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

ARTICLE IN PRESS Journal of Arid Environments 72 (2008) 1620– 1630

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Field thermal biology in Phymaturus lizards: Comparisons from the Andes to the Patagonian steppe in Argentina N.R. Ibargu¨engoytı´a 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 zoologı´a, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, Unidad Postal Universidad del Comahue, San Carlos de Bariloche, 8400 Rı´o Negro, Argentina b Consejo Nacional de investigaciones Cientı´ficas y Te´cnicas (CONICET), Argentina c Departamento de Biologı´a e Instituto y Museo de Ciencias Naturales, Facultad de Ciencias Exactas, Fı´sicas y Naturales, Universidad Nacional de San Juan, San Juan, Argentina d Department of Biological Sciences, Minnesota State University, Mankato, MN 56001, USA

a r t i c l e i n f o

abstract

Article history: Received 8 August 2007 Received in revised form 2 February 2008 Accepted 28 March 2008 Available online 27 May 2008

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.

Keywords: Bioenergetics Liolaemidae Reproduction Thermophysiology Thigmothermy

1. Introduction Thermal relations with the environment profoundly affect almost every aspect of an ectotherm’s life. Microhabitat selection and thermoregulatory behaviour are closely related and strongly influence lizard life histories by affecting body temperatures 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 of the major environmental factors that changes with elevation and latitude. Thus, an understanding of the effects of the thermal environment on individuals along an elevational and latitudinal gradient may aid in the explanation of geographic

 Corresponding author at: Departamento de zoologı´a, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, Unidad Postal Universidad del Comahue, San Carlos de Bariloche, 8400 Rı´o Negro, Argentina. Tel.: +54 2944 428505; fax: +54 2944 422111. E-mail addresses: [email protected] (N.R. Ibargu¨engoytı´a), [email protected] (J.C. Acosta), [email protected] (J.D. Krenz).

0140-1963/$ - see front matter & 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jaridenv.2008.03.018

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differences in life history (Beaupre, 1995). The role of habitat and microhabitat use in lizards is crucial to anticipate the potential 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 of activities an animal may engage in, but there are other factors influencing whether an animal chooses to be active. For example, the trade-offs among the availability of heat sources, the interactions with competitors, and the threat of predation (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 not likely to be found, especially if the numerous trade-offs that result from the existence of competing bioenergetic functions and the interactions of individuals with their environment are considered (Sears, 2005). For example, ectotherms living at high latitudes or altitudes face great physical challenges because of seasonal extremes in climate and they have adapted to long cold winters and short summer breeding seasons (Andrews, 1998; Ibargu¨engoytı´a and Casalins, 2007; Spellerberg, 1976). Nevertheless, lizards living at high elevations, where solar radiation can be more intense, often are able to behaviourally 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 crevices where they spend much of their time during the activity season (Cei, 1986, 1993). Phymaturus is distributed in the highlands of the Andes, in the volcanic plateaus of Patagonia, from Catamarca to the southern border of Chubut in Argentina, and is present on the Chilean side of the Andes. These species are restricted to arid and semi-arid ecosystems in Argentina that include several different habitats characterized by cold and snowy winters (Vuille and Ammann, 1997), such as the Monte Desert of central Argentina, the Patagonian steppes, the Chaco xeric woodlands, and the Andean Puna ˜ ent et al., 2006). In these environments, lizards are limited by high annual and daily thermal (Cei, 1986; Roig-Jun amplitudes, 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 physiological performance is dependent upon availability of suitable microhabitats. For instance, geographic variation in the thermal environment 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 (Ibargu¨engoytı´a, 2004; see Lobo and Quinteros, 2005), Phymaturus antofagastensis, (Boretto and Ibargu¨engoyı´a, 2006) and Phymaturus punae (Boretto et al., 2007) show biennial female reproductive cycles and are herbivorous (Cei, 1986; Espinoza et al., 2004). But, Phymaturus zapalensis—an omnivore—is the only species that can perform an annual cycle (J.M. Boretto and N.R. Ibargu¨engoytı´a, unpublished data). However, previous data on the thermal biology of the genus Phymaturus is limited to only the field and preferred body temperatures of P. vociferator (Labra and Vidal, 2003) and P. tenebrosus (Ibargu¨engoytı´a, 2005). Both species are mainly thigmothermic, with mean body temperatures (Tb) during activity being lower than preferred body temperatures (Tp; P. vociferator mean Tb ¼ 22.5 1C; mean Tp ¼ 35.8 1C, Labra and Vidal, 2003; P. tenebrosus mean Tb ¼ 28.95 1C, mean Tp ¼ 31.13 1C, Ibargu¨engoytı´a, 2005). Previous studies on Phymaturus have suggested that the low environmental temperatures throughout the year and the short activity seasons lengthen reproductive cycles (Ibargu¨engoytı´a and Casalins, 2007), decrease growth rate, delay sexual maturity, and decrease fecundity (Piantoni et al., 2006a). Herein, we compare field body and microenvironmental temperatures 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, microenvironmental temperature, body size and mass, reproductive condition, and sex. Finally, we explore the balance among body temperature, 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 the northern edge of San Juan Province, Argentina (281590 –291020 S; 691290 –691050 W, 3100–4200 m elevation) during two periods (5–9 December 2004 and 7–12 February 2005), (2) P. zapalensis (N ¼ 64) collected in the proximity of the National Park Laguna Blanca, Zapala, Neuque´n Province, Argentina (391440 S and 701220 W, 824–1312 m elevation) from September to March (2004–2007), and (3) P. tenebrosus (N ¼ 32) captured in the Patagonian steppe, in La Fragua, Pilcaniyeu, Rı´o Negro province, Argentina (41–41.51S and 70.5–71.41W, 926–1000 m elevation) from November to March (2000–2005). Some of P. tenebrosus specimens (N ¼ 21) were captured previously for another study (Ibargu¨engoytı´a, 2005) and were used in the present study for comparison purposes. The lizards were captured by hand or loop from 9 to 20 h. 2.2. Study area ˜ a and Altoandina phytogeographic provinces in P. punae inhabits the Provincial Reserve San Guillermo, within the Punen the 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 as Stipa 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 Blanca Lagoon can be partially frozen during winter and the mean annual precipitation is 176 mm (Cabrera, 1976). The landscape is characterized 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 the Subandino District, characterized by having the coldest and most humid climates of the phyto-geographic province, and a mean annual precipitation ranging from 200 to 350 mm (Cabrera, 1976). The vegetation is represented principally by Festuca 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, Argentinean Air Force, the Secretary of Mining of the San Juan Government, and the Laguna Blanca National Park. The photoperiod data were obtained from the Argentinean Manual for pilots (Direccio´n de Tra´nsito Ae´reo, 1991). The air temperatures of Laguna Blanca were corrected for differences in altitude (6 1C km1; Ferna´ndez-Garcı´a, 1996) from temperatures obtained at the Neuque´n 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 1302 thermometer (TES Electrical Electronic Corporation, Taipei, Taiwan, 70.01 1C). Luminescence (luximeter Extech model 401025, 7lux) and wind speed (Turbo meter, 70.1 m s1) were also recorded in the microenvironments of P. zapalensis and P. tenebrosus when lizards were found outside the rock crevices. The substratum and air temperature 1 cm above the ground of P. punae microenvironments were recorded using a fast-reading thermometer (Miller–Weber; 70.1 1C). Date and time 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 (in P. zapalensis and P. tenebrosus), or a Miller–Weber fast-reading thermometer (in P. punae) introduced ca. 1 cm inside the cloaca. 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 inside the 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 features following Boretto and Ibargu¨engoytı´a (unpublished data), Boretto et al. (2007), and Ibargu¨engoytı´a (2004). Lizards were killed for further research in reproductive biology (see Boretto et al., 2007; Ibargu¨engoytı´a, 2004; Boretto and Ibargu¨engoytı´a, unpublished data) by intraperitoneal administration of sodium thiopental, fixed in Bouin’s solution for 24 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, Fı´sicas 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 differences tests were conducted. Normality and variance-homogeneity assumptions were tested using the Kolmogorov–Smirnov and Levene tests, respectively. When normality or variance-homogeneity assumptions were violated, non-parametric tests were 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. In P. punae, adult males were significantly larger than females (t-test, t35 ¼ 3.22, Po0.003). The frequency of tails cut or regenerated 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) or in 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 damage did not show inter-specific differences (w2, w22 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. punaeP. zapalensis ¼ 9.17; QP. punaeP. 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. ZP. punae– P. zapalensis,241 ¼ 3.96; punaeP. tenebrosus, 240 ¼ 3.92; ZP. zapalensisP. 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 h1, medianP. zapalensis ¼ 18.81 km h1, and medianP. tenebrosus ¼ 19.67 km h1). 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 used inside the rock crevices (P. punae: t-student, t T s ;46 ¼ 5.37; t T a ;46 ¼ 6.01, Po0.001; P. zapalensis: Mann–Whitney, T T s ;63 ¼ 1114.50, T T a ;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 three species. In P. punae’s microenvironments the Ta and Ts showed a significant relationship with time (regression, OUT: F T a ;1;33 ¼ 7.57, F T s ;1;33 ¼ 5:01, Po0.02; IN: F T a ;1;13 ¼ 19:21, F T s ;1;13 ¼ 24:37, Po0.001). But, the capture date (December and Table 1 Mean7SE 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

Phymaturus punae Females Males Juveniles Overall

91.1271.30 98.0571.62 63.7373.02 87.7072.22

Phymaturus zapalensis Females Males Juveniles Overall Phymaturus tenebrosus Females Males Juveniles Overall

Range

N

Body mass

Range

N

80–100 85–114 52–80 52–114

17 20 11 48

– – – –

– – – –

– – – –

88.62 82.11 70.89 80.9071.41

79.02–95.72 72.64–90.05 58.52–82.86 58.52–95.72

20 22 14 56

24.75 21.00 12.50 20.3270.85

17–37 17.5–27 6–22 6–37

17 21 13 51

94.76 94.86 7.75 93.7571.73

80.7–110.32 88.64–98.42 69.38–77.17 69.38–110.32

18 11 3 32

31.3572.08 31.0071.32 10.00 29.2971.62

16–48 24–38 9–15 9–48

17 11 3 31

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Table 2 Mean7SE 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 seg1) of Phymaturus punae, Phymaturus zapalensis, and Phymaturus tenebrosus outside (OUT) and inside (IN) the rock crevices Tb Female

Ts

Ta

Solar radiation

Wind Speed

– –

– –

Male

Juvenile

Overall

Phymaturus punae OUT 27.6471.06 (10) IN 16.7572.36 (7)

29.7570.54 (16) 20.0072.73 (4)

31.0270.84 (8) 22.8072.68 (3)

29.4570.48 (34) 18.9771.57 (14)

28 (34) 17.5171.82 (14)

25 (34) 16.5171.22 (14)

Phymaturus zapalensis OUT 25.6071.35 (10) IN 16.9672.45 (11)

27.6172.37 (8) 16.1271.27 (21)

26.0472.55 (5) 14.1172.08 (9)

26.4071.11 (23) 15.9071.01 (41)

27.3771.11 (23) 18 (40)

24.7771.01 (20) 18 (22)

1177745.70 (15) 893 (28)

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)

1.5670.30 (15) 1.10 (23)

0.45 (20)

February) did not influence Ta or Ts (OUT: Mann–Whitney, T T a ¼ 181, T T s ¼ 219, N ¼ 34, P40.1; IN: ANCOVA, F T a ;1;14 ¼ 3.07, F T s ;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 date or time (stepwise regression, F T s ;2;22 ¼ 0:72, F T a ;2;19 ¼ 0:31, P40.5). Inside the rock crevices Ta did not vary with date or time (F T a ;2;21 ¼ 1:11, P40.35), and Ts varied significantly only with date (stepwise regression, F T s ;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 date or time (regression, F T s ;2;26 ¼ 1:86, P40.17), but Ta showed a significant relationship with date (F T a ;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 median wind 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 show differences in Ta or in Ts (Mann–Whitney, T T a ¼ 227:50, N ¼ 36; T T s 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 whether outside or inside rock crevices (t-test, tout,32 ¼ 0.22; tIN,12 ¼ 1.43; P40.17). Consequently, data of both capture dates were pooled 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 (stepwise regression, 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 was significantly higher than Ta and Ts (paired t-student, t T b T a ;33 ¼ 8:032, t T b T s ;33 ¼ 3:015, Po0.005). In contrast, the Tb of lizards inside rock crevices was significantly higher than Ta but not significantly different from Ts (paired t-student, t T b T a ;13 ¼ 3:85, Po0.002; t T b T s ;13 ¼ 2:168, P40.049). Comparisons of Tb among males, females, and juveniles of active individuals were significantly different only between females 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 rock crevices did not show differences among males, females and juveniles (ANOVA, F2,13 ¼ 1.236, P40.328). A coloration shift was observed between lizards found in and out of rock crevices. The latter were lighter and bright green, and there was an intense 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 (stepwise regression, 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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1625

40 35

P. punae

30 25 20 15 10 5 0 40

30 P. zapalensis

Body temperature (°C)

35

25 20 15 10 5 0 40 35

P. tenebrosus

30 25 20 15 10 5 0 8

10

12

14 Time (h)

16

18

20

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.

There were no differences between Tb and Ts or Ta for lizards outside (paired t-test, t T s ;22 ¼ 1:30, t T a ;19 ¼ 2:17, P40.05), or inside rock crevices (paired t-test, t T s ;39 ¼ 2:28, t T a ;21 ¼ 1:20, P40.05). The Tb showed a significant relationship only with Ts (stepwise regression, FOUT: 1,19 ¼ 18.98; FIN: 1,21 ¼ 65.36, Po0.0001). In lizards outside rock crevices there were not significant 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 as the only significant covariable in the model (ANCOVA, F2,40 ¼ 0.49, Po0.62).

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1626

50 45

P. punae

40 35 30 25 20 15 10

45 40 P. zapalensis

Body temperature (°C)

50

35 30 25 20 15 10 50 45

P. tenebrosus

40 35 30 25 20 15 10 10

15

20

25

30

35

40

Substrate temperature (°C)

45

50

10

20

30

40

50

Air temperature (°C)

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.

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). The Tb was higher than Ta (pair t-test, t T a ;22 ¼ 4:44, Po0.001) but was not different from Ts (t T s ;20 ¼ 0:56, P40.58). There was a significant relationship only between Tb and Ts (regression, F1,16 ¼ 18.66, Po0.001), but not between Tb and Ta, wind or solar radiation (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 each species (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 in P. 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 differences considering date and time as significant covariables in the model (ANCOVA, F1,54 ¼ 1.47, Po0.23).

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40

1627

(28) (23)

(34)

Body temperature (°C)

35

30

25

20

15

10 20 (40) Residuals (Tb vs date and time)

15 10 (14) 5 0 -5 -10 -15

nae

u P. p

s

s

nsi

ale

ap P. z

osu ebr

en P. t

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.

4. Discussion and conclusions Geographic variation in thermal environment caused by altitude and latitude may produce variation in the availability of thermally suitable microhabitats necessary for the achievement and maintenance of body temperature within a range that 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 and habits. The three species follow the air and substrate temperatures when they are inside the rock crevices, but they show paradoxical results when they are outside the rock crevices. For example, in a high-altitude site, P. punae experience the lowest air temperatures, and they have the lowest Tb when inside the rock crevices, but they have the highest Tb outside the rock crevices compared to P. zapalensis (Fig. 3). The three species each seem to be using predominately either heliothermy or thigmothermy, a decision strongly influenced by the local environment. In this way, P. punae, because of the greater 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 the intermediate latitude and altitude, are usually inside the rock crevices and show the lowest Tb (Figs. 1 and 3). This difference seems paradoxical, but generalizations for patterns of geographic variation in life histories of lizards are not likely to be found, especially if the numerous trade-offs that result from the interactions of individuals with their environment are considered (Sears, 2005). Thermal environment is not a strict determinant of microhabitat use by lizards, since all substrates afford suitable microclimates at least some of the time. However, substrates differ in the abundance and accessibility of microclimates that would facilitate precise thermoregulation (Adolph, 1990). Lizards often choose habitats and microhabitats that allow them 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 only microenvironmental 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 outside the rock crevices, were much higher than those experienced when they are inside the rock crevices. Inside the rock crevices the lizards were behaving as thermo-conformers; body temperatures of lizards in retreats followed the environmental temperatures, showing a stronger correlation with the rock surface temperatures than the air temperatures and increasing during the warmer hours of the day. However, outside the rock crevices, the correlation of body temperature with the microenvironmental 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 that the definitive determination of thermoregulation requires either (1) the use of null hypotheses generated using metal lizard 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 by basking while flattening their bodies to maximize their surface area for the absorption of solar radiation and to contact the substrate surface to maximize the conduction of heat from the substrate and to minimize convective heat loss, as has been reported for the horned lizard Phrynosoma douglassi (Christian, 1998). The relationship of Tb with time of day inside the rock crevices, but not outside, suggests thermoregulation (Fig. 1). These results are in agreement with the colouration shifts observed in P. punae but not in P. zapalensis or P. tenebrosus. Greater melanism in the inactive individuals would help them to capture the sun-light that enters in the rock crevices, while the shift toward lighter, less-absorptive colours during activity would allow them to reflect more radiation at high altitude. The body shifts in body melanism have been recorded in 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 behaviour is considered an important strategy for lizards at high elevation (Navas, 2003). P. zapalensis and P. tenebrosus are mainly thigmothermic species (Ibargu¨engoytı´a, 2005; and present results). Body temperatures of these species are influenced mainly by rock temperature, which was the most constant environmental variable during the day and throughout the activity season. Nevertheless, a correlation of body and environmental temperatures in P. zapalensis, throughout the season and time of the day, showed more limitations for thermoregulation in this species than in P. tenebrosus (Ibargu¨engoytı´a, 2005; and present results, Fig. 2) and in P. punae. In active individuals, the lowest Ta and Ts associated with P. zapalensis was 17 and 20 1C, respectively, with a Tb of 19 1C, while in P. tenebrosus the lowest 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 strong correlation of environmental temperatures and Tb in P. zapalensis may arise through the lack of opportunity or willingness to bask or behaviourally elevate body temperatures above environmental temperatures as has been observed in the crevice-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 (371200 S and 711180 W, 1700 m; Labra and Vidal, 2003). We discarded the hypothesis of lower temperatures in P. zapalensis as an effect of predator avoidance because the proportion of individuals with tail damage did not differ among the three species. However, variation in the frequency of tail 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 velocities cause 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, being outside 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 the selection of the body temperatures of the species (Tracy and Christian, 1986). Espinoza et al. (2004) show that most herbivorous liolaemids occur in regions that are much cooler than those inhabited by other herbivorous reptiles, but they nevertheless also need the high body temperatures required by other herbivorous lizards. Accordingly, we found that P. punae and P. tenebrosus, although inhabiting harsher environments at higher altitudes and latitudes, respectively, than P. zapalensis, are strictly herbivorous and P. punae has higher body temperature. In contrast, even though the genus Phymaturus has been considered entirely herbivorous, a view supported by our observations of strict herbivory in captive P. punae and P. tenebrosus, P. zapalensis has been observed in captivity to behave omnivorously by eating insects in addition to leaves and flowers (J.M. Boretto and N. R. Ibargu¨engoytı´a, unpublished data). In some environments, ectotherms must at times forgo surface activity because thermally suitable microhabitats are not available. For terrestrially foraging reptiles, thermal constraints on surface use may limit food harvesting by reducing available 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 the crevices to feed. Furthermore, herbivorous reptiles have a particular problem assimilating energy from their food. Plant material is less energy-dense than the food of carnivorous lizards and digestion of plant material is a slower, temperaturedependent 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 temperatures or an ancestral trait remains to be elucidated, but its absence among congeners would suggest a recent derivation. The amount of energy available for growth and reproduction is related to the difference between harvested energy and the sum of resting metabolism and activity costs (Beaupre, 1995). In this study we found a paradoxical result in the relationship between reproduction and field body temperatures. Sex, reproductive state, size and body mass have been shown to alter the temperature relationships of lizards (Mathies and Andrews, 1997; Smith and Ballinger, 1995). Nevertheless, we did not find a relationship among these variables, except in a higher Tb in juvenile P. punae compared with females. This is probably the result of a combination of body mass and different habits as is the case for other liolaemids (Carothers et al., 1998) and Lacerta monticola from high altitudes (Carrascal et al., 1992). Low body temperatures in Sceloporus at high elevations in the tropics are correlated with impaired performances in locomotion, digestion, and other physiological attributes such as a protraction in the reproductive cycles (Andrews, 1998; Me´ndez-de la Cruz et al., 1998). In addition, animals living in more-variable environments may have sharply reduced reproductive fitness when habitat quality is low (Martı´n and Lo´pez, 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 been shown to be biennial, conducting vitellogenesis for 10–12 months followed by 4–5 months of pregnancy during the next activity season (Boretto and Ibargu¨engoyı´a, 2006; Boretto et al., 2007; Ibargu¨engoytı´a, 2004). In contrast, P. zapalensis, despite having low body temperature, is the only congener that can complete the reproductive cycle in 1 year, although they often skip years, probably caused by limitations on the ability to store fat reserves (Boretto and N.R. Ibargu¨engoytı´a, unpublished data). The three species in this study hibernate during winter and during the activity season they have similar body temperatures and use similar microenvironmental retreats. However, the observations that P. zapalensis spends more time in rock crevices and has lower body temperatures suggest that lizards might face the trade-off between the risk of predation and having to endure thermal extremes by remaining either exposed or in retreats. P. zapalensis seems to cope with these constraints by exploiting a longer activity season, and by having higher plasticity. P. zapalensis is more eurithermic, being active over a broader range of temperatures, and has an omnivorous diet that allows it to acquire more energy 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-Martı´nez families ˜ ez for serving as guides in for assistance in the fieldwork. We also want to extend thanks to A. Carrizo and A. Montan Provincial Reserve San Guillermo and to the National Meteorological Service, Argentinean Air Force and the Laguna Blanca National Park for providing climate data. This work was partially supported by Universidad Nacional del Comahue and CONICET PIP5625. Appendix A Mean air temperatures vs. month at the collection sites of P. punae (circles and solid line), P. zapalensis (triangles and dotted 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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