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Journal of Arid Environments

Journal of Arid Environments 72 (2008) 1620– 1630

0140-19

doi:10.1

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Univers

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journal homepage: www.elsevier.com/locate/jaridenv

Field thermal biology in Phymaturus lizards: Comparisons from theAndes to the Patagonian steppe in Argentina

N.R. Ibarguengoytıa a,b,�, J.C. Acosta c, J.M. Boretto a,b, H.J. Villavicencio b,c,J.A. Marinero b, J.D. Krenz d

a Departamento de zoologıa, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, Unidad Postal Universidad del Comahue,

San Carlos de Bariloche, 8400 Rıo Negro, Argentinab Consejo Nacional de investigaciones Cientıficas y Tecnicas (CONICET), Argentinac Departamento de Biologıa e Instituto y Museo de Ciencias Naturales, Facultad de Ciencias Exactas, Fısicas y Naturales, Universidad Nacional de San Juan,

San Juan, Argentinad Department of Biological Sciences, Minnesota State University, Mankato, MN 56001, USA

a r t i c l e i n f o

Article history:

Received 8 August 2007

Received in revised form

2 February 2008

Accepted 28 March 2008Available online 27 May 2008

Keywords:

Bioenergetics

Liolaemidae

Reproduction

Thermophysiology

Thigmothermy

63/$ - see front matter & 2008 Elsevier Ltd.

016/j.jaridenv.2008.03.018

responding author at: Departamento de zo

idad del Comahue, San Carlos de Bariloche,

ail addresses: norai@bariloche.com.ar (N.R.

a b s t r a c t

The genus Phymaturus (Liolaemidae) is a group of rock-dwelling and viviparous lizards

distributed in the highlands of the Andes and on the volcanic plateaus of Patagonia,

Argentina. They are restricted to harsh environments characterized by cold-temperate

summers and snowy winters that constrain growth, fecundity, and length of reproductive

cycles. In the present study, the field body temperatures of Phymaturus punae, Phymaturus

zapalensis, and Phymaturus tenebrosus distributed along a latitudinal and altitudinal

gradient are analysed in relation to differences in their life histories. Each of the three

species shows differences in their body temperatures depending if they are inside or

outside the rock crevices. As was expected, body temperatures of lizards inside the rock

crevices follow the air and substrate temperatures, but outside the crevices, a paradox

was observed. P. zapalensis, living in the most-temperate climate and with body

temperatures no different than P. tenebrosus, unexpectedly had lower body temperatures

than P. punae, living at 4000 m elevation. Our results suggest that diet, the ability to be

active over a broad thermal range, and a longer activity season can counteract the effect of

body temperature on the timing and allocation of energy to growth, maturation and

reproduction.

& 2008 Elsevier Ltd. All rights reserved.

1. Introduction

Thermal relations with the environment profoundly affect almost every aspect of an ectotherm’s life. Microhabitatselection and thermoregulatory behaviour are closely related and strongly influence lizard life histories by affecting bodytemperatures that in turn influence activity and critical physiological rates including metabolism, digestion (Beaupre,1995), growth (Piantoni et al., 2006a, b), and reproduction (Sears, 2005; Shine, 2004). The thermal environment is one ofthe major environmental factors that changes with elevation and latitude. Thus, an understanding of the effects of thethermal environment on individuals along an elevational and latitudinal gradient may aid in the explanation of geographic

All rights reserved.

ologıa, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, Unidad Postal

8400 Rıo Negro, Argentina. Tel.: +54 2944 428505; fax: +54 2944 422111.

Ibarguengoytıa), jcacosta@sinectis.com.ar (J.C. Acosta), john.krenz@mnsu.edu (J.D. Krenz).

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differences in life history (Beaupre, 1995). The role of habitat and microhabitat use in lizards is crucial to anticipate thepotential impacts of such environmental changes and to suggest possible conservation strategies (Smith and Ballinger,2001).

Temporal and spatial aspects of the thermal environment will largely determine the limits to the duration and types ofactivities an animal may engage in, but there are other factors influencing whether an animal chooses to be active. Forexample, the trade-offs among the availability of heat sources, the interactions with competitors, and the threat ofpredation (hence the costs of thermoregulation), will also determine the time span for activity (Sears, 2005).

Consequently, simple generalizable explanations for patterns of geographic variation in life histories of lizards are notlikely to be found, especially if the numerous trade-offs that result from the existence of competing bioenergetic functionsand the interactions of individuals with their environment are considered (Sears, 2005). For example, ectotherms living athigh latitudes or altitudes face great physical challenges because of seasonal extremes in climate and they have adapted tolong cold winters and short summer breeding seasons (Andrews, 1998; Ibarguengoytıa and Casalins, 2007; Spellerberg,1976). Nevertheless, lizards living at high elevations, where solar radiation can be more intense, often are able tobehaviourally compensate for the cool environment and attain higher body temperatures (Christian, 1998; Pearson, 1954;Pearson and Bradford, 1976).

Lizards of the genus Phymaturus are robust rock-dwellers with flattened bodies that can squeeze into small rock creviceswhere they spend much of their time during the activity season (Cei, 1986, 1993). Phymaturus is distributed in thehighlands of the Andes, in the volcanic plateaus of Patagonia, from Catamarca to the southern border of Chubut inArgentina, and is present on the Chilean side of the Andes. These species are restricted to arid and semi-arid ecosystems inArgentina that include several different habitats characterized by cold and snowy winters (Vuille and Ammann, 1997), suchas the Monte Desert of central Argentina, the Patagonian steppes, the Chaco xeric woodlands, and the Andean Puna(Cei, 1986; Roig-Junent et al., 2006). In these environments, lizards are limited by high annual and daily thermalamplitudes, and remain inactive from mid-autumn until mid-spring (Cei, 1986).

Achievement and maintenance of body temperature within a range that allows activity and optimizes physiologicalperformance is dependent upon availability of suitable microhabitats. For instance, geographic variation in the thermalenvironment may produce geographic variation in the availability of thermally suitable microhabitats (Grant and Dunham,1990). Phymaturus vociferator from National Park Laguna La Laja, Chile (Habit and Ortiz, 1996; see Pincheira-Donoso, 2004),Phymaturus tenebrosus (Ibarguengoytıa, 2004; see Lobo and Quinteros, 2005), Phymaturus antofagastensis, (Boretto andIbarguengoyıa, 2006) and Phymaturus punae (Boretto et al., 2007) show biennial female reproductive cycles and areherbivorous (Cei, 1986; Espinoza et al., 2004). But, Phymaturus zapalensis—an omnivore—is the only species that canperform an annual cycle (J.M. Boretto and N.R. Ibarguengoytıa, unpublished data). However, previous data on the thermalbiology of the genus Phymaturus is limited to only the field and preferred body temperatures of P. vociferator (Labra andVidal, 2003) and P. tenebrosus (Ibarguengoytıa, 2005). Both species are mainly thigmothermic, with mean bodytemperatures (Tb) during activity being lower than preferred body temperatures (Tp; P. vociferator mean Tb ¼ 22.5 1C; meanTp ¼ 35.8 1C, Labra and Vidal, 2003; P. tenebrosus mean Tb ¼ 28.95 1C, mean Tp ¼ 31.13 1C, Ibarguengoytıa, 2005).

Previous studies on Phymaturus have suggested that the low environmental temperatures throughout the year and theshort activity seasons lengthen reproductive cycles (Ibarguengoytıa and Casalins, 2007), decrease growth rate, delay sexualmaturity, and decrease fecundity (Piantoni et al., 2006a). Herein, we compare field body and microenvironmentaltemperatures of lizards captured outside and inside rock crevices of three species: P. punae, P. zapalensis, and P. tenebrosus,

ranging from 281 at 4200 m to 411 at 926 m. We examine the relationships among body temperature, microenvironmentaltemperature, body size and mass, reproductive condition, and sex. Finally, we explore the balance among bodytemperature, diet and the length of the reproductive cycles in females.

2. Materials and methods

2.1. Specimens

Three sets of specimens were used: (1) P. punae (N ¼ 48) captured in the Provincial Reserve San Guillermo on thenorthern edge of San Juan Province, Argentina (281590–291020S; 691290–691050W, 3100–4200 m elevation) during twoperiods (5–9 December 2004 and 7–12 February 2005), (2) P. zapalensis (N ¼ 64) collected in the proximity of the NationalPark Laguna Blanca, Zapala, Neuquen Province, Argentina (391440S and 701220W, 824–1312 m elevation) from September toMarch (2004–2007), and (3) P. tenebrosus (N ¼ 32) captured in the Patagonian steppe, in La Fragua, Pilcaniyeu, Rıo Negroprovince, Argentina (41–41.51S and 70.5–71.41W, 926–1000 m elevation) from November to March (2000–2005). Some ofP. tenebrosus specimens (N ¼ 21) were captured previously for another study (Ibarguengoytıa, 2005) and were used in thepresent study for comparison purposes. The lizards were captured by hand or loop from 9 to 20 h.

2.2. Study area

P. punae inhabits the Provincial Reserve San Guillermo, within the Punena and Altoandina phytogeographic provinces inthe highlands of the Andes, an area of over 170,000 ha characterized by cold climate with low temperatures for most of the

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year (Haene et al., 2000). The phytogeographic region is characterized by Zigophyllaceas such as Larrea nitida, Larrea

divaricada, Bulnesia retamo, Lycium, Adesmia and Senecio. In the openings between rocks, xerophytes and graminoids such asStipa are also abundant (Cajal et al., 1981).

P. zapalensis and P. tenebrosus inhabit Patagonia, a phytogeographic province characterized by dry and cold climates,intense winds from the west (especially in summer), snow in winter and freezing temperatures most of the year (Cabrera,1976). P. zapalensis were collected near the National Park Laguna Blanca in the Occidental District, where the Laguna BlancaLagoon can be partially frozen during winter and the mean annual precipitation is 176 mm (Cabrera, 1976). The landscape ischaracterized by plateaus with steppe vegetation over sandy soil dominated by Mulinum spinosum, Haplopappus pectinatus,Senecio filaginoides and Senecio subulatus (Cabrera, 1976). P. tenebrosus were collected in the locality of La Fragua, in theSubandino District, characterized by having the coldest and most humid climates of the phyto-geographic province, and amean annual precipitation ranging from 200 to 350 mm (Cabrera, 1976). The vegetation is represented principally byFestuca pallecens, Poa lanuginosa, Bromus macranthus, Stipa speciosa, Habranthus bagnoldii (Cabrera, 1976).

2.3. Data recorded

2.3.1. Climate data

Monthly mean temperatures and wind velocities were obtained from the National Meteorological Service, ArgentineanAir Force, the Secretary of Mining of the San Juan Government, and the Laguna Blanca National Park. The photoperiod datawere obtained from the Argentinean Manual for pilots (Direccion de Transito Aereo, 1991). The air temperatures of LagunaBlanca were corrected for differences in altitude (�6 1C km�1; Fernandez-Garcıa, 1996) from temperatures obtained at theNeuquen International Airport (271 m elevation).

2.3.2. Microenvironmental data

The substratum temperature (Ts, rock or soil, TES TP-K03 substrate probe) and air temperature 1 cm above the ground(Ta, TES TP-K02 gas probe) were measured and recorded at capture site. Thermocouples were connected to a TES 1302thermometer (TES Electrical Electronic Corporation, Taipei, Taiwan, 70.01 1C). Luminescence (luximeter Extech model401025, 7lux) and wind speed (Turbo meter, 70.1 m s�1) were also recorded in the microenvironments of P. zapalensis andP. tenebrosus when lizards were found outside the rock crevices. The substratum and air temperature 1 cm above theground of P. punae microenvironments were recorded using a fast-reading thermometer (Miller–Weber; 70.1 1C). Date andtime of day at capture (time) were also registered for each lizard.

2.3.3. Field body temperature

Body temperature (sensu Pough and Gans, 1982) was taken using a catheter probe TES TP-K01, 1.62 mm diameter (inP. zapalensis and P. tenebrosus), or a Miller–Weber fast-reading thermometer (in P. punae) introduced ca. 1 cm inside thecloaca. Individuals were handled by the head to avoid heat transfer and temperature was recorded within 20 s of capture.The extent of skin melanism was also noted.

Because temperatures differed significantly depending on whether lizards were captured in (IN) or out of rock crevices(OUT), we analysed each group of data independently when comparing the three species. Data of P. tenebrosus found insidethe rock crevices were not included in the temperature analyses because of the low sample size (N ¼ 4).

2.4. Autopsy procedures

Lizards were brought to the laboratory where the snout-vent length (SVL, vernier calliper 70.02 mm), and body mass(BW, with a 10-g Pesola spring scale 70.5 g) were measured and recorded. The presence of tail injuries (cut or regenerated)was recorded. Individuals were assigned as juvenile, adult male and female by the presence of gametogenic featuresfollowing Boretto and Ibarguengoytıa (unpublished data), Boretto et al. (2007), and Ibarguengoytıa (2004). Lizards werekilled for further research in reproductive biology (see Boretto et al., 2007; Ibarguengoytıa, 2004; Boretto andIbarguengoytıa, unpublished data) by intraperitoneal administration of sodium thiopental, fixed in Bouin’s solution for24 h or in 10% formaldehyde, and preserved in 70% ethanol.

The specimens of P. punae are stored at the Department of Biology and Institute and Museum of Natural Science,Facultad de Ciencias Exactas, Fısicas y Naturales, Universidad Nacional de San Juan, and the specimens of P. zapalensis and P.

tenebrosus at Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, San Carlos de Bariloche,Argentina (CRUB-UNC).

2.5. Statistical analyses

When the analysis of covariance test (ANCOVA) was significant, the least significant differences, and mean differencestests were conducted. Normality and variance-homogeneity assumptions were tested using the Kolmogorov–Smirnov andLevene tests, respectively. When normality or variance-homogeneity assumptions were violated, non-parametric testswere used. Means are given 71 SE and medians were used instead when normality were violated.

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3. Results

3.1. Body size, mass, and tails cut or regenerated

Mean (7SE; or median) SVLs and body masses of adults (overall and by sex) of the three species are in Table 1. InP. punae, adult males were significantly larger than females (t-test, t35 ¼ �3.22, Po0.003). The frequency of tails cut orregenerated was 31.8% (N ¼ 44). The BWs were not recorded.

In contrast, P. zapalensis females were significantly longer and heavier than males (Mann–Whitney, TSVL ¼ 610, N ¼ 44;TBW ¼ 467, N ¼ 40, Po0.008). The frequency of tails cut or regenerated was 21% (N ¼ 62).

However, adult males and females of P. tenebrosus did not show differences in SVL (Mann–Whitney, T ¼ 148, P40.46) orin BW (t-test, t26 ¼ 0.12, P40.90). The proportion of tails cut or regenerated was 25% (N ¼ 32).

3.1.1. Inter-specific comparisons

P. zapalensis was significantly smaller in SVL than P. punae and P. tenebrosus (Kruskal–Wallis, H2 ¼ 32.67, Po0.001;Dunn’s, QP. zapalensis vs P. punae ¼ 4.07, QP. zapalensis vs P. tenebrosus ¼ 5.33; Po0.001). The analysis of the frequency of tail damagedid not show inter-specific differences (w2, w2

2 ¼ 1:31, P40.52).

3.2. Climate: air temperature and wind

The median air temperature for P. punae (1.3 1C) was significantly lower for P. zapalensis (8.9 1C) and P. tenebrosus

(8 1C, Kruskal–Wallis, H2,382 ¼ 98.23, Po0.001; Dunn’s method, QP. punae�P. zapalensis ¼ 9.17; QP. punae�P. tenebrosus ¼ 8.43,Po0.05). But, there was no significant difference between P. tenebrosus and P. zapalensis (Q ¼ 0.81, P40.05; Appendix A).However, the distributions of the mean monthly temperatures were significantly different among the three localities(two-sample Kolmogorov–Smirnov test, ZP. punae– P. zapalensis,241 ¼ 3.96; ZP. punae�P. tenebrosus, 240 ¼ 3.92;ZP. zapalensis�P. tenebrosus,283 ¼ 1.65, Appendix A). Wind speeds did not differ among the three localities (Kruskal–Wallis,H2,271 ¼ 0.21, P40.90; medianP. punae ¼ 19.98 km h�1, medianP. zapalensis ¼ 18.81 km h�1, and medianP. tenebrosus ¼ 19.67 km h�1).

3.3. Microenvironmental temperatures at capture site

The Ts and Ta outside rock crevices used by P. punae and P. zapalensis lizards were significantly higher than those usedinside the rock crevices (P. punae: t-student, tTs

;46 ¼ 5.37; tTa;46 ¼ 6.01, Po0.001; P. zapalensis: Mann–Whitney,

TTs ;63 ¼ 1114.50, TTa ;42 ¼ 563.00, Po0.001; Table 2).For each species, Ts was higher than Ta outside but not inside the rock crevices (P. punae: OUT: paired t-test, t33 ¼ �7.99,

Po0.001; IN: t13 ¼ �1.24, Po0.23; P. zapalensis: OUT: t19 ¼ 3.91, Po0.001; IN: t21 ¼ 0.55, P40.59; P. tenebrosus: OUT:t22 ¼ 3.63, Po0.001, Table 2).

The dependence between the microenvironmental temperatures and either date or time was different among the threespecies. In P. punae’s microenvironments the Ta and Ts showed a significant relationship with time (regression, OUT:FTa ;1;33 ¼ 7.57, FTs ;1;33 ¼ 5:01, Po0.02; IN: FTa ;1;13 ¼ 19:21, FTs ;1;13 ¼ 24:37, Po0.001). But, the capture date (December and

Table 1Mean7SE or median, range, and sample size (N) of snout-vent length (SVL, mm) and body mass (BW, g) of females, males and overall the sample of

Phymaturus punae, Phymaturus zapalensis, and Phymaturus tenebrosus

Reproductive condition and sex SVL Range N Body mass Range N

Phymaturus punae

Females 91.1271.30 80–100 17 – – –

Males 98.0571.62 85–114 20 – – –

Juveniles 63.7373.02 52–80 11 – – –

Overall 87.7072.22 52–114 48 – – –

Phymaturus zapalensis

Females 88.62 79.02–95.72 20 24.75 17–37 17

Males 82.11 72.64–90.05 22 21.00 17.5–27 21

Juveniles 70.89 58.52–82.86 14 12.50 6–22 13

Overall 80.9071.41 58.52–95.72 56 20.3270.85 6–37 51

Phymaturus tenebrosus

Females 94.76 80.7–110.32 18 31.3572.08 16–48 17

Males 94.86 88.64–98.42 11 31.0071.32 24–38 11

Juveniles 7.75 69.38–77.17 3 10.00 9–15 3

Overall 93.7571.73 69.38–110.32 32 29.2971.62 9–48 31

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Table 2Mean7SE or median, and sample size (N) of temperatures (1C) of the body (Tb), rock surface (Ts), and air (Ta), solar radiation (SR, luxes) and wind speed

(m seg�1) of Phymaturus punae, Phymaturus zapalensis, and Phymaturus tenebrosus outside (OUT) and inside (IN) the rock crevices

Tb Ts Ta Solar radiation Wind Speed

Female Male Juvenile Overall

Phymaturus punae

OUT 27.6471.06 (10) 29.7570.54 (16) 31.0270.84 (8) 29.4570.48 (34) 28 (34) 25 (34) – –

IN 16.7572.36 (7) 20.0072.73 (4) 22.8072.68 (3) 18.9771.57 (14) 17.5171.82 (14) 16.5171.22 (14) – –

Phymaturus zapalensis

OUT 25.6071.35 (10) 27.6172.37 (8) 26.0472.55 (5) 26.4071.11 (23) 27.3771.11 (23) 24.7771.01 (20) 1177745.70 (15) 1.5670.30 (15)

IN 16.9672.45 (11) 16.1271.27 (21) 14.1172.08 (9) 15.9071.01 (41) 18 (40) 18 (22) 893 (28) 1.10 (23)

Phymaturus tenebrosus

OUT 29.18070.83 (16) 29.9071.44 (10) 2872 (2) 29.3570.69 (28) 30.0971.53 (27) 24.3471.00 (23) 1170.52792.34 (21) 0.45 (20)

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February) did not influence Ta or Ts (OUT: Mann–Whitney, TTa¼ 181, TTs

¼ 219, N ¼ 34, P40.1; IN: ANCOVA, FTa ;1;14 ¼ 3.07,FTs ;1;14 ¼ 0.23, P40.28, including time as a significant covariable).

In the microenvironments of P. zapalensis Ts or Ta outside rock crevices did not show a significant relationship with dateor time (stepwise regression, FTs ;2;22 ¼ 0:72, FTa ;2;19 ¼ 0:31, P40.5). Inside the rock crevices Ta did not vary with date or time(FTa ;2;21 ¼ 1:11, P40.35), and Ts varied significantly only with date (stepwise regression, FTs ;1;39 ¼ 18:85, Po0.001).

In the microenvironments of P. tenebrosus, the Ts outside rock crevices did not show a significant relationship with dateor time (regression, FTs ;2;26 ¼ 1:86, P40.17), but Ta showed a significant relationship with date (FTa ;1;22 ¼ 9:57, Po0.005).

3.3.1. Inter-specific comparisons

The three species were found only on rock promontories either inside or outside rock crevices from 10:35 to 20:30 h.There were not significant differences among species in Ta (ANOVA, F2,76 ¼ 0.16; p40.85), or in Ts (Kruskal–Wallis,H2 ¼ 1.27, P40.53) of microenvironments of lizards outside rock crevices. Solar radiation for P. zapalensis and P. tenebrosus

outside the rock crevices did not show significant differences (Mann–Whitney, T ¼ 258, N ¼ 36, P40.54), but the medianwind speed was greater in the microenvironments of P. zapalensis than in those of P. tenebrosus (Mann–Whitney, T ¼ 332.5,N ¼ 34, Po0.01, Table 1). The microenvironments of P. punae and P. zapalensis inside the rock crevices did not showdifferences in Ta or in Ts (Mann–Whitney, TTa ¼ 227:50, N ¼ 36; TTs ¼ 421, N ¼ 53, P40.31).

3.4. Body temperature

3.4.1. Phymaturus punae

there was no difference in Tb between the individuals captured in December and those captured in February whetheroutside or inside rock crevices (t-test, tout,32 ¼ �0.22; tIN,12 ¼ 1.43; P40.17). Consequently, data of both capture dates werepooled for further analyses. The Tb of lizards inside rock crevices showed an increase with time of day (regression,FIN: 1,13 ¼ 33.31, Po0.001). But the Tb of lizards outside rock crevices did not (Regression, FOUT: 1,33 ¼ 2.11, P40.15; Fig. 1).

The Tb of lizards found either in or out of crevices showed a significant and positive relationship with Ts and Ta (stepwiseregression, FOUT: 1,33 ¼ 16.19, FIN: 1,13 ¼ 79.62, Po0.0001; Fig. 2). The Tb of lizards found outside the rock crevices wassignificantly higher than Ta and Ts (paired t-student, tTb�Ta ;33 ¼ 8:032, tTb�Ts ;33 ¼ 3:015, Po0.005). In contrast, the Tb oflizards inside rock crevices was significantly higher than Ta but not significantly different from Ts (paired t-student,tTb�Ta ;13 ¼ 3:85, Po0.002; tTb�Ts ;13 ¼ 2:168, P40.049).

Comparisons of Tb among males, females, and juveniles of active individuals were significantly different only betweenfemales and juveniles (ANOVA, F2,33 ¼ 3.69, Po0.037; Holm–Sidak, t ¼ 2.647, Po0.0127, Table 2). The Tb of lizards in rockcrevices did not show differences among males, females and juveniles (ANOVA, F2,13 ¼ 1.236, P40.328). A coloration shiftwas observed between lizards found in and out of rock crevices. The latter were lighter and bright green, and there was anintense melanism only in the males’ heads. But, the former were melanic over all of the body.

3.4.2. Phymaturus zapalensis

The Tb of lizards outside rock crevices did not show a significant relationship with either time or date (stepwiseregression, F2,22 ¼ 0.05, P40.95). But, there was a positive relationship between Tb and date in lizards inside rock crevices(stepwise regression, F1,40 ¼ 11.06, Po0.002).

The Tb of lizards outside rock crevices was significantly higher than that of lizards inside rock crevices (ANCOVA,F1,64 ¼ 45.24, Po0.001) including date as the only significant covariable in the model.

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Fig. 1. Body temperature vs. time of lizards outside (black dots) and inside (white circles) rock crevices of P. punae, P. zapalensis, and P. tenebrosus. Linear

regressions with 95% confidence intervals are indicated.

N.R. Ibarguengoytıa et al. / Journal of Arid Environments 72 (2008) 1620–1630 1625

There were no differences between Tb and Ts or Ta for lizards outside (paired t-test, tTs ;22 ¼ �1:30, tTa ;19 ¼ 2:17, P40.05),or inside rock crevices (paired t-test, tTs ;39 ¼ �2:28, tTa ;21 ¼ �1:20, P40.05). The Tb showed a significant relationship onlywith Ts (stepwise regression, FOUT: 1,19 ¼ 18.98; FIN: 1,21 ¼ 65.36, Po0.0001). In lizards outside rock crevices there were notsignificant relationships between Tb and wind or solar radiation (F2,11 ¼ 0.29, P40.75).

Body temperatures of active males, females, and juveniles were not significantly different (ANOVA, F2,22 ¼ 0.31,P40.73). lizards inside the rock crevices were not different in Tb among males, females, and juveniles considering date asthe only significant covariable in the model (ANCOVA, F2,40 ¼ 0.49, Po0.62).

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P. p

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Fig. 2. Body temperature vs. substrate and air temperatures of P. punae, P. zapalensis, and P. tenebrosus during activity. Regression lines are indicated.

Dashed lines indicate Y ¼ X relationships.

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3.4.3. Phymaturus tenebrosus

The Tb did not show a significant relationship with either time or date (stepwise regression, F2,27 ¼ 0.320, P40.729). TheTb was higher than Ta (pair t-test, tTa ;22 ¼ 4:44, Po0.001) but was not different from Ts (tTs ;20 ¼ �0:56, P40.58). There was asignificant relationship only between Tb and Ts (regression, F1,16 ¼ 18.66, Po0.001), but not between Tb and Ta, wind or solarradiation (all P40.5). Body temperatures of males and females did not show significant differences (t-test, t23 ¼ �0.57,P40.57).

The Tb did not show a significant relationship with SVL in individuals captured in or outside of rock crevices in eachspecies (P. punae: Regression, FOUT, 1,33 ¼ 0.134, FIN, 1,13 ¼ 0.918; P. zapalensis: FOUT; 2,12 ¼ 0.41; FIN; 2,36 ¼ 1.62; P. tenebrosus:FOUT; 1,27 ¼ 0.25, P40.1).

The p. punae and P. zapalensis outside had a higher Tb than those found inside rock crevices (p. punae:Kolmogorov–Smirnov test, Z ¼ 2.60, N ¼ 48, Po0.0001; P. zapalensis: t-test, t62 ¼ 6.58, Po0.001; Table 2).

3.4.4. Inter-specific comparisons

The only significant differences in Tb of lizards outside the rock crevices among the three species was a lower Tb inP. zapalensis compared with P. punae (Kruskal–wallis, H2 ¼ 5.99, Po0.05; Dunn’s method, QP. punae vs. P. zapalensis ¼ 2.30,QP. tenebrosus vs. P. zapalensis ¼ 1.97, QP. punae vs. P. tenebrosus ¼ 1.63; Fig. 3).

Body temperatures of lizards inside the rock crevices of P. punae and P. zapalensis did not show significant differencesconsidering date and time as significant covariables in the model (ANCOVA, F1,54 ¼ 1.47, Po0.23).

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Bod

y te

mpe

ratu

re (

° C)

10

15

20

25

30

35

40

P. punae

P. zapalensis

P. tenebrosus

Res

idua

ls (

Tb

vs d

ate

and

time)

-15

-10

-5

0

5

10

15

20

(34) (23)(28)

(14)

(40)

Fig. 3. Body temperature outside rock crevices (A) and residuals obtained from the multiple regression of body temperature inside the rock crevices vs.

date and time (B) of P. punae, P. zapalensis, and P. tenebrosus. Values in parentheses indicate sample size.

N.R. Ibarguengoytıa et al. / Journal of Arid Environments 72 (2008) 1620–1630 1627

4. Discussion and conclusions

Geographic variation in thermal environment caused by altitude and latitude may produce variation in the availabilityof thermally suitable microhabitats necessary for the achievement and maintenance of body temperature within a rangethat allows activity and optimizes physiological performance (Beaupre, 1995). However, we found that P. punae,P. zapalensis, and P. tenebrosus, living in different altitudinal and latitudinal sites, share similar microenvironments andhabits. The three species follow the air and substrate temperatures when they are inside the rock crevices, but theyshow paradoxical results when they are outside the rock crevices. For example, in a high-altitude site, P. punae experiencethe lowest air temperatures, and they have the lowest Tb when inside the rock crevices, but they have the highest Tb outsidethe rock crevices compared to P. zapalensis (Fig. 3). The three species each seem to be using predominately eitherheliothermy or thigmothermy, a decision strongly influenced by the local environment. In this way, P. punae, because of thegreater availability of radiation at altitudes up to 3600 m elevation, is heliothermic and can attain the highest Tb. P.

zapalensis and P. tenebrosus, at lower altitudes, are mostly thigmothermic. P. zapalensis, although they live in theintermediate latitude and altitude, are usually inside the rock crevices and show the lowest Tb (Figs. 1 and 3). Thisdifference seems paradoxical, but generalizations for patterns of geographic variation in life histories of lizards are notlikely to be found, especially if the numerous trade-offs that result from the interactions of individuals with theirenvironment are considered (Sears, 2005).

Thermal environment is not a strict determinant of microhabitat use by lizards, since all substrates afford suitablemicroclimates at least some of the time. However, substrates differ in the abundance and accessibility of microclimatesthat would facilitate precise thermoregulation (Adolph, 1990). Lizards often choose habitats and microhabitats that allowthem to maintain the appropriate body temperature (Smith and Ballinger, 2001). P. punae, P. zapalensis, and P. tenebrosus

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use the rocky habitats similarly for basking, obtaining heat by conduction, and refuging from predators. The onlymicroenvironmental difference we found was a higher wind velocity experienced by P. zapalensis.

As was expected in a cold temperate climate, the microenvironmental temperatures experienced by the lizards outsidethe rock crevices, were much higher than those experienced when they are inside the rock crevices. Inside the rock crevicesthe lizards were behaving as thermo-conformers; body temperatures of lizards in retreats followed the environmentaltemperatures, showing a stronger correlation with the rock surface temperatures than the air temperatures and increasingduring the warmer hours of the day. However, outside the rock crevices, the correlation of body temperature with themicroenvironmental temperatures and time of day varied among the three species (Figs. 1 and 2).

We do not have any specific information pertaining to the thermoregulatory behaviour of Phymaturus, considering thatthe definitive determination of thermoregulation requires either (1) the use of null hypotheses generated using metallizard models (Hertz et al., 1993) or (2) behavioural observations of thermoregulatory behaviour (e.g. Carrascal et al., 1992;Pearson and Bradford, 1976). Nevertheless, some indirect evidence exists that suggests that P. punae and P. tenebrosus

actively thermoregulate, while P. zapalensis behaves almost as a thermo-conformer.The body temperature of P. punae was higher than both air and surface temperatures suggesting that this species is

mainly heliothermic. This species showed an ability to raise the body temperature above air and substrate temperature bybasking while flattening their bodies to maximize their surface area for the absorption of solar radiation and to contact thesubstrate surface to maximize the conduction of heat from the substrate and to minimize convective heat loss, as has beenreported for the horned lizard Phrynosoma douglassi (Christian, 1998). The relationship of Tb with time of day inside the rockcrevices, but not outside, suggests thermoregulation (Fig. 1). These results are in agreement with the colouration shiftsobserved in P. punae but not in P. zapalensis or P. tenebrosus. Greater melanism in the inactive individuals would help themto capture the sun-light that enters in the rock crevices, while the shift toward lighter, less-absorptive colours duringactivity would allow them to reflect more radiation at high altitude. The body shifts in body melanism have been recordedin other South American liolaemids such as Liolaemus tenuis, Liolaemus lemniscatus (Labra and Vidal, 2003), and Liolaemus

nigroviridis (Carothers et al., 1998). The heliothermic character of P. punae is not unexpected because the basking behaviouris considered an important strategy for lizards at high elevation (Navas, 2003).

P. zapalensis and P. tenebrosus are mainly thigmothermic species (Ibarguengoytıa, 2005; and present results). Bodytemperatures of these species are influenced mainly by rock temperature, which was the most constant environmentalvariable during the day and throughout the activity season. Nevertheless, a correlation of body and environmentaltemperatures in P. zapalensis, throughout the season and time of the day, showed more limitations for thermoregulation inthis species than in P. tenebrosus (Ibarguengoytıa, 2005; and present results, Fig. 2) and in P. punae. In active individuals, thelowest Ta and Ts associated with P. zapalensis was 17 and 20 1C, respectively, with a Tb of 19 1C, while in P. tenebrosus thelowest Ta and Ts was 15 and 17 1C with a Tb of 26 1C, and in P. punae Ta and Ts were 16 and 17 1C with a Tb of 22 1C. The strongcorrelation of environmental temperatures and Tb in P. zapalensis may arise through the lack of opportunity or willingnessto bask or behaviourally elevate body temperatures above environmental temperatures as has been observed in thecrevice-dwelling lizard Xenosaurus newmanorum (Lemos-Espinal et al., 1998). Low body temperatures were also found in P.

vociferator (mean 7SD ¼ 22.573.9; N ¼ 59) from Laguna La Laja, Chile (371200S and 711180W, 1700 m; Labra and Vidal,2003). We discarded the hypothesis of lower temperatures in P. zapalensis as an effect of predator avoidance because theproportion of individuals with tail damage did not differ among the three species. However, variation in the frequency oftail injuries may be the result of not only differences in predator density but also differences in prey behaviour. In addition,we failed to find differences in Ts or Ta between P. tenebrosus and P. zapalensis localities. However, greater wind velocitiescause greater convective heat loss (Tracy and Christian, 1986), and that seems to explain the lower Tb found in P. zapalensis.

Nevertheless, P. zapalensis is active more hours per day than the other species and seems to be more eurithermal, beingoutside the rock crevices over a broader Tb range (Fig. 3).

The thermal environment profoundly affects almost every aspect of an ectotherm’s life (Torr and Shine, 1993).Nevertheless, there is a complex interplay of scenopoetic (physical and chemical) and bionomic axes playing a role in theselection of the body temperatures of the species (Tracy and Christian, 1986). Espinoza et al. (2004) show that mostherbivorous liolaemids occur in regions that are much cooler than those inhabited by other herbivorous reptiles, but theynevertheless also need the high body temperatures required by other herbivorous lizards. Accordingly, we found thatP. punae and P. tenebrosus, although inhabiting harsher environments at higher altitudes and latitudes, respectively, thanP. zapalensis, are strictly herbivorous and P. punae has higher body temperature. In contrast, even though the genusPhymaturus has been considered entirely herbivorous, a view supported by our observations of strict herbivory in captiveP. punae and P. tenebrosus, P. zapalensis has been observed in captivity to behave omnivorously by eating insects in additionto leaves and flowers (J.M. Boretto and N. R. Ibarguengoytıa, unpublished data).

In some environments, ectotherms must at times forgo surface activity because thermally suitable microhabitats are notavailable. For terrestrially foraging reptiles, thermal constraints on surface use may limit food harvesting by reducingavailable foraging time. Likewise, the range of available microhabitats may also affect the range of available Tb (Beaupre,1995). The omnivorous habit of P. zapalensis allows this saxicolous species to feed while they are inside the rocks crevices,augmenting their energy budget in comparison to the strictly herbivorous Phymaturus species that have to go outside thecrevices to feed. Furthermore, herbivorous reptiles have a particular problem assimilating energy from their food. Plantmaterial is less energy-dense than the food of carnivorous lizards and digestion of plant material is a slower, temperature-dependent process (Tracy, 1994).

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Whether omnivory in P. zapalensis is a recent adaptation to greater limits in the attainment of high body temperaturesor an ancestral trait remains to be elucidated, but its absence among congeners would suggest a recent derivation. Theamount of energy available for growth and reproduction is related to the difference between harvested energy and the sumof resting metabolism and activity costs (Beaupre, 1995). In this study we found a paradoxical result in the relationshipbetween reproduction and field body temperatures. Sex, reproductive state, size and body mass have been shown to alterthe temperature relationships of lizards (Mathies and Andrews, 1997; Smith and Ballinger, 1995). Nevertheless, we did notfind a relationship among these variables, except in a higher Tb in juvenile P. punae compared with females. This is probablythe result of a combination of body mass and different habits as is the case for other liolaemids (Carothers et al., 1998) andLacerta monticola from high altitudes (Carrascal et al., 1992).

Low body temperatures in Sceloporus at high elevations in the tropics are correlated with impaired performances inlocomotion, digestion, and other physiological attributes such as a protraction in the reproductive cycles (Andrews, 1998;Mendez-de la Cruz et al., 1998). In addition, animals living in more-variable environments may have sharply reducedreproductive fitness when habitat quality is low (Martın and Lopez, 1998). Accordingly, lizards of the genus Phymaturus

living in arid environments at high altitudes and latitudes, with snowy winters and warm and dry summers, have beenshown to be biennial, conducting vitellogenesis for 10–12 months followed by 4–5 months of pregnancy during the nextactivity season (Boretto and Ibarguengoyıa, 2006; Boretto et al., 2007; Ibarguengoytıa, 2004). In contrast, P. zapalensis,despite having low body temperature, is the only congener that can complete the reproductive cycle in 1 year, althoughthey often skip years, probably caused by limitations on the ability to store fat reserves (Boretto and N.R. Ibarguengoytıa,unpublished data).

The three species in this study hibernate during winter and during the activity season they have similar bodytemperatures and use similar microenvironmental retreats. However, the observations that P. zapalensis spends more timein rock crevices and has lower body temperatures suggest that lizards might face the trade-off between the risk ofpredation and having to endure thermal extremes by remaining either exposed or in retreats. P. zapalensis seems to copewith these constraints by exploiting a longer activity season, and by having higher plasticity. P. zapalensis is moreeurithermic, being active over a broader range of temperatures, and has an omnivorous diet that allows it to acquire moreenergy and protein than P. punae or P. tenebrosus.

Acknowledgments

We thank M. Martinez, D. Recabarren, M. Jordan, J. Gutierrez, R. Blanco, and the Boretto and Guevara-Martınez familiesfor assistance in the fieldwork. We also want to extend thanks to A. Carrizo and A. Montanez for serving as guides inProvincial Reserve San Guillermo and to the National Meteorological Service, Argentinean Air Force and the Laguna BlancaNational Park for providing climate data. This work was partially supported by Universidad Nacional del Comahue andCONICET PIP5625.

Appendix A

Mean air temperatures vs. month at the collection sites of P. punae (circles and solid line), P. zapalensis (triangles anddotted line), and P. tenebrosus (dots and dashed line). The polynomial regressions are indicated.

Appendix B. Supplementary Materials

Supplementary data associated with this article can be found in the online version at doi:10.1016/j.jaridenv.2008.03.018.

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