLHLL
3636
4646
037076
034045
Table 4 The effect of climate variables on snout-vent length (SVL) Results of multiple regression with SVL as a dependent variable andclimatic factors as predictors
Effect of temperature Effect of precipitation120573 plusmn SE 119905 119875 120573 plusmn SE 119905 119875
Phoenicolacertalaevis
DD minus021 plusmn 021 minus098 0328 minus018 plusmn 021 minus085 0399CC minus0615 plusmn 017 minus351 00009 minus009 plusmn 017 minus054 0588
Ophisops elegansDD minus027 plusmn 011 minus251 0013 026 plusmn 011 238 0019CC minus032 plusmn 012 minus266 0009 025 plusmn 012 208 0041
Acanthodactylusboskianus
DD minus003 plusmn 009 minus034 0727 0136 plusmn 009 137 0207CC minus013 plusmn 011 minus115 0251 021 plusmn 011 minus177 0079
Mesalina guttulata DD minus003 plusmn 009 minus041 068 021 plusmn 009 236 0019CC minus014 plusmn 009 minus151 0134 033 plusmn 009 339 0001
International Journal of Zoology 7
SVL
(mm
)
Average annual temperature (∘C)
60
56
52
48
44
40
8 10 12 14 16 18 20
(a)
SVL
(mm
)
60
56
52
48
44
40
100 200 300 400 500 700 800600 900
Average annual precipitation (mm)
(b)
Figure 3 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Ophisops elegans solidline with circles males dashed line with triangles females
The corporeal ratios and especially lengths (Table 2)are noticeably influenced by the local climate conditionsRegression analysis indicates that the sexes generally followsimilar trends in their corporal dimensions and becomesignificantly larger at higher latitudes By analogy with SVLappendages were positively correlated with precipitation andwere negatively correlated with temperature In additionin both sexes the longer femora may be associated withincreased precipitation However after accounting for SVLa MANCOVA reveals a nonsignificant effect of both abi-otic predictors on limb size (Table 5) Multiple regressiondemonstrates the equivalency of two climate influences intheir relationships with SVL (Table 4) Furthermore malesand females in general did not differ from one another intheir responses to either temperature (120573 = minus027plusmn011 versus120573 = minus032 plusmn 012) or precipitation (120573 = 026 plusmn 011 versus120573 = 025 plusmn 012) gradient
A boskianus In the desert habitats of this species temperaturewas uncorrelated with latitude (119903 = minus0082 119875 = 0247)across the observed geographic range There is however apronounced latitudinal precipitation gradient (119903 = 0815119875 lt 00001) and a negative relationship between annualaverages of temperature and precipitation 119903 = minus0367 119875 lt00001 In this lizard the sexes differ in respect to theirenvironmental-morphological connection (Figures 4(a) and4(b)) The SVL of males did not correlate consistently withtemperature (slope = minus021 plusmn 029 119903 = minus0067 119875 = 0485)and precipitation (slope = 001 plusmn 0008 119903 = 0134 119875 =0160) whereas the SVL of females varied in relation to thesevariables slope = minus081 plusmn 034 119903 = minus0243 119875 = 0021 andslope = 002 plusmn 0007 119903 = 0280 119875 = 0007 for temperatureand precipitation respectively
Corporeal measurements (Table 2) showed a close rela-tionship with rainfall in both sexes and increased precip-itation is correlated to shorter extremities relative to SVLDespite the fact that the appendages tend to lengthen relativeto their SVL with rise in temperature this abiotic component
would seem to affect only hind limb segments (FeL and TbL)The MANCOVA results (Table 6) also suggest that withinboth sexes the temperature gradient significantly contributesonly to HLL variation Precipitation had a significant effecton hind extremity in both sexes furthermore within males itinfluenced the variation in FLL as well Analysis of combinedeffect of environmental variables when both temperature andprecipitation were regressed against SVL (Table 4) revealsthe role of moisture as a major predictor of intraspecificvariability Moreover males and females were similar in thistrend 120573 = minus003 plusmn 009 (temperature) 120573 = 0136 plusmn 009(precipitation) for males and 120573 = 013 plusmn 011 versus 120573 =021 plusmn 011 for females respectively
M guttulata The studied geographic range of this desertlacertid is characterized by a highly significant correlationbetween latitude and both temperature (119903 = 0657 119875 lt00001) and precipitation (119903 = 0682 119875 lt 00001) whereastemperature was uncorrelated with precipitation (119903 = 0030119875 = 0654) In both sexes SVL (Figures 5(a) and 5(b))increased along a rainfall gradient slope = 0006 plusmn 0002 119903 =0215 119875 = 0018 for males slope = 001 plusmn 0004 119903 = 0317119875 = 0001 for females Continuous sampling also revealed aninsignificant relationship between temperature and SVL inthis species Regression analysis (Table 2) indicated an impor-tant role of precipitation in the creation of clines in body andlimb dimensions Moreover spatial changes of both climaticcomponents may induce some allometric shifts in latitudinalspace Thus temperature rise has led to the appearance oflonger (relative to SVL) extremities among females Thisobservation was confirmed by MANCOVA a significantassociation was observed between either FLL or HLLandtemperature as well as between HLL and precipitation Inmales this approach however indicates a nonsignificanteffect of both climatic variables on limb dimensions (Table 7)
Similarly to other desert dwellers (A boskianus) in thisspecies too precipitation level is a stronger ecological deter-minant of body length (Table 4) than temperature gradient
8 International Journal of Zoology
Table 5 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Ophisops elegans with SVL as a covariate
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
1717
1616
012048
026071
081121
140147
06720278
01860155
Covariate(SVL)
FLLHLL
11
11
25225696
5291525
16331432
28643183
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
101138
251265
651347
1359552
00130067
00010023
Error FLLHLL
6565
4242
015039
018047
Precipitation FLLHLL
2323
1717
013056
024064
083156
129130
06730086
02430241
Covariate(SVL)
FLLHLL
11
11
21864902
5341481
14061366
28222971
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
123201
263305
796559
1393612
00060021
00010018
Error FLLHLL
5959
4141
015035
018049
14 16 18 20 22 24
SVL
(mm
)
Average annual temperature (∘C)
85
80
75
70
65
60
55
50
(a)
SVL
(mm
)
85
80
75
70
65
60
55
50
0 50 150 200100 250 300
Average annual precipitation (mm)
(b)
Figure 4 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Acanthodactylusboskianus solid line with circles males dashed line with triangles females
119875 = 0019 120573 = 021plusmn009 versus119875 = 0680 120573 = minus003plusmn009for males 119875 = 0001 120573 = 033 plusmn 009 versus 119875 = 0134120573 = minus014 plusmn 009 for females respectively
4 Discussion
Despite the inability of ectotherms to produce significantmetabolic heat the interaction between body size and heatbalance based on a set of behavioural anatomical andphysiological mechanisms [51] that contribute to fitnessmight explain the peculiarity of ecological drivers in sizeclines among these animalsThe relationship between habitatconditions and morphological variables (body tail or limbdimensions) and consequent shifts in phenology due toclimate change have been observed across a wide range ofreptile taxa [52ndash54] It is possible that in diurnal squamates
environmental conditions may favour selection for smaller-sized individuals [55] which due to the ability to achievemore accurate adjustment of their body temperature havebetter thermoregulatory capacities [56] and thus display highactivity levels In terrestrial ectotherms thermoregulation isrealized behaviourally by habitat selection and daily activitypattern [57] while at the same time morphological special-ization may also essentially facilitate it [55] For exampleShine and Madsen [58] pointed out that for relatively smallreptile species behavioural thermoregulation seems to bemore important especially in conditions of high diurnalthermal heterogeneity In this context desert reptiles inhab-iting warmer regions with lower thermoregulatory costs mayadjust their body temperature mainly behaviourally andthus invest less in adjustment of either body size or shapein relation to ambient temperature Despite the great data
International Journal of Zoology 9
Table 6 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Acanthodactylus boskianus with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
3535
2828
089151
053131
141191
125175
01180012
02390040
Covariate(SVL)
FLLHLL
11
11
60441731
34366125
95262186
80188176
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
203445
4952911
320562
11563885
00780021
0001lt0001
Error FLLHLL
6565
5151
063079
042074
Precipitation FLLHLL
3333
3131
086151
046116
178186
101171
00230016
04810049
Covariate(SVL)
FLLHLL
11
11
64151792
23944222
13182201
51436151
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
161422
7043482
332518
15145073
00730026
lt0001lt0001
Error FLLHLL
6767
4848
048081
046068
14 16 18 20 22 24
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
Average annual temperature (∘C)
(a)
0 50 150 200100 250 300 350 400 450 500 550
Average annual precipitation (mm)
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
(b)
Figure 5The relationship between SVL and (a) average annual temperature and (b) average annual precipitation inMesalina guttulata solidline with circles males dashed line with triangles females
dispersion (as shown in the scatter plots) it was foundthat among the two ldquodesertrdquo species studied (M guttulataand A boskianus) only females of the latter were smallerin hot temperatures whereas in both sexes of the formeras well as in A boskianus males SVL did not correlatewith temperature In the Mediterranean region P laevisand O elegans inhabit cooler climates than the desert Aboskianus and M guttulata In these environments largergravid reptiles in addition to the buffering effects of thebehavioural thermoregulation supplied by the mother [5960] can provide greater temperature stability during thepreoviposition period Volynchik [19] however found that alarge-bodied local viper (Vipera palaestinae) with a Mediter-ranean distribution pattern does not follow Bergmannrsquos ruleor its converse At the same time the most ldquocold-lovingrdquolizard (O elegans) in my own sample obeyed Bergmannrsquos
rule growing larger in cooler environments On the otherhand in desert habitats this pattern of greater thermal inertiaseems to be less important and the behavioural componentof thermoregulation becomes paramount
The impact of ambient temperature on external mor-phology is also significant in respect to relative extremitylengths different degrees of intraspecific variability in limbproportions supporting Allenrsquos rule were observed in all thespecies studied The present findings indicate that temper-ature decrease across the observed habitats could lead toreduction in size of extremity segments relative to bodylength thus constituting a compensatory adaptation to eithercooler or hotter areas I noted an allometric shift in humerusforearm femur and tibia lengths relative to SVL along atemperature gradient among P laevis A similar relationshipbetween average annual temperature and corporeal ratioswas
10 International Journal of Zoology
Table 7 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) inMesalina guttulata with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
2525
2424
021045
024054
156143
181191
00650110
00290019
Covariate(SVL)
FLLHLL
11
11
20084405
9872011
14751407
72797114
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
4501082
8922073
33113455
65837331
lt0001lt0001
lt0001lt0001
Error FLLHLL
9191
6969
013031
013028
Precipitation FLLHLL
2828
2525
019041
022056
142129
162211
01070181
00590008
Covariate(SVL)
FLLHLL
11
11
19504181
9631908
14091307
68667094
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
356901
8021918
25752817
57177133
lt0001lt0001
lt0001lt0001
Error FLLHLL
8888
6868
013032
014026
noted in females of M guttulata Among A boskianus totalhind limb length significantly correlated with both thermalregime and rainfall gradient Hence both Mediterraneanand desert reptiles follow a similar pattern in their bodyshape variation and may benefit from various morphologicalmodifications matched to habitat range
Body temperature changes affect reptile ecology [61]becoming more important to ectotherms living in coolerenvironments which complicate attaining proper body tem-perature [58 62] In support of this my results show the asso-ciation between biogeographic origins of the species exam-ined and their relationship with environmental variables Oninterspecific comparison the most pronounced distinctionswere noted in phenotypic responses to the temperature gra-dient between Mediterranean and desert inhabitants whilethe between-species differences for precipitation-related vari-ation were weaker As expected both Mediterranean regionspecies (P laevis O elegans) display significantly strongerresponses to temperature than desert dwellers (A boskianusM guttulata) Apparently the cooler locations of the formerforce them to exhibit more consistent morphological vari-ability in respect to temperature changes whereas for desertspecies such habitat-morphology connection seems to be lessimportant It is highly likely that the speciesrsquo sensitivity tothe environment is associated not only with their ecologicaldifferentiation but also with body size ranges within thesample Thus this might be one possible explanation for thedifferent albeit relatively minor responses to temperaturebetween ecologically similar species (ie P laevis versus Oelegans andA boskianus versusM guttulata) that were notedhere In the examined samples L laevis owing to its greatermeasurement ranges than O elegans has a higher potentialfor more consistent matching of its body dimensions to theobserved temperature gradient The same is true for the twodesert lizardsA boskianus due to its extended body and limb
ranges in comparison with M guttulata displays a strongermorphological-environmental link
The examination of gender-specific habitat-morphologyinteractions revealed that within three of the four species (Plaevis A boskianus and M guttulata) sensitivity to the envi-ronment is coupledwith sex Considering the effect of climatevariables on SVL the findings demonstrate that females ingeneral show a more consistent link between temperatureand bodylimb measurements than males while the effectof precipitation on external characters was similar for bothsexes Moreover in P laevis SVL was significantly morestrongly correlated with the temperature gradient in femalesthan in malesThese observations indicate the sex-associatedeffect of natural selection pointing to different thermal andmetabolic demands inmales and femalesThus it is likely thatin females the increased body size in colder environmentsis associated with reproduction-induced requirements Thispattern suggests that females due to increased thermalrequirements particularly during vitellogenesis [63] aremore able to generate a range of suitable morphologicalmodifications for maintenance of optimal body temperaturein local environments Overall my findings indicate thatalthough females show amore consistent correlation betweenSVL and a temperature gradient than males the body shapechanges involving both body and limb dimensions arerather preliminary in explaining the observed intersexualdivergence in the habitat-morphology relationship
Environmental conditions within the nest experiencedduring early ontogenesis especially temperature and mois-ture of substrate can significantly affect development andgrowth trajectories of individuals in oviparous reptiles [64ndash68] As observed in many species either posthatching phe-notype or offspring fitness are closely associated with thermalregime [63 69ndash71] In both the laboratory and in naturalnests [64] temperature is traditionally considered to be animportant environmental determinant of reptile size while
International Journal of Zoology 11
the effect of water-related factors is more complex Severalrecent studies have tested the effect of substrate moistureduring incubation of eggs on a diverse range of reptile speciesSignificant effects are found in certain species [66 68 72 73]but not in others [74ndash76] that may reflect either differentwater permeability of the eggshell or interspecific variationin the water content of eggs [77] On the other hand theappearance of morphological variation along a precipitationgradient which in desert lizards is even more evident thanthe temperature-related variability can be considered as aresponse to the local habitats In reptiles food availabilitystrongly affects growth trajectories and is one of the possibledeterminants of body size and shape [78ndash80] Overall inarid regions where vegetation and arthropod fauna aredetermined primarily by precipitation [11] wetter localitiesprovide better food resources to lizards at the populationlevel The present findings suggest that among desert speciesthe possible spatial differences in prey availability and thusin nutrition levels may lead to morphometric differentiationbetween specimens inhabiting dry or wet sites Howeverdetailed studies on possible dietary variation linked tolocal environments are necessary to answer the question ofwhether the habitat conditions which are dependent on pre-cipitation have an effect on body dimensions in these lizards
A nonphylogenetic approach suggests that lizard speciestend to exhibit strong morphological specialization in rela-tion to their habitat [53 81] Variation in body charactersrelated to locomotion which in turn is associated withsubstrate pattern has been observed across many lizard taxa[54 82ndash84] Unfortunately based on available datasets Icould not evaluate whether the shift in substrate usage isassociated with limb proportion changes and so a rationalexplanation for the effect of vegetation on limb lengthsthrough its dependence upon hydrothermal regime remainsto be determined My findings show that generally theexamined species indicate a uniform pattern in extremitiessize variation fore and especially hind limb lengths werepositively correlated with temperature and negatively withprecipitation The results indicate that ecological adaptationto abiotic factors is a powerful source of extremity sizevariation which is under the effect of natural selection Inlizards the morphology-performance relationships suggestthat ground-dwelling species from open landscapes shouldpossess relatively long limb segments to their body length[53] This body shape pattern increases stride length provid-ing better sprinting abilities [85 86] Furthermore shorterextremities may facilitate the locomotion in highly vegetatedareas where long limbs may be disadvantageous [53] In thiscontextmyfindings suggest that various body shape patternssuch as relatively shortlong limbs or their segments whichare suited to the environmental requirements may reflect anadaptation to either dense or sparse vegetation resulting fromdifferent rainfall intensities across the distribution range
Finally given the potential importance of habitats forlimb size variation lizardsmay also use their protruding bodyparts as additional (together with body surface area) heatexchangers In these reptiles for optimal balance betweenheat gain and heat loss isometric size changes to a certainextent are a ldquotwo-edged swordrdquo inwhich high thermal inertia
of large bodies is accompanied by slow heating rates and viceversa In this respect among desert dwellers relatively longextremities and small size enhance heat exchange and seemto be a morphological adaptation for effective thermoreg-ulation In desert areas large daily fluctuations of temper-ature force the ectotherms to quickly respond to changingconditions and rapidly reach the necessary metabolic ratesfor locomotor activity Long-limbed individuals which havean increased surface area-to-volume ratio may enhancetheir heating and cooling abilities through more effectiveinteractions between the body and either solar radiationor surface temperature gradient Hence a consistent linkbetween environmental variables and limb lengths can alsobe explained by their importance for maintenance of optimalbody temperature in local environments As shown above thefact that the extremity size-environment link is more obviousin respect to hind limbs than to fore ones reinforces thishypothesis relatively large hind limbs having an increasedheat exchange capacity are much more powerful tool foreffective thermoregulation than small fore extremities
In summary the lacertid lizards I studied generallyfollowed the ecogeographic rules of Bergmann and AllenIn addition the findings indicate both intersexual and inter-specific differences in the habitat-morphology relationshipwhich can be considered within the framework of theirfunctional connectionMydata provide evidence that femalestend to show stronger relationships between climate vari-ables and body dimensions than males In desert speciestemperature has a smaller effect than rainfall on lizardphenotypes Under a constant dry climate water availabilityseems to be the most important abiotic factor in reptileecology In this respect due to the strong association betweenprecipitation and productivity my findings could also beinterpreted as evidence for the hypothesis that different bodysize patterns are linked to the spatial variation in primaryproduction that is the ldquoresource rulerdquo In the Mediterraneanregion lizards the thermal regime is apparently the maindriving force of morphological variability The present studysuggests a complex link between environmental variablesand morphological characters within lacertid species Thephysical conditions such as temperature and precipitationgradient were shown to be able to significantly affect bothbody and limb dimensions and thus as a powerful sourceof variation they play an important role in lizard mor-phology However general statements about the habitat-morphology relationships and their potential importance formaintenance of optimal body temperature in reptiles arehard to make due to the enormous diversity of variationsin body composition and physiology across species sexesand even individuals and the difficulty in evaluating enoughmechanisms in enough species Consequently additionalfield and experimental studies testing both body size andshape variations and their relationships with environmentalvariables especially at the intraspecific level and accountingfor sex-specific aspects are needed to help determine whetherthe observed patterns are common across species and to whatextent they are important for effective thermoregulation
12 International Journal of Zoology
Conflict of Interests
The author declares that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The author would like to thank Shai Meiri for his helpfulcomments on earlier drafts of the paper The author thanksErezMaza for assistancewith data preparationAnat Feldmanfor provision of the GIS-compatible temperature data andNaomi Paz for linguistic editing The author also thanks theIsrael Ministry of Science Culture and Sport for supportingthe National Collections of Natural History at Tel AvivUniversity as a biodiversity environment and agricultureresearch knowledge centre
References
[1] E Mayr Animal Species and Evolution Harvard UniversityPress Cambridge Mass USA 1963
[2] C Ray ldquoThe application of Bergmannrsquos and Allenrsquos rules to thepoikilothermsrdquo Journal of Morphology vol 106 pp 85ndash1081960
[3] TM Blackburn K J Gaston andN Loder ldquoGeographic gradi-ents in body size a clarification of Bergmannrsquos rulerdquo Diversityand Distributions vol 5 no 4 pp 165ndash174 1999
[4] K J Gaston and TM Blackburn Pattern and Process inMacro-ecology Blackwell Malden Mass USA 2000
[5] C Bergmann ldquoUber die verhaltnisse der warmeokonomie derthiere zu ihrer grosserdquo Gottinger Studien vol 3 pp 595ndash7081847
[6] J A Allen ldquoThe influence of physical conditions in the genesisof speciesrdquo Radical Review vol 1 pp 108ndash140 1877
[7] F C James ldquoGeographic size variation in birds and its relation-ship with climaterdquo Ecology vol 51 pp 365ndash390 1970
[8] C D Burnett ldquoGeographic and climatic correlates of morpho-logical variation inEptesicus fuscusrdquo Journal ofMammalogy vol64 no 3 pp 437ndash444 1983
[9] C C Lindsey ldquoBody sizes of poikilotherm vertebrates at differ-ent latitudesrdquo Evolution vol 20 pp 456ndash465 1966
[10] M L Rosenzweig ldquoThe strategy of body size in mammaliancarnivoresrdquo American Midland Naturalist vol 80 pp 299ndash3151968
[11] Y Yom-Tov and E Geffen ldquoGeographic variation in body sizethe effects of ambient temperature and precipitationrdquoOecologiavol 148 no 2 pp 213ndash218 2006
[12] Y Yom-Tov and H Nix ldquoClimatological correlates for body sizeof five species of Australian mammalsrdquo Biological Journal of theLinnean Society vol 29 no 4 pp 245ndash262 1986
[13] D Pincheira-Donoso and SMeiri ldquoAn intercontinental analysisof climate-driven body size clines in reptiles no support forpatterns no signals of processesrdquo Evolutionary Biology vol 40no 4 pp 562ndash578 2013
[14] K G Ashton M C Tracy and A de Queiroz ldquoIs Bergmannrsquosrule valid for mammalsrdquoThe American Naturalist vol 156 no4 pp 390ndash415 2000
[15] S Meiri and T Dayan ldquoOn the validity of Bergmannrsquos rulerdquoJournal of Biogeography vol 30 no 3 pp 331ndash351 2003
[16] K G Ashton ldquoSensitivity of intraspecific latitudinal clines ofbody size for tetrapods to sampling latitude and body sizerdquoIntegrative and Comparative Biology vol 44 no 6 pp 403ndash4122004
[17] K G Ashton and C R Feldman ldquoBergmannrsquos rule in nonavianreptiles turtles follow it lizards and snakes reverse itrdquoEvolutionvol 57 no 5 pp 1151ndash1163 2003
[18] M A Olalla-Tarraga M A Rodrıguez and B A HawkinsldquoBroad-scale patterns of body size in squamate reptiles ofEurope and North Americardquo Journal of Biogeography vol 33no 5 pp 781ndash793 2006
[19] S Volynchik ldquoMorphological variability in Vipera palaesti-nae along an environmental gradientrdquo Asian HerpetologicalResearch vol 3 pp 227ndash239 2012
[20] D Pincheira-Donoso D J Hodgson and T Tregenza ldquoTheevolution of body size under environmental gradients inectothermswhy shouldBergmannrsquos rule apply to lizardsrdquoBMCEvolutionary Biology vol 8 no 1 article 68 2008
[21] R C Stillwell ldquoAre latitudinal clines in body size adaptiverdquoOikos vol 119 no 9 pp 1387ndash1390 2010
[22] S Meiri ldquoBergmannrsquos rulemdashwhatrsquos in a namerdquo Global Ecologyand Biogeography vol 20 no 1 pp 203ndash207 2011
[23] D Pincheira-Donoso ldquoPredictable variation of range-sizesacross an extreme environmental gradient in a lizard adaptiveradiation evolutionary and ecological inferencesrdquo PLoS ONEvol 6 no 12 Article ID e28942 2011
[24] K G Ashton ldquoDo amphibians follow Bergmannrsquos rulerdquo Cana-dian Journal of Zoology vol 80 no 4 pp 708ndash716 2002
[25] M J Angilletta Jr T D Steury andMW Sears ldquoTemperaturegrowth rate and body size in ectotherms fitting pieces of a life-history puzzlerdquo Integrative and Comparative Biology vol 44 no6 pp 498ndash509 2004
[26] C E Oufiero G E A Gartner S C Adolph and T GarlandldquoLatitudinal and climatic variation in body size and dorsalscale counts in Sceloporus lizards a phylogenetic perspectiverdquoEvolution vol 65 no 12 pp 3590ndash3607 2011
[27] S Meiri ldquoEvolution and ecology of lizard body sizesrdquo GlobalEcology and Biogeography vol 17 no 6 pp 724ndash734 2008
[28] D Atkinson and RM Sibly ldquoWhy are organisms usually biggerin colder environments Making sense of a life history puzzlerdquoTrends in Ecology amp Evolution vol 12 pp 235ndash239 1997
[29] F B Cruz L A Fitzgerald R E Espinoza and J A Schulte IIldquoThe importance of phylogenetic scale in tests of Bergmannrsquosand Rapoportrsquos rules lessons from a clade of South Americanlizardsrdquo Journal of Evolutionary Biology vol 18 no 6 pp 1559ndash1574 2005
[30] T AMousseau ldquoEctotherms follow the converse to BergmannrsquosRulerdquo Evolution vol 51 pp 630ndash632 1997
[31] R N Reed ldquoInterspecific patterns of species richness geo-graphic range size and body size among NewWorld venomoussnakesrdquo Ecography vol 26 no 1 pp 107ndash117 2003
[32] D Pincheira-Donoso T Tregenza and D J Hodgson ldquoBodysize evolution in South American Liolaemus lizards of theboulengeri clade a contrasting reassessmentrdquo Journal of Evolu-tionary Biology vol 20 no 5 pp 2067ndash2071 2007
[33] M J Angilletta P H Niewiarowski A E Dunham A Leacheand W P Porter ldquoBergmannrsquos clines in ectotherms illustratinga life-historical perspective with sceloporine lizardsrdquoTheAmer-ican Naturalist vol 164 pp E168ndashE183 2004
[34] M Andersson Sexual Selection Princeton University PressPrinceton NJ USA 1994
International Journal of Zoology 13
[35] F Brana ldquoSexual dimorphism in lacertid lizards male headincrease vs female abdomen increaserdquo Oikos vol 75 pp 511ndash523 1996
[36] E R Pianka ldquoLizard species density in the Kalahari desertrdquoEcology vol 52 pp 1024ndash1029 1971
[37] E R Pianka ldquoSome intercontinental comparisons of desertlizardsrdquoNational Geographic Research vol 1 no 4 pp 490ndash5041985
[38] B H Brattstrom ldquoSocial and thermoregulatory behavior of thebearded dragon Amphibolurus barbatusrdquo Copeia vol 3 pp484ndash497 1971
[39] G C Grigg and F Seebacher ldquoField test of a paradigm hyster-esis of heart rate in thermoregulation by a free-ranging lizard(Pogona barbata)rdquo Proceedings of the Royal Society B BiologicalSciences vol 266 no 1425 pp 1291ndash1297 1999
[40] F Seebacher and C E Franklin ldquoControl of heart rate duringthermoregulation in the heliothermic lizard Pogona barbataimportance of cholinergic and adrenergic mechanismsrdquo TheJournal of Experimental Biology vol 204 no 24 pp 4361ndash43662001
[41] G J Tattersall and R M Gerlach ldquoHypoxia progressivelylowers thermal gaping thresholds in bearded dragons Pogonavitticepsrdquo The Journal of Experimental Biology vol 208 no 17pp 3321ndash3330 2005
[42] D F DeNardo T E Zubal and T C M Hoffman ldquoCloacalevaporative cooling a previously undescribedmeans of increas-ing evaporative water loss at higher temperatures in a desertectotherm theGilamonsterHeloderma suspectumrdquoThe Journalof Experimental Biology vol 207 no 6 pp 945ndash953 2004
[43] S Jaffe ldquoClimate of Israelrdquo inTheZoogeography of Israel Y Yom-Tov and E Tchernov Eds pp 79ndash92 Dr W Junk PublishersDordrecht The Netherlands 1988
[44] U Roll L Stone and S Meiri ldquoHot-spot facts and artifacts-questioning Israelrsquos great biodiversityrdquo Israel Journal of Ecologyand Evolution vol 55 no 3 pp 263ndash279 2009
[45] W Bischoff and J F Schmidtler ldquoNew data on the distributionmorphology and habitat choice of the Lacerta laevis-kulzericomplexrdquo Natura Croatica vol 8 no 3 pp 211ndash222 1999
[46] A Disi D Modry P Necas and L Rifai Amphibians andReptiles of the Hashemite Kingdom of Jordan An Atlas and FieldGuide Edit Chimaira Frankfurt Germany 2001
[47] A Bouskila and P Amitai Handbook of Amphibians andReptiles of Israel Keter Publishing House Jerusalem Israel2001 (Hebrew)
[48] A Bar and G Haimovitch A Field Guide to Reptiles andAmphibians of Israel Pazbar LTD Herzliya Israel 2012
[49] Y L Werner ldquoGeographic sympatry of Acanthodactylus opheo-durus with A boskianus in the Levantrdquo Zoology in the MiddleEast vol 1 pp 92ndash95 1986
[50] R J Hijmans S E Cameron J L Parra P G Jones and AJarvis ldquoVery high resolution interpolated climate surfaces forglobal land areasrdquo International Journal of Climatology vol 25no 15 pp 1965ndash1978 2005
[51] R B Huey ldquoTemperature physiology and the ecology ofreptilesrdquo inBiology of the Reptilia CGans and FH Pough Edsvol 12 of Physiology (C) pp 25ndash91 Academic Press New YorkNY USA 1982
[52] D J Irschick and J B Losos ldquoDo lizards avoid habitats inwhich performance is submaximal The relationship betweensprinting capabilities and structural habitat use in Caribbeananolesrdquo The American Naturalist vol 154 no 3 pp 293ndash3051999
[53] B Vanhooydonck and R Van Damme ldquoEvolutionary relation-ships between body shape and habitat use in lacertid lizardsrdquoEvolutionary Ecology Research vol 1 no 7 pp 785ndash805 1999
[54] J Melville and R Swain ldquoEvolutionary relationships betweenmorphology performance and habitat openness in the lizardgenus Niveoscincus (Scincidae Lygosominae)rdquo Biological Jour-nal of the Linnean Society vol 70 no 4 pp 667ndash683 2000
[55] R B Huey and M Slatkin ldquoCost and benefits of lizard thermo-regulationrdquo The Quarterly Review of Biology vol 51 no 3 pp363ndash384 1976
[56] R D Stevenson ldquoBody size and limits to the daily range of bodytemperature in terrestrial ectothermsrdquoTheAmericanNaturalistvol 125 pp 102ndash117 1985
[57] B W Grant ldquoTrade-offs in activity time and physiologicalperformance for thermoregulating desert lizards Sceloporusmerriamirdquo Ecology vol 71 no 6 pp 2323ndash2333 1990
[58] R Shine and T Madsen ldquoIs thermoregulation unimportant tomost reptiles An example using water pythons (Liasis fuscus)in tropical AustraliardquoPhysiological Zoology vol 69 pp 252ndash2691996
[59] R Shine ldquoReptilian viviparity in cold climates testing theassumptions of an evolutionary hypothesisrdquo Oecologia vol 57no 3 pp 397ndash405 1983
[60] C R Peterson A R Gibson andM E Dorcas ldquoSnake thermalecology the causes and consequences of body temperaturevariationrdquo in Snakes Ecology and Behavior R A Seigel and J TCollins Eds pp 241ndash314 McGraw-Hill New York NY USA1993
[61] R B Huey and J G Kingsolver ldquoEvolution of thermal sensitiv-ity of ectotherm performancerdquo Trends in Ecology and Evolutionvol 4 no 5 pp 131ndash135 1989
[62] J A Dıaz D Bauwens and B Asensio ldquoA comparative studyof the relation between heating rates and ambient temperaturesin lacertid lizardsrdquo Physiological Zoology vol 69 pp 1359ndash13831996
[63] D C Deeming ldquoPost-hatching phenotypic effects of incubationin reptilesrdquo in Reptilian Incubation Environment Evolutionand Behaviour D C Deeming Ed pp 229ndash251 NottinghamUniversity Press Nottingham UK 2004
[64] R Shine M J Elphick and P S Harlow ldquoThe influence ofnatural incubation environments on the phenotypic traits ofhatchling lizardrdquo Ecology vol 78 pp 2559ndash2568 1997
[65] T Flatt R Shine P A Borges-Landaez and S J DownesldquoPhenotypic variation in an oviparousmontane lizard (Bassianaduperreyi) the effects of thermal and hydric incubation envi-ronmentsrdquo Biological Journal of the Linnean Society vol 74 no3 pp 339ndash350 2001
[66] R Shine and M J Elphick ldquoThe effect of short-term weatherfluctuations on temperatures inside lizard nests and on thephenotypic traits of hatchling lizardsrdquo Biological Journal of theLinnean Society vol 72 no 4 pp 555ndash565 2001
[67] O Lourdais R Shine X Bonnet M Guillon and G NaulleauldquoClimate affects embryonic development in a viviparous snakeVipera aspisrdquo Oikos vol 104 no 3 pp 551ndash560 2004
[68] V Delmas X Bonnet M Girondot and A-C Prevot-JulliardldquoVarying hydric conditions during incubation influence eggwater exchange and hatchling phenotype in the red-eared sliderturtlerdquo Physiological and Biochemical Zoology vol 81 no 3 pp345ndash355 2008
[69] X-F Yan X-L Tang F Yue et al ldquoInfluence of ambient temper-ature onmaternal thermoregulation and neonate phenotypes in
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
Submit your manuscripts athttpwwwhindawicom
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International Journal of
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Microbiology
International Journal of Zoology 7
SVL
(mm
)
Average annual temperature (∘C)
60
56
52
48
44
40
8 10 12 14 16 18 20
(a)
SVL
(mm
)
60
56
52
48
44
40
100 200 300 400 500 700 800600 900
Average annual precipitation (mm)
(b)
Figure 3 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Ophisops elegans solidline with circles males dashed line with triangles females
The corporeal ratios and especially lengths (Table 2)are noticeably influenced by the local climate conditionsRegression analysis indicates that the sexes generally followsimilar trends in their corporal dimensions and becomesignificantly larger at higher latitudes By analogy with SVLappendages were positively correlated with precipitation andwere negatively correlated with temperature In additionin both sexes the longer femora may be associated withincreased precipitation However after accounting for SVLa MANCOVA reveals a nonsignificant effect of both abi-otic predictors on limb size (Table 5) Multiple regressiondemonstrates the equivalency of two climate influences intheir relationships with SVL (Table 4) Furthermore malesand females in general did not differ from one another intheir responses to either temperature (120573 = minus027plusmn011 versus120573 = minus032 plusmn 012) or precipitation (120573 = 026 plusmn 011 versus120573 = 025 plusmn 012) gradient
A boskianus In the desert habitats of this species temperaturewas uncorrelated with latitude (119903 = minus0082 119875 = 0247)across the observed geographic range There is however apronounced latitudinal precipitation gradient (119903 = 0815119875 lt 00001) and a negative relationship between annualaverages of temperature and precipitation 119903 = minus0367 119875 lt00001 In this lizard the sexes differ in respect to theirenvironmental-morphological connection (Figures 4(a) and4(b)) The SVL of males did not correlate consistently withtemperature (slope = minus021 plusmn 029 119903 = minus0067 119875 = 0485)and precipitation (slope = 001 plusmn 0008 119903 = 0134 119875 =0160) whereas the SVL of females varied in relation to thesevariables slope = minus081 plusmn 034 119903 = minus0243 119875 = 0021 andslope = 002 plusmn 0007 119903 = 0280 119875 = 0007 for temperatureand precipitation respectively
Corporeal measurements (Table 2) showed a close rela-tionship with rainfall in both sexes and increased precip-itation is correlated to shorter extremities relative to SVLDespite the fact that the appendages tend to lengthen relativeto their SVL with rise in temperature this abiotic component
would seem to affect only hind limb segments (FeL and TbL)The MANCOVA results (Table 6) also suggest that withinboth sexes the temperature gradient significantly contributesonly to HLL variation Precipitation had a significant effecton hind extremity in both sexes furthermore within males itinfluenced the variation in FLL as well Analysis of combinedeffect of environmental variables when both temperature andprecipitation were regressed against SVL (Table 4) revealsthe role of moisture as a major predictor of intraspecificvariability Moreover males and females were similar in thistrend 120573 = minus003 plusmn 009 (temperature) 120573 = 0136 plusmn 009(precipitation) for males and 120573 = 013 plusmn 011 versus 120573 =021 plusmn 011 for females respectively
M guttulata The studied geographic range of this desertlacertid is characterized by a highly significant correlationbetween latitude and both temperature (119903 = 0657 119875 lt00001) and precipitation (119903 = 0682 119875 lt 00001) whereastemperature was uncorrelated with precipitation (119903 = 0030119875 = 0654) In both sexes SVL (Figures 5(a) and 5(b))increased along a rainfall gradient slope = 0006 plusmn 0002 119903 =0215 119875 = 0018 for males slope = 001 plusmn 0004 119903 = 0317119875 = 0001 for females Continuous sampling also revealed aninsignificant relationship between temperature and SVL inthis species Regression analysis (Table 2) indicated an impor-tant role of precipitation in the creation of clines in body andlimb dimensions Moreover spatial changes of both climaticcomponents may induce some allometric shifts in latitudinalspace Thus temperature rise has led to the appearance oflonger (relative to SVL) extremities among females Thisobservation was confirmed by MANCOVA a significantassociation was observed between either FLL or HLLandtemperature as well as between HLL and precipitation Inmales this approach however indicates a nonsignificanteffect of both climatic variables on limb dimensions (Table 7)
Similarly to other desert dwellers (A boskianus) in thisspecies too precipitation level is a stronger ecological deter-minant of body length (Table 4) than temperature gradient
8 International Journal of Zoology
Table 5 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Ophisops elegans with SVL as a covariate
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
1717
1616
012048
026071
081121
140147
06720278
01860155
Covariate(SVL)
FLLHLL
11
11
25225696
5291525
16331432
28643183
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
101138
251265
651347
1359552
00130067
00010023
Error FLLHLL
6565
4242
015039
018047
Precipitation FLLHLL
2323
1717
013056
024064
083156
129130
06730086
02430241
Covariate(SVL)
FLLHLL
11
11
21864902
5341481
14061366
28222971
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
123201
263305
796559
1393612
00060021
00010018
Error FLLHLL
5959
4141
015035
018049
14 16 18 20 22 24
SVL
(mm
)
Average annual temperature (∘C)
85
80
75
70
65
60
55
50
(a)
SVL
(mm
)
85
80
75
70
65
60
55
50
0 50 150 200100 250 300
Average annual precipitation (mm)
(b)
Figure 4 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Acanthodactylusboskianus solid line with circles males dashed line with triangles females
119875 = 0019 120573 = 021plusmn009 versus119875 = 0680 120573 = minus003plusmn009for males 119875 = 0001 120573 = 033 plusmn 009 versus 119875 = 0134120573 = minus014 plusmn 009 for females respectively
4 Discussion
Despite the inability of ectotherms to produce significantmetabolic heat the interaction between body size and heatbalance based on a set of behavioural anatomical andphysiological mechanisms [51] that contribute to fitnessmight explain the peculiarity of ecological drivers in sizeclines among these animalsThe relationship between habitatconditions and morphological variables (body tail or limbdimensions) and consequent shifts in phenology due toclimate change have been observed across a wide range ofreptile taxa [52ndash54] It is possible that in diurnal squamates
environmental conditions may favour selection for smaller-sized individuals [55] which due to the ability to achievemore accurate adjustment of their body temperature havebetter thermoregulatory capacities [56] and thus display highactivity levels In terrestrial ectotherms thermoregulation isrealized behaviourally by habitat selection and daily activitypattern [57] while at the same time morphological special-ization may also essentially facilitate it [55] For exampleShine and Madsen [58] pointed out that for relatively smallreptile species behavioural thermoregulation seems to bemore important especially in conditions of high diurnalthermal heterogeneity In this context desert reptiles inhab-iting warmer regions with lower thermoregulatory costs mayadjust their body temperature mainly behaviourally andthus invest less in adjustment of either body size or shapein relation to ambient temperature Despite the great data
International Journal of Zoology 9
Table 6 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Acanthodactylus boskianus with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
3535
2828
089151
053131
141191
125175
01180012
02390040
Covariate(SVL)
FLLHLL
11
11
60441731
34366125
95262186
80188176
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
203445
4952911
320562
11563885
00780021
0001lt0001
Error FLLHLL
6565
5151
063079
042074
Precipitation FLLHLL
3333
3131
086151
046116
178186
101171
00230016
04810049
Covariate(SVL)
FLLHLL
11
11
64151792
23944222
13182201
51436151
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
161422
7043482
332518
15145073
00730026
lt0001lt0001
Error FLLHLL
6767
4848
048081
046068
14 16 18 20 22 24
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
Average annual temperature (∘C)
(a)
0 50 150 200100 250 300 350 400 450 500 550
Average annual precipitation (mm)
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
(b)
Figure 5The relationship between SVL and (a) average annual temperature and (b) average annual precipitation inMesalina guttulata solidline with circles males dashed line with triangles females
dispersion (as shown in the scatter plots) it was foundthat among the two ldquodesertrdquo species studied (M guttulataand A boskianus) only females of the latter were smallerin hot temperatures whereas in both sexes of the formeras well as in A boskianus males SVL did not correlatewith temperature In the Mediterranean region P laevisand O elegans inhabit cooler climates than the desert Aboskianus and M guttulata In these environments largergravid reptiles in addition to the buffering effects of thebehavioural thermoregulation supplied by the mother [5960] can provide greater temperature stability during thepreoviposition period Volynchik [19] however found that alarge-bodied local viper (Vipera palaestinae) with a Mediter-ranean distribution pattern does not follow Bergmannrsquos ruleor its converse At the same time the most ldquocold-lovingrdquolizard (O elegans) in my own sample obeyed Bergmannrsquos
rule growing larger in cooler environments On the otherhand in desert habitats this pattern of greater thermal inertiaseems to be less important and the behavioural componentof thermoregulation becomes paramount
The impact of ambient temperature on external mor-phology is also significant in respect to relative extremitylengths different degrees of intraspecific variability in limbproportions supporting Allenrsquos rule were observed in all thespecies studied The present findings indicate that temper-ature decrease across the observed habitats could lead toreduction in size of extremity segments relative to bodylength thus constituting a compensatory adaptation to eithercooler or hotter areas I noted an allometric shift in humerusforearm femur and tibia lengths relative to SVL along atemperature gradient among P laevis A similar relationshipbetween average annual temperature and corporeal ratioswas
10 International Journal of Zoology
Table 7 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) inMesalina guttulata with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
2525
2424
021045
024054
156143
181191
00650110
00290019
Covariate(SVL)
FLLHLL
11
11
20084405
9872011
14751407
72797114
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
4501082
8922073
33113455
65837331
lt0001lt0001
lt0001lt0001
Error FLLHLL
9191
6969
013031
013028
Precipitation FLLHLL
2828
2525
019041
022056
142129
162211
01070181
00590008
Covariate(SVL)
FLLHLL
11
11
19504181
9631908
14091307
68667094
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
356901
8021918
25752817
57177133
lt0001lt0001
lt0001lt0001
Error FLLHLL
8888
6868
013032
014026
noted in females of M guttulata Among A boskianus totalhind limb length significantly correlated with both thermalregime and rainfall gradient Hence both Mediterraneanand desert reptiles follow a similar pattern in their bodyshape variation and may benefit from various morphologicalmodifications matched to habitat range
Body temperature changes affect reptile ecology [61]becoming more important to ectotherms living in coolerenvironments which complicate attaining proper body tem-perature [58 62] In support of this my results show the asso-ciation between biogeographic origins of the species exam-ined and their relationship with environmental variables Oninterspecific comparison the most pronounced distinctionswere noted in phenotypic responses to the temperature gra-dient between Mediterranean and desert inhabitants whilethe between-species differences for precipitation-related vari-ation were weaker As expected both Mediterranean regionspecies (P laevis O elegans) display significantly strongerresponses to temperature than desert dwellers (A boskianusM guttulata) Apparently the cooler locations of the formerforce them to exhibit more consistent morphological vari-ability in respect to temperature changes whereas for desertspecies such habitat-morphology connection seems to be lessimportant It is highly likely that the speciesrsquo sensitivity tothe environment is associated not only with their ecologicaldifferentiation but also with body size ranges within thesample Thus this might be one possible explanation for thedifferent albeit relatively minor responses to temperaturebetween ecologically similar species (ie P laevis versus Oelegans andA boskianus versusM guttulata) that were notedhere In the examined samples L laevis owing to its greatermeasurement ranges than O elegans has a higher potentialfor more consistent matching of its body dimensions to theobserved temperature gradient The same is true for the twodesert lizardsA boskianus due to its extended body and limb
ranges in comparison with M guttulata displays a strongermorphological-environmental link
The examination of gender-specific habitat-morphologyinteractions revealed that within three of the four species (Plaevis A boskianus and M guttulata) sensitivity to the envi-ronment is coupledwith sex Considering the effect of climatevariables on SVL the findings demonstrate that females ingeneral show a more consistent link between temperatureand bodylimb measurements than males while the effectof precipitation on external characters was similar for bothsexes Moreover in P laevis SVL was significantly morestrongly correlated with the temperature gradient in femalesthan in malesThese observations indicate the sex-associatedeffect of natural selection pointing to different thermal andmetabolic demands inmales and femalesThus it is likely thatin females the increased body size in colder environmentsis associated with reproduction-induced requirements Thispattern suggests that females due to increased thermalrequirements particularly during vitellogenesis [63] aremore able to generate a range of suitable morphologicalmodifications for maintenance of optimal body temperaturein local environments Overall my findings indicate thatalthough females show amore consistent correlation betweenSVL and a temperature gradient than males the body shapechanges involving both body and limb dimensions arerather preliminary in explaining the observed intersexualdivergence in the habitat-morphology relationship
Environmental conditions within the nest experiencedduring early ontogenesis especially temperature and mois-ture of substrate can significantly affect development andgrowth trajectories of individuals in oviparous reptiles [64ndash68] As observed in many species either posthatching phe-notype or offspring fitness are closely associated with thermalregime [63 69ndash71] In both the laboratory and in naturalnests [64] temperature is traditionally considered to be animportant environmental determinant of reptile size while
International Journal of Zoology 11
the effect of water-related factors is more complex Severalrecent studies have tested the effect of substrate moistureduring incubation of eggs on a diverse range of reptile speciesSignificant effects are found in certain species [66 68 72 73]but not in others [74ndash76] that may reflect either differentwater permeability of the eggshell or interspecific variationin the water content of eggs [77] On the other hand theappearance of morphological variation along a precipitationgradient which in desert lizards is even more evident thanthe temperature-related variability can be considered as aresponse to the local habitats In reptiles food availabilitystrongly affects growth trajectories and is one of the possibledeterminants of body size and shape [78ndash80] Overall inarid regions where vegetation and arthropod fauna aredetermined primarily by precipitation [11] wetter localitiesprovide better food resources to lizards at the populationlevel The present findings suggest that among desert speciesthe possible spatial differences in prey availability and thusin nutrition levels may lead to morphometric differentiationbetween specimens inhabiting dry or wet sites Howeverdetailed studies on possible dietary variation linked tolocal environments are necessary to answer the question ofwhether the habitat conditions which are dependent on pre-cipitation have an effect on body dimensions in these lizards
A nonphylogenetic approach suggests that lizard speciestend to exhibit strong morphological specialization in rela-tion to their habitat [53 81] Variation in body charactersrelated to locomotion which in turn is associated withsubstrate pattern has been observed across many lizard taxa[54 82ndash84] Unfortunately based on available datasets Icould not evaluate whether the shift in substrate usage isassociated with limb proportion changes and so a rationalexplanation for the effect of vegetation on limb lengthsthrough its dependence upon hydrothermal regime remainsto be determined My findings show that generally theexamined species indicate a uniform pattern in extremitiessize variation fore and especially hind limb lengths werepositively correlated with temperature and negatively withprecipitation The results indicate that ecological adaptationto abiotic factors is a powerful source of extremity sizevariation which is under the effect of natural selection Inlizards the morphology-performance relationships suggestthat ground-dwelling species from open landscapes shouldpossess relatively long limb segments to their body length[53] This body shape pattern increases stride length provid-ing better sprinting abilities [85 86] Furthermore shorterextremities may facilitate the locomotion in highly vegetatedareas where long limbs may be disadvantageous [53] In thiscontextmyfindings suggest that various body shape patternssuch as relatively shortlong limbs or their segments whichare suited to the environmental requirements may reflect anadaptation to either dense or sparse vegetation resulting fromdifferent rainfall intensities across the distribution range
Finally given the potential importance of habitats forlimb size variation lizardsmay also use their protruding bodyparts as additional (together with body surface area) heatexchangers In these reptiles for optimal balance betweenheat gain and heat loss isometric size changes to a certainextent are a ldquotwo-edged swordrdquo inwhich high thermal inertia
of large bodies is accompanied by slow heating rates and viceversa In this respect among desert dwellers relatively longextremities and small size enhance heat exchange and seemto be a morphological adaptation for effective thermoreg-ulation In desert areas large daily fluctuations of temper-ature force the ectotherms to quickly respond to changingconditions and rapidly reach the necessary metabolic ratesfor locomotor activity Long-limbed individuals which havean increased surface area-to-volume ratio may enhancetheir heating and cooling abilities through more effectiveinteractions between the body and either solar radiationor surface temperature gradient Hence a consistent linkbetween environmental variables and limb lengths can alsobe explained by their importance for maintenance of optimalbody temperature in local environments As shown above thefact that the extremity size-environment link is more obviousin respect to hind limbs than to fore ones reinforces thishypothesis relatively large hind limbs having an increasedheat exchange capacity are much more powerful tool foreffective thermoregulation than small fore extremities
In summary the lacertid lizards I studied generallyfollowed the ecogeographic rules of Bergmann and AllenIn addition the findings indicate both intersexual and inter-specific differences in the habitat-morphology relationshipwhich can be considered within the framework of theirfunctional connectionMydata provide evidence that femalestend to show stronger relationships between climate vari-ables and body dimensions than males In desert speciestemperature has a smaller effect than rainfall on lizardphenotypes Under a constant dry climate water availabilityseems to be the most important abiotic factor in reptileecology In this respect due to the strong association betweenprecipitation and productivity my findings could also beinterpreted as evidence for the hypothesis that different bodysize patterns are linked to the spatial variation in primaryproduction that is the ldquoresource rulerdquo In the Mediterraneanregion lizards the thermal regime is apparently the maindriving force of morphological variability The present studysuggests a complex link between environmental variablesand morphological characters within lacertid species Thephysical conditions such as temperature and precipitationgradient were shown to be able to significantly affect bothbody and limb dimensions and thus as a powerful sourceof variation they play an important role in lizard mor-phology However general statements about the habitat-morphology relationships and their potential importance formaintenance of optimal body temperature in reptiles arehard to make due to the enormous diversity of variationsin body composition and physiology across species sexesand even individuals and the difficulty in evaluating enoughmechanisms in enough species Consequently additionalfield and experimental studies testing both body size andshape variations and their relationships with environmentalvariables especially at the intraspecific level and accountingfor sex-specific aspects are needed to help determine whetherthe observed patterns are common across species and to whatextent they are important for effective thermoregulation
12 International Journal of Zoology
Conflict of Interests
The author declares that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The author would like to thank Shai Meiri for his helpfulcomments on earlier drafts of the paper The author thanksErezMaza for assistancewith data preparationAnat Feldmanfor provision of the GIS-compatible temperature data andNaomi Paz for linguistic editing The author also thanks theIsrael Ministry of Science Culture and Sport for supportingthe National Collections of Natural History at Tel AvivUniversity as a biodiversity environment and agricultureresearch knowledge centre
References
[1] E Mayr Animal Species and Evolution Harvard UniversityPress Cambridge Mass USA 1963
[2] C Ray ldquoThe application of Bergmannrsquos and Allenrsquos rules to thepoikilothermsrdquo Journal of Morphology vol 106 pp 85ndash1081960
[3] TM Blackburn K J Gaston andN Loder ldquoGeographic gradi-ents in body size a clarification of Bergmannrsquos rulerdquo Diversityand Distributions vol 5 no 4 pp 165ndash174 1999
[4] K J Gaston and TM Blackburn Pattern and Process inMacro-ecology Blackwell Malden Mass USA 2000
[5] C Bergmann ldquoUber die verhaltnisse der warmeokonomie derthiere zu ihrer grosserdquo Gottinger Studien vol 3 pp 595ndash7081847
[6] J A Allen ldquoThe influence of physical conditions in the genesisof speciesrdquo Radical Review vol 1 pp 108ndash140 1877
[7] F C James ldquoGeographic size variation in birds and its relation-ship with climaterdquo Ecology vol 51 pp 365ndash390 1970
[8] C D Burnett ldquoGeographic and climatic correlates of morpho-logical variation inEptesicus fuscusrdquo Journal ofMammalogy vol64 no 3 pp 437ndash444 1983
[9] C C Lindsey ldquoBody sizes of poikilotherm vertebrates at differ-ent latitudesrdquo Evolution vol 20 pp 456ndash465 1966
[10] M L Rosenzweig ldquoThe strategy of body size in mammaliancarnivoresrdquo American Midland Naturalist vol 80 pp 299ndash3151968
[11] Y Yom-Tov and E Geffen ldquoGeographic variation in body sizethe effects of ambient temperature and precipitationrdquoOecologiavol 148 no 2 pp 213ndash218 2006
[12] Y Yom-Tov and H Nix ldquoClimatological correlates for body sizeof five species of Australian mammalsrdquo Biological Journal of theLinnean Society vol 29 no 4 pp 245ndash262 1986
[13] D Pincheira-Donoso and SMeiri ldquoAn intercontinental analysisof climate-driven body size clines in reptiles no support forpatterns no signals of processesrdquo Evolutionary Biology vol 40no 4 pp 562ndash578 2013
[14] K G Ashton M C Tracy and A de Queiroz ldquoIs Bergmannrsquosrule valid for mammalsrdquoThe American Naturalist vol 156 no4 pp 390ndash415 2000
[15] S Meiri and T Dayan ldquoOn the validity of Bergmannrsquos rulerdquoJournal of Biogeography vol 30 no 3 pp 331ndash351 2003
[16] K G Ashton ldquoSensitivity of intraspecific latitudinal clines ofbody size for tetrapods to sampling latitude and body sizerdquoIntegrative and Comparative Biology vol 44 no 6 pp 403ndash4122004
[17] K G Ashton and C R Feldman ldquoBergmannrsquos rule in nonavianreptiles turtles follow it lizards and snakes reverse itrdquoEvolutionvol 57 no 5 pp 1151ndash1163 2003
[18] M A Olalla-Tarraga M A Rodrıguez and B A HawkinsldquoBroad-scale patterns of body size in squamate reptiles ofEurope and North Americardquo Journal of Biogeography vol 33no 5 pp 781ndash793 2006
[19] S Volynchik ldquoMorphological variability in Vipera palaesti-nae along an environmental gradientrdquo Asian HerpetologicalResearch vol 3 pp 227ndash239 2012
[20] D Pincheira-Donoso D J Hodgson and T Tregenza ldquoTheevolution of body size under environmental gradients inectothermswhy shouldBergmannrsquos rule apply to lizardsrdquoBMCEvolutionary Biology vol 8 no 1 article 68 2008
[21] R C Stillwell ldquoAre latitudinal clines in body size adaptiverdquoOikos vol 119 no 9 pp 1387ndash1390 2010
[22] S Meiri ldquoBergmannrsquos rulemdashwhatrsquos in a namerdquo Global Ecologyand Biogeography vol 20 no 1 pp 203ndash207 2011
[23] D Pincheira-Donoso ldquoPredictable variation of range-sizesacross an extreme environmental gradient in a lizard adaptiveradiation evolutionary and ecological inferencesrdquo PLoS ONEvol 6 no 12 Article ID e28942 2011
[24] K G Ashton ldquoDo amphibians follow Bergmannrsquos rulerdquo Cana-dian Journal of Zoology vol 80 no 4 pp 708ndash716 2002
[25] M J Angilletta Jr T D Steury andMW Sears ldquoTemperaturegrowth rate and body size in ectotherms fitting pieces of a life-history puzzlerdquo Integrative and Comparative Biology vol 44 no6 pp 498ndash509 2004
[26] C E Oufiero G E A Gartner S C Adolph and T GarlandldquoLatitudinal and climatic variation in body size and dorsalscale counts in Sceloporus lizards a phylogenetic perspectiverdquoEvolution vol 65 no 12 pp 3590ndash3607 2011
[27] S Meiri ldquoEvolution and ecology of lizard body sizesrdquo GlobalEcology and Biogeography vol 17 no 6 pp 724ndash734 2008
[28] D Atkinson and RM Sibly ldquoWhy are organisms usually biggerin colder environments Making sense of a life history puzzlerdquoTrends in Ecology amp Evolution vol 12 pp 235ndash239 1997
[29] F B Cruz L A Fitzgerald R E Espinoza and J A Schulte IIldquoThe importance of phylogenetic scale in tests of Bergmannrsquosand Rapoportrsquos rules lessons from a clade of South Americanlizardsrdquo Journal of Evolutionary Biology vol 18 no 6 pp 1559ndash1574 2005
[30] T AMousseau ldquoEctotherms follow the converse to BergmannrsquosRulerdquo Evolution vol 51 pp 630ndash632 1997
[31] R N Reed ldquoInterspecific patterns of species richness geo-graphic range size and body size among NewWorld venomoussnakesrdquo Ecography vol 26 no 1 pp 107ndash117 2003
[32] D Pincheira-Donoso T Tregenza and D J Hodgson ldquoBodysize evolution in South American Liolaemus lizards of theboulengeri clade a contrasting reassessmentrdquo Journal of Evolu-tionary Biology vol 20 no 5 pp 2067ndash2071 2007
[33] M J Angilletta P H Niewiarowski A E Dunham A Leacheand W P Porter ldquoBergmannrsquos clines in ectotherms illustratinga life-historical perspective with sceloporine lizardsrdquoTheAmer-ican Naturalist vol 164 pp E168ndashE183 2004
[34] M Andersson Sexual Selection Princeton University PressPrinceton NJ USA 1994
International Journal of Zoology 13
[35] F Brana ldquoSexual dimorphism in lacertid lizards male headincrease vs female abdomen increaserdquo Oikos vol 75 pp 511ndash523 1996
[36] E R Pianka ldquoLizard species density in the Kalahari desertrdquoEcology vol 52 pp 1024ndash1029 1971
[37] E R Pianka ldquoSome intercontinental comparisons of desertlizardsrdquoNational Geographic Research vol 1 no 4 pp 490ndash5041985
[38] B H Brattstrom ldquoSocial and thermoregulatory behavior of thebearded dragon Amphibolurus barbatusrdquo Copeia vol 3 pp484ndash497 1971
[39] G C Grigg and F Seebacher ldquoField test of a paradigm hyster-esis of heart rate in thermoregulation by a free-ranging lizard(Pogona barbata)rdquo Proceedings of the Royal Society B BiologicalSciences vol 266 no 1425 pp 1291ndash1297 1999
[40] F Seebacher and C E Franklin ldquoControl of heart rate duringthermoregulation in the heliothermic lizard Pogona barbataimportance of cholinergic and adrenergic mechanismsrdquo TheJournal of Experimental Biology vol 204 no 24 pp 4361ndash43662001
[41] G J Tattersall and R M Gerlach ldquoHypoxia progressivelylowers thermal gaping thresholds in bearded dragons Pogonavitticepsrdquo The Journal of Experimental Biology vol 208 no 17pp 3321ndash3330 2005
[42] D F DeNardo T E Zubal and T C M Hoffman ldquoCloacalevaporative cooling a previously undescribedmeans of increas-ing evaporative water loss at higher temperatures in a desertectotherm theGilamonsterHeloderma suspectumrdquoThe Journalof Experimental Biology vol 207 no 6 pp 945ndash953 2004
[43] S Jaffe ldquoClimate of Israelrdquo inTheZoogeography of Israel Y Yom-Tov and E Tchernov Eds pp 79ndash92 Dr W Junk PublishersDordrecht The Netherlands 1988
[44] U Roll L Stone and S Meiri ldquoHot-spot facts and artifacts-questioning Israelrsquos great biodiversityrdquo Israel Journal of Ecologyand Evolution vol 55 no 3 pp 263ndash279 2009
[45] W Bischoff and J F Schmidtler ldquoNew data on the distributionmorphology and habitat choice of the Lacerta laevis-kulzericomplexrdquo Natura Croatica vol 8 no 3 pp 211ndash222 1999
[46] A Disi D Modry P Necas and L Rifai Amphibians andReptiles of the Hashemite Kingdom of Jordan An Atlas and FieldGuide Edit Chimaira Frankfurt Germany 2001
[47] A Bouskila and P Amitai Handbook of Amphibians andReptiles of Israel Keter Publishing House Jerusalem Israel2001 (Hebrew)
[48] A Bar and G Haimovitch A Field Guide to Reptiles andAmphibians of Israel Pazbar LTD Herzliya Israel 2012
[49] Y L Werner ldquoGeographic sympatry of Acanthodactylus opheo-durus with A boskianus in the Levantrdquo Zoology in the MiddleEast vol 1 pp 92ndash95 1986
[50] R J Hijmans S E Cameron J L Parra P G Jones and AJarvis ldquoVery high resolution interpolated climate surfaces forglobal land areasrdquo International Journal of Climatology vol 25no 15 pp 1965ndash1978 2005
[51] R B Huey ldquoTemperature physiology and the ecology ofreptilesrdquo inBiology of the Reptilia CGans and FH Pough Edsvol 12 of Physiology (C) pp 25ndash91 Academic Press New YorkNY USA 1982
[52] D J Irschick and J B Losos ldquoDo lizards avoid habitats inwhich performance is submaximal The relationship betweensprinting capabilities and structural habitat use in Caribbeananolesrdquo The American Naturalist vol 154 no 3 pp 293ndash3051999
[53] B Vanhooydonck and R Van Damme ldquoEvolutionary relation-ships between body shape and habitat use in lacertid lizardsrdquoEvolutionary Ecology Research vol 1 no 7 pp 785ndash805 1999
[54] J Melville and R Swain ldquoEvolutionary relationships betweenmorphology performance and habitat openness in the lizardgenus Niveoscincus (Scincidae Lygosominae)rdquo Biological Jour-nal of the Linnean Society vol 70 no 4 pp 667ndash683 2000
[55] R B Huey and M Slatkin ldquoCost and benefits of lizard thermo-regulationrdquo The Quarterly Review of Biology vol 51 no 3 pp363ndash384 1976
[56] R D Stevenson ldquoBody size and limits to the daily range of bodytemperature in terrestrial ectothermsrdquoTheAmericanNaturalistvol 125 pp 102ndash117 1985
[57] B W Grant ldquoTrade-offs in activity time and physiologicalperformance for thermoregulating desert lizards Sceloporusmerriamirdquo Ecology vol 71 no 6 pp 2323ndash2333 1990
[58] R Shine and T Madsen ldquoIs thermoregulation unimportant tomost reptiles An example using water pythons (Liasis fuscus)in tropical AustraliardquoPhysiological Zoology vol 69 pp 252ndash2691996
[59] R Shine ldquoReptilian viviparity in cold climates testing theassumptions of an evolutionary hypothesisrdquo Oecologia vol 57no 3 pp 397ndash405 1983
[60] C R Peterson A R Gibson andM E Dorcas ldquoSnake thermalecology the causes and consequences of body temperaturevariationrdquo in Snakes Ecology and Behavior R A Seigel and J TCollins Eds pp 241ndash314 McGraw-Hill New York NY USA1993
[61] R B Huey and J G Kingsolver ldquoEvolution of thermal sensitiv-ity of ectotherm performancerdquo Trends in Ecology and Evolutionvol 4 no 5 pp 131ndash135 1989
[62] J A Dıaz D Bauwens and B Asensio ldquoA comparative studyof the relation between heating rates and ambient temperaturesin lacertid lizardsrdquo Physiological Zoology vol 69 pp 1359ndash13831996
[63] D C Deeming ldquoPost-hatching phenotypic effects of incubationin reptilesrdquo in Reptilian Incubation Environment Evolutionand Behaviour D C Deeming Ed pp 229ndash251 NottinghamUniversity Press Nottingham UK 2004
[64] R Shine M J Elphick and P S Harlow ldquoThe influence ofnatural incubation environments on the phenotypic traits ofhatchling lizardrdquo Ecology vol 78 pp 2559ndash2568 1997
[65] T Flatt R Shine P A Borges-Landaez and S J DownesldquoPhenotypic variation in an oviparousmontane lizard (Bassianaduperreyi) the effects of thermal and hydric incubation envi-ronmentsrdquo Biological Journal of the Linnean Society vol 74 no3 pp 339ndash350 2001
[66] R Shine and M J Elphick ldquoThe effect of short-term weatherfluctuations on temperatures inside lizard nests and on thephenotypic traits of hatchling lizardsrdquo Biological Journal of theLinnean Society vol 72 no 4 pp 555ndash565 2001
[67] O Lourdais R Shine X Bonnet M Guillon and G NaulleauldquoClimate affects embryonic development in a viviparous snakeVipera aspisrdquo Oikos vol 104 no 3 pp 551ndash560 2004
[68] V Delmas X Bonnet M Girondot and A-C Prevot-JulliardldquoVarying hydric conditions during incubation influence eggwater exchange and hatchling phenotype in the red-eared sliderturtlerdquo Physiological and Biochemical Zoology vol 81 no 3 pp345ndash355 2008
[69] X-F Yan X-L Tang F Yue et al ldquoInfluence of ambient temper-ature onmaternal thermoregulation and neonate phenotypes in
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
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BioinformaticsAdvances in
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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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Signal TransductionJournal of
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BioMed Research International
Evolutionary BiologyInternational Journal of
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Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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Stem CellsInternational
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Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
8 International Journal of Zoology
Table 5 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Ophisops elegans with SVL as a covariate
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
1717
1616
012048
026071
081121
140147
06720278
01860155
Covariate(SVL)
FLLHLL
11
11
25225696
5291525
16331432
28643183
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
101138
251265
651347
1359552
00130067
00010023
Error FLLHLL
6565
4242
015039
018047
Precipitation FLLHLL
2323
1717
013056
024064
083156
129130
06730086
02430241
Covariate(SVL)
FLLHLL
11
11
21864902
5341481
14061366
28222971
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
123201
263305
796559
1393612
00060021
00010018
Error FLLHLL
5959
4141
015035
018049
14 16 18 20 22 24
SVL
(mm
)
Average annual temperature (∘C)
85
80
75
70
65
60
55
50
(a)
SVL
(mm
)
85
80
75
70
65
60
55
50
0 50 150 200100 250 300
Average annual precipitation (mm)
(b)
Figure 4 The relationship between SVL and (a) average annual temperature and (b) average annual precipitation in Acanthodactylusboskianus solid line with circles males dashed line with triangles females
119875 = 0019 120573 = 021plusmn009 versus119875 = 0680 120573 = minus003plusmn009for males 119875 = 0001 120573 = 033 plusmn 009 versus 119875 = 0134120573 = minus014 plusmn 009 for females respectively
4 Discussion
Despite the inability of ectotherms to produce significantmetabolic heat the interaction between body size and heatbalance based on a set of behavioural anatomical andphysiological mechanisms [51] that contribute to fitnessmight explain the peculiarity of ecological drivers in sizeclines among these animalsThe relationship between habitatconditions and morphological variables (body tail or limbdimensions) and consequent shifts in phenology due toclimate change have been observed across a wide range ofreptile taxa [52ndash54] It is possible that in diurnal squamates
environmental conditions may favour selection for smaller-sized individuals [55] which due to the ability to achievemore accurate adjustment of their body temperature havebetter thermoregulatory capacities [56] and thus display highactivity levels In terrestrial ectotherms thermoregulation isrealized behaviourally by habitat selection and daily activitypattern [57] while at the same time morphological special-ization may also essentially facilitate it [55] For exampleShine and Madsen [58] pointed out that for relatively smallreptile species behavioural thermoregulation seems to bemore important especially in conditions of high diurnalthermal heterogeneity In this context desert reptiles inhab-iting warmer regions with lower thermoregulatory costs mayadjust their body temperature mainly behaviourally andthus invest less in adjustment of either body size or shapein relation to ambient temperature Despite the great data
International Journal of Zoology 9
Table 6 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Acanthodactylus boskianus with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
3535
2828
089151
053131
141191
125175
01180012
02390040
Covariate(SVL)
FLLHLL
11
11
60441731
34366125
95262186
80188176
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
203445
4952911
320562
11563885
00780021
0001lt0001
Error FLLHLL
6565
5151
063079
042074
Precipitation FLLHLL
3333
3131
086151
046116
178186
101171
00230016
04810049
Covariate(SVL)
FLLHLL
11
11
64151792
23944222
13182201
51436151
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
161422
7043482
332518
15145073
00730026
lt0001lt0001
Error FLLHLL
6767
4848
048081
046068
14 16 18 20 22 24
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
Average annual temperature (∘C)
(a)
0 50 150 200100 250 300 350 400 450 500 550
Average annual precipitation (mm)
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
(b)
Figure 5The relationship between SVL and (a) average annual temperature and (b) average annual precipitation inMesalina guttulata solidline with circles males dashed line with triangles females
dispersion (as shown in the scatter plots) it was foundthat among the two ldquodesertrdquo species studied (M guttulataand A boskianus) only females of the latter were smallerin hot temperatures whereas in both sexes of the formeras well as in A boskianus males SVL did not correlatewith temperature In the Mediterranean region P laevisand O elegans inhabit cooler climates than the desert Aboskianus and M guttulata In these environments largergravid reptiles in addition to the buffering effects of thebehavioural thermoregulation supplied by the mother [5960] can provide greater temperature stability during thepreoviposition period Volynchik [19] however found that alarge-bodied local viper (Vipera palaestinae) with a Mediter-ranean distribution pattern does not follow Bergmannrsquos ruleor its converse At the same time the most ldquocold-lovingrdquolizard (O elegans) in my own sample obeyed Bergmannrsquos
rule growing larger in cooler environments On the otherhand in desert habitats this pattern of greater thermal inertiaseems to be less important and the behavioural componentof thermoregulation becomes paramount
The impact of ambient temperature on external mor-phology is also significant in respect to relative extremitylengths different degrees of intraspecific variability in limbproportions supporting Allenrsquos rule were observed in all thespecies studied The present findings indicate that temper-ature decrease across the observed habitats could lead toreduction in size of extremity segments relative to bodylength thus constituting a compensatory adaptation to eithercooler or hotter areas I noted an allometric shift in humerusforearm femur and tibia lengths relative to SVL along atemperature gradient among P laevis A similar relationshipbetween average annual temperature and corporeal ratioswas
10 International Journal of Zoology
Table 7 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) inMesalina guttulata with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
2525
2424
021045
024054
156143
181191
00650110
00290019
Covariate(SVL)
FLLHLL
11
11
20084405
9872011
14751407
72797114
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
4501082
8922073
33113455
65837331
lt0001lt0001
lt0001lt0001
Error FLLHLL
9191
6969
013031
013028
Precipitation FLLHLL
2828
2525
019041
022056
142129
162211
01070181
00590008
Covariate(SVL)
FLLHLL
11
11
19504181
9631908
14091307
68667094
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
356901
8021918
25752817
57177133
lt0001lt0001
lt0001lt0001
Error FLLHLL
8888
6868
013032
014026
noted in females of M guttulata Among A boskianus totalhind limb length significantly correlated with both thermalregime and rainfall gradient Hence both Mediterraneanand desert reptiles follow a similar pattern in their bodyshape variation and may benefit from various morphologicalmodifications matched to habitat range
Body temperature changes affect reptile ecology [61]becoming more important to ectotherms living in coolerenvironments which complicate attaining proper body tem-perature [58 62] In support of this my results show the asso-ciation between biogeographic origins of the species exam-ined and their relationship with environmental variables Oninterspecific comparison the most pronounced distinctionswere noted in phenotypic responses to the temperature gra-dient between Mediterranean and desert inhabitants whilethe between-species differences for precipitation-related vari-ation were weaker As expected both Mediterranean regionspecies (P laevis O elegans) display significantly strongerresponses to temperature than desert dwellers (A boskianusM guttulata) Apparently the cooler locations of the formerforce them to exhibit more consistent morphological vari-ability in respect to temperature changes whereas for desertspecies such habitat-morphology connection seems to be lessimportant It is highly likely that the speciesrsquo sensitivity tothe environment is associated not only with their ecologicaldifferentiation but also with body size ranges within thesample Thus this might be one possible explanation for thedifferent albeit relatively minor responses to temperaturebetween ecologically similar species (ie P laevis versus Oelegans andA boskianus versusM guttulata) that were notedhere In the examined samples L laevis owing to its greatermeasurement ranges than O elegans has a higher potentialfor more consistent matching of its body dimensions to theobserved temperature gradient The same is true for the twodesert lizardsA boskianus due to its extended body and limb
ranges in comparison with M guttulata displays a strongermorphological-environmental link
The examination of gender-specific habitat-morphologyinteractions revealed that within three of the four species (Plaevis A boskianus and M guttulata) sensitivity to the envi-ronment is coupledwith sex Considering the effect of climatevariables on SVL the findings demonstrate that females ingeneral show a more consistent link between temperatureand bodylimb measurements than males while the effectof precipitation on external characters was similar for bothsexes Moreover in P laevis SVL was significantly morestrongly correlated with the temperature gradient in femalesthan in malesThese observations indicate the sex-associatedeffect of natural selection pointing to different thermal andmetabolic demands inmales and femalesThus it is likely thatin females the increased body size in colder environmentsis associated with reproduction-induced requirements Thispattern suggests that females due to increased thermalrequirements particularly during vitellogenesis [63] aremore able to generate a range of suitable morphologicalmodifications for maintenance of optimal body temperaturein local environments Overall my findings indicate thatalthough females show amore consistent correlation betweenSVL and a temperature gradient than males the body shapechanges involving both body and limb dimensions arerather preliminary in explaining the observed intersexualdivergence in the habitat-morphology relationship
Environmental conditions within the nest experiencedduring early ontogenesis especially temperature and mois-ture of substrate can significantly affect development andgrowth trajectories of individuals in oviparous reptiles [64ndash68] As observed in many species either posthatching phe-notype or offspring fitness are closely associated with thermalregime [63 69ndash71] In both the laboratory and in naturalnests [64] temperature is traditionally considered to be animportant environmental determinant of reptile size while
International Journal of Zoology 11
the effect of water-related factors is more complex Severalrecent studies have tested the effect of substrate moistureduring incubation of eggs on a diverse range of reptile speciesSignificant effects are found in certain species [66 68 72 73]but not in others [74ndash76] that may reflect either differentwater permeability of the eggshell or interspecific variationin the water content of eggs [77] On the other hand theappearance of morphological variation along a precipitationgradient which in desert lizards is even more evident thanthe temperature-related variability can be considered as aresponse to the local habitats In reptiles food availabilitystrongly affects growth trajectories and is one of the possibledeterminants of body size and shape [78ndash80] Overall inarid regions where vegetation and arthropod fauna aredetermined primarily by precipitation [11] wetter localitiesprovide better food resources to lizards at the populationlevel The present findings suggest that among desert speciesthe possible spatial differences in prey availability and thusin nutrition levels may lead to morphometric differentiationbetween specimens inhabiting dry or wet sites Howeverdetailed studies on possible dietary variation linked tolocal environments are necessary to answer the question ofwhether the habitat conditions which are dependent on pre-cipitation have an effect on body dimensions in these lizards
A nonphylogenetic approach suggests that lizard speciestend to exhibit strong morphological specialization in rela-tion to their habitat [53 81] Variation in body charactersrelated to locomotion which in turn is associated withsubstrate pattern has been observed across many lizard taxa[54 82ndash84] Unfortunately based on available datasets Icould not evaluate whether the shift in substrate usage isassociated with limb proportion changes and so a rationalexplanation for the effect of vegetation on limb lengthsthrough its dependence upon hydrothermal regime remainsto be determined My findings show that generally theexamined species indicate a uniform pattern in extremitiessize variation fore and especially hind limb lengths werepositively correlated with temperature and negatively withprecipitation The results indicate that ecological adaptationto abiotic factors is a powerful source of extremity sizevariation which is under the effect of natural selection Inlizards the morphology-performance relationships suggestthat ground-dwelling species from open landscapes shouldpossess relatively long limb segments to their body length[53] This body shape pattern increases stride length provid-ing better sprinting abilities [85 86] Furthermore shorterextremities may facilitate the locomotion in highly vegetatedareas where long limbs may be disadvantageous [53] In thiscontextmyfindings suggest that various body shape patternssuch as relatively shortlong limbs or their segments whichare suited to the environmental requirements may reflect anadaptation to either dense or sparse vegetation resulting fromdifferent rainfall intensities across the distribution range
Finally given the potential importance of habitats forlimb size variation lizardsmay also use their protruding bodyparts as additional (together with body surface area) heatexchangers In these reptiles for optimal balance betweenheat gain and heat loss isometric size changes to a certainextent are a ldquotwo-edged swordrdquo inwhich high thermal inertia
of large bodies is accompanied by slow heating rates and viceversa In this respect among desert dwellers relatively longextremities and small size enhance heat exchange and seemto be a morphological adaptation for effective thermoreg-ulation In desert areas large daily fluctuations of temper-ature force the ectotherms to quickly respond to changingconditions and rapidly reach the necessary metabolic ratesfor locomotor activity Long-limbed individuals which havean increased surface area-to-volume ratio may enhancetheir heating and cooling abilities through more effectiveinteractions between the body and either solar radiationor surface temperature gradient Hence a consistent linkbetween environmental variables and limb lengths can alsobe explained by their importance for maintenance of optimalbody temperature in local environments As shown above thefact that the extremity size-environment link is more obviousin respect to hind limbs than to fore ones reinforces thishypothesis relatively large hind limbs having an increasedheat exchange capacity are much more powerful tool foreffective thermoregulation than small fore extremities
In summary the lacertid lizards I studied generallyfollowed the ecogeographic rules of Bergmann and AllenIn addition the findings indicate both intersexual and inter-specific differences in the habitat-morphology relationshipwhich can be considered within the framework of theirfunctional connectionMydata provide evidence that femalestend to show stronger relationships between climate vari-ables and body dimensions than males In desert speciestemperature has a smaller effect than rainfall on lizardphenotypes Under a constant dry climate water availabilityseems to be the most important abiotic factor in reptileecology In this respect due to the strong association betweenprecipitation and productivity my findings could also beinterpreted as evidence for the hypothesis that different bodysize patterns are linked to the spatial variation in primaryproduction that is the ldquoresource rulerdquo In the Mediterraneanregion lizards the thermal regime is apparently the maindriving force of morphological variability The present studysuggests a complex link between environmental variablesand morphological characters within lacertid species Thephysical conditions such as temperature and precipitationgradient were shown to be able to significantly affect bothbody and limb dimensions and thus as a powerful sourceof variation they play an important role in lizard mor-phology However general statements about the habitat-morphology relationships and their potential importance formaintenance of optimal body temperature in reptiles arehard to make due to the enormous diversity of variationsin body composition and physiology across species sexesand even individuals and the difficulty in evaluating enoughmechanisms in enough species Consequently additionalfield and experimental studies testing both body size andshape variations and their relationships with environmentalvariables especially at the intraspecific level and accountingfor sex-specific aspects are needed to help determine whetherthe observed patterns are common across species and to whatextent they are important for effective thermoregulation
12 International Journal of Zoology
Conflict of Interests
The author declares that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The author would like to thank Shai Meiri for his helpfulcomments on earlier drafts of the paper The author thanksErezMaza for assistancewith data preparationAnat Feldmanfor provision of the GIS-compatible temperature data andNaomi Paz for linguistic editing The author also thanks theIsrael Ministry of Science Culture and Sport for supportingthe National Collections of Natural History at Tel AvivUniversity as a biodiversity environment and agricultureresearch knowledge centre
References
[1] E Mayr Animal Species and Evolution Harvard UniversityPress Cambridge Mass USA 1963
[2] C Ray ldquoThe application of Bergmannrsquos and Allenrsquos rules to thepoikilothermsrdquo Journal of Morphology vol 106 pp 85ndash1081960
[3] TM Blackburn K J Gaston andN Loder ldquoGeographic gradi-ents in body size a clarification of Bergmannrsquos rulerdquo Diversityand Distributions vol 5 no 4 pp 165ndash174 1999
[4] K J Gaston and TM Blackburn Pattern and Process inMacro-ecology Blackwell Malden Mass USA 2000
[5] C Bergmann ldquoUber die verhaltnisse der warmeokonomie derthiere zu ihrer grosserdquo Gottinger Studien vol 3 pp 595ndash7081847
[6] J A Allen ldquoThe influence of physical conditions in the genesisof speciesrdquo Radical Review vol 1 pp 108ndash140 1877
[7] F C James ldquoGeographic size variation in birds and its relation-ship with climaterdquo Ecology vol 51 pp 365ndash390 1970
[8] C D Burnett ldquoGeographic and climatic correlates of morpho-logical variation inEptesicus fuscusrdquo Journal ofMammalogy vol64 no 3 pp 437ndash444 1983
[9] C C Lindsey ldquoBody sizes of poikilotherm vertebrates at differ-ent latitudesrdquo Evolution vol 20 pp 456ndash465 1966
[10] M L Rosenzweig ldquoThe strategy of body size in mammaliancarnivoresrdquo American Midland Naturalist vol 80 pp 299ndash3151968
[11] Y Yom-Tov and E Geffen ldquoGeographic variation in body sizethe effects of ambient temperature and precipitationrdquoOecologiavol 148 no 2 pp 213ndash218 2006
[12] Y Yom-Tov and H Nix ldquoClimatological correlates for body sizeof five species of Australian mammalsrdquo Biological Journal of theLinnean Society vol 29 no 4 pp 245ndash262 1986
[13] D Pincheira-Donoso and SMeiri ldquoAn intercontinental analysisof climate-driven body size clines in reptiles no support forpatterns no signals of processesrdquo Evolutionary Biology vol 40no 4 pp 562ndash578 2013
[14] K G Ashton M C Tracy and A de Queiroz ldquoIs Bergmannrsquosrule valid for mammalsrdquoThe American Naturalist vol 156 no4 pp 390ndash415 2000
[15] S Meiri and T Dayan ldquoOn the validity of Bergmannrsquos rulerdquoJournal of Biogeography vol 30 no 3 pp 331ndash351 2003
[16] K G Ashton ldquoSensitivity of intraspecific latitudinal clines ofbody size for tetrapods to sampling latitude and body sizerdquoIntegrative and Comparative Biology vol 44 no 6 pp 403ndash4122004
[17] K G Ashton and C R Feldman ldquoBergmannrsquos rule in nonavianreptiles turtles follow it lizards and snakes reverse itrdquoEvolutionvol 57 no 5 pp 1151ndash1163 2003
[18] M A Olalla-Tarraga M A Rodrıguez and B A HawkinsldquoBroad-scale patterns of body size in squamate reptiles ofEurope and North Americardquo Journal of Biogeography vol 33no 5 pp 781ndash793 2006
[19] S Volynchik ldquoMorphological variability in Vipera palaesti-nae along an environmental gradientrdquo Asian HerpetologicalResearch vol 3 pp 227ndash239 2012
[20] D Pincheira-Donoso D J Hodgson and T Tregenza ldquoTheevolution of body size under environmental gradients inectothermswhy shouldBergmannrsquos rule apply to lizardsrdquoBMCEvolutionary Biology vol 8 no 1 article 68 2008
[21] R C Stillwell ldquoAre latitudinal clines in body size adaptiverdquoOikos vol 119 no 9 pp 1387ndash1390 2010
[22] S Meiri ldquoBergmannrsquos rulemdashwhatrsquos in a namerdquo Global Ecologyand Biogeography vol 20 no 1 pp 203ndash207 2011
[23] D Pincheira-Donoso ldquoPredictable variation of range-sizesacross an extreme environmental gradient in a lizard adaptiveradiation evolutionary and ecological inferencesrdquo PLoS ONEvol 6 no 12 Article ID e28942 2011
[24] K G Ashton ldquoDo amphibians follow Bergmannrsquos rulerdquo Cana-dian Journal of Zoology vol 80 no 4 pp 708ndash716 2002
[25] M J Angilletta Jr T D Steury andMW Sears ldquoTemperaturegrowth rate and body size in ectotherms fitting pieces of a life-history puzzlerdquo Integrative and Comparative Biology vol 44 no6 pp 498ndash509 2004
[26] C E Oufiero G E A Gartner S C Adolph and T GarlandldquoLatitudinal and climatic variation in body size and dorsalscale counts in Sceloporus lizards a phylogenetic perspectiverdquoEvolution vol 65 no 12 pp 3590ndash3607 2011
[27] S Meiri ldquoEvolution and ecology of lizard body sizesrdquo GlobalEcology and Biogeography vol 17 no 6 pp 724ndash734 2008
[28] D Atkinson and RM Sibly ldquoWhy are organisms usually biggerin colder environments Making sense of a life history puzzlerdquoTrends in Ecology amp Evolution vol 12 pp 235ndash239 1997
[29] F B Cruz L A Fitzgerald R E Espinoza and J A Schulte IIldquoThe importance of phylogenetic scale in tests of Bergmannrsquosand Rapoportrsquos rules lessons from a clade of South Americanlizardsrdquo Journal of Evolutionary Biology vol 18 no 6 pp 1559ndash1574 2005
[30] T AMousseau ldquoEctotherms follow the converse to BergmannrsquosRulerdquo Evolution vol 51 pp 630ndash632 1997
[31] R N Reed ldquoInterspecific patterns of species richness geo-graphic range size and body size among NewWorld venomoussnakesrdquo Ecography vol 26 no 1 pp 107ndash117 2003
[32] D Pincheira-Donoso T Tregenza and D J Hodgson ldquoBodysize evolution in South American Liolaemus lizards of theboulengeri clade a contrasting reassessmentrdquo Journal of Evolu-tionary Biology vol 20 no 5 pp 2067ndash2071 2007
[33] M J Angilletta P H Niewiarowski A E Dunham A Leacheand W P Porter ldquoBergmannrsquos clines in ectotherms illustratinga life-historical perspective with sceloporine lizardsrdquoTheAmer-ican Naturalist vol 164 pp E168ndashE183 2004
[34] M Andersson Sexual Selection Princeton University PressPrinceton NJ USA 1994
International Journal of Zoology 13
[35] F Brana ldquoSexual dimorphism in lacertid lizards male headincrease vs female abdomen increaserdquo Oikos vol 75 pp 511ndash523 1996
[36] E R Pianka ldquoLizard species density in the Kalahari desertrdquoEcology vol 52 pp 1024ndash1029 1971
[37] E R Pianka ldquoSome intercontinental comparisons of desertlizardsrdquoNational Geographic Research vol 1 no 4 pp 490ndash5041985
[38] B H Brattstrom ldquoSocial and thermoregulatory behavior of thebearded dragon Amphibolurus barbatusrdquo Copeia vol 3 pp484ndash497 1971
[39] G C Grigg and F Seebacher ldquoField test of a paradigm hyster-esis of heart rate in thermoregulation by a free-ranging lizard(Pogona barbata)rdquo Proceedings of the Royal Society B BiologicalSciences vol 266 no 1425 pp 1291ndash1297 1999
[40] F Seebacher and C E Franklin ldquoControl of heart rate duringthermoregulation in the heliothermic lizard Pogona barbataimportance of cholinergic and adrenergic mechanismsrdquo TheJournal of Experimental Biology vol 204 no 24 pp 4361ndash43662001
[41] G J Tattersall and R M Gerlach ldquoHypoxia progressivelylowers thermal gaping thresholds in bearded dragons Pogonavitticepsrdquo The Journal of Experimental Biology vol 208 no 17pp 3321ndash3330 2005
[42] D F DeNardo T E Zubal and T C M Hoffman ldquoCloacalevaporative cooling a previously undescribedmeans of increas-ing evaporative water loss at higher temperatures in a desertectotherm theGilamonsterHeloderma suspectumrdquoThe Journalof Experimental Biology vol 207 no 6 pp 945ndash953 2004
[43] S Jaffe ldquoClimate of Israelrdquo inTheZoogeography of Israel Y Yom-Tov and E Tchernov Eds pp 79ndash92 Dr W Junk PublishersDordrecht The Netherlands 1988
[44] U Roll L Stone and S Meiri ldquoHot-spot facts and artifacts-questioning Israelrsquos great biodiversityrdquo Israel Journal of Ecologyand Evolution vol 55 no 3 pp 263ndash279 2009
[45] W Bischoff and J F Schmidtler ldquoNew data on the distributionmorphology and habitat choice of the Lacerta laevis-kulzericomplexrdquo Natura Croatica vol 8 no 3 pp 211ndash222 1999
[46] A Disi D Modry P Necas and L Rifai Amphibians andReptiles of the Hashemite Kingdom of Jordan An Atlas and FieldGuide Edit Chimaira Frankfurt Germany 2001
[47] A Bouskila and P Amitai Handbook of Amphibians andReptiles of Israel Keter Publishing House Jerusalem Israel2001 (Hebrew)
[48] A Bar and G Haimovitch A Field Guide to Reptiles andAmphibians of Israel Pazbar LTD Herzliya Israel 2012
[49] Y L Werner ldquoGeographic sympatry of Acanthodactylus opheo-durus with A boskianus in the Levantrdquo Zoology in the MiddleEast vol 1 pp 92ndash95 1986
[50] R J Hijmans S E Cameron J L Parra P G Jones and AJarvis ldquoVery high resolution interpolated climate surfaces forglobal land areasrdquo International Journal of Climatology vol 25no 15 pp 1965ndash1978 2005
[51] R B Huey ldquoTemperature physiology and the ecology ofreptilesrdquo inBiology of the Reptilia CGans and FH Pough Edsvol 12 of Physiology (C) pp 25ndash91 Academic Press New YorkNY USA 1982
[52] D J Irschick and J B Losos ldquoDo lizards avoid habitats inwhich performance is submaximal The relationship betweensprinting capabilities and structural habitat use in Caribbeananolesrdquo The American Naturalist vol 154 no 3 pp 293ndash3051999
[53] B Vanhooydonck and R Van Damme ldquoEvolutionary relation-ships between body shape and habitat use in lacertid lizardsrdquoEvolutionary Ecology Research vol 1 no 7 pp 785ndash805 1999
[54] J Melville and R Swain ldquoEvolutionary relationships betweenmorphology performance and habitat openness in the lizardgenus Niveoscincus (Scincidae Lygosominae)rdquo Biological Jour-nal of the Linnean Society vol 70 no 4 pp 667ndash683 2000
[55] R B Huey and M Slatkin ldquoCost and benefits of lizard thermo-regulationrdquo The Quarterly Review of Biology vol 51 no 3 pp363ndash384 1976
[56] R D Stevenson ldquoBody size and limits to the daily range of bodytemperature in terrestrial ectothermsrdquoTheAmericanNaturalistvol 125 pp 102ndash117 1985
[57] B W Grant ldquoTrade-offs in activity time and physiologicalperformance for thermoregulating desert lizards Sceloporusmerriamirdquo Ecology vol 71 no 6 pp 2323ndash2333 1990
[58] R Shine and T Madsen ldquoIs thermoregulation unimportant tomost reptiles An example using water pythons (Liasis fuscus)in tropical AustraliardquoPhysiological Zoology vol 69 pp 252ndash2691996
[59] R Shine ldquoReptilian viviparity in cold climates testing theassumptions of an evolutionary hypothesisrdquo Oecologia vol 57no 3 pp 397ndash405 1983
[60] C R Peterson A R Gibson andM E Dorcas ldquoSnake thermalecology the causes and consequences of body temperaturevariationrdquo in Snakes Ecology and Behavior R A Seigel and J TCollins Eds pp 241ndash314 McGraw-Hill New York NY USA1993
[61] R B Huey and J G Kingsolver ldquoEvolution of thermal sensitiv-ity of ectotherm performancerdquo Trends in Ecology and Evolutionvol 4 no 5 pp 131ndash135 1989
[62] J A Dıaz D Bauwens and B Asensio ldquoA comparative studyof the relation between heating rates and ambient temperaturesin lacertid lizardsrdquo Physiological Zoology vol 69 pp 1359ndash13831996
[63] D C Deeming ldquoPost-hatching phenotypic effects of incubationin reptilesrdquo in Reptilian Incubation Environment Evolutionand Behaviour D C Deeming Ed pp 229ndash251 NottinghamUniversity Press Nottingham UK 2004
[64] R Shine M J Elphick and P S Harlow ldquoThe influence ofnatural incubation environments on the phenotypic traits ofhatchling lizardrdquo Ecology vol 78 pp 2559ndash2568 1997
[65] T Flatt R Shine P A Borges-Landaez and S J DownesldquoPhenotypic variation in an oviparousmontane lizard (Bassianaduperreyi) the effects of thermal and hydric incubation envi-ronmentsrdquo Biological Journal of the Linnean Society vol 74 no3 pp 339ndash350 2001
[66] R Shine and M J Elphick ldquoThe effect of short-term weatherfluctuations on temperatures inside lizard nests and on thephenotypic traits of hatchling lizardsrdquo Biological Journal of theLinnean Society vol 72 no 4 pp 555ndash565 2001
[67] O Lourdais R Shine X Bonnet M Guillon and G NaulleauldquoClimate affects embryonic development in a viviparous snakeVipera aspisrdquo Oikos vol 104 no 3 pp 551ndash560 2004
[68] V Delmas X Bonnet M Girondot and A-C Prevot-JulliardldquoVarying hydric conditions during incubation influence eggwater exchange and hatchling phenotype in the red-eared sliderturtlerdquo Physiological and Biochemical Zoology vol 81 no 3 pp345ndash355 2008
[69] X-F Yan X-L Tang F Yue et al ldquoInfluence of ambient temper-ature onmaternal thermoregulation and neonate phenotypes in
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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International Journal of
Volume 2014
Zoology
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Molecular Biology International
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International Journal of
Microbiology
International Journal of Zoology 9
Table 6 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) in Acanthodactylus boskianus with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
3535
2828
089151
053131
141191
125175
01180012
02390040
Covariate(SVL)
FLLHLL
11
11
60441731
34366125
95262186
80188176
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
203445
4952911
320562
11563885
00780021
0001lt0001
Error FLLHLL
6565
5151
063079
042074
Precipitation FLLHLL
3333
3131
086151
046116
178186
101171
00230016
04810049
Covariate(SVL)
FLLHLL
11
11
64151792
23944222
13182201
51436151
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
161422
7043482
332518
15145073
00730026
lt0001lt0001
Error FLLHLL
6767
4848
048081
046068
14 16 18 20 22 24
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
Average annual temperature (∘C)
(a)
0 50 150 200100 250 300 350 400 450 500 550
Average annual precipitation (mm)
SVL
(mm
)
58
56
54
52
50
48
46
44
42
40
38
(b)
Figure 5The relationship between SVL and (a) average annual temperature and (b) average annual precipitation inMesalina guttulata solidline with circles males dashed line with triangles females
dispersion (as shown in the scatter plots) it was foundthat among the two ldquodesertrdquo species studied (M guttulataand A boskianus) only females of the latter were smallerin hot temperatures whereas in both sexes of the formeras well as in A boskianus males SVL did not correlatewith temperature In the Mediterranean region P laevisand O elegans inhabit cooler climates than the desert Aboskianus and M guttulata In these environments largergravid reptiles in addition to the buffering effects of thebehavioural thermoregulation supplied by the mother [5960] can provide greater temperature stability during thepreoviposition period Volynchik [19] however found that alarge-bodied local viper (Vipera palaestinae) with a Mediter-ranean distribution pattern does not follow Bergmannrsquos ruleor its converse At the same time the most ldquocold-lovingrdquolizard (O elegans) in my own sample obeyed Bergmannrsquos
rule growing larger in cooler environments On the otherhand in desert habitats this pattern of greater thermal inertiaseems to be less important and the behavioural componentof thermoregulation becomes paramount
The impact of ambient temperature on external mor-phology is also significant in respect to relative extremitylengths different degrees of intraspecific variability in limbproportions supporting Allenrsquos rule were observed in all thespecies studied The present findings indicate that temper-ature decrease across the observed habitats could lead toreduction in size of extremity segments relative to bodylength thus constituting a compensatory adaptation to eithercooler or hotter areas I noted an allometric shift in humerusforearm femur and tibia lengths relative to SVL along atemperature gradient among P laevis A similar relationshipbetween average annual temperature and corporeal ratioswas
10 International Journal of Zoology
Table 7 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) inMesalina guttulata with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
2525
2424
021045
024054
156143
181191
00650110
00290019
Covariate(SVL)
FLLHLL
11
11
20084405
9872011
14751407
72797114
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
4501082
8922073
33113455
65837331
lt0001lt0001
lt0001lt0001
Error FLLHLL
9191
6969
013031
013028
Precipitation FLLHLL
2828
2525
019041
022056
142129
162211
01070181
00590008
Covariate(SVL)
FLLHLL
11
11
19504181
9631908
14091307
68667094
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
356901
8021918
25752817
57177133
lt0001lt0001
lt0001lt0001
Error FLLHLL
8888
6868
013032
014026
noted in females of M guttulata Among A boskianus totalhind limb length significantly correlated with both thermalregime and rainfall gradient Hence both Mediterraneanand desert reptiles follow a similar pattern in their bodyshape variation and may benefit from various morphologicalmodifications matched to habitat range
Body temperature changes affect reptile ecology [61]becoming more important to ectotherms living in coolerenvironments which complicate attaining proper body tem-perature [58 62] In support of this my results show the asso-ciation between biogeographic origins of the species exam-ined and their relationship with environmental variables Oninterspecific comparison the most pronounced distinctionswere noted in phenotypic responses to the temperature gra-dient between Mediterranean and desert inhabitants whilethe between-species differences for precipitation-related vari-ation were weaker As expected both Mediterranean regionspecies (P laevis O elegans) display significantly strongerresponses to temperature than desert dwellers (A boskianusM guttulata) Apparently the cooler locations of the formerforce them to exhibit more consistent morphological vari-ability in respect to temperature changes whereas for desertspecies such habitat-morphology connection seems to be lessimportant It is highly likely that the speciesrsquo sensitivity tothe environment is associated not only with their ecologicaldifferentiation but also with body size ranges within thesample Thus this might be one possible explanation for thedifferent albeit relatively minor responses to temperaturebetween ecologically similar species (ie P laevis versus Oelegans andA boskianus versusM guttulata) that were notedhere In the examined samples L laevis owing to its greatermeasurement ranges than O elegans has a higher potentialfor more consistent matching of its body dimensions to theobserved temperature gradient The same is true for the twodesert lizardsA boskianus due to its extended body and limb
ranges in comparison with M guttulata displays a strongermorphological-environmental link
The examination of gender-specific habitat-morphologyinteractions revealed that within three of the four species (Plaevis A boskianus and M guttulata) sensitivity to the envi-ronment is coupledwith sex Considering the effect of climatevariables on SVL the findings demonstrate that females ingeneral show a more consistent link between temperatureand bodylimb measurements than males while the effectof precipitation on external characters was similar for bothsexes Moreover in P laevis SVL was significantly morestrongly correlated with the temperature gradient in femalesthan in malesThese observations indicate the sex-associatedeffect of natural selection pointing to different thermal andmetabolic demands inmales and femalesThus it is likely thatin females the increased body size in colder environmentsis associated with reproduction-induced requirements Thispattern suggests that females due to increased thermalrequirements particularly during vitellogenesis [63] aremore able to generate a range of suitable morphologicalmodifications for maintenance of optimal body temperaturein local environments Overall my findings indicate thatalthough females show amore consistent correlation betweenSVL and a temperature gradient than males the body shapechanges involving both body and limb dimensions arerather preliminary in explaining the observed intersexualdivergence in the habitat-morphology relationship
Environmental conditions within the nest experiencedduring early ontogenesis especially temperature and mois-ture of substrate can significantly affect development andgrowth trajectories of individuals in oviparous reptiles [64ndash68] As observed in many species either posthatching phe-notype or offspring fitness are closely associated with thermalregime [63 69ndash71] In both the laboratory and in naturalnests [64] temperature is traditionally considered to be animportant environmental determinant of reptile size while
International Journal of Zoology 11
the effect of water-related factors is more complex Severalrecent studies have tested the effect of substrate moistureduring incubation of eggs on a diverse range of reptile speciesSignificant effects are found in certain species [66 68 72 73]but not in others [74ndash76] that may reflect either differentwater permeability of the eggshell or interspecific variationin the water content of eggs [77] On the other hand theappearance of morphological variation along a precipitationgradient which in desert lizards is even more evident thanthe temperature-related variability can be considered as aresponse to the local habitats In reptiles food availabilitystrongly affects growth trajectories and is one of the possibledeterminants of body size and shape [78ndash80] Overall inarid regions where vegetation and arthropod fauna aredetermined primarily by precipitation [11] wetter localitiesprovide better food resources to lizards at the populationlevel The present findings suggest that among desert speciesthe possible spatial differences in prey availability and thusin nutrition levels may lead to morphometric differentiationbetween specimens inhabiting dry or wet sites Howeverdetailed studies on possible dietary variation linked tolocal environments are necessary to answer the question ofwhether the habitat conditions which are dependent on pre-cipitation have an effect on body dimensions in these lizards
A nonphylogenetic approach suggests that lizard speciestend to exhibit strong morphological specialization in rela-tion to their habitat [53 81] Variation in body charactersrelated to locomotion which in turn is associated withsubstrate pattern has been observed across many lizard taxa[54 82ndash84] Unfortunately based on available datasets Icould not evaluate whether the shift in substrate usage isassociated with limb proportion changes and so a rationalexplanation for the effect of vegetation on limb lengthsthrough its dependence upon hydrothermal regime remainsto be determined My findings show that generally theexamined species indicate a uniform pattern in extremitiessize variation fore and especially hind limb lengths werepositively correlated with temperature and negatively withprecipitation The results indicate that ecological adaptationto abiotic factors is a powerful source of extremity sizevariation which is under the effect of natural selection Inlizards the morphology-performance relationships suggestthat ground-dwelling species from open landscapes shouldpossess relatively long limb segments to their body length[53] This body shape pattern increases stride length provid-ing better sprinting abilities [85 86] Furthermore shorterextremities may facilitate the locomotion in highly vegetatedareas where long limbs may be disadvantageous [53] In thiscontextmyfindings suggest that various body shape patternssuch as relatively shortlong limbs or their segments whichare suited to the environmental requirements may reflect anadaptation to either dense or sparse vegetation resulting fromdifferent rainfall intensities across the distribution range
Finally given the potential importance of habitats forlimb size variation lizardsmay also use their protruding bodyparts as additional (together with body surface area) heatexchangers In these reptiles for optimal balance betweenheat gain and heat loss isometric size changes to a certainextent are a ldquotwo-edged swordrdquo inwhich high thermal inertia
of large bodies is accompanied by slow heating rates and viceversa In this respect among desert dwellers relatively longextremities and small size enhance heat exchange and seemto be a morphological adaptation for effective thermoreg-ulation In desert areas large daily fluctuations of temper-ature force the ectotherms to quickly respond to changingconditions and rapidly reach the necessary metabolic ratesfor locomotor activity Long-limbed individuals which havean increased surface area-to-volume ratio may enhancetheir heating and cooling abilities through more effectiveinteractions between the body and either solar radiationor surface temperature gradient Hence a consistent linkbetween environmental variables and limb lengths can alsobe explained by their importance for maintenance of optimalbody temperature in local environments As shown above thefact that the extremity size-environment link is more obviousin respect to hind limbs than to fore ones reinforces thishypothesis relatively large hind limbs having an increasedheat exchange capacity are much more powerful tool foreffective thermoregulation than small fore extremities
In summary the lacertid lizards I studied generallyfollowed the ecogeographic rules of Bergmann and AllenIn addition the findings indicate both intersexual and inter-specific differences in the habitat-morphology relationshipwhich can be considered within the framework of theirfunctional connectionMydata provide evidence that femalestend to show stronger relationships between climate vari-ables and body dimensions than males In desert speciestemperature has a smaller effect than rainfall on lizardphenotypes Under a constant dry climate water availabilityseems to be the most important abiotic factor in reptileecology In this respect due to the strong association betweenprecipitation and productivity my findings could also beinterpreted as evidence for the hypothesis that different bodysize patterns are linked to the spatial variation in primaryproduction that is the ldquoresource rulerdquo In the Mediterraneanregion lizards the thermal regime is apparently the maindriving force of morphological variability The present studysuggests a complex link between environmental variablesand morphological characters within lacertid species Thephysical conditions such as temperature and precipitationgradient were shown to be able to significantly affect bothbody and limb dimensions and thus as a powerful sourceof variation they play an important role in lizard mor-phology However general statements about the habitat-morphology relationships and their potential importance formaintenance of optimal body temperature in reptiles arehard to make due to the enormous diversity of variationsin body composition and physiology across species sexesand even individuals and the difficulty in evaluating enoughmechanisms in enough species Consequently additionalfield and experimental studies testing both body size andshape variations and their relationships with environmentalvariables especially at the intraspecific level and accountingfor sex-specific aspects are needed to help determine whetherthe observed patterns are common across species and to whatextent they are important for effective thermoregulation
12 International Journal of Zoology
Conflict of Interests
The author declares that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The author would like to thank Shai Meiri for his helpfulcomments on earlier drafts of the paper The author thanksErezMaza for assistancewith data preparationAnat Feldmanfor provision of the GIS-compatible temperature data andNaomi Paz for linguistic editing The author also thanks theIsrael Ministry of Science Culture and Sport for supportingthe National Collections of Natural History at Tel AvivUniversity as a biodiversity environment and agricultureresearch knowledge centre
References
[1] E Mayr Animal Species and Evolution Harvard UniversityPress Cambridge Mass USA 1963
[2] C Ray ldquoThe application of Bergmannrsquos and Allenrsquos rules to thepoikilothermsrdquo Journal of Morphology vol 106 pp 85ndash1081960
[3] TM Blackburn K J Gaston andN Loder ldquoGeographic gradi-ents in body size a clarification of Bergmannrsquos rulerdquo Diversityand Distributions vol 5 no 4 pp 165ndash174 1999
[4] K J Gaston and TM Blackburn Pattern and Process inMacro-ecology Blackwell Malden Mass USA 2000
[5] C Bergmann ldquoUber die verhaltnisse der warmeokonomie derthiere zu ihrer grosserdquo Gottinger Studien vol 3 pp 595ndash7081847
[6] J A Allen ldquoThe influence of physical conditions in the genesisof speciesrdquo Radical Review vol 1 pp 108ndash140 1877
[7] F C James ldquoGeographic size variation in birds and its relation-ship with climaterdquo Ecology vol 51 pp 365ndash390 1970
[8] C D Burnett ldquoGeographic and climatic correlates of morpho-logical variation inEptesicus fuscusrdquo Journal ofMammalogy vol64 no 3 pp 437ndash444 1983
[9] C C Lindsey ldquoBody sizes of poikilotherm vertebrates at differ-ent latitudesrdquo Evolution vol 20 pp 456ndash465 1966
[10] M L Rosenzweig ldquoThe strategy of body size in mammaliancarnivoresrdquo American Midland Naturalist vol 80 pp 299ndash3151968
[11] Y Yom-Tov and E Geffen ldquoGeographic variation in body sizethe effects of ambient temperature and precipitationrdquoOecologiavol 148 no 2 pp 213ndash218 2006
[12] Y Yom-Tov and H Nix ldquoClimatological correlates for body sizeof five species of Australian mammalsrdquo Biological Journal of theLinnean Society vol 29 no 4 pp 245ndash262 1986
[13] D Pincheira-Donoso and SMeiri ldquoAn intercontinental analysisof climate-driven body size clines in reptiles no support forpatterns no signals of processesrdquo Evolutionary Biology vol 40no 4 pp 562ndash578 2013
[14] K G Ashton M C Tracy and A de Queiroz ldquoIs Bergmannrsquosrule valid for mammalsrdquoThe American Naturalist vol 156 no4 pp 390ndash415 2000
[15] S Meiri and T Dayan ldquoOn the validity of Bergmannrsquos rulerdquoJournal of Biogeography vol 30 no 3 pp 331ndash351 2003
[16] K G Ashton ldquoSensitivity of intraspecific latitudinal clines ofbody size for tetrapods to sampling latitude and body sizerdquoIntegrative and Comparative Biology vol 44 no 6 pp 403ndash4122004
[17] K G Ashton and C R Feldman ldquoBergmannrsquos rule in nonavianreptiles turtles follow it lizards and snakes reverse itrdquoEvolutionvol 57 no 5 pp 1151ndash1163 2003
[18] M A Olalla-Tarraga M A Rodrıguez and B A HawkinsldquoBroad-scale patterns of body size in squamate reptiles ofEurope and North Americardquo Journal of Biogeography vol 33no 5 pp 781ndash793 2006
[19] S Volynchik ldquoMorphological variability in Vipera palaesti-nae along an environmental gradientrdquo Asian HerpetologicalResearch vol 3 pp 227ndash239 2012
[20] D Pincheira-Donoso D J Hodgson and T Tregenza ldquoTheevolution of body size under environmental gradients inectothermswhy shouldBergmannrsquos rule apply to lizardsrdquoBMCEvolutionary Biology vol 8 no 1 article 68 2008
[21] R C Stillwell ldquoAre latitudinal clines in body size adaptiverdquoOikos vol 119 no 9 pp 1387ndash1390 2010
[22] S Meiri ldquoBergmannrsquos rulemdashwhatrsquos in a namerdquo Global Ecologyand Biogeography vol 20 no 1 pp 203ndash207 2011
[23] D Pincheira-Donoso ldquoPredictable variation of range-sizesacross an extreme environmental gradient in a lizard adaptiveradiation evolutionary and ecological inferencesrdquo PLoS ONEvol 6 no 12 Article ID e28942 2011
[24] K G Ashton ldquoDo amphibians follow Bergmannrsquos rulerdquo Cana-dian Journal of Zoology vol 80 no 4 pp 708ndash716 2002
[25] M J Angilletta Jr T D Steury andMW Sears ldquoTemperaturegrowth rate and body size in ectotherms fitting pieces of a life-history puzzlerdquo Integrative and Comparative Biology vol 44 no6 pp 498ndash509 2004
[26] C E Oufiero G E A Gartner S C Adolph and T GarlandldquoLatitudinal and climatic variation in body size and dorsalscale counts in Sceloporus lizards a phylogenetic perspectiverdquoEvolution vol 65 no 12 pp 3590ndash3607 2011
[27] S Meiri ldquoEvolution and ecology of lizard body sizesrdquo GlobalEcology and Biogeography vol 17 no 6 pp 724ndash734 2008
[28] D Atkinson and RM Sibly ldquoWhy are organisms usually biggerin colder environments Making sense of a life history puzzlerdquoTrends in Ecology amp Evolution vol 12 pp 235ndash239 1997
[29] F B Cruz L A Fitzgerald R E Espinoza and J A Schulte IIldquoThe importance of phylogenetic scale in tests of Bergmannrsquosand Rapoportrsquos rules lessons from a clade of South Americanlizardsrdquo Journal of Evolutionary Biology vol 18 no 6 pp 1559ndash1574 2005
[30] T AMousseau ldquoEctotherms follow the converse to BergmannrsquosRulerdquo Evolution vol 51 pp 630ndash632 1997
[31] R N Reed ldquoInterspecific patterns of species richness geo-graphic range size and body size among NewWorld venomoussnakesrdquo Ecography vol 26 no 1 pp 107ndash117 2003
[32] D Pincheira-Donoso T Tregenza and D J Hodgson ldquoBodysize evolution in South American Liolaemus lizards of theboulengeri clade a contrasting reassessmentrdquo Journal of Evolu-tionary Biology vol 20 no 5 pp 2067ndash2071 2007
[33] M J Angilletta P H Niewiarowski A E Dunham A Leacheand W P Porter ldquoBergmannrsquos clines in ectotherms illustratinga life-historical perspective with sceloporine lizardsrdquoTheAmer-ican Naturalist vol 164 pp E168ndashE183 2004
[34] M Andersson Sexual Selection Princeton University PressPrinceton NJ USA 1994
International Journal of Zoology 13
[35] F Brana ldquoSexual dimorphism in lacertid lizards male headincrease vs female abdomen increaserdquo Oikos vol 75 pp 511ndash523 1996
[36] E R Pianka ldquoLizard species density in the Kalahari desertrdquoEcology vol 52 pp 1024ndash1029 1971
[37] E R Pianka ldquoSome intercontinental comparisons of desertlizardsrdquoNational Geographic Research vol 1 no 4 pp 490ndash5041985
[38] B H Brattstrom ldquoSocial and thermoregulatory behavior of thebearded dragon Amphibolurus barbatusrdquo Copeia vol 3 pp484ndash497 1971
[39] G C Grigg and F Seebacher ldquoField test of a paradigm hyster-esis of heart rate in thermoregulation by a free-ranging lizard(Pogona barbata)rdquo Proceedings of the Royal Society B BiologicalSciences vol 266 no 1425 pp 1291ndash1297 1999
[40] F Seebacher and C E Franklin ldquoControl of heart rate duringthermoregulation in the heliothermic lizard Pogona barbataimportance of cholinergic and adrenergic mechanismsrdquo TheJournal of Experimental Biology vol 204 no 24 pp 4361ndash43662001
[41] G J Tattersall and R M Gerlach ldquoHypoxia progressivelylowers thermal gaping thresholds in bearded dragons Pogonavitticepsrdquo The Journal of Experimental Biology vol 208 no 17pp 3321ndash3330 2005
[42] D F DeNardo T E Zubal and T C M Hoffman ldquoCloacalevaporative cooling a previously undescribedmeans of increas-ing evaporative water loss at higher temperatures in a desertectotherm theGilamonsterHeloderma suspectumrdquoThe Journalof Experimental Biology vol 207 no 6 pp 945ndash953 2004
[43] S Jaffe ldquoClimate of Israelrdquo inTheZoogeography of Israel Y Yom-Tov and E Tchernov Eds pp 79ndash92 Dr W Junk PublishersDordrecht The Netherlands 1988
[44] U Roll L Stone and S Meiri ldquoHot-spot facts and artifacts-questioning Israelrsquos great biodiversityrdquo Israel Journal of Ecologyand Evolution vol 55 no 3 pp 263ndash279 2009
[45] W Bischoff and J F Schmidtler ldquoNew data on the distributionmorphology and habitat choice of the Lacerta laevis-kulzericomplexrdquo Natura Croatica vol 8 no 3 pp 211ndash222 1999
[46] A Disi D Modry P Necas and L Rifai Amphibians andReptiles of the Hashemite Kingdom of Jordan An Atlas and FieldGuide Edit Chimaira Frankfurt Germany 2001
[47] A Bouskila and P Amitai Handbook of Amphibians andReptiles of Israel Keter Publishing House Jerusalem Israel2001 (Hebrew)
[48] A Bar and G Haimovitch A Field Guide to Reptiles andAmphibians of Israel Pazbar LTD Herzliya Israel 2012
[49] Y L Werner ldquoGeographic sympatry of Acanthodactylus opheo-durus with A boskianus in the Levantrdquo Zoology in the MiddleEast vol 1 pp 92ndash95 1986
[50] R J Hijmans S E Cameron J L Parra P G Jones and AJarvis ldquoVery high resolution interpolated climate surfaces forglobal land areasrdquo International Journal of Climatology vol 25no 15 pp 1965ndash1978 2005
[51] R B Huey ldquoTemperature physiology and the ecology ofreptilesrdquo inBiology of the Reptilia CGans and FH Pough Edsvol 12 of Physiology (C) pp 25ndash91 Academic Press New YorkNY USA 1982
[52] D J Irschick and J B Losos ldquoDo lizards avoid habitats inwhich performance is submaximal The relationship betweensprinting capabilities and structural habitat use in Caribbeananolesrdquo The American Naturalist vol 154 no 3 pp 293ndash3051999
[53] B Vanhooydonck and R Van Damme ldquoEvolutionary relation-ships between body shape and habitat use in lacertid lizardsrdquoEvolutionary Ecology Research vol 1 no 7 pp 785ndash805 1999
[54] J Melville and R Swain ldquoEvolutionary relationships betweenmorphology performance and habitat openness in the lizardgenus Niveoscincus (Scincidae Lygosominae)rdquo Biological Jour-nal of the Linnean Society vol 70 no 4 pp 667ndash683 2000
[55] R B Huey and M Slatkin ldquoCost and benefits of lizard thermo-regulationrdquo The Quarterly Review of Biology vol 51 no 3 pp363ndash384 1976
[56] R D Stevenson ldquoBody size and limits to the daily range of bodytemperature in terrestrial ectothermsrdquoTheAmericanNaturalistvol 125 pp 102ndash117 1985
[57] B W Grant ldquoTrade-offs in activity time and physiologicalperformance for thermoregulating desert lizards Sceloporusmerriamirdquo Ecology vol 71 no 6 pp 2323ndash2333 1990
[58] R Shine and T Madsen ldquoIs thermoregulation unimportant tomost reptiles An example using water pythons (Liasis fuscus)in tropical AustraliardquoPhysiological Zoology vol 69 pp 252ndash2691996
[59] R Shine ldquoReptilian viviparity in cold climates testing theassumptions of an evolutionary hypothesisrdquo Oecologia vol 57no 3 pp 397ndash405 1983
[60] C R Peterson A R Gibson andM E Dorcas ldquoSnake thermalecology the causes and consequences of body temperaturevariationrdquo in Snakes Ecology and Behavior R A Seigel and J TCollins Eds pp 241ndash314 McGraw-Hill New York NY USA1993
[61] R B Huey and J G Kingsolver ldquoEvolution of thermal sensitiv-ity of ectotherm performancerdquo Trends in Ecology and Evolutionvol 4 no 5 pp 131ndash135 1989
[62] J A Dıaz D Bauwens and B Asensio ldquoA comparative studyof the relation between heating rates and ambient temperaturesin lacertid lizardsrdquo Physiological Zoology vol 69 pp 1359ndash13831996
[63] D C Deeming ldquoPost-hatching phenotypic effects of incubationin reptilesrdquo in Reptilian Incubation Environment Evolutionand Behaviour D C Deeming Ed pp 229ndash251 NottinghamUniversity Press Nottingham UK 2004
[64] R Shine M J Elphick and P S Harlow ldquoThe influence ofnatural incubation environments on the phenotypic traits ofhatchling lizardrdquo Ecology vol 78 pp 2559ndash2568 1997
[65] T Flatt R Shine P A Borges-Landaez and S J DownesldquoPhenotypic variation in an oviparousmontane lizard (Bassianaduperreyi) the effects of thermal and hydric incubation envi-ronmentsrdquo Biological Journal of the Linnean Society vol 74 no3 pp 339ndash350 2001
[66] R Shine and M J Elphick ldquoThe effect of short-term weatherfluctuations on temperatures inside lizard nests and on thephenotypic traits of hatchling lizardsrdquo Biological Journal of theLinnean Society vol 72 no 4 pp 555ndash565 2001
[67] O Lourdais R Shine X Bonnet M Guillon and G NaulleauldquoClimate affects embryonic development in a viviparous snakeVipera aspisrdquo Oikos vol 104 no 3 pp 551ndash560 2004
[68] V Delmas X Bonnet M Girondot and A-C Prevot-JulliardldquoVarying hydric conditions during incubation influence eggwater exchange and hatchling phenotype in the red-eared sliderturtlerdquo Physiological and Biochemical Zoology vol 81 no 3 pp345ndash355 2008
[69] X-F Yan X-L Tang F Yue et al ldquoInfluence of ambient temper-ature onmaternal thermoregulation and neonate phenotypes in
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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International Journal of
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Zoology
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ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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International Journal of
Microbiology
10 International Journal of Zoology
Table 7 Results of a MANCOVA examining the effect of temperature and precipitation on total fore limb length (FLL) and total hind limblength (HLL) inMesalina guttulata with SVL as a covariate Significant effects are marked in bold letter
Sourceof variation
Dependentvariable
df MS 119865 119875
DD CC DD CC DD CC DD CC
Temperature FLLHLL
2525
2424
021045
024054
156143
181191
00650110
00290019
Covariate(SVL)
FLLHLL
11
11
20084405
9872011
14751407
72797114
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
4501082
8922073
33113455
65837331
lt0001lt0001
lt0001lt0001
Error FLLHLL
9191
6969
013031
013028
Precipitation FLLHLL
2828
2525
019041
022056
142129
162211
01070181
00590008
Covariate(SVL)
FLLHLL
11
11
19504181
9631908
14091307
68667094
lt0001lt0001
lt0001lt0001
Factors FLLHLL
11
11
356901
8021918
25752817
57177133
lt0001lt0001
lt0001lt0001
Error FLLHLL
8888
6868
013032
014026
noted in females of M guttulata Among A boskianus totalhind limb length significantly correlated with both thermalregime and rainfall gradient Hence both Mediterraneanand desert reptiles follow a similar pattern in their bodyshape variation and may benefit from various morphologicalmodifications matched to habitat range
Body temperature changes affect reptile ecology [61]becoming more important to ectotherms living in coolerenvironments which complicate attaining proper body tem-perature [58 62] In support of this my results show the asso-ciation between biogeographic origins of the species exam-ined and their relationship with environmental variables Oninterspecific comparison the most pronounced distinctionswere noted in phenotypic responses to the temperature gra-dient between Mediterranean and desert inhabitants whilethe between-species differences for precipitation-related vari-ation were weaker As expected both Mediterranean regionspecies (P laevis O elegans) display significantly strongerresponses to temperature than desert dwellers (A boskianusM guttulata) Apparently the cooler locations of the formerforce them to exhibit more consistent morphological vari-ability in respect to temperature changes whereas for desertspecies such habitat-morphology connection seems to be lessimportant It is highly likely that the speciesrsquo sensitivity tothe environment is associated not only with their ecologicaldifferentiation but also with body size ranges within thesample Thus this might be one possible explanation for thedifferent albeit relatively minor responses to temperaturebetween ecologically similar species (ie P laevis versus Oelegans andA boskianus versusM guttulata) that were notedhere In the examined samples L laevis owing to its greatermeasurement ranges than O elegans has a higher potentialfor more consistent matching of its body dimensions to theobserved temperature gradient The same is true for the twodesert lizardsA boskianus due to its extended body and limb
ranges in comparison with M guttulata displays a strongermorphological-environmental link
The examination of gender-specific habitat-morphologyinteractions revealed that within three of the four species (Plaevis A boskianus and M guttulata) sensitivity to the envi-ronment is coupledwith sex Considering the effect of climatevariables on SVL the findings demonstrate that females ingeneral show a more consistent link between temperatureand bodylimb measurements than males while the effectof precipitation on external characters was similar for bothsexes Moreover in P laevis SVL was significantly morestrongly correlated with the temperature gradient in femalesthan in malesThese observations indicate the sex-associatedeffect of natural selection pointing to different thermal andmetabolic demands inmales and femalesThus it is likely thatin females the increased body size in colder environmentsis associated with reproduction-induced requirements Thispattern suggests that females due to increased thermalrequirements particularly during vitellogenesis [63] aremore able to generate a range of suitable morphologicalmodifications for maintenance of optimal body temperaturein local environments Overall my findings indicate thatalthough females show amore consistent correlation betweenSVL and a temperature gradient than males the body shapechanges involving both body and limb dimensions arerather preliminary in explaining the observed intersexualdivergence in the habitat-morphology relationship
Environmental conditions within the nest experiencedduring early ontogenesis especially temperature and mois-ture of substrate can significantly affect development andgrowth trajectories of individuals in oviparous reptiles [64ndash68] As observed in many species either posthatching phe-notype or offspring fitness are closely associated with thermalregime [63 69ndash71] In both the laboratory and in naturalnests [64] temperature is traditionally considered to be animportant environmental determinant of reptile size while
International Journal of Zoology 11
the effect of water-related factors is more complex Severalrecent studies have tested the effect of substrate moistureduring incubation of eggs on a diverse range of reptile speciesSignificant effects are found in certain species [66 68 72 73]but not in others [74ndash76] that may reflect either differentwater permeability of the eggshell or interspecific variationin the water content of eggs [77] On the other hand theappearance of morphological variation along a precipitationgradient which in desert lizards is even more evident thanthe temperature-related variability can be considered as aresponse to the local habitats In reptiles food availabilitystrongly affects growth trajectories and is one of the possibledeterminants of body size and shape [78ndash80] Overall inarid regions where vegetation and arthropod fauna aredetermined primarily by precipitation [11] wetter localitiesprovide better food resources to lizards at the populationlevel The present findings suggest that among desert speciesthe possible spatial differences in prey availability and thusin nutrition levels may lead to morphometric differentiationbetween specimens inhabiting dry or wet sites Howeverdetailed studies on possible dietary variation linked tolocal environments are necessary to answer the question ofwhether the habitat conditions which are dependent on pre-cipitation have an effect on body dimensions in these lizards
A nonphylogenetic approach suggests that lizard speciestend to exhibit strong morphological specialization in rela-tion to their habitat [53 81] Variation in body charactersrelated to locomotion which in turn is associated withsubstrate pattern has been observed across many lizard taxa[54 82ndash84] Unfortunately based on available datasets Icould not evaluate whether the shift in substrate usage isassociated with limb proportion changes and so a rationalexplanation for the effect of vegetation on limb lengthsthrough its dependence upon hydrothermal regime remainsto be determined My findings show that generally theexamined species indicate a uniform pattern in extremitiessize variation fore and especially hind limb lengths werepositively correlated with temperature and negatively withprecipitation The results indicate that ecological adaptationto abiotic factors is a powerful source of extremity sizevariation which is under the effect of natural selection Inlizards the morphology-performance relationships suggestthat ground-dwelling species from open landscapes shouldpossess relatively long limb segments to their body length[53] This body shape pattern increases stride length provid-ing better sprinting abilities [85 86] Furthermore shorterextremities may facilitate the locomotion in highly vegetatedareas where long limbs may be disadvantageous [53] In thiscontextmyfindings suggest that various body shape patternssuch as relatively shortlong limbs or their segments whichare suited to the environmental requirements may reflect anadaptation to either dense or sparse vegetation resulting fromdifferent rainfall intensities across the distribution range
Finally given the potential importance of habitats forlimb size variation lizardsmay also use their protruding bodyparts as additional (together with body surface area) heatexchangers In these reptiles for optimal balance betweenheat gain and heat loss isometric size changes to a certainextent are a ldquotwo-edged swordrdquo inwhich high thermal inertia
of large bodies is accompanied by slow heating rates and viceversa In this respect among desert dwellers relatively longextremities and small size enhance heat exchange and seemto be a morphological adaptation for effective thermoreg-ulation In desert areas large daily fluctuations of temper-ature force the ectotherms to quickly respond to changingconditions and rapidly reach the necessary metabolic ratesfor locomotor activity Long-limbed individuals which havean increased surface area-to-volume ratio may enhancetheir heating and cooling abilities through more effectiveinteractions between the body and either solar radiationor surface temperature gradient Hence a consistent linkbetween environmental variables and limb lengths can alsobe explained by their importance for maintenance of optimalbody temperature in local environments As shown above thefact that the extremity size-environment link is more obviousin respect to hind limbs than to fore ones reinforces thishypothesis relatively large hind limbs having an increasedheat exchange capacity are much more powerful tool foreffective thermoregulation than small fore extremities
In summary the lacertid lizards I studied generallyfollowed the ecogeographic rules of Bergmann and AllenIn addition the findings indicate both intersexual and inter-specific differences in the habitat-morphology relationshipwhich can be considered within the framework of theirfunctional connectionMydata provide evidence that femalestend to show stronger relationships between climate vari-ables and body dimensions than males In desert speciestemperature has a smaller effect than rainfall on lizardphenotypes Under a constant dry climate water availabilityseems to be the most important abiotic factor in reptileecology In this respect due to the strong association betweenprecipitation and productivity my findings could also beinterpreted as evidence for the hypothesis that different bodysize patterns are linked to the spatial variation in primaryproduction that is the ldquoresource rulerdquo In the Mediterraneanregion lizards the thermal regime is apparently the maindriving force of morphological variability The present studysuggests a complex link between environmental variablesand morphological characters within lacertid species Thephysical conditions such as temperature and precipitationgradient were shown to be able to significantly affect bothbody and limb dimensions and thus as a powerful sourceof variation they play an important role in lizard mor-phology However general statements about the habitat-morphology relationships and their potential importance formaintenance of optimal body temperature in reptiles arehard to make due to the enormous diversity of variationsin body composition and physiology across species sexesand even individuals and the difficulty in evaluating enoughmechanisms in enough species Consequently additionalfield and experimental studies testing both body size andshape variations and their relationships with environmentalvariables especially at the intraspecific level and accountingfor sex-specific aspects are needed to help determine whetherthe observed patterns are common across species and to whatextent they are important for effective thermoregulation
12 International Journal of Zoology
Conflict of Interests
The author declares that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The author would like to thank Shai Meiri for his helpfulcomments on earlier drafts of the paper The author thanksErezMaza for assistancewith data preparationAnat Feldmanfor provision of the GIS-compatible temperature data andNaomi Paz for linguistic editing The author also thanks theIsrael Ministry of Science Culture and Sport for supportingthe National Collections of Natural History at Tel AvivUniversity as a biodiversity environment and agricultureresearch knowledge centre
References
[1] E Mayr Animal Species and Evolution Harvard UniversityPress Cambridge Mass USA 1963
[2] C Ray ldquoThe application of Bergmannrsquos and Allenrsquos rules to thepoikilothermsrdquo Journal of Morphology vol 106 pp 85ndash1081960
[3] TM Blackburn K J Gaston andN Loder ldquoGeographic gradi-ents in body size a clarification of Bergmannrsquos rulerdquo Diversityand Distributions vol 5 no 4 pp 165ndash174 1999
[4] K J Gaston and TM Blackburn Pattern and Process inMacro-ecology Blackwell Malden Mass USA 2000
[5] C Bergmann ldquoUber die verhaltnisse der warmeokonomie derthiere zu ihrer grosserdquo Gottinger Studien vol 3 pp 595ndash7081847
[6] J A Allen ldquoThe influence of physical conditions in the genesisof speciesrdquo Radical Review vol 1 pp 108ndash140 1877
[7] F C James ldquoGeographic size variation in birds and its relation-ship with climaterdquo Ecology vol 51 pp 365ndash390 1970
[8] C D Burnett ldquoGeographic and climatic correlates of morpho-logical variation inEptesicus fuscusrdquo Journal ofMammalogy vol64 no 3 pp 437ndash444 1983
[9] C C Lindsey ldquoBody sizes of poikilotherm vertebrates at differ-ent latitudesrdquo Evolution vol 20 pp 456ndash465 1966
[10] M L Rosenzweig ldquoThe strategy of body size in mammaliancarnivoresrdquo American Midland Naturalist vol 80 pp 299ndash3151968
[11] Y Yom-Tov and E Geffen ldquoGeographic variation in body sizethe effects of ambient temperature and precipitationrdquoOecologiavol 148 no 2 pp 213ndash218 2006
[12] Y Yom-Tov and H Nix ldquoClimatological correlates for body sizeof five species of Australian mammalsrdquo Biological Journal of theLinnean Society vol 29 no 4 pp 245ndash262 1986
[13] D Pincheira-Donoso and SMeiri ldquoAn intercontinental analysisof climate-driven body size clines in reptiles no support forpatterns no signals of processesrdquo Evolutionary Biology vol 40no 4 pp 562ndash578 2013
[14] K G Ashton M C Tracy and A de Queiroz ldquoIs Bergmannrsquosrule valid for mammalsrdquoThe American Naturalist vol 156 no4 pp 390ndash415 2000
[15] S Meiri and T Dayan ldquoOn the validity of Bergmannrsquos rulerdquoJournal of Biogeography vol 30 no 3 pp 331ndash351 2003
[16] K G Ashton ldquoSensitivity of intraspecific latitudinal clines ofbody size for tetrapods to sampling latitude and body sizerdquoIntegrative and Comparative Biology vol 44 no 6 pp 403ndash4122004
[17] K G Ashton and C R Feldman ldquoBergmannrsquos rule in nonavianreptiles turtles follow it lizards and snakes reverse itrdquoEvolutionvol 57 no 5 pp 1151ndash1163 2003
[18] M A Olalla-Tarraga M A Rodrıguez and B A HawkinsldquoBroad-scale patterns of body size in squamate reptiles ofEurope and North Americardquo Journal of Biogeography vol 33no 5 pp 781ndash793 2006
[19] S Volynchik ldquoMorphological variability in Vipera palaesti-nae along an environmental gradientrdquo Asian HerpetologicalResearch vol 3 pp 227ndash239 2012
[20] D Pincheira-Donoso D J Hodgson and T Tregenza ldquoTheevolution of body size under environmental gradients inectothermswhy shouldBergmannrsquos rule apply to lizardsrdquoBMCEvolutionary Biology vol 8 no 1 article 68 2008
[21] R C Stillwell ldquoAre latitudinal clines in body size adaptiverdquoOikos vol 119 no 9 pp 1387ndash1390 2010
[22] S Meiri ldquoBergmannrsquos rulemdashwhatrsquos in a namerdquo Global Ecologyand Biogeography vol 20 no 1 pp 203ndash207 2011
[23] D Pincheira-Donoso ldquoPredictable variation of range-sizesacross an extreme environmental gradient in a lizard adaptiveradiation evolutionary and ecological inferencesrdquo PLoS ONEvol 6 no 12 Article ID e28942 2011
[24] K G Ashton ldquoDo amphibians follow Bergmannrsquos rulerdquo Cana-dian Journal of Zoology vol 80 no 4 pp 708ndash716 2002
[25] M J Angilletta Jr T D Steury andMW Sears ldquoTemperaturegrowth rate and body size in ectotherms fitting pieces of a life-history puzzlerdquo Integrative and Comparative Biology vol 44 no6 pp 498ndash509 2004
[26] C E Oufiero G E A Gartner S C Adolph and T GarlandldquoLatitudinal and climatic variation in body size and dorsalscale counts in Sceloporus lizards a phylogenetic perspectiverdquoEvolution vol 65 no 12 pp 3590ndash3607 2011
[27] S Meiri ldquoEvolution and ecology of lizard body sizesrdquo GlobalEcology and Biogeography vol 17 no 6 pp 724ndash734 2008
[28] D Atkinson and RM Sibly ldquoWhy are organisms usually biggerin colder environments Making sense of a life history puzzlerdquoTrends in Ecology amp Evolution vol 12 pp 235ndash239 1997
[29] F B Cruz L A Fitzgerald R E Espinoza and J A Schulte IIldquoThe importance of phylogenetic scale in tests of Bergmannrsquosand Rapoportrsquos rules lessons from a clade of South Americanlizardsrdquo Journal of Evolutionary Biology vol 18 no 6 pp 1559ndash1574 2005
[30] T AMousseau ldquoEctotherms follow the converse to BergmannrsquosRulerdquo Evolution vol 51 pp 630ndash632 1997
[31] R N Reed ldquoInterspecific patterns of species richness geo-graphic range size and body size among NewWorld venomoussnakesrdquo Ecography vol 26 no 1 pp 107ndash117 2003
[32] D Pincheira-Donoso T Tregenza and D J Hodgson ldquoBodysize evolution in South American Liolaemus lizards of theboulengeri clade a contrasting reassessmentrdquo Journal of Evolu-tionary Biology vol 20 no 5 pp 2067ndash2071 2007
[33] M J Angilletta P H Niewiarowski A E Dunham A Leacheand W P Porter ldquoBergmannrsquos clines in ectotherms illustratinga life-historical perspective with sceloporine lizardsrdquoTheAmer-ican Naturalist vol 164 pp E168ndashE183 2004
[34] M Andersson Sexual Selection Princeton University PressPrinceton NJ USA 1994
International Journal of Zoology 13
[35] F Brana ldquoSexual dimorphism in lacertid lizards male headincrease vs female abdomen increaserdquo Oikos vol 75 pp 511ndash523 1996
[36] E R Pianka ldquoLizard species density in the Kalahari desertrdquoEcology vol 52 pp 1024ndash1029 1971
[37] E R Pianka ldquoSome intercontinental comparisons of desertlizardsrdquoNational Geographic Research vol 1 no 4 pp 490ndash5041985
[38] B H Brattstrom ldquoSocial and thermoregulatory behavior of thebearded dragon Amphibolurus barbatusrdquo Copeia vol 3 pp484ndash497 1971
[39] G C Grigg and F Seebacher ldquoField test of a paradigm hyster-esis of heart rate in thermoregulation by a free-ranging lizard(Pogona barbata)rdquo Proceedings of the Royal Society B BiologicalSciences vol 266 no 1425 pp 1291ndash1297 1999
[40] F Seebacher and C E Franklin ldquoControl of heart rate duringthermoregulation in the heliothermic lizard Pogona barbataimportance of cholinergic and adrenergic mechanismsrdquo TheJournal of Experimental Biology vol 204 no 24 pp 4361ndash43662001
[41] G J Tattersall and R M Gerlach ldquoHypoxia progressivelylowers thermal gaping thresholds in bearded dragons Pogonavitticepsrdquo The Journal of Experimental Biology vol 208 no 17pp 3321ndash3330 2005
[42] D F DeNardo T E Zubal and T C M Hoffman ldquoCloacalevaporative cooling a previously undescribedmeans of increas-ing evaporative water loss at higher temperatures in a desertectotherm theGilamonsterHeloderma suspectumrdquoThe Journalof Experimental Biology vol 207 no 6 pp 945ndash953 2004
[43] S Jaffe ldquoClimate of Israelrdquo inTheZoogeography of Israel Y Yom-Tov and E Tchernov Eds pp 79ndash92 Dr W Junk PublishersDordrecht The Netherlands 1988
[44] U Roll L Stone and S Meiri ldquoHot-spot facts and artifacts-questioning Israelrsquos great biodiversityrdquo Israel Journal of Ecologyand Evolution vol 55 no 3 pp 263ndash279 2009
[45] W Bischoff and J F Schmidtler ldquoNew data on the distributionmorphology and habitat choice of the Lacerta laevis-kulzericomplexrdquo Natura Croatica vol 8 no 3 pp 211ndash222 1999
[46] A Disi D Modry P Necas and L Rifai Amphibians andReptiles of the Hashemite Kingdom of Jordan An Atlas and FieldGuide Edit Chimaira Frankfurt Germany 2001
[47] A Bouskila and P Amitai Handbook of Amphibians andReptiles of Israel Keter Publishing House Jerusalem Israel2001 (Hebrew)
[48] A Bar and G Haimovitch A Field Guide to Reptiles andAmphibians of Israel Pazbar LTD Herzliya Israel 2012
[49] Y L Werner ldquoGeographic sympatry of Acanthodactylus opheo-durus with A boskianus in the Levantrdquo Zoology in the MiddleEast vol 1 pp 92ndash95 1986
[50] R J Hijmans S E Cameron J L Parra P G Jones and AJarvis ldquoVery high resolution interpolated climate surfaces forglobal land areasrdquo International Journal of Climatology vol 25no 15 pp 1965ndash1978 2005
[51] R B Huey ldquoTemperature physiology and the ecology ofreptilesrdquo inBiology of the Reptilia CGans and FH Pough Edsvol 12 of Physiology (C) pp 25ndash91 Academic Press New YorkNY USA 1982
[52] D J Irschick and J B Losos ldquoDo lizards avoid habitats inwhich performance is submaximal The relationship betweensprinting capabilities and structural habitat use in Caribbeananolesrdquo The American Naturalist vol 154 no 3 pp 293ndash3051999
[53] B Vanhooydonck and R Van Damme ldquoEvolutionary relation-ships between body shape and habitat use in lacertid lizardsrdquoEvolutionary Ecology Research vol 1 no 7 pp 785ndash805 1999
[54] J Melville and R Swain ldquoEvolutionary relationships betweenmorphology performance and habitat openness in the lizardgenus Niveoscincus (Scincidae Lygosominae)rdquo Biological Jour-nal of the Linnean Society vol 70 no 4 pp 667ndash683 2000
[55] R B Huey and M Slatkin ldquoCost and benefits of lizard thermo-regulationrdquo The Quarterly Review of Biology vol 51 no 3 pp363ndash384 1976
[56] R D Stevenson ldquoBody size and limits to the daily range of bodytemperature in terrestrial ectothermsrdquoTheAmericanNaturalistvol 125 pp 102ndash117 1985
[57] B W Grant ldquoTrade-offs in activity time and physiologicalperformance for thermoregulating desert lizards Sceloporusmerriamirdquo Ecology vol 71 no 6 pp 2323ndash2333 1990
[58] R Shine and T Madsen ldquoIs thermoregulation unimportant tomost reptiles An example using water pythons (Liasis fuscus)in tropical AustraliardquoPhysiological Zoology vol 69 pp 252ndash2691996
[59] R Shine ldquoReptilian viviparity in cold climates testing theassumptions of an evolutionary hypothesisrdquo Oecologia vol 57no 3 pp 397ndash405 1983
[60] C R Peterson A R Gibson andM E Dorcas ldquoSnake thermalecology the causes and consequences of body temperaturevariationrdquo in Snakes Ecology and Behavior R A Seigel and J TCollins Eds pp 241ndash314 McGraw-Hill New York NY USA1993
[61] R B Huey and J G Kingsolver ldquoEvolution of thermal sensitiv-ity of ectotherm performancerdquo Trends in Ecology and Evolutionvol 4 no 5 pp 131ndash135 1989
[62] J A Dıaz D Bauwens and B Asensio ldquoA comparative studyof the relation between heating rates and ambient temperaturesin lacertid lizardsrdquo Physiological Zoology vol 69 pp 1359ndash13831996
[63] D C Deeming ldquoPost-hatching phenotypic effects of incubationin reptilesrdquo in Reptilian Incubation Environment Evolutionand Behaviour D C Deeming Ed pp 229ndash251 NottinghamUniversity Press Nottingham UK 2004
[64] R Shine M J Elphick and P S Harlow ldquoThe influence ofnatural incubation environments on the phenotypic traits ofhatchling lizardrdquo Ecology vol 78 pp 2559ndash2568 1997
[65] T Flatt R Shine P A Borges-Landaez and S J DownesldquoPhenotypic variation in an oviparousmontane lizard (Bassianaduperreyi) the effects of thermal and hydric incubation envi-ronmentsrdquo Biological Journal of the Linnean Society vol 74 no3 pp 339ndash350 2001
[66] R Shine and M J Elphick ldquoThe effect of short-term weatherfluctuations on temperatures inside lizard nests and on thephenotypic traits of hatchling lizardsrdquo Biological Journal of theLinnean Society vol 72 no 4 pp 555ndash565 2001
[67] O Lourdais R Shine X Bonnet M Guillon and G NaulleauldquoClimate affects embryonic development in a viviparous snakeVipera aspisrdquo Oikos vol 104 no 3 pp 551ndash560 2004
[68] V Delmas X Bonnet M Girondot and A-C Prevot-JulliardldquoVarying hydric conditions during incubation influence eggwater exchange and hatchling phenotype in the red-eared sliderturtlerdquo Physiological and Biochemical Zoology vol 81 no 3 pp345ndash355 2008
[69] X-F Yan X-L Tang F Yue et al ldquoInfluence of ambient temper-ature onmaternal thermoregulation and neonate phenotypes in
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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International Journal of
Volume 2014
Zoology
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Molecular Biology International
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International Journal of
Microbiology
International Journal of Zoology 11
the effect of water-related factors is more complex Severalrecent studies have tested the effect of substrate moistureduring incubation of eggs on a diverse range of reptile speciesSignificant effects are found in certain species [66 68 72 73]but not in others [74ndash76] that may reflect either differentwater permeability of the eggshell or interspecific variationin the water content of eggs [77] On the other hand theappearance of morphological variation along a precipitationgradient which in desert lizards is even more evident thanthe temperature-related variability can be considered as aresponse to the local habitats In reptiles food availabilitystrongly affects growth trajectories and is one of the possibledeterminants of body size and shape [78ndash80] Overall inarid regions where vegetation and arthropod fauna aredetermined primarily by precipitation [11] wetter localitiesprovide better food resources to lizards at the populationlevel The present findings suggest that among desert speciesthe possible spatial differences in prey availability and thusin nutrition levels may lead to morphometric differentiationbetween specimens inhabiting dry or wet sites Howeverdetailed studies on possible dietary variation linked tolocal environments are necessary to answer the question ofwhether the habitat conditions which are dependent on pre-cipitation have an effect on body dimensions in these lizards
A nonphylogenetic approach suggests that lizard speciestend to exhibit strong morphological specialization in rela-tion to their habitat [53 81] Variation in body charactersrelated to locomotion which in turn is associated withsubstrate pattern has been observed across many lizard taxa[54 82ndash84] Unfortunately based on available datasets Icould not evaluate whether the shift in substrate usage isassociated with limb proportion changes and so a rationalexplanation for the effect of vegetation on limb lengthsthrough its dependence upon hydrothermal regime remainsto be determined My findings show that generally theexamined species indicate a uniform pattern in extremitiessize variation fore and especially hind limb lengths werepositively correlated with temperature and negatively withprecipitation The results indicate that ecological adaptationto abiotic factors is a powerful source of extremity sizevariation which is under the effect of natural selection Inlizards the morphology-performance relationships suggestthat ground-dwelling species from open landscapes shouldpossess relatively long limb segments to their body length[53] This body shape pattern increases stride length provid-ing better sprinting abilities [85 86] Furthermore shorterextremities may facilitate the locomotion in highly vegetatedareas where long limbs may be disadvantageous [53] In thiscontextmyfindings suggest that various body shape patternssuch as relatively shortlong limbs or their segments whichare suited to the environmental requirements may reflect anadaptation to either dense or sparse vegetation resulting fromdifferent rainfall intensities across the distribution range
Finally given the potential importance of habitats forlimb size variation lizardsmay also use their protruding bodyparts as additional (together with body surface area) heatexchangers In these reptiles for optimal balance betweenheat gain and heat loss isometric size changes to a certainextent are a ldquotwo-edged swordrdquo inwhich high thermal inertia
of large bodies is accompanied by slow heating rates and viceversa In this respect among desert dwellers relatively longextremities and small size enhance heat exchange and seemto be a morphological adaptation for effective thermoreg-ulation In desert areas large daily fluctuations of temper-ature force the ectotherms to quickly respond to changingconditions and rapidly reach the necessary metabolic ratesfor locomotor activity Long-limbed individuals which havean increased surface area-to-volume ratio may enhancetheir heating and cooling abilities through more effectiveinteractions between the body and either solar radiationor surface temperature gradient Hence a consistent linkbetween environmental variables and limb lengths can alsobe explained by their importance for maintenance of optimalbody temperature in local environments As shown above thefact that the extremity size-environment link is more obviousin respect to hind limbs than to fore ones reinforces thishypothesis relatively large hind limbs having an increasedheat exchange capacity are much more powerful tool foreffective thermoregulation than small fore extremities
In summary the lacertid lizards I studied generallyfollowed the ecogeographic rules of Bergmann and AllenIn addition the findings indicate both intersexual and inter-specific differences in the habitat-morphology relationshipwhich can be considered within the framework of theirfunctional connectionMydata provide evidence that femalestend to show stronger relationships between climate vari-ables and body dimensions than males In desert speciestemperature has a smaller effect than rainfall on lizardphenotypes Under a constant dry climate water availabilityseems to be the most important abiotic factor in reptileecology In this respect due to the strong association betweenprecipitation and productivity my findings could also beinterpreted as evidence for the hypothesis that different bodysize patterns are linked to the spatial variation in primaryproduction that is the ldquoresource rulerdquo In the Mediterraneanregion lizards the thermal regime is apparently the maindriving force of morphological variability The present studysuggests a complex link between environmental variablesand morphological characters within lacertid species Thephysical conditions such as temperature and precipitationgradient were shown to be able to significantly affect bothbody and limb dimensions and thus as a powerful sourceof variation they play an important role in lizard mor-phology However general statements about the habitat-morphology relationships and their potential importance formaintenance of optimal body temperature in reptiles arehard to make due to the enormous diversity of variationsin body composition and physiology across species sexesand even individuals and the difficulty in evaluating enoughmechanisms in enough species Consequently additionalfield and experimental studies testing both body size andshape variations and their relationships with environmentalvariables especially at the intraspecific level and accountingfor sex-specific aspects are needed to help determine whetherthe observed patterns are common across species and to whatextent they are important for effective thermoregulation
12 International Journal of Zoology
Conflict of Interests
The author declares that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The author would like to thank Shai Meiri for his helpfulcomments on earlier drafts of the paper The author thanksErezMaza for assistancewith data preparationAnat Feldmanfor provision of the GIS-compatible temperature data andNaomi Paz for linguistic editing The author also thanks theIsrael Ministry of Science Culture and Sport for supportingthe National Collections of Natural History at Tel AvivUniversity as a biodiversity environment and agricultureresearch knowledge centre
References
[1] E Mayr Animal Species and Evolution Harvard UniversityPress Cambridge Mass USA 1963
[2] C Ray ldquoThe application of Bergmannrsquos and Allenrsquos rules to thepoikilothermsrdquo Journal of Morphology vol 106 pp 85ndash1081960
[3] TM Blackburn K J Gaston andN Loder ldquoGeographic gradi-ents in body size a clarification of Bergmannrsquos rulerdquo Diversityand Distributions vol 5 no 4 pp 165ndash174 1999
[4] K J Gaston and TM Blackburn Pattern and Process inMacro-ecology Blackwell Malden Mass USA 2000
[5] C Bergmann ldquoUber die verhaltnisse der warmeokonomie derthiere zu ihrer grosserdquo Gottinger Studien vol 3 pp 595ndash7081847
[6] J A Allen ldquoThe influence of physical conditions in the genesisof speciesrdquo Radical Review vol 1 pp 108ndash140 1877
[7] F C James ldquoGeographic size variation in birds and its relation-ship with climaterdquo Ecology vol 51 pp 365ndash390 1970
[8] C D Burnett ldquoGeographic and climatic correlates of morpho-logical variation inEptesicus fuscusrdquo Journal ofMammalogy vol64 no 3 pp 437ndash444 1983
[9] C C Lindsey ldquoBody sizes of poikilotherm vertebrates at differ-ent latitudesrdquo Evolution vol 20 pp 456ndash465 1966
[10] M L Rosenzweig ldquoThe strategy of body size in mammaliancarnivoresrdquo American Midland Naturalist vol 80 pp 299ndash3151968
[11] Y Yom-Tov and E Geffen ldquoGeographic variation in body sizethe effects of ambient temperature and precipitationrdquoOecologiavol 148 no 2 pp 213ndash218 2006
[12] Y Yom-Tov and H Nix ldquoClimatological correlates for body sizeof five species of Australian mammalsrdquo Biological Journal of theLinnean Society vol 29 no 4 pp 245ndash262 1986
[13] D Pincheira-Donoso and SMeiri ldquoAn intercontinental analysisof climate-driven body size clines in reptiles no support forpatterns no signals of processesrdquo Evolutionary Biology vol 40no 4 pp 562ndash578 2013
[14] K G Ashton M C Tracy and A de Queiroz ldquoIs Bergmannrsquosrule valid for mammalsrdquoThe American Naturalist vol 156 no4 pp 390ndash415 2000
[15] S Meiri and T Dayan ldquoOn the validity of Bergmannrsquos rulerdquoJournal of Biogeography vol 30 no 3 pp 331ndash351 2003
[16] K G Ashton ldquoSensitivity of intraspecific latitudinal clines ofbody size for tetrapods to sampling latitude and body sizerdquoIntegrative and Comparative Biology vol 44 no 6 pp 403ndash4122004
[17] K G Ashton and C R Feldman ldquoBergmannrsquos rule in nonavianreptiles turtles follow it lizards and snakes reverse itrdquoEvolutionvol 57 no 5 pp 1151ndash1163 2003
[18] M A Olalla-Tarraga M A Rodrıguez and B A HawkinsldquoBroad-scale patterns of body size in squamate reptiles ofEurope and North Americardquo Journal of Biogeography vol 33no 5 pp 781ndash793 2006
[19] S Volynchik ldquoMorphological variability in Vipera palaesti-nae along an environmental gradientrdquo Asian HerpetologicalResearch vol 3 pp 227ndash239 2012
[20] D Pincheira-Donoso D J Hodgson and T Tregenza ldquoTheevolution of body size under environmental gradients inectothermswhy shouldBergmannrsquos rule apply to lizardsrdquoBMCEvolutionary Biology vol 8 no 1 article 68 2008
[21] R C Stillwell ldquoAre latitudinal clines in body size adaptiverdquoOikos vol 119 no 9 pp 1387ndash1390 2010
[22] S Meiri ldquoBergmannrsquos rulemdashwhatrsquos in a namerdquo Global Ecologyand Biogeography vol 20 no 1 pp 203ndash207 2011
[23] D Pincheira-Donoso ldquoPredictable variation of range-sizesacross an extreme environmental gradient in a lizard adaptiveradiation evolutionary and ecological inferencesrdquo PLoS ONEvol 6 no 12 Article ID e28942 2011
[24] K G Ashton ldquoDo amphibians follow Bergmannrsquos rulerdquo Cana-dian Journal of Zoology vol 80 no 4 pp 708ndash716 2002
[25] M J Angilletta Jr T D Steury andMW Sears ldquoTemperaturegrowth rate and body size in ectotherms fitting pieces of a life-history puzzlerdquo Integrative and Comparative Biology vol 44 no6 pp 498ndash509 2004
[26] C E Oufiero G E A Gartner S C Adolph and T GarlandldquoLatitudinal and climatic variation in body size and dorsalscale counts in Sceloporus lizards a phylogenetic perspectiverdquoEvolution vol 65 no 12 pp 3590ndash3607 2011
[27] S Meiri ldquoEvolution and ecology of lizard body sizesrdquo GlobalEcology and Biogeography vol 17 no 6 pp 724ndash734 2008
[28] D Atkinson and RM Sibly ldquoWhy are organisms usually biggerin colder environments Making sense of a life history puzzlerdquoTrends in Ecology amp Evolution vol 12 pp 235ndash239 1997
[29] F B Cruz L A Fitzgerald R E Espinoza and J A Schulte IIldquoThe importance of phylogenetic scale in tests of Bergmannrsquosand Rapoportrsquos rules lessons from a clade of South Americanlizardsrdquo Journal of Evolutionary Biology vol 18 no 6 pp 1559ndash1574 2005
[30] T AMousseau ldquoEctotherms follow the converse to BergmannrsquosRulerdquo Evolution vol 51 pp 630ndash632 1997
[31] R N Reed ldquoInterspecific patterns of species richness geo-graphic range size and body size among NewWorld venomoussnakesrdquo Ecography vol 26 no 1 pp 107ndash117 2003
[32] D Pincheira-Donoso T Tregenza and D J Hodgson ldquoBodysize evolution in South American Liolaemus lizards of theboulengeri clade a contrasting reassessmentrdquo Journal of Evolu-tionary Biology vol 20 no 5 pp 2067ndash2071 2007
[33] M J Angilletta P H Niewiarowski A E Dunham A Leacheand W P Porter ldquoBergmannrsquos clines in ectotherms illustratinga life-historical perspective with sceloporine lizardsrdquoTheAmer-ican Naturalist vol 164 pp E168ndashE183 2004
[34] M Andersson Sexual Selection Princeton University PressPrinceton NJ USA 1994
International Journal of Zoology 13
[35] F Brana ldquoSexual dimorphism in lacertid lizards male headincrease vs female abdomen increaserdquo Oikos vol 75 pp 511ndash523 1996
[36] E R Pianka ldquoLizard species density in the Kalahari desertrdquoEcology vol 52 pp 1024ndash1029 1971
[37] E R Pianka ldquoSome intercontinental comparisons of desertlizardsrdquoNational Geographic Research vol 1 no 4 pp 490ndash5041985
[38] B H Brattstrom ldquoSocial and thermoregulatory behavior of thebearded dragon Amphibolurus barbatusrdquo Copeia vol 3 pp484ndash497 1971
[39] G C Grigg and F Seebacher ldquoField test of a paradigm hyster-esis of heart rate in thermoregulation by a free-ranging lizard(Pogona barbata)rdquo Proceedings of the Royal Society B BiologicalSciences vol 266 no 1425 pp 1291ndash1297 1999
[40] F Seebacher and C E Franklin ldquoControl of heart rate duringthermoregulation in the heliothermic lizard Pogona barbataimportance of cholinergic and adrenergic mechanismsrdquo TheJournal of Experimental Biology vol 204 no 24 pp 4361ndash43662001
[41] G J Tattersall and R M Gerlach ldquoHypoxia progressivelylowers thermal gaping thresholds in bearded dragons Pogonavitticepsrdquo The Journal of Experimental Biology vol 208 no 17pp 3321ndash3330 2005
[42] D F DeNardo T E Zubal and T C M Hoffman ldquoCloacalevaporative cooling a previously undescribedmeans of increas-ing evaporative water loss at higher temperatures in a desertectotherm theGilamonsterHeloderma suspectumrdquoThe Journalof Experimental Biology vol 207 no 6 pp 945ndash953 2004
[43] S Jaffe ldquoClimate of Israelrdquo inTheZoogeography of Israel Y Yom-Tov and E Tchernov Eds pp 79ndash92 Dr W Junk PublishersDordrecht The Netherlands 1988
[44] U Roll L Stone and S Meiri ldquoHot-spot facts and artifacts-questioning Israelrsquos great biodiversityrdquo Israel Journal of Ecologyand Evolution vol 55 no 3 pp 263ndash279 2009
[45] W Bischoff and J F Schmidtler ldquoNew data on the distributionmorphology and habitat choice of the Lacerta laevis-kulzericomplexrdquo Natura Croatica vol 8 no 3 pp 211ndash222 1999
[46] A Disi D Modry P Necas and L Rifai Amphibians andReptiles of the Hashemite Kingdom of Jordan An Atlas and FieldGuide Edit Chimaira Frankfurt Germany 2001
[47] A Bouskila and P Amitai Handbook of Amphibians andReptiles of Israel Keter Publishing House Jerusalem Israel2001 (Hebrew)
[48] A Bar and G Haimovitch A Field Guide to Reptiles andAmphibians of Israel Pazbar LTD Herzliya Israel 2012
[49] Y L Werner ldquoGeographic sympatry of Acanthodactylus opheo-durus with A boskianus in the Levantrdquo Zoology in the MiddleEast vol 1 pp 92ndash95 1986
[50] R J Hijmans S E Cameron J L Parra P G Jones and AJarvis ldquoVery high resolution interpolated climate surfaces forglobal land areasrdquo International Journal of Climatology vol 25no 15 pp 1965ndash1978 2005
[51] R B Huey ldquoTemperature physiology and the ecology ofreptilesrdquo inBiology of the Reptilia CGans and FH Pough Edsvol 12 of Physiology (C) pp 25ndash91 Academic Press New YorkNY USA 1982
[52] D J Irschick and J B Losos ldquoDo lizards avoid habitats inwhich performance is submaximal The relationship betweensprinting capabilities and structural habitat use in Caribbeananolesrdquo The American Naturalist vol 154 no 3 pp 293ndash3051999
[53] B Vanhooydonck and R Van Damme ldquoEvolutionary relation-ships between body shape and habitat use in lacertid lizardsrdquoEvolutionary Ecology Research vol 1 no 7 pp 785ndash805 1999
[54] J Melville and R Swain ldquoEvolutionary relationships betweenmorphology performance and habitat openness in the lizardgenus Niveoscincus (Scincidae Lygosominae)rdquo Biological Jour-nal of the Linnean Society vol 70 no 4 pp 667ndash683 2000
[55] R B Huey and M Slatkin ldquoCost and benefits of lizard thermo-regulationrdquo The Quarterly Review of Biology vol 51 no 3 pp363ndash384 1976
[56] R D Stevenson ldquoBody size and limits to the daily range of bodytemperature in terrestrial ectothermsrdquoTheAmericanNaturalistvol 125 pp 102ndash117 1985
[57] B W Grant ldquoTrade-offs in activity time and physiologicalperformance for thermoregulating desert lizards Sceloporusmerriamirdquo Ecology vol 71 no 6 pp 2323ndash2333 1990
[58] R Shine and T Madsen ldquoIs thermoregulation unimportant tomost reptiles An example using water pythons (Liasis fuscus)in tropical AustraliardquoPhysiological Zoology vol 69 pp 252ndash2691996
[59] R Shine ldquoReptilian viviparity in cold climates testing theassumptions of an evolutionary hypothesisrdquo Oecologia vol 57no 3 pp 397ndash405 1983
[60] C R Peterson A R Gibson andM E Dorcas ldquoSnake thermalecology the causes and consequences of body temperaturevariationrdquo in Snakes Ecology and Behavior R A Seigel and J TCollins Eds pp 241ndash314 McGraw-Hill New York NY USA1993
[61] R B Huey and J G Kingsolver ldquoEvolution of thermal sensitiv-ity of ectotherm performancerdquo Trends in Ecology and Evolutionvol 4 no 5 pp 131ndash135 1989
[62] J A Dıaz D Bauwens and B Asensio ldquoA comparative studyof the relation between heating rates and ambient temperaturesin lacertid lizardsrdquo Physiological Zoology vol 69 pp 1359ndash13831996
[63] D C Deeming ldquoPost-hatching phenotypic effects of incubationin reptilesrdquo in Reptilian Incubation Environment Evolutionand Behaviour D C Deeming Ed pp 229ndash251 NottinghamUniversity Press Nottingham UK 2004
[64] R Shine M J Elphick and P S Harlow ldquoThe influence ofnatural incubation environments on the phenotypic traits ofhatchling lizardrdquo Ecology vol 78 pp 2559ndash2568 1997
[65] T Flatt R Shine P A Borges-Landaez and S J DownesldquoPhenotypic variation in an oviparousmontane lizard (Bassianaduperreyi) the effects of thermal and hydric incubation envi-ronmentsrdquo Biological Journal of the Linnean Society vol 74 no3 pp 339ndash350 2001
[66] R Shine and M J Elphick ldquoThe effect of short-term weatherfluctuations on temperatures inside lizard nests and on thephenotypic traits of hatchling lizardsrdquo Biological Journal of theLinnean Society vol 72 no 4 pp 555ndash565 2001
[67] O Lourdais R Shine X Bonnet M Guillon and G NaulleauldquoClimate affects embryonic development in a viviparous snakeVipera aspisrdquo Oikos vol 104 no 3 pp 551ndash560 2004
[68] V Delmas X Bonnet M Girondot and A-C Prevot-JulliardldquoVarying hydric conditions during incubation influence eggwater exchange and hatchling phenotype in the red-eared sliderturtlerdquo Physiological and Biochemical Zoology vol 81 no 3 pp345ndash355 2008
[69] X-F Yan X-L Tang F Yue et al ldquoInfluence of ambient temper-ature onmaternal thermoregulation and neonate phenotypes in
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
12 International Journal of Zoology
Conflict of Interests
The author declares that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
The author would like to thank Shai Meiri for his helpfulcomments on earlier drafts of the paper The author thanksErezMaza for assistancewith data preparationAnat Feldmanfor provision of the GIS-compatible temperature data andNaomi Paz for linguistic editing The author also thanks theIsrael Ministry of Science Culture and Sport for supportingthe National Collections of Natural History at Tel AvivUniversity as a biodiversity environment and agricultureresearch knowledge centre
References
[1] E Mayr Animal Species and Evolution Harvard UniversityPress Cambridge Mass USA 1963
[2] C Ray ldquoThe application of Bergmannrsquos and Allenrsquos rules to thepoikilothermsrdquo Journal of Morphology vol 106 pp 85ndash1081960
[3] TM Blackburn K J Gaston andN Loder ldquoGeographic gradi-ents in body size a clarification of Bergmannrsquos rulerdquo Diversityand Distributions vol 5 no 4 pp 165ndash174 1999
[4] K J Gaston and TM Blackburn Pattern and Process inMacro-ecology Blackwell Malden Mass USA 2000
[5] C Bergmann ldquoUber die verhaltnisse der warmeokonomie derthiere zu ihrer grosserdquo Gottinger Studien vol 3 pp 595ndash7081847
[6] J A Allen ldquoThe influence of physical conditions in the genesisof speciesrdquo Radical Review vol 1 pp 108ndash140 1877
[7] F C James ldquoGeographic size variation in birds and its relation-ship with climaterdquo Ecology vol 51 pp 365ndash390 1970
[8] C D Burnett ldquoGeographic and climatic correlates of morpho-logical variation inEptesicus fuscusrdquo Journal ofMammalogy vol64 no 3 pp 437ndash444 1983
[9] C C Lindsey ldquoBody sizes of poikilotherm vertebrates at differ-ent latitudesrdquo Evolution vol 20 pp 456ndash465 1966
[10] M L Rosenzweig ldquoThe strategy of body size in mammaliancarnivoresrdquo American Midland Naturalist vol 80 pp 299ndash3151968
[11] Y Yom-Tov and E Geffen ldquoGeographic variation in body sizethe effects of ambient temperature and precipitationrdquoOecologiavol 148 no 2 pp 213ndash218 2006
[12] Y Yom-Tov and H Nix ldquoClimatological correlates for body sizeof five species of Australian mammalsrdquo Biological Journal of theLinnean Society vol 29 no 4 pp 245ndash262 1986
[13] D Pincheira-Donoso and SMeiri ldquoAn intercontinental analysisof climate-driven body size clines in reptiles no support forpatterns no signals of processesrdquo Evolutionary Biology vol 40no 4 pp 562ndash578 2013
[14] K G Ashton M C Tracy and A de Queiroz ldquoIs Bergmannrsquosrule valid for mammalsrdquoThe American Naturalist vol 156 no4 pp 390ndash415 2000
[15] S Meiri and T Dayan ldquoOn the validity of Bergmannrsquos rulerdquoJournal of Biogeography vol 30 no 3 pp 331ndash351 2003
[16] K G Ashton ldquoSensitivity of intraspecific latitudinal clines ofbody size for tetrapods to sampling latitude and body sizerdquoIntegrative and Comparative Biology vol 44 no 6 pp 403ndash4122004
[17] K G Ashton and C R Feldman ldquoBergmannrsquos rule in nonavianreptiles turtles follow it lizards and snakes reverse itrdquoEvolutionvol 57 no 5 pp 1151ndash1163 2003
[18] M A Olalla-Tarraga M A Rodrıguez and B A HawkinsldquoBroad-scale patterns of body size in squamate reptiles ofEurope and North Americardquo Journal of Biogeography vol 33no 5 pp 781ndash793 2006
[19] S Volynchik ldquoMorphological variability in Vipera palaesti-nae along an environmental gradientrdquo Asian HerpetologicalResearch vol 3 pp 227ndash239 2012
[20] D Pincheira-Donoso D J Hodgson and T Tregenza ldquoTheevolution of body size under environmental gradients inectothermswhy shouldBergmannrsquos rule apply to lizardsrdquoBMCEvolutionary Biology vol 8 no 1 article 68 2008
[21] R C Stillwell ldquoAre latitudinal clines in body size adaptiverdquoOikos vol 119 no 9 pp 1387ndash1390 2010
[22] S Meiri ldquoBergmannrsquos rulemdashwhatrsquos in a namerdquo Global Ecologyand Biogeography vol 20 no 1 pp 203ndash207 2011
[23] D Pincheira-Donoso ldquoPredictable variation of range-sizesacross an extreme environmental gradient in a lizard adaptiveradiation evolutionary and ecological inferencesrdquo PLoS ONEvol 6 no 12 Article ID e28942 2011
[24] K G Ashton ldquoDo amphibians follow Bergmannrsquos rulerdquo Cana-dian Journal of Zoology vol 80 no 4 pp 708ndash716 2002
[25] M J Angilletta Jr T D Steury andMW Sears ldquoTemperaturegrowth rate and body size in ectotherms fitting pieces of a life-history puzzlerdquo Integrative and Comparative Biology vol 44 no6 pp 498ndash509 2004
[26] C E Oufiero G E A Gartner S C Adolph and T GarlandldquoLatitudinal and climatic variation in body size and dorsalscale counts in Sceloporus lizards a phylogenetic perspectiverdquoEvolution vol 65 no 12 pp 3590ndash3607 2011
[27] S Meiri ldquoEvolution and ecology of lizard body sizesrdquo GlobalEcology and Biogeography vol 17 no 6 pp 724ndash734 2008
[28] D Atkinson and RM Sibly ldquoWhy are organisms usually biggerin colder environments Making sense of a life history puzzlerdquoTrends in Ecology amp Evolution vol 12 pp 235ndash239 1997
[29] F B Cruz L A Fitzgerald R E Espinoza and J A Schulte IIldquoThe importance of phylogenetic scale in tests of Bergmannrsquosand Rapoportrsquos rules lessons from a clade of South Americanlizardsrdquo Journal of Evolutionary Biology vol 18 no 6 pp 1559ndash1574 2005
[30] T AMousseau ldquoEctotherms follow the converse to BergmannrsquosRulerdquo Evolution vol 51 pp 630ndash632 1997
[31] R N Reed ldquoInterspecific patterns of species richness geo-graphic range size and body size among NewWorld venomoussnakesrdquo Ecography vol 26 no 1 pp 107ndash117 2003
[32] D Pincheira-Donoso T Tregenza and D J Hodgson ldquoBodysize evolution in South American Liolaemus lizards of theboulengeri clade a contrasting reassessmentrdquo Journal of Evolu-tionary Biology vol 20 no 5 pp 2067ndash2071 2007
[33] M J Angilletta P H Niewiarowski A E Dunham A Leacheand W P Porter ldquoBergmannrsquos clines in ectotherms illustratinga life-historical perspective with sceloporine lizardsrdquoTheAmer-ican Naturalist vol 164 pp E168ndashE183 2004
[34] M Andersson Sexual Selection Princeton University PressPrinceton NJ USA 1994
International Journal of Zoology 13
[35] F Brana ldquoSexual dimorphism in lacertid lizards male headincrease vs female abdomen increaserdquo Oikos vol 75 pp 511ndash523 1996
[36] E R Pianka ldquoLizard species density in the Kalahari desertrdquoEcology vol 52 pp 1024ndash1029 1971
[37] E R Pianka ldquoSome intercontinental comparisons of desertlizardsrdquoNational Geographic Research vol 1 no 4 pp 490ndash5041985
[38] B H Brattstrom ldquoSocial and thermoregulatory behavior of thebearded dragon Amphibolurus barbatusrdquo Copeia vol 3 pp484ndash497 1971
[39] G C Grigg and F Seebacher ldquoField test of a paradigm hyster-esis of heart rate in thermoregulation by a free-ranging lizard(Pogona barbata)rdquo Proceedings of the Royal Society B BiologicalSciences vol 266 no 1425 pp 1291ndash1297 1999
[40] F Seebacher and C E Franklin ldquoControl of heart rate duringthermoregulation in the heliothermic lizard Pogona barbataimportance of cholinergic and adrenergic mechanismsrdquo TheJournal of Experimental Biology vol 204 no 24 pp 4361ndash43662001
[41] G J Tattersall and R M Gerlach ldquoHypoxia progressivelylowers thermal gaping thresholds in bearded dragons Pogonavitticepsrdquo The Journal of Experimental Biology vol 208 no 17pp 3321ndash3330 2005
[42] D F DeNardo T E Zubal and T C M Hoffman ldquoCloacalevaporative cooling a previously undescribedmeans of increas-ing evaporative water loss at higher temperatures in a desertectotherm theGilamonsterHeloderma suspectumrdquoThe Journalof Experimental Biology vol 207 no 6 pp 945ndash953 2004
[43] S Jaffe ldquoClimate of Israelrdquo inTheZoogeography of Israel Y Yom-Tov and E Tchernov Eds pp 79ndash92 Dr W Junk PublishersDordrecht The Netherlands 1988
[44] U Roll L Stone and S Meiri ldquoHot-spot facts and artifacts-questioning Israelrsquos great biodiversityrdquo Israel Journal of Ecologyand Evolution vol 55 no 3 pp 263ndash279 2009
[45] W Bischoff and J F Schmidtler ldquoNew data on the distributionmorphology and habitat choice of the Lacerta laevis-kulzericomplexrdquo Natura Croatica vol 8 no 3 pp 211ndash222 1999
[46] A Disi D Modry P Necas and L Rifai Amphibians andReptiles of the Hashemite Kingdom of Jordan An Atlas and FieldGuide Edit Chimaira Frankfurt Germany 2001
[47] A Bouskila and P Amitai Handbook of Amphibians andReptiles of Israel Keter Publishing House Jerusalem Israel2001 (Hebrew)
[48] A Bar and G Haimovitch A Field Guide to Reptiles andAmphibians of Israel Pazbar LTD Herzliya Israel 2012
[49] Y L Werner ldquoGeographic sympatry of Acanthodactylus opheo-durus with A boskianus in the Levantrdquo Zoology in the MiddleEast vol 1 pp 92ndash95 1986
[50] R J Hijmans S E Cameron J L Parra P G Jones and AJarvis ldquoVery high resolution interpolated climate surfaces forglobal land areasrdquo International Journal of Climatology vol 25no 15 pp 1965ndash1978 2005
[51] R B Huey ldquoTemperature physiology and the ecology ofreptilesrdquo inBiology of the Reptilia CGans and FH Pough Edsvol 12 of Physiology (C) pp 25ndash91 Academic Press New YorkNY USA 1982
[52] D J Irschick and J B Losos ldquoDo lizards avoid habitats inwhich performance is submaximal The relationship betweensprinting capabilities and structural habitat use in Caribbeananolesrdquo The American Naturalist vol 154 no 3 pp 293ndash3051999
[53] B Vanhooydonck and R Van Damme ldquoEvolutionary relation-ships between body shape and habitat use in lacertid lizardsrdquoEvolutionary Ecology Research vol 1 no 7 pp 785ndash805 1999
[54] J Melville and R Swain ldquoEvolutionary relationships betweenmorphology performance and habitat openness in the lizardgenus Niveoscincus (Scincidae Lygosominae)rdquo Biological Jour-nal of the Linnean Society vol 70 no 4 pp 667ndash683 2000
[55] R B Huey and M Slatkin ldquoCost and benefits of lizard thermo-regulationrdquo The Quarterly Review of Biology vol 51 no 3 pp363ndash384 1976
[56] R D Stevenson ldquoBody size and limits to the daily range of bodytemperature in terrestrial ectothermsrdquoTheAmericanNaturalistvol 125 pp 102ndash117 1985
[57] B W Grant ldquoTrade-offs in activity time and physiologicalperformance for thermoregulating desert lizards Sceloporusmerriamirdquo Ecology vol 71 no 6 pp 2323ndash2333 1990
[58] R Shine and T Madsen ldquoIs thermoregulation unimportant tomost reptiles An example using water pythons (Liasis fuscus)in tropical AustraliardquoPhysiological Zoology vol 69 pp 252ndash2691996
[59] R Shine ldquoReptilian viviparity in cold climates testing theassumptions of an evolutionary hypothesisrdquo Oecologia vol 57no 3 pp 397ndash405 1983
[60] C R Peterson A R Gibson andM E Dorcas ldquoSnake thermalecology the causes and consequences of body temperaturevariationrdquo in Snakes Ecology and Behavior R A Seigel and J TCollins Eds pp 241ndash314 McGraw-Hill New York NY USA1993
[61] R B Huey and J G Kingsolver ldquoEvolution of thermal sensitiv-ity of ectotherm performancerdquo Trends in Ecology and Evolutionvol 4 no 5 pp 131ndash135 1989
[62] J A Dıaz D Bauwens and B Asensio ldquoA comparative studyof the relation between heating rates and ambient temperaturesin lacertid lizardsrdquo Physiological Zoology vol 69 pp 1359ndash13831996
[63] D C Deeming ldquoPost-hatching phenotypic effects of incubationin reptilesrdquo in Reptilian Incubation Environment Evolutionand Behaviour D C Deeming Ed pp 229ndash251 NottinghamUniversity Press Nottingham UK 2004
[64] R Shine M J Elphick and P S Harlow ldquoThe influence ofnatural incubation environments on the phenotypic traits ofhatchling lizardrdquo Ecology vol 78 pp 2559ndash2568 1997
[65] T Flatt R Shine P A Borges-Landaez and S J DownesldquoPhenotypic variation in an oviparousmontane lizard (Bassianaduperreyi) the effects of thermal and hydric incubation envi-ronmentsrdquo Biological Journal of the Linnean Society vol 74 no3 pp 339ndash350 2001
[66] R Shine and M J Elphick ldquoThe effect of short-term weatherfluctuations on temperatures inside lizard nests and on thephenotypic traits of hatchling lizardsrdquo Biological Journal of theLinnean Society vol 72 no 4 pp 555ndash565 2001
[67] O Lourdais R Shine X Bonnet M Guillon and G NaulleauldquoClimate affects embryonic development in a viviparous snakeVipera aspisrdquo Oikos vol 104 no 3 pp 551ndash560 2004
[68] V Delmas X Bonnet M Girondot and A-C Prevot-JulliardldquoVarying hydric conditions during incubation influence eggwater exchange and hatchling phenotype in the red-eared sliderturtlerdquo Physiological and Biochemical Zoology vol 81 no 3 pp345ndash355 2008
[69] X-F Yan X-L Tang F Yue et al ldquoInfluence of ambient temper-ature onmaternal thermoregulation and neonate phenotypes in
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
International Journal of Zoology 13
[35] F Brana ldquoSexual dimorphism in lacertid lizards male headincrease vs female abdomen increaserdquo Oikos vol 75 pp 511ndash523 1996
[36] E R Pianka ldquoLizard species density in the Kalahari desertrdquoEcology vol 52 pp 1024ndash1029 1971
[37] E R Pianka ldquoSome intercontinental comparisons of desertlizardsrdquoNational Geographic Research vol 1 no 4 pp 490ndash5041985
[38] B H Brattstrom ldquoSocial and thermoregulatory behavior of thebearded dragon Amphibolurus barbatusrdquo Copeia vol 3 pp484ndash497 1971
[39] G C Grigg and F Seebacher ldquoField test of a paradigm hyster-esis of heart rate in thermoregulation by a free-ranging lizard(Pogona barbata)rdquo Proceedings of the Royal Society B BiologicalSciences vol 266 no 1425 pp 1291ndash1297 1999
[40] F Seebacher and C E Franklin ldquoControl of heart rate duringthermoregulation in the heliothermic lizard Pogona barbataimportance of cholinergic and adrenergic mechanismsrdquo TheJournal of Experimental Biology vol 204 no 24 pp 4361ndash43662001
[41] G J Tattersall and R M Gerlach ldquoHypoxia progressivelylowers thermal gaping thresholds in bearded dragons Pogonavitticepsrdquo The Journal of Experimental Biology vol 208 no 17pp 3321ndash3330 2005
[42] D F DeNardo T E Zubal and T C M Hoffman ldquoCloacalevaporative cooling a previously undescribedmeans of increas-ing evaporative water loss at higher temperatures in a desertectotherm theGilamonsterHeloderma suspectumrdquoThe Journalof Experimental Biology vol 207 no 6 pp 945ndash953 2004
[43] S Jaffe ldquoClimate of Israelrdquo inTheZoogeography of Israel Y Yom-Tov and E Tchernov Eds pp 79ndash92 Dr W Junk PublishersDordrecht The Netherlands 1988
[44] U Roll L Stone and S Meiri ldquoHot-spot facts and artifacts-questioning Israelrsquos great biodiversityrdquo Israel Journal of Ecologyand Evolution vol 55 no 3 pp 263ndash279 2009
[45] W Bischoff and J F Schmidtler ldquoNew data on the distributionmorphology and habitat choice of the Lacerta laevis-kulzericomplexrdquo Natura Croatica vol 8 no 3 pp 211ndash222 1999
[46] A Disi D Modry P Necas and L Rifai Amphibians andReptiles of the Hashemite Kingdom of Jordan An Atlas and FieldGuide Edit Chimaira Frankfurt Germany 2001
[47] A Bouskila and P Amitai Handbook of Amphibians andReptiles of Israel Keter Publishing House Jerusalem Israel2001 (Hebrew)
[48] A Bar and G Haimovitch A Field Guide to Reptiles andAmphibians of Israel Pazbar LTD Herzliya Israel 2012
[49] Y L Werner ldquoGeographic sympatry of Acanthodactylus opheo-durus with A boskianus in the Levantrdquo Zoology in the MiddleEast vol 1 pp 92ndash95 1986
[50] R J Hijmans S E Cameron J L Parra P G Jones and AJarvis ldquoVery high resolution interpolated climate surfaces forglobal land areasrdquo International Journal of Climatology vol 25no 15 pp 1965ndash1978 2005
[51] R B Huey ldquoTemperature physiology and the ecology ofreptilesrdquo inBiology of the Reptilia CGans and FH Pough Edsvol 12 of Physiology (C) pp 25ndash91 Academic Press New YorkNY USA 1982
[52] D J Irschick and J B Losos ldquoDo lizards avoid habitats inwhich performance is submaximal The relationship betweensprinting capabilities and structural habitat use in Caribbeananolesrdquo The American Naturalist vol 154 no 3 pp 293ndash3051999
[53] B Vanhooydonck and R Van Damme ldquoEvolutionary relation-ships between body shape and habitat use in lacertid lizardsrdquoEvolutionary Ecology Research vol 1 no 7 pp 785ndash805 1999
[54] J Melville and R Swain ldquoEvolutionary relationships betweenmorphology performance and habitat openness in the lizardgenus Niveoscincus (Scincidae Lygosominae)rdquo Biological Jour-nal of the Linnean Society vol 70 no 4 pp 667ndash683 2000
[55] R B Huey and M Slatkin ldquoCost and benefits of lizard thermo-regulationrdquo The Quarterly Review of Biology vol 51 no 3 pp363ndash384 1976
[56] R D Stevenson ldquoBody size and limits to the daily range of bodytemperature in terrestrial ectothermsrdquoTheAmericanNaturalistvol 125 pp 102ndash117 1985
[57] B W Grant ldquoTrade-offs in activity time and physiologicalperformance for thermoregulating desert lizards Sceloporusmerriamirdquo Ecology vol 71 no 6 pp 2323ndash2333 1990
[58] R Shine and T Madsen ldquoIs thermoregulation unimportant tomost reptiles An example using water pythons (Liasis fuscus)in tropical AustraliardquoPhysiological Zoology vol 69 pp 252ndash2691996
[59] R Shine ldquoReptilian viviparity in cold climates testing theassumptions of an evolutionary hypothesisrdquo Oecologia vol 57no 3 pp 397ndash405 1983
[60] C R Peterson A R Gibson andM E Dorcas ldquoSnake thermalecology the causes and consequences of body temperaturevariationrdquo in Snakes Ecology and Behavior R A Seigel and J TCollins Eds pp 241ndash314 McGraw-Hill New York NY USA1993
[61] R B Huey and J G Kingsolver ldquoEvolution of thermal sensitiv-ity of ectotherm performancerdquo Trends in Ecology and Evolutionvol 4 no 5 pp 131ndash135 1989
[62] J A Dıaz D Bauwens and B Asensio ldquoA comparative studyof the relation between heating rates and ambient temperaturesin lacertid lizardsrdquo Physiological Zoology vol 69 pp 1359ndash13831996
[63] D C Deeming ldquoPost-hatching phenotypic effects of incubationin reptilesrdquo in Reptilian Incubation Environment Evolutionand Behaviour D C Deeming Ed pp 229ndash251 NottinghamUniversity Press Nottingham UK 2004
[64] R Shine M J Elphick and P S Harlow ldquoThe influence ofnatural incubation environments on the phenotypic traits ofhatchling lizardrdquo Ecology vol 78 pp 2559ndash2568 1997
[65] T Flatt R Shine P A Borges-Landaez and S J DownesldquoPhenotypic variation in an oviparousmontane lizard (Bassianaduperreyi) the effects of thermal and hydric incubation envi-ronmentsrdquo Biological Journal of the Linnean Society vol 74 no3 pp 339ndash350 2001
[66] R Shine and M J Elphick ldquoThe effect of short-term weatherfluctuations on temperatures inside lizard nests and on thephenotypic traits of hatchling lizardsrdquo Biological Journal of theLinnean Society vol 72 no 4 pp 555ndash565 2001
[67] O Lourdais R Shine X Bonnet M Guillon and G NaulleauldquoClimate affects embryonic development in a viviparous snakeVipera aspisrdquo Oikos vol 104 no 3 pp 551ndash560 2004
[68] V Delmas X Bonnet M Girondot and A-C Prevot-JulliardldquoVarying hydric conditions during incubation influence eggwater exchange and hatchling phenotype in the red-eared sliderturtlerdquo Physiological and Biochemical Zoology vol 81 no 3 pp345ndash355 2008
[69] X-F Yan X-L Tang F Yue et al ldquoInfluence of ambient temper-ature onmaternal thermoregulation and neonate phenotypes in
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
14 International Journal of Zoology
a viviparous lizard Eremias multiocellata during the gestationperiodrdquo Journal of Thermal Biology vol 36 no 3 pp 187ndash1922011
[70] G C Packard and M J Packard ldquoThe physiological ecology ofreptilian eggs and embryosrdquo in Biology of the Reptilia C Gansand R B Huey Eds vol 16 pp 525ndash605 Alan Liss New YorkNY USA 1988
[71] D C Deeming and M W Ferguson ldquoPhysiological effectsof incubation temperature on embryonic development in rep-tiles and birdsrdquo in Egg Incubation Its Effects on EmbryonicDevelopment in Birds and Reptiles D C Deeming and MW J Ferguson Eds pp 147ndash171 Cambridge University PressCambridge UK 1991
[72] B Zhao Y Chen Y Wang P Ding and W G Du ldquoDoes thehydric environment affect the incubation of small rigid-shelledturtle eggsrdquo Comparative Biochemistry and Physiology A vol164 pp 66ndash70 2013
[73] R Shine and G P Brown ldquoEffects of seasonally varying hydricconditions on hatchling phenotypes of keelback snakes (Tropid-onophis mairii Colubridae) from the Australian wet-dry trop-icsrdquo Biological Journal of the Linnean Society vol 76 no 3 pp339ndash347 2002
[74] D T Booth and C Y Yu ldquoInfluence of the hydric environmenton water exchange and hatchlings of rigid-shelled turtle eggsrdquoPhysiological and Biochemical Zoology vol 82 no 4 pp 382ndash387 2009
[75] X Tang F Yue M Ma NWang J He and Q Chen ldquoEffects ofthermal and hydric conditions on egg incubation and hatchlingphenotypes in two PhrynocephaluslizardsrdquoAsianHerpetologicalResearch vol 3 pp 184ndash191 2012
[76] W-G Du and R Shine ldquoThe influence of hydric environmentsduring egg incubation on embryonic heart rates and offspringphenotypes in a scincid lizard (Lampropholis guichenoti)rdquoComparative Biochemistry and Physiology A Molecular andIntegrative Physiology vol 151 no 1 pp 102ndash107 2008
[77] G C Packard ldquoWater relations of chelonian eggs and embryosis wetter betterrdquoAmerican Zoologist vol 39 no 2 pp 289ndash3031999
[78] TMadsen andR Shine ldquoPhenotypic plasticity in body sizes andsexual size dimorphism in European grass snakesrdquo Evolutionvol 47 pp 321ndash325 1993
[79] M A Krause G M Burghardt and J C Gillingham ldquoBodysize plasticity and local variation of relative head and bodysize sexual dimorphism in garter snakes (Thamnophis sirtalis)rdquoJournal of Zoology vol 261 no 4 pp 399ndash407 2003
[80] A Kaliontzopoulou D C Adams A van der Meijden APerera and M A Carretero ldquoRelationships between headmorphology bite performance and ecology in two species ofPodarciswall lizardsrdquoEvolutionary Ecology vol 26 pp 825ndash8452012
[81] D J Irschick L J Vitt P Zani and J B Losos ldquoA comparisonof evolutionary radiations in mainland and Caribbean Anolislizardsrdquo Ecology vol 78 pp 2191ndash2203 1997
[82] J B Losos ldquoThe evolution of form and function morphologyand locomotor performance in West Indian Anolis lizardsrdquoEvolution vol 44 no 5 pp 1189ndash1203 1990
[83] D B Miles ldquoCovariation between morphology and locomotorperformance in sceloporine lizardsrdquo in Lizard Ecology Histor-ical and Experimental Perspectives L J Vitt and E R PiankaEds pp 207ndash235 Princeton University Press Princeton NJUSA 1994
[84] T Kohlsdorf T Garland Jr and C A Navas ldquoLimb and taillengths in relation to substrate usage in Tropidurus lizardsrdquoJournal of Morphology vol 248 no 2 pp 151ndash164 2001
[85] T Garland Jr and J B Losos ldquoEcological morphology of loco-motor performance in squamate reptilesrdquo in Ecological Mor-phology Integrative Organismal Biology P C Wainright andS M Reilly Eds pp 240ndash302 University of Chicago PressChicago Ill USA 1994
[86] R Van Damme B Vanhooydonck P Aerts and F De VreeldquoEvolution of lizard locomotion context and constraintrdquo inVertebrate Biomechanics and Evolution V Bells J P Gascand A Casinos Eds pp 267ndash282 BIOS Scientific PublishersOxford UK 2003
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology