Effect of Altitude on Thermal Responses of Liolaemus Pictus Argentinus in Argentina

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11 Effect of altitude on thermal responses of Liolaemus pictus argentinus 13 in Argentina

15 Joel Gutie´rrez a,n, John D. Krenz b, Nora R. Ibarguengoytı¨ ´a a,c

a 17 Departamento de Zoologıá del Centro Regional Universitario Bariloche, Unidad Postal Universidad Nacional Del Comahue, Quintral 1250, San Carlos de Bariloche, Rıó Negro 8400, Argentina b Department of Biological Sciences, Minnesota State University, Mankato, MN 56001, USA 19 c INIBIOMA-CONICET, Universidad Nacional Del Comahue, Quintral 1250, San Carlos de Bariloche, Rıó Negro 8400, Argentina

21 article info abstract 23 Article history: Reptiles that live in cooler environments hibernate longer and, when active, limit daily activity times, 25 Received 12 April 2010 allocate more time and energy toward thermoregulation, and consequently experience life-history Accepted 6 July 2010 constraints such as reduced fecundity and supra-annual reproductive cycles. This pattern becomes 27 more extreme with increasing latitude and altitude. We compared the thermal biology of two Keywords: populations of Liolaemus pictus argentinus living at two altitudes (771 and 1700 m asl). Environ- 29 Lizards mental, microenvironmental, and operative temperatures were studied in order to describe the capture Thermoregulation sites, sources of heat, and availability of microenvironments appropriate for thermoregulation. The Cold climate body temperatures of L. p. argentinus at capture (Tb) and the preferred temperatures in the laboratory 31 Liolaemidae (Tp) were recorded and integrated with operative temperatures to calculate the effectiveness of thermoregulation. The high-altitude population was found to have a lower mean T (29 1C compared 33 b with 33 1C), while the Tp values for both populations were similar (36.7 1C). The analysis of operative

temperatures and Tb in relation to Tp showed that L. p. argentinus behaves as a moderate 35 thermoregulator at high altitude and as a poor thermoregulator at the low-altitude site probably due in part to the avoidance of predation risk. 37 & 2010 Published by Elsevier Ltd. 67

39 69

41 71 1. Introduction sunny patches when they achieve temperatures that are close to maximal body temperatures and are inactive at mid-day (Hertz 43 73 Temperature, especially in ectotherms, plays a fundamental et al., 1983; Sinervo et al., 2010). Not only are lizard body temperatures (T ) lower at higher altitudes and latitudes, but also 45 role in determining life-history patterns because of its inﬂuence b 75 on the rate of metabolism and bioenergetics. Environmental they are less variable (Hertz et al., 1983). In the genus Anolis, many attributes of thermal physiology differ markedly among 47 heterogeneity creates a variety of microclimates and ectotherms 77 typically move between microhabitats at appropriate times to closely related species and vary in concert with environmental temperatures (Hertz et al., 1983). Species differences have been 49 thermoregulate. Their success often depends on the availability of 79 suitable thermal microclimates (Smith and Ballinger, 2001), observed in the mean Tb and preferred body temperature (as determined using a thermal gradient in the laboratory), range of 51 which, if available, allow ectotherms such as lizards to attain 81 higher body temperatures and consequently higher rates of activity temperature, and critical thermal maxima. For example, Anolis cristatellus from Puerto Rico actively thermoregulates in 53 metabolism, locomotion, and digestion, resulting in more energy 83 for maintenance and production (Shine, 2004). open environments, but passively loses or gains heat in shaded environments such as a closed-canopy forest (Hertz et al 1993). In 55 Many species of lizards exhibit differences in thermoregula- 85 tory behaviors at different altitudes because of differences in the contrast, in low-insolation environments, the possibility of active thermoregulation is virtually eliminated as shown for the 57 thermal environment (Adolph, 1990; Adolph and Porter, 1993). 87 For example, lizards that inhabit cold mountain environments Australian dragon, Hypsilurus spinipes, and the lizard Xenosaurus newmanorum (Lemos-Espinal et al., 1998). In other cases, lizards 59 bask for longer periods and are less active than lizards at lower 89 elevations. In contrast, lizards in warmer climates typically avoid thermoregulate nearly all year (e.g., Podarcis melisellensis and Podarcis muralis; Smith and Ballinger, 2001. In addition, micro- 61 91 environmental variation affects the activity regime of Sceloporus n merriami populations along altitudinal gradients (Smith and 63 Q1 Corresponding author. 93 E-mail address: [email protected] (J. Gutie´rrez). Ballinger, 2001), and of species such as pristidactylus torquatus 95 65 0306-4565/$ - see front matter & 2010 Published by Elsevier Ltd. doi:10.1016/j.jtherbio.2010.07.001

Please cite this article as: Gutie´rrez, J., et al., Effect of altitude on thermal responses of Liolaemus pictus argentinus in Argentina. J. Thermal Biol. (2010), doi:10.1016/j.jtherbio.2010.07.001 2 J. Gutie´rrez et al. / Journal of Thermal Biology ] (]]]]) ]]]–]]]

1 and pristidactylus volcanensis in Chile that inhabit the closed- 2.2. Estimation of preferred body temperatures 67 canopy Nothofagus forest versus open-canopy forests, respectively 3 (Labra and Rosenmann, 1992). Body temperature preference experiments were conducted the 69 Liolaemus pictus argentinus (Liolaemidae) is a viviparous and day after capture. Lizards were placed individually in open-top 5 insectivorous species with a wide distribution in the Patagonian terraria (200 45 18 cm3) each with a sand floor and a thermal 71 Andes of Neuqueń, Rıó Negro, and Chubut provinces of Argentina gradient produced by a line of four infra-red lamps overhead (one 7 (39–43 1S and 520–1600 m asl (Donoso-Barros, 1966; Cei, 1986; 250 W, two 150 W, and one 100 W). The lamps were adjusted to 73 Scolaro, 2005)). Previous studies of L. p. argentinus different heights to make a linear substratum gradient from 9 (Ibarguengoytı¨ á and Cussac, 2002), Liolaemus elongates, and 15–69 1C. Lizard body temperatures were measured every 10 min 75 Phymaturus tenebrosus (Ibarguengoytı¨ á, 2005; Ibarguengoytı¨ á for 5 h using ultra thin (1 mm) catheter thermocouples located 11 et al., 2008) suggest that environments characterized by low approximately 10 mm inside the cloaca and fastened to the base 77 temperatures throughout the year and short activity seasons limit of the lizard’s tail to keep the thermocouple in position during the 13 the opportunities for thermoregulation and in turn influence experiment (TES 1302 thermometer, TES Electrical Electronic 79 several life-history traits. These species are predominantly Corp., Taipei, Taiwan, 70.03 1C). All measurements were taken so 15 heliothermal and at low altitude (Ibarguengoytı¨ á and Cussac, as to minimize interference with their normal activities. The 81 2002) a mean Tb of 33.2 1C was observed, which is similar to that duration of the experiments corresponded to previous trials that 17 of other liolaemids (32.5 1C, N¼45 lizards; Medina et al., 2009). measured the amount of time required for Liolaemus bibronii 83 Herein we report differences in thermal physiology in L. p. (Medina et al., 2009), Liolaemus pictus (Gutie´rrez, 2009), 19 argentinus between high and low altitude populations in close and several other liolaemids (Liolaemus lineomaculatus, Liolaemus 85 proximity. boulengeri, L. elongatus, and Liolaemus fitzingeri; Ibarguengoytı¨ á, 21 unpublished data) to reach their preferred temperature 87 asymptote. 23 We estimated the mean and range of the preferred body 89

temperature (Tp) for each individual. The set-point range (Tset), 25 2. Materials and methods considered as the temperatures within the interquartile range of 91 the observations, was also noted because earlier studies show 27 2.1. Study areas and ﬁeld methods neurophysiological evidence that ectotherms regulate between 93 upper and lower set-point temperatures rather than around a

29 The two ﬁeld sites in northwestern Patagonia, Argentina, are Cerro single Tb (Barber and Crawford, 1977; Firth and Turner, 1982). The 95 Challhuaco (41115057.900Sand71117057.400 W; 1615–1769 m asl) and interquartile range represents the natural settings caused by the 31 Melipal Beach on lake Nahuel Huapi (41107041.5300Sand711 hypothalamic thermostat in lizards and ﬁshes (Barber and 97 20044.8700W, 771 m asl), both near the city of San Carlos de Bariloche Crawford, 1977; Firth and Turner, 1982). In order to measure

33 in Rı´o Negro Province. Lizards (N¼30) were captured by loop or hand the average extent to which L. p. argentinus experienced Tb values 99 at high altitude in December 2005, in January, April, and December outside the set-point range, the sum of absolute values of the

35 2006, and in February 2007. At low altitude, 33 lizards were captured deviations of Tb from Tset of each individual was calculated 101 in February and March of 2006 and 2007. All captures were (individual deviation¼db). The db values obtained for each lizard 37 authorized by the Wild Life Service of the Province of Rı´oNegro were used to estimate the mean and range of Tp, Tset, and mean db 103 and Nahuel Huapi National Park. of each population.

39 The microenvironment at each capture site was described The index of mean thermal quality of the habitat (de) was 105 by measuring the following variables: substratum temperature calculated as the deviation of Te from the mean Tset for each 41 (Ts, TESTP-K03 substrate probe) and air temperature 1 cm above population. The existence of active selection of the microhabitats 107 the ground (Ta, TESTP-K02 gas probe) recorded with thermo- and the effectiveness of thermoregulation was obtained as E¼

43 couples connected to a TES 1302 thermometer (TES Electrical 1–(db/de); this formula integrates the average degree to which the 109 7 1 Electronic Corp., Taipei, Taiwan, 0.03 C), wind velocity lizards experienced Tb values outside the set-point range (db) and 7 45 (Turbometer, 0.1 m/s), humidity (Micro-meteorological Station, the corresponding de. Thermoregulation is considered effective 111 Lutron LM-8000), and luminescence (Luximeter Extech model when E is close to 1, thermoconforming when E is close to 0, and 47 401025, 7lux). moderately effective if E is close to 0.50 (Hertz et al., 1993; 113 Body temperatures (Tb) were measured in the cloaca using a Bauwens et al., 1996; Medina et al., 2009). 49 thermocouple (TES TP-K01; 1.62 mm diameter). Lizards were 115 handled by the head and the measurements were done within 51 20 s after capture in order to minimize heat transfer to the animal. 119 A data logger (HOBO) was installed at each ﬁeld site to record 2.3. Statistical analyses 53 environmental temperatures hourly for 1 yr in order to estimate 121 the mean environmental temperature. In addition, 20 copper We used the statistical software programs Sigma Stat 3.5s, 55 models were installed in different microenvironments at each SPSSs 11.0, and 10.0s Sigma Plot for statistical analysis. The 123 site—the size of the model was 63 10 3mm3 and they were dependence between variables was analyzed by simple or multi- 57 hollow copper pipes painted black and a small hole allowed the ple stepwise regressions. The differences between sample means 125 insertion of a thermocouple. Temperatures of the models were were analyzed using paired, when observations were related, or

59 tested simultaneously against the body temperatures (Tb) of live L. unpaired t-tests. For more than two tests, we used a one-way 127 p. argentinus under a heat source in laboratory. Temperatures of analysis of variance for repeated meaures. The assumptions of 61 the model and the live individual showed a tight correlation normality and homogeneity of variance for parametric procedures 129 (r2¼0.90, Po0.0001, N¼50; Ibarguengoytı¨ ´a et al., 2009), con- were checked using Kolmogorov–Smirnov and Levene’s tests, 63 ﬁrming that the models acquired temperatures similar to that of a respectively. When the assumptions of normality or homogeneity 131 non-thermoregulating lizard. The temperatures were recorded 3 of variance were not met, we used equivalent nonparametric tests 65 or 4 times daily for each model to estimate the mean operative such as Mann–Whitney or Kruskal–Wallis tests for comparison of 133

temperatures (Te). means of two independent samples. The signiﬁcance level used

Please cite this article as: Gutie´rrez, J., et al., Effect of altitude on thermal responses of Liolaemus pictus argentinus in Argentina. J. Thermal Biol. (2010), doi:10.1016/j.jtherbio.2010.07.001 J. Gutie´rrez et al. / Journal of Thermal Biology ] (]]]]) ]]]–]]] 3

1 for all statistical tests was 5% (Sokal and Rohlf, 1969; Norusis, while feeding, basking, or during activities related to reproduction 67 1986). from 11:00 to 18:00 h. There was no difference between sites in

3 either body mass (t-test, t53¼1.83; P40.07) or SVL (Mann– 69 Whitney, TSVL¼1022.00, N¼66, P40.29). 5 3. Results 71 3.2. Environmental and body temperatures 7 3.1. Body sizes 73 Mean monthly temperatures differed between sites year- 9 75 Thirty-three animals were captured at each site. At both round except during December, January, March, and April capture sites all the specimens were captured outside shelters, (Fig. 1). The environmental temperatures at high altitude stayed 11 77 below 0 1C from June to October while at low altitude the lower values were observed from June to September but monthly means 13 79 were never below 0 1C. In December and January, the low altitude site was cooler (Fig. 1). 15 81 The mean Tb was signiﬁcantly warmer than Ts and Ta in both populations (paired t-tests, high altitude: t ¼ 2:41, Po0. 17 Tb Ts1,27 83 023; tTbTa1,28 ¼4:95, Po0.001; low altitude: tTbTs1,31 ¼ 5:58, Po0.001; tT T 1,23 ¼ 5:71, Po0.001; Fig. 2 and Table 1). Mean Tb 19 b a 85 was signiﬁcantly cooler at high altitude (t61¼3.16, Po0.002; Table 2). 21 87

23 3.3. Operative temperatures (Te) 89

25 At high altitude, T were significantly lower than T (Mann– 91 Fig. 1. Mean monthly temperature at the high altitude site (circles) and low e b altitude site (squares). Regression and confidence intervals (95%) were drawn Whitney, T1,69¼1275.0, Po0.002, median Te¼24.9 1C, median 27 considering the best-fit curve generated by the program Table Curve 2D. Tb¼28.8 1C). At low altitude, Te did not differ significantly from 93

29 95

31 97

33 99

35 101

37 103

39 105

41 107

43 109

45 111

47 113

49 115

51 119

53 121

55 123

57 125

59 127

61 129

63 131

65 133 Fig. 2. Relationship between body temperature and substratum temperatures (Ts) and air temperatures (Ta). Dashed lines indicate Y¼X relationships. Curves indicate 95% conﬁdence intervals. Solid lines are the temperature set-points.

Please cite this article as: Gutie´rrez, J., et al., Effect of altitude on thermal responses of Liolaemus pictus argentinus in Argentina. J. Thermal Biol. (2010), doi:10.1016/j.jtherbio.2010.07.001 4 J. Gutie´rrez et al. / Journal of Thermal Biology ] (]]]]) ]]]–]]]

1 Table 1 67

Physical environmental characteristics of high and low altitude sites. Humidity (H%), luminosity (Luxes), wind velocities (m/sec), substrate temperature (Ts, 1C) and air 1 3 temperature (Ta, C). Values shown are mean, +/ standard error, (sample size), and range. 69

Altitude Humidity Luminosity Environmental character 5 71 Wind Substrate temperature Air temperature 7 73 High 27.3671.53 (21) 18.7–46.1 1131.57103.6 (30) 226–2200 1.9570.37 (28) 0–7.1 24.970.9 (28) 11.5–46.0 22.871.0 (28) 14.3–37.2 Low 29.0771.41 (33) 18.7–55.5 1232.9798.6 (33) 230–2900 1.7370.35 (33) 0–7.0 26.170.9(32) 15.7–38.6 23.270.9(24) 16.6–36.0 9 75

11 77

13 Table 2 79 Thermal statistics for each site. Values shown are mean, +/ standard error, or median and (sample size). Ranges are also shown for body temperature (Tb) and operative temperature (T ). Other measures shown are preferred body temperature (T ), index of the average thermal quality of a habitat from an organism’s perspective (d ), and 15 e p e 81 individual deviation of Tb from Tset (db). All temperatures are in 1C.

17 Altitude Tb Te Tp de db 83

High 28.970.8 (30) (22.7–37.0) 24.9 (44) (20.6–37.9) 36.270.4 (27) 9.47 (40) 5.670.8 (27) 19 85 Low 32.670.9 (33) (22.3–43.5) 31.3 (77) (17.7–59.5) 35.670.5 (30) 5.20 (77) 6.571.0 (30)

21 87

23 89

7 25 A. High Altitude 91 Te =24.9 (44)

27 6 93

29 95 5 31 97 4 33 99

3 35 101

T 37 2 p 103

39 105 1 T b 41 107 0 43 22 24 26 28 30 32 34 36 38 40 42 44 109 7 45 Te = 31.3 (77) B. Low Altitude 111

47 6 113 Number of observations 49 5 115

51 119 4 53 121 3 55 123

T 57 2 p 125

59 1 127 Tb 61 129 0 22 24 26 28 30 32 34 36 38 40 42 44 63 Body temperature (ºC) 131 65 133 Fig. 3. Frequency of body temperature (Tb, bars) of lizards from high (panel A) and low altitude (panel B) sites. The arrows indicate mean Tb and Tp and the vertical lines

indicate the lower and upper set-point of the Tp (dashed lines) and the median of operative temperature (solid line, Te).

Please cite this article as: Gutie´rrez, J., et al., Effect of altitude on thermal responses of Liolaemus pictus argentinus in Argentina. J. Thermal Biol. (2010), doi:10.1016/j.jtherbio.2010.07.001 J. Gutie´rrez et al. / Journal of Thermal Biology ] (]]]]) ]]]–]]] 5

1 the Tb (Mann–Whitney, T1,110¼1884.5, P40.73, median Our analysis of microenvironmental temperatures and Tb 67 Te¼31.3 1C, median Tb¼32.7 1C; Table 2). shows that this species gains heat mainly through solar radiation 3 and loses heat passively by conduction and convection, evidence 69 of their heliothermic character, and this corroborates the results 3.4. Preferred temperatures in the laboratory (Tp) 5 obtained by Ibarguengoytı¨ á and Cussac (2002; Fig. 2). The lower 71 body temperatures we observed at high altitude were likely At high altitude, T ranginge from 31.5 to 39.1 1C, was 7 p caused by shady conditions under the closed forest canopy. On 73 significantly larger than Tb (paired t-test, t26¼11.15, Po0.0001). the other hand, at the low altitude beach, although less protected At low altitude, the range of T varied from 32.6 to 39.3 1C and 9 p from the wind, lizards usually had sun-lit conditions and rocky 75 was significantly greater than T (paired t-test, t ¼3.73, b 29 microenvironments and thus a greater thermal inertia. These Po0.001). The Tp values were not different between sites 11 conditions apparently allowed lizards to maintain higher body 77 (Mann–Whitney, T ¼825, P40.51), and did not differ between 1,57 temperatures and to lose less heat by conduction. This difference localities within groups of males, females, or juveniles (Kruskal– 13 could also be explained by differences in ambient temperature 79 Wallis, H ¼1.47, P40.48). High altitude set points were 2,57 between the two sites. 34.370.7 and 38.270.3 1C while the low altitude set points 15 The T values at the high altitude site were similar to that of 81 were 34.670.6 and 38.070.3 1C(Fig. 3; Table 2). b other Patagonian lizards from similar latitudes in the steppe 17 environment such as L. bibronii (28 1C 43.01; Medina et al., 2009) 83 3.5. Individual deviation values (db), index of mean thermal quality and L. elongatus (29.8 1C, 41.61; Norusis,ˇ 1986). In contrast the 19 of the habitat (de), and effectiveness of thermoregulation (E) body temperatures of lizards at the low-latitude site were similar 85 to that of L. elongatus and L. p. argentinus (33.2 1C) obtained on the

21 The individual deviation values (db) were 5.670.8 (N¼27) at shore of Moreno Lake (Ibarguengoytı¨ ´a and Cussac, 2002) and with 87 high altitude and 6.571.0 (N¼30) at low altitude. The individual those of Liolaemus wiegmannii (32–36 1C; Martori et al., 1998) and

23 deviation values (db) were not signiﬁcantly different between Liolaemus koslowskyi (34.8 1C; Martori et al., 2002), which inhabit 89 sites (t-Student, t55¼1.83, P40.07). Nevertheless, 81% of the Tb warmer environments at lower latitudes in Rio Cuarto in the 25 values at high altitude were lower than the lower set-point, while Province of Cordoba, and on the plains of Monte de Anillaco in 91

73% of the Tb values at low altitude were greater than the La Rioja, respectively. 27 upper set-point. The range of body temperatures during activity in the ﬁeld can 93

The index of mean thermal quality of the habitat (de) was vary according to body mass and size and shape of the body 29 9.5 (N¼40) in the high altitude site and 5.2 (N¼77) in the low (Christian, 1998) and also according to reproductive conditions 95

altitude site. Most of the Te values at high altitude (97.5%) were (Smith and Ballinger, 1994). Many studies of lizard thermoregula-

31 lower than the lower set-point. But, this was true only for 62.4% of tion show Tb values outside of the set-point temperatures in their 97 the Te values at low altitude. In addition, some low altitude values natural environment due to different factors such as the presence 33 (24.6%) were greater than the upper set-point. The values of de of predators, low availability of thermal microenvironments, or 99 were significantly greater at high altitude (Mann–Whitney, restrictions imposed by sociality or stage of reproduction (Hertz 35 T1,117¼2850, Po0.005; medianhigh¼9.5 1C and medianlow¼ et al., 1983; Autumn and De Nardo, 1995). Thermoregulation in 101 5.2 1C). The E values were 0.404 and 0.242 at high and low many occasions may be effective, but lizards that move between 37 altitude, respectively. sun and shade use energy in locomotion, which otherwise could 103 be used for reproduction, growth, or other functions (Huey and 39 Slatkin, 1976). Consequently, the most adaptive thermoregulatory 105 4. Discussion behavior may not result in the best match between body 41 temperature and preferred temperature. Instead, for example, 107 Monthly mean air temperatures and operative temperatures at passive thermoregulation in lizards that inhabit cold climates or 43 the high-elevation site, in the Nothofagus forest near the summit shady forests can be from time to time more beneficial than an 109 of Challhuaco Mountain, were lower than those at the low- active or very precise thermoregulation (Huey and Slatkin, 1976). 45 elevation site (Fig. 1). Although from April to August the We measured preferred temperatures that were significantly 111

temperature is low at both sites, at high altitude the lower warmer than Tb values at the time of capture, probably due to a 47 temperatures last until October, leaving the lizards inactive in scarcity of thermal microenvironments that could be used to 113

their burrows under the snow, while at the beach the mean obtain high temperatures in the wild. Nevertheless, Tp values 49 temperature in September was 4 1C and lizards were active in the were not different between the two populations (36 1C). The 115 warmest part of the day. Nevertheless, the mean temperatures, preferred temperatures we observed were similar to a report for 51 from mid-November to mid-January were warmer at high Liolaemus (34–36 1C); Labra, 1998) and others (Medina et al., 119 altitude, possibly due to greater radiation there and due to the 2009; 30–37 1C), suggesting conservation of this character within 53 buffering effect of water at the beach (Koeppen, 1948). the species and the genus (Labra, 1998). The latter study also 121

Lizards take advantage of thermal resources through thermo- found strong evidence for a phylogenetic effect on Tp, while Tb 55 regulatory behavior (Randall et al., 1997) and differences in seems to be the result of adaptation to the local temperature and 123 behaviors and activity periods have been observed along climate (Labra, 1998; Labra et al., 2009). 57 latitudinal (Medina et al., 2009) and altitudinal gradients (Hertz The availability of favorable microenvironments can be 125

et al., 1983). However, optimal thermoregulation may trade off indicated by Te and by the difference between operative 59 with costs in feeding rate, reproductive activity, and predation temperatures and the set-point of preferred temperatures 127

risk. We observed lower activity temperatures at high elevation determined in the laboratory (de). Operative temperatures were 61 (29 1C compared with 33 1C), which may be explained by lower (median Te ¼24.9 1C) and the de was greater (median 129 differences in ambient temperature between the two sites. A de¼9.5 1C) at high altitude compared with low altitude (median 63 similar pattern was observed in Agama savignyi and Stellio stellio Te¼31.3 1C, median de ¼5.2 1C), indicating lower availability 131 from Israel (Hertz et al., 1983) and in the genus Sceloporus, whose of thermal environments on the mountain. These high de 65 mean body temperatures in tropical latitudes decrease with values were similar to those found for the steppe lizard 133

altitude from 35 to 31 1C(Andrews, 1998). L. bibronii (de¼8.4–10.9 1C; Medina et al., 2009) but much greater

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1 than those found for Anolis populations in tropical climates Bauwens, D., Hertz, P.E., Castilla, A.M., 1996. Thermoregulation in a lacertid lizard: the relative contributions of distinct behavioral mechanisms. Ecology 77, (de ¼0.1–9.2 1C; Sinervo et al., 2010), Podarcis hispanica atrata 65 1 1818–1830. 3 (de ¼6.3 C; Bauwens et al., 1996), and for the genus Cei, J.M., 1986. Reptiles del Centro, Centro-oeste y sur de la Argentina. 67 Varanus (de¼2–8 1C; Christian and Weavers, 1996), likely the Herpetofauna de las Zonas Aridas y Semia´ridas. Museo Regionale di Scienze 5 result of the rigors of living in the cold microenvironments in Naturali, Monografia IV, Torino. 69 Christian, K.A., 1998. Thermoregulation by the short-horned lizard Phrystosoma Patagonia. duglassi at high elevation. J. Therm Biol. 23, 395–399. 7 Likewise, db values indicate the difference between field body Christian, K.A., Weavers, B.W., 1996. Thermoregulation of monitor Lizard in 71 temperatures and those preferred in the laboratory. The lower Austria: an evaluation of methods in thermal biology. Ecol. Monogr. 66 (2), 9 and upper set-points in both localities were similar and no 139–157. 73 Donoso-Barros, R., 1966. Reptiles de Chile. Ediciones de la Universidad de Chile, significant differences were found in db. Nevertheless, because Santiago de Chile. 11 body temperatures were mostly below the set-point range at high Firth, B.T., Turner, J.S., 1982. Sensory, neural, and hormonal aspects of thermo- 75 altitude but above the set-point range at low altitude (Fig. 3), we regulation. In: Gans, C., Pough, F.H. (Eds.), Biology of the Reptilia, vol. 12: Physiology C, Physiological and Ecology. Academic Press, New York, pp. 13 conclude that the forested mountain environment provides little 213–274. 77 opportunity for thermoregulation (high de). In contrast, the Tb of Gutie´rrez, J., 2009. 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Rev. 21 as predators), thereby placing themselves in microenvironments Biol. 51, 363–384. 85 Ibarguengoytı¨ á, N.R., Cussac, V.E., 2002. Body temperatures of two viviparous that are thermally suboptimal (Fig. 3). Liolaemus lizard species, in Patagonia rain forest and steppe. .Herpetol J. 12, 23 Efficiency in the regulation of temperature, indicated by E, 131–134. 87 characterizes L. p. argentinus as a moderate thermoregulator at Ibarguengoytı¨ á, N.R., 2005. Field, selected body temperature, and thermal 25 high altitude (E¼0.4) and more as a thermoconformer at low tolerance of the syntopic lizards Phymaturus patagonicus and Liolaemus 89 elongatus (Iguania: Liolaemidae). J. Arid Environ. 62, 73–86. altitude (E¼0.24). In the former case, it appears that a lack of Ibarguengoytı¨ á, N.R., Acosta, J.C., Boretto, J.M., Villavisencio, H.J., Marinero, J.A., 27 suitable thermal microenvironments prevents the attainment of Krenz, J.D., 2008. 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Please cite this article as: Gutie´rrez, J., et al., Effect of altitude on thermal responses of Liolaemus pictus argentinus in Argentina. J. Thermal Biol. (2010), doi:10.1016/j.jtherbio.2010.07.001