Selected Body Temperature and Thermoregulatory Behavior in the Sit-And-Wait Foraging Lizard Pseudocordylus Melanotus Melanotus

Herpetological Monographs, 23 2009, 108–122 E 2009 by The Herpetologists’ League, Inc.

SELECTED BODY TEMPERATURE AND THERMOREGULATORY BEHAVIOR IN THE SIT-AND-WAIT FORAGING LIZARD PSEUDOCORDYLUS MELANOTUS MELANOTUS

1,2 SUZANNE MCCONNACHIE ,GRAHAM J. ALEXANDER, AND MARTIN J. WHITING School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Private Bag 3, Wits, 2050, South Africa

ABSTRACT: We investigated the thermoregulatory abilities and behavior of Pseudocordylus melanotus melanotus (Drakensberg crag lizard) in terms of the relationship between the operative temperature (Te), selected temperature (Tsel), set-point range (Tset) and field active body temperature (field Tsel), exposure to low temperature, body posture and activity. The Te range for P. m. melanotus was about 58 C (23.20 C in winter to 54.94 C in summer). In a laboratory thermal gradient, in a setting that is independent of ecological costs or thermal constraints, lizards maintained Tset (defined as the interquartile range of Tsel, after Hertz et al., 1993) between 29.00 6 0.36 C and 31.78 6 0.16 C in winter and 29.61 6 0.28 C and 32.47 6 0.18 C in summer. The mean Tsel was 30.08 6 0.14 C in winter and 30.99 6 0.11 C in summer. In the field, however, lizards achieved significantly lower Tb, which suggests that the thermal environment limited the Tb that lizards were able to achieve. Lizards were active for significantly longer and selected significantly higher Tb in summer than in winter. During winter, lizards spent a significant amount of time at Tb below their lower critical limiting temperature (defined by loss of righting). The most frequently assumed body postures in summer were those where the head or body were raised, whereas, in winter, lizards usually lay with head and body flat on the rock substrate. We suggest that these differences reflect the physiological requirements of the lizards: Head-up postures in sit-and-wait foragers are consistent with scanning for prey while head-down postures are likely motivated by thermoregulatory needs. It is clear that P. m. melanotus can thermoregulate efficiently, but the Tb maintained may be constrained by the range of Te available to the lizards in their natural environment. Pseudocordylus m. melanotus currently appears to be geographically constrained by low environmental temperatures at the edge of its range. Should global warming become a reality in southern Africa, this species could inadvertently benefit by occupying new habitat that was previously unavailable because of thermal constraints. Key words: Lizard; Operative temperature; Pseudocordylus; Selected temperature; Set-point range; Sit- and-wait forager; Thermoregulation; Thermoregulatory behavior.

CAREFUL regulation of body temperature activity times (Huey, 1974). The Tb of lizards (Tb) reduces the risk of exposure to extreme is thus dependent on both the variation in temperatures that may be lethal, and also environmental temperature and on their increases the duration spent at physiologically ability to regulate heat exchange (Beck, favorable Tb (Huey et al., 1989). Physiological 1996; Carrascal et al., 1992; De Witt, 1967; benefits are maximized in an ideal environ- Peterson, 1987; Tosini et al., 1992). ment where there are few or no environmen- Many diurnal heliothermic lizards are able tal constraints, and lizards will usually select to regulate Tb at high levels if they bask in optimal Tb when active (Huey and Slatkin, sunlight during the day (Bennett, 1980). The 1976). In natural settings, however, the range of Tb selected (Tsel) is generally thermal environment is heterogeneous and considered to be the range at which the lizard lizards thermoregulate by shuttling between can most effectively capture prey, escape hot and cold microclimates (or between predators, dig nest holes, engage in social sunlight and shade), through posture modifi- behavior or undertake any energetically de- cations (such that the surface area exposed to manding activity (Bartholomew, 1977), and heat sources is altered) and by regulating usually refers to the Tb adopted in laboratory thermal gradients. Hertz et al. (1993) suggest

1 that estimates of the upper and lower set PRESENT ADDRESS: School of Biological and Conser- points for T should be taken as the vation Sciences, University of KwaZulu-Natal, Private Bag sel X01, Scottsville, 3209, South Africa temperatures representing the interquartile 2 CORRESPONDENCE: e-mail, [email protected] range (mid-50% of observed selected temper-

108 2009] HERPETOLOGICAL MONOGRAPHS 109 atures; set-point range; Tset). The Tb selected determined by air and substrate temperature, has also been shown to be affected by which limits thermoregulatory options (Adolph numerous factors (Huey, 1982) including and Porter, 1993). reproductive condition (Andrews et al., 1997; Diurnal lizards tend to be more active Beuchat, 1986; Gibbons and Semlitsch, 1987; during times when environmental tempera- Rock et al., 2000; Rock et al., 2002; Schwarz- tures are optimal (Martı´n and Salvador, 1995). kopf and Shine, 1991), gender (Gibbons and Duration of activity periods are typically Semlitsch, 1987; Huey and Pianka, 2007; Rock longer (Adolph and Porter, 1996) and bouts et al., 2000; Rock et al., 2002), digestive state of activity usually bimodal (Firth and Belan, (Beck, 1996; Gibbons and Semlitsch, 1987), 1998; Foa` and Bertolucci, 2001; Gannon and risk of predation (Downes and Shine, 1998; Secoy, 1985) in summer. Generally, in winter, Shah et al., 2004), social factors (Downes and activity can be expected to be sporadic (e.g., Shine, 1998), and season (Christian and Bed- Podarcis sicula; Foa` et al., 1992) and, in spring ford, 1995; Gibbons and Semlitsch, 1987; and autumn, activity is usually unimodal (e.g., Pentecost, 1974). Podarcis sicula, Foa` and Bertolucci, 2001), Behavioral modification of heat flux can be especially in temperate species. effected through the modification of basking Pseudocordylus melanotus melanotus (Dra- frequency or duration, regulation of activity kensberg crag lizard) is a strictly saxicolous, times, changes in body posture and modifica- diurnal, cordylid lizard. Since most rocky tion of microhabitat use (Bauwens et al., 1996; outcrops on which the lizard occurs are Carrascal et al., 1992; Hertz, 1992; Hertz and spatially heterogeneous, it is likely that they Huey, 1981; Huey and Pianka, 1977; Huey are also a highly heterogeneous environment and Slatkin, 1976; Melville and Swain, 1997; from a thermal perspective. Pseudocordylus Muth, 1977; Waldschmidt, 1980; Willmer et m. melanotus is an extreme sit-and-wait al., 2005). Generally, when the environment is forager (Cooper et al., 1997), suggesting either cool, lizards will select more exposed basking distinct thermoregulatory behavior in terms of sites, and more shaded sites during warm activity time, postures and positions, or wide periods (Cowles and Bogert, 1944; Huey and thermal preferences because it spends a large Pianka, 1977; Sherwood et al., 2005), and portion of its day in exposed positions. Here, shuttling pattern is adapted to the use of we (1) measured the Tset and Tsel of the lizard particular basking sites, non-basking retreats, in the laboratory where there are few and shade (Spellerberg, 1972). A lizard will thermoregulatory constraints and minimal utilize the available microclimates which fall stress, (2) measured the field achieved Tb within their preferred thermal range and may with respect to Tsel and evaluated the lizards only use a certain proportion of the available ability to thermoregulate, (3) measured the microclimates (Angert et al., 2002; Grant and range of operative temperatures (Te) available Dunham, 1988). The duration spent thermo- to lizards in order to quantify the thermal regulating depends on the thermal properties environment, (4) quantified thermoregulatory and availability of microclimates (Gvozˇdı´k, behavior in terms of activity and body 2002). posturing for P. m. melanotus, and (5) Postural changes alter the body’s orienta- assessed the risk of exposure to low temper- tion to the sun (Bartholomew, 1977; Wals- atures in the field. berg, 1992) and body position to control the surface area exposed to solar radiation (Pe- MATERIALS AND METHODS terson, 1987). Although changes in body posture affect radiative heat exchange, they Study Animal and Site have the greatest effect on rates of conductive Pseudocordylus m. melanotus is a member and convective heat exchange when the of the Cordylidae, a family endemic to Africa, difference between air and substrate temper- is saxicolous, and occur on rocky outcrops ature is greatest, usually during the hottest (Branch, 1998), where individuals are con- time of day (Roberts et al., 1993). During spicuous when perching on rocks (McConna- periods of inactivity in retreats, Tb is largely chie and Whiting, 2003). This species exhibits 110 HERPETOLOGICAL MONOGRAPHS [No. 23 well-developed sexual dimorphism such that captive conditions. Duration spent in captivity males are larger and more colorful than (three categories) had no significant effect on females (Mouton and van Wyk, 1993). Snout– Tsel (repeated measures ANOVA, F12,780 5 vent length (SVL) of adults ranges between 80 1.11, P 5 0.35). and 120 mm, but may reach a maximum of The thermal gradient consisted of a 1 3 1.5 143 mm in males (Branch, 1998). 3 0.5 m wooden enclosure. The gradient was All lizards used in this study originated from divided lengthways into three separate com- the Suikerbosrand Nature Reserve (SNR), partments. Heat was provided at one end of approximately 40 km southeast of Johannes- each compartment by a 250 W infrared lamp. burg, South Africa (26u 279–26u 349 S, 28u Cooling was achieved with a copper cooling 099–28u 219 E; 1800 m a. s. l.). The habitat in plate connected to a water bath at the this area is typically Highveld Grassland opposite end of the enclosure. A single lizard (Rutherford and Westfall, 1986) and is was placed in each compartment (only three dominated by Eragrostis, Hyparrhenia, The- lizards could be tested at a time). Since meda,andSetaria species (Panagos, 1999). individuals could not be tested simultaneous- Numerous rocky outcrops suitable for P. m. ly, the experiment was repeated 11 times in melanotus occur in the higher altitude parts of winter and 15 times in summer. Lizards were the reserve. Rainfall is less than 500 mm per placed in the thermal gradient overnight year and is summer seasonal. The climate is before the trials began and the lamps were typically temperate; winters are cold and dry, turned on 30 min before the first reading was with frequent frosts and very occasional snow, taken. Body temperature was recorded every while summer temperatures frequently ex- hour (from 0900 h to 1600 h) for two days by ceed 30 C. inserting a thermocouple probe approximately The lizards were housed individually in 300 10 mm into the cloaca (after Sievert and 3 300 3 500 mm glass terraria with a tile Hutchison, 1989). The Tset was estimated for shelter. Food (mealworm larvae and beetles; each lizard by determining the interquartile Tenebrio sp.) and water were supplied ad range of Tb selected in the thermal gradient libitum. Lizards were maintained in a tem- (after Hertz et al., 1993). Tsel for each lizard perature controlled room (28 6 1 C) with a was calculated as the mean Tb selected in the light:dark cycle of 12:12 h. thermal gradient. Field study.—Field work was conducted at Selected Body Temperature and Suikerbosrand Nature Reserve (SNR) during Set-Point Range February–March (n 5 18 lizards; summer) Laboratory study.—Lizards were separated and May–June 2004 (n 5 20 lizards; winter). into three categories based on the length of All lizards were captured by noosing, individ- time they had been in captivity. The first ually marked using color-coded plastic collars category of lizards had been in captivity for 12 and toe clipping, measured (SVL, nearest to 18 mo for the winter and summer mea- 1 mm; head length, head width, nearest sures, respectively. Category two lizards had 0.01 mm) and weighed (nearest 1 g). No only been acclimated in captivity for between lizards captured for the summer study were two weeks (winter) and six months (summer). used in winter. In order to measure Tb in the The third category lizards were captured for field, small temperature data loggers (17 mm the summer study only and were therefore diameter, 6 mm thick; thermochron iBut- only acclimated for two weeks before mea- tonsH; Dallas semiconductor, Texas, USA) sures. The Tsel of captive lizards was measured were surgically implanted into each lizard. in a thermal gradient in the laboratory in Lizards were anesthetized using 2% isoflour- winter (n 5 32 lizards, 2 categories) and ane gas and a small incision was made into the summer (n 5 43 lizards, three categories). peritoneal cavity. The data loggers, which Individuals of this species have previously were pre-programmed to record body tem- been maintained in captivity in excess of three perature every 20 min, were coated with wax years (S. McConnachie, pers. obs.; lizards and sterilized with hibicol. Data loggers captured as adults) and appear to adapt well to weighed three grams and were less than 2009] HERPETOLOGICAL MONOGRAPHS 111

TABLE 1.—Summary of mean body size (mass [g] and lizards may have retreated into crevices (see snout–vent length [SVL, mm]) and selected body Alexander, 2007, for a more detailed justifi- temperature (Tsel) for winter (n 5 32 lizards) and summer cation of this method). Field T was related (n 5 43 lizards) for the lizard Pseudocordylus m. sel melanotus. Means presented 6 SE. to Tset by calculating the time when lizard Tb fell within Tset (calculated from laboratory Season Winter Summer measures). Mass Males 45.53 6 3.14 50.02 6 2.11 The first three days of data were excluded Females 30.62 6 2.66 35.13 6 1.81 to remove possible effects of surgery or stress. All 39.47 6 2.50 42.76 6 1.83 Days on which lizards did not emerge from SVL Males 117.05 6 2.57 119.35 6 1.77 Females 104.38 6 3.28 107.68 6 2.03 their crevices (i.e., when Tb co-varied with All 111.91 6 2.28 113.67 6 1.63 crevice Te) were also excluded from the Tsel Males 30.23 6 0.17 30.68 6 0.15 analysis. Females 29.86 6 0.22 31.30 6 0.16 All 30.08 6 0.14 30.99 6 0.11 Operative Temperature In order to select an appropriate model for measuring operative temperature (T ), two 10% of lizard body mass (see Table 1). The e painted (black or white), 100 mm lengths of wax-coated data logger was inserted into the 28 mm diameter copper pipe models (filled body cavity through the incision, which was with water or empty) were empirically com- sutured, cleaned and covered with Tega- pared to the T of live lizards in the dermTM. Lizards were released at the point b laboratory. We calibrated models by placing of capture at SNR within four days of capture; them in a 300 3 200 3 250 mm terrarium all lizards had a recovery period—at least with a lizard (male, mass 5 43.4 g, SVL 5 120 36 h—after surgery, prior to being released. mm). Thermocouple wires were inserted Lizards were recaptured (also by noosing) approximately 10 mm into the models and after a minimum of three weeks and data separately into the lizard’s cloaca and attached loggers were removed using similar proce- to a data logger (MC Systems, 120-02 EX; dures to those used in implantation. Of the 38 Cape Town), which recorded lizard T and lizards with implanted data loggers (18 b the temperature of the models every minute summer and 20 winter), 22 lizards were for one hour under various heating and recaptured (11 each for summer and winter), cooling regimes. The lizard was monitored resulting in an overall recapture success of throughout to ensure that it was not experi- 58%. All lizards were returned to the point of encing discomfort and behaved normally. capture at SNR after removal of the data Measures of T were then compared to loggers and identification collars. The wax b coating on the data loggers was removed and data were downloaded and compared in terms of field Tsel and exposure to low temperatures. Operative temperatures were measured at SNR concurrently for comparison with recorded body temperatures (see below). Field Tsel was calculated for each lizard over the period recorded on the implanted data loggers (approximately 28 days) and was calculated as the mean Tb over the period when the lizards were active. This period started with the highest Tb reached in the morning and ended at the highest Tb before a three-hour continuous decrease (10 consecu- tive decreasing Tb measures) in Tb in the FIG. 1.—Example of field body temperature measured afternoon or evening (Fig. 1). The three-hour over 24 h using a data logger and indicating the range decrease allowed the inclusion of shorter (grey area) over which the mean selected body temper- periods of reduced Tb during the day when ature was calculated for Pseudocordylus m. melanotus. 112 HERPETOLOGICAL MONOGRAPHS [No. 23

such that one model received morning sunshine and the other afternoon sunshine. Records from the models were used as measures of the highest and lowest temperatures available to the lizards. The Te was related to Tset by calculating the time Te fell within Tset (calculated from laboratory measures). Thermoregulatory Behavior Behavioral thermoregulation in P. m. melanotus was quantified in terms of the duration that lizards were active and the frequency that FIG. 2.—Relationship between lizard body temperature each body posture was assumed by lizards and temperature in two copper tube models with the closest representative thermal properties of Pseudocordy- during a specific period. Activity time was lus m. melanotus (100 mm of 28 mm diameter copper quantified by inference: Tb profiles were pipe, painted black and filled with water). Model 1: measured using implanted thermochron iBut- heating, r2 5 0.97, y 5 0.78x + 5.43; cooling, r2 5 0.97, y tons and duration of activity was taken as the 5 0.76x + 4.62. Model 2: heating, r2 5 0.88, y 5 0.70x + 7.91; cooling, r2 5 0.98, y 5 0.75x + 4.82. P , 0.001 in time from the first rapid increase in Tb until all cases. the time of the highest temperature before a three-hour continuous decrease in Tb. Initia- tion of activity in the morning was easily measures of Te using regression analysis. diagnosed by a rapid increase in Tb when the Hertz et al. (1993) suggest that, where heating lizard first emerged and began basking. Once and cooling rates of models and small the Tb reached the plateau phase, Tb was kept ectotherms are similar, comparisons of Tb in a narrow range by the lizard. and Te will give an indication of whether the Body posture and position were recorded animals are actively thermoregulating. There- during focal animal sampling in the field at fore, the lizard models were considered good SNR. Individual lizards were observed con- 2 Te models based on the high R values and the tinuously for 30 min in summer when they slope of the regression was close to 1. The were encountered in the field. Since lower model that proved to be the best indicator of levels of activity were expected in winter, Te representative thermal properties for P. m. observations were 60 min to ensure sufficient melanotus was the black-painted copper pipe observation time during winter. Owing to filled with water (r2 5 0.97 for heating and their strict site fidelity and distinct color cooling; slope 5 0.78 and 0.76 for heating and pattern, some individuals were observed on cooling, respectively; Fig. 2). more than one occasion. Observation times Lizard Te was measured in the field at SNR for lizards observed on more than one between summer 2002 and winter 2004. occasion were summed. Body postures and Three models (black, 100 mm lengths of positions assumed by the lizards were catego- 28 mm diameter copper pipe filled with rized as follows (Fig. 3): water) were placed at a single locality in the field and connected to a data logger (MC (a) Prostrate (head and body flat on the rock Systems, 12-02 EX; Cape Town), which was surface). programmed to log temperatures of the (b) Prostrate with head raised. models every 20 min. Models were placed (c) Upper body raised (front of body and individually in microhabitats where lizards head raised, forelegs partially or fully would be expected to equilibrate at the extended, abdomen and tail flat on rock lowest and highest Tb: In a crevice (approx- surface). imately 100 mm deep with 150–200 mm of (d) Body raised (whole body raised off rock rock on either side; limited by the size and surface, all legs partially of fully extend- shape of the model) and on the rock surface ed). 2009] HERPETOLOGICAL MONOGRAPHS 113

FIG. 3.—Categories of body postures and positions assumed by Pseudocordylus m. melanotus. (a) prostrate; (b) prostrate with head raised; (c) upper body raised; (d) body raised; (e) legs raised; (f) side of rock; (g) on side of rock extended. See text for details.

(e) Legs raised (body and head flat, hind legs observation time in winter was 91 h 41 min. and feet raised off rock surface). Focal sampling started at 0700 h (GMT + 2) (f) Side of rock (on side of rock, head and continued through the day until no more extended above top of rock). lizards were observed; this was usually be- (g) Side of rock extended (on side of rock tween 1700 h and 1800 h (Fig. 4). In winter, with head and upper body extended the first lizards were observed between above top of rock, forelegs partially or 0900 h and 1000 h. fully extended, sometimes body raised off rock surface). Exposure to Low Temperatures (h) Other (any other body posture or posi- Exposure to low temperatures was calcu- tion assumed). lated as the number of days in an average 30- day period that the lizards experienced In summer, 122 focals were recorded for 92 periods where their Tb was at or below 10 C individual lizards (53 male and 39 female). In (below lower critical limiting temperature, winter, 117 focals were recorded for 50 CTMin; see McConnachie et al., 2007). individual lizards (28 male and 22 female). Lizards were incapacitated at any tempera- Not all lizards were observed for the entire 30 tures below CTMin and had compromised or 60 min focal duration since lizards were locomotory ability (McConnachie et al., 2007). occasionally obscured from view by rocks or The proportion of time at or below 10 C was vegetation and one to four focals were also determined as a measure of the time conducted per lizard. Mean (6 SE) observa- spent at or below 10 C. During summer, no tion time per lizard in summer was 34.76 6 lizards experienced periods where their Tb 2.59 min and ranged between two and was below 10 C. 120 min and the total, overall observation time in summer was 51 h 55 min. Mean Statistical Analyses (6 SE) observation time per lizard in winter Data were analyzed using Excel and STA- was 110.02 6 25.76 min and ranged between TISTICA 5.5 E and all tests were conducted at two and 1066 min and the total, overall a 5% level of significance. All data were tested 114 HERPETOLOGICAL MONOGRAPHS [No. 23

FIG. 4.—Temporal spread of focal starting times from when the first Pseudocordylus m. melanotus was observed in the morning (0700 h) until the last lizard was observed in the afternoon (between 1700 h and 1800 h); summer 5 open, winter 5 black. for normality (Lilliefors’ test) before applying Field study.—Body mass and SVL were parametric statistics. All means are presented significantly correlated (r 5 0.92, P , 0.001). 6 standard error (SE). Snout–vent length of male and female lizards in the summer and winter groups were not significantly different (ANOVA, F 5 2.55, RESULTS 3,18 P 5 0.09). In summer, larger individuals Selected Body Temperature and attained significantly lower field Tsel (regres- Set-Point Range sion analysis, P 5 0.008, r2 5 0.58; Fig. 6). Laboratory study.—Mean Tset was 29.00 6 Field Tsel and body size in winter were not 0.36 to 31.78 6 0.16 C and 29.61 6 0.28 to significantly related (regression analysis, mass, 32.47 6 0.18 C in winter and summer, P 5 0.63, r2 5 0.03; SVL, P 5 0.77, r2 5 respectively. Body sizes and mean Tsel of 0.01). males and females are summarized in Table 1. On days where lizards were actively ther- The mean Tsel for all lizards was 30.08 6 moregulating, lizard Tb followed a very 0.14 C and 30.99 6 0.11 C for winter and different pattern to the minimum and maxi- summer, respectively. Male and female lizards mum Te (Fig. 7). Mean (6 SE) field Tsel did not select significantly different tempera- during summer was 28.91 6 0.26 C, and tures between seasons (repeated measures during winter was 26.30 6 0.47 C. Lizards ANOVA with gender and season as factors: attained significantly higher temperatures in F7,903 5 0.51, P . 0.5). Post hoc, lizards summer than winter (ANCOVA with gender, selected significantly higher temperatures in mass and SVL as covariates, F1,17 5 20.88, P summer (t71 5 4.27, P , 0.001). In both , 0.001). Time where Tb was within Tset did summer and winter, body size and Tsel were not differ significantly between male and not significantly related (SVL and body mass, P female lizards during summer or winter 2 . 0.05 and r , 0.1). Overall, difference in Tsel (summer, t268 5 1.97, P 5 0.68, n 5 5 between time intervals were not significantly females, 6 males; winter, t198 5 1.97, P 5 different (ANOVA, winter, F6,190 5 0.20, P 5 0.75, n 5 4 females, 7 males; Fig. 8). Lizards 0.97; summer, F6,195 5 0.85, P 5 0.53). No spent significantly longer periods in summer pattern of Tsel was evident during photophase where their Tb was within Tset than during for either winter or summer measures (AN- winter (t20 5 2.09, P , 0.001, n 5 22 lizards; OVA, winter, F1,6 5 0.20, P 5 .97; summer, summer, 179.00 6 13.65 min/day; winter, F1,6 5 0.86, P 5 0.53; Fig. 5). 55.50 6 7.89 min/day). 2009] HERPETOLOGICAL MONOGRAPHS 115

FIG. 5.—Mean selected body temperature (6 SE) of lizards in a thermal gradient between 1000 h and 1600 h during (a) winter (n 5 32 lizards) and (b) summer (n 5 43 lizards). Letters indicate significant differences between days and time intervals (Post hoc Tukey P , 0.05).

Operative Temperature and on 21.71 6 2.05 days out of an average During winter, crevice temperature rarely 30-day period in winter (i.e., 72.36% 6 0.68 of winter days). exceeded 10 C, and the lowest recorded Te in a crevice was 24.25 C, recorded during July Lizards shuttled between rock crevices, full 2002. For 2004, during the period when sunshine and areas in the shadows of rocks, or lizards carried implanted thermochron iBut- vegetation adjacent to the rock. Lizards tons and were active in the field, operative tended to either face the sun directly, face temperatures varied between 23.20 C and directly away from the sun thus receiving full 54.94 C (in crevice and outside in the sunshine on their backs, or turned side-on to sunshine; Table 2). Periods where Te fell the sun. Although males and females exhibited within Tset were significantly longer in winter similar postures and microhabitat selection, than in summer (t56 5 2.00, P 5 0.04, n 5 there were clear seasonal differences. The 58 days; summer, 46.90 6 6.22 min/day; most frequently assumed postures in summer winter, 74.48 6 12.27 min/day). were (b) prostrate with head raised and (c) Thermoregulatory Behavior Lizards were active for significantly longer during summer than in winter (t20 5 9.96, P , 0.001). In summer, lizards emerged at 0816 h 6 0011 h (GMT + 2) and were active for 8 h 51.84 min 6 20.80 min, returning to their retreats at 1707 h 6 0010 h. Summer activity duration did not differ significantly between males and females (t9 5 0.05, P 5 0.96). In winter, lizards emerged at 1048 h 6 0041 h and were active for 4 h 20.61 min 6 17.59 min, returning to their retreats at 1431 h 6 0013 h, and did not differ between males and females (t9 5 0.43, P 5 0.68). Lizards were active for significantly more days FIG. 6.—The relationship between selected body temperature (Tsel) in the field and snout–vent length 2 in summer than in winter (t20 524.05, P 5 during summer for Pseudocordylus m. melanotus (r 5 0.001), and were active every day in summer 0.58, P 5 0.008, y 520.07x + 36.79). 116 HERPETOLOGICAL MONOGRAPHS [No. 23

FIG. 7.—Example of field active body temperature (Tb) of a lizard (solid line) relative to operative temperatures (Te; dotted lines) over an average three-day period (each peak indicates a day) during (a) summer and (b) winter at Suikerbosrand Nature Reserve. Active thermoregulation is evident in the difference between the measured Tb and Te inside a crevice and outside in the sunshine. During the night lizard Tb is buffered by rock and therefore does not drop to the Te outside its retreat. During the day (peaks), lizards actively thermoregulate such that Tb does not match the Te. In winter (b), lizards are active for short periods only (indicated by narrower peaks in Tb) and, in this case, the lizard does not leave its retreat (indicated by the peak in Tb mirroring that of the peak in crevice temperature). upper body raised, and (d) legs raised and Exposure to Low Temperatures other postures and positions were only In an average 30-day period in winter, observed during focal animal sampling in the lizards experienced 27.91 6 1.24 days with afternoon (Fig. 9). In winter, the most fre- periods of 11 h 1.8 min 6 1 h 46.2 min (33.51 quently assumed postures were (a) prostrate, 6 5.41 20 min intervals) spent at or below (c) upper body raised and (f) side of rock. 10 C (CTMin). This means that lizards are Other postures observed were only observed spending approximately 47% of their time at in the afternoon, including (b) head raised and or below their CTMin during winter, and (g) side of rock extended (Fig. 9). were therefore incapacitated for a significant 2009] HERPETOLOGICAL MONOGRAPHS 117

TABLE 2.—Minimum (nighttime) and maximum (daytime) operative temperatures (C) measured inside and outside a crevice during summer and winter 2004 at Suikerbosrand Nature Reserve.

Summer Winter Crevice Min 21.8 20.7 Max 29.4 18.3 Outside Min 10.6 23.2 Max 54.9 42.3

being active for longer periods in summer, available Te within Tset was longer in winter FIG. 8.—Time where field body temperature fell within and was also within Tset for a greater the set-point range (Tset) measured in the laboratory during summer and winter for male and female Pseudo- proportion of the activity time (33% in winter cordylus m. melanotus. Letters indicate significant differ- as opposed to 11% in summer). In summer, ence between seasons, but not between genders within however, Te often exceeded the upper limit of seasons (P , 0.05). Tset (up to ca. 55 C). This suggests that there was greater thermoregulatory opportunity for portion of the day. The lowest Tb experienced the lizards in summer. Changes in position by lizards during summer was 14.15 6 0.15 C, and posture, and shuttling between sunshine while the lowest Tb experienced by lizards and shade were obvious thermoregulatory during winter was 7.27 6 0.38 C. behaviors. These behaviors are consistent with those associated with both heliotherms and DISCUSSION thigmotherms, thus suggesting a mixed ther- The operative temperature range for P. m. moregulatory strategy in P. m. melanotus. melanotus was 23.20 C to 54.94 C in the Selected Tb in many lizards generally coldest and hottest microclimates, respective- approach 30 C (e.g., Andrews and Kenney, ly. This means that lizards had a wide range of 1990; Angilletta et al., 1999; Arad et al., 1989; environmental thermal opportunities over the Grbac and Bauwens, 2001; Rocha and Vrci- seasons (although not necessarily at one bradic, 1996). The Tsel measured for P. m. melanotus is thus within the range expected instant in time). The Tb measured in the laboratory thermal gradient was higher than for lizards, as well as for other cordylid lizards. field Tsel, which suggests that there may be Selected Tb measured in thermal gradients for limitations to the lizards’ thermal environ- Cordylus vittifer and C. jonesi was 32.1 C ment, particularly in winter. (Skinner, 1991) and 33.5 C (Wheeler, 1986), During summer, lizards did not experience respectively. In summer, the field Tb of P. m. Tb below 10 C. The lowest Tb experienced melanotus is similar to those of other cordy- during summer was approximately 14 C. lids. Bauwens et al. (1999) reported the range During winter, lizards experienced periods of field Tb for Cordylus cataphractus, C. where their Tb was below 10 C approximately macropholis, C. niger, C. polyzonus, and P. 28 days out of 30, and the lowest Tb capensis to be between 29 and 32 C. experienced was approximately 7 C. This The Tsel of male and female P. m. melanotus suggests that, during summer, lizards will was not significantly different for either rarely, if ever, experience Tb below their summer or winter measures. This result is CTMin, whereas, in winter, lizards spend a not surprising: A recent review of gender significant amount of time (47%) unable to differences in aspects of thermal biology move. among 56 species from seven lizard clades Lizards were active for significantly shorter found minor differences (,1 C in mean body periods during winter than during summer temperature; Huey and Pianka, 2007; also see and activity time in winter was around half Lailvaux, 2007 for a review). Gender differ- that of activity time during summer. Despite ence in Tsel is usually explained by reproduc- 118 HERPETOLOGICAL MONOGRAPHS [No. 23

FIG. 9.—Frequency of postures and positions assumed by Pseudocordylus m. melanotus during the morning and afternoon in summer and winter: (a) prostrate, (b) prostrate with head raised, (c) upper body raised, (d) body raised, (e) legs raised, (f) side of rock, (g) side of rock extended, (h) other. Frequency calculated as the percentage of focals in which the posture or position was observed. tive condition where gravid females either regimes remain constant (Rismiller and Held- select higher or lower Tb than non-gravid maier, 1982, 1988). In P. m. melanotus,the females or males. For example, gravid female thermal environment may not be limiting Sceloporus jarrovi (Beuchat, 1986) and S. because most lizards are active during winter, grammicus (Andrews et al., 1997) have lower even if only for a few days in a given month. Tsel than non-gravid females and males, Food availability could be a limiting factor whereas, gravid female Haplodactylus macu- since some reptiles are known to select higher latus selects higher Tb than post-parturient/ Tb after eating (e.g., Beck, 1996; Brown and non-gravid females and males (Rock et al., Griffin, 2005; Gibson et al., 1989). 2000; Rock et al., 2002). Young of P. m. The lowest temperature in the coldest melanotus are born during late summer microclimate (i.e., in a crevice) was 24C (Flemming, 1993). Some females observed in winter 2002. This is 1.15 C above the during the field study may therefore have measured lower lethal temperature (25.15 C; been gravid. The direct effects of reproductive McConnachie et al., 2007), and 14 C below status on thermoregulation in this species, the measured lower critical limiting temper- however, remain to be investigated. ature (CTMin ca. 10 C; McConnachie et al., Pseudocordylus m. melanotus selected high- 2007). In addition, crevice temperature rarely er Tb in summer than in winter. Christian and exceeds 10 C during winter and Tb of lizards Bedford (1995) suggest that seasonal shifts in measured in the field is below CTMin for preferred Tb could be due to acclimatization approximately 47% of the time. This suggests in response to environmental temperatures, that lizards are significantly affected by the photoperiod, reduced food availability, and thermal environment in winter and are totally hormonal cycles. This has been noted in incapacitated, or effectively comatose, during Lacerta viridis, where seasonal changes in most winter nights. Although a colder accli- Tb are not solely dependent on the availability mation temperature may have resulted in of thermal resources, but also photoperiod, lower CTMin values, free-ranging lizards, especially where food availability and thermal although they experience lower nighttime 2009] HERPETOLOGICAL MONOGRAPHS 119 temperatures, are selecting high Tb when they and Belan, 1998). On days when P. m. are active during winter. melanotus are active in winter, Tb measured The lowest recorded temperature in the in the field suggests that activity is unimodal. coldest microclimate during summer was This is likely because lizards maintain high Tb 1.09 C (0020 h, October 2004), suggesting for short periods only once during the day. In that lizards do occasionally experience envi- summer, high Tb is maintained throughout ronmental temperatures below CTMin during the day, which also suggests a unimodal summer, but for relatively short periods. The activity pattern. During focal animal sam- hottest recorded temperature was 54.94 C pling, however, the number of lizards active outside in full sunshine. Consequently, lizards during the heat of midday in summer was would be able to attain significantly higher Tb lower, which suggests a degree of bimodality than they are actually selecting. The discrep- of activity. ancy between the laboratory and field mea- Even when thermal conditions are suitable, sures of Tsel may therefore be explained by not all lizards within a population are simul- variations in individuals and territory struc- taneously active (Martı´n and Salvador, 1995), ture; for example, some lizards may hold but basking lizards are exposed, thus increas- territories which have fewer thermal resourc- ing the probability that they will be observed es, or restricted available microclimates, thus (Foa` et al., 1992). So, although P. m. restricting the Te available in any particular melanotus appear to be active, they may, in area. fact, seek out suitable retreat sites during the Since measures of Tsel in thermal gradients hottest times of the day. Based on differences are indicative of Tb selected and maintained in between Tb and Te it is clear that P. m. an environment with few or no thermoregu- melanotus are thermoregulating throughout latory constraints, this suggests that there may the day. Although they may not be active, they be environmental constraints on the thermo- are selecting retreats where they can still regulatory ability of P. m. melanotus. The maintain Tb at a selected level. Huey et al. lizards were, however, actively thermoregu- (1989) suggest that retreats offer equivalent, lating in the field. This is evident in the or sometimes superior, thermoregulatory op- discrepancy between the Tb and Te measures portunities to those available in more exposed (see Fig. 7). Also, the highest Te recorded environments. These periods of inactivity may (54.94 C) is obviously too high for the lizards be important in avoiding environmental ex- to withstand (see also McConnachie and tremes (Kearney, 2002), conserving energy or Alexander, 2004), so lizards would have to water (Martı´n and Lo´pez, 2000), and avoiding avoid places where their Tb might exceed their predators (Webb and Whiting, 2005). critical limiting maximum. Body temperatures Four strategies of heat regulation in lizards are thus maintained at a level which is have been identified. These include (1) determined primarily by the environment gaining external heat or avoiding heat loss to and the lizards ability to behaviorally regulate the environment, (2) retaining internal heat, its Tb through activity, shuttling or postural (3) generating internal heat, and (4) losing changes. excess heat or avoiding heat gain from hot Generally, activity in reptiles during cool environments (Muth, 1977; Sherwood et al., periods is more sporadic, shorter and uni- 2005). Generating and retaining internal heat modal, while, in summer, activity is regular, (2 and 3) generally constitute physiological longer and bimodal. For example, the prairie measures of heat regulation, while losing and rattlesnake, Crotalus viridis viridis, shows gaining external heat (1 and 4) include unimodal activity in spring and autumn with behavioral thermoregulation. Sherwood et a peak during midday, and bimodal activity in al.’s (2005) descriptions of external heat loss summer with a peak in the morning and again and heat gain are clearly evident in the in the afternoon (Gannon and Secoy, 1985); behavior of P. m. melanotus. In gaining the scincid lizard Tiliqua rugosa exhibits external heat, lizards bask in sunlight on cold bimodal activity during summer also with mornings and gain heat from radiation and peaks in the morning and afternoon (Firth conduction from warmed surfaces. Once an 120 HERPETOLOGICAL MONOGRAPHS [No. 23 optimal level has been reached, the lizards Acknowledgments.—Gauteng Nature Conservation and become active, seeking food, while using N. Green granted permission to work at Suikerbosrand Nature Reserve (permit numbers: 1143, 021, 0476, 0756). behavioral and physiological methods of Tb Thanks to D. Reddy for collecting the winter focal maintenance. sampling data. The Animal Ethics Screening Committee The most frequently assumed postures, of the University of the Witwatersrand cleared all throughout the day, were (b) prostrate with experimental procedures. This study was funded by grants to G. J. Alexander and M. J. Whiting from the National head raised and (c) upper body raised (see Research Foundation (NRF) and the University of the Figs. 2 and 9). This suggests that lizards are Witwatersrand. Opinions expressed and conclusions effectively using both solar radiation and arrived at are not necessarily to be attributed to the NRF. conduction from the rock surface (i.e., a combination of heliothermic and thigmother- LITERATURE CITED mic thermoregulation). Generally, lizards as- ADOLPH, S. C., AND W. P. PORTER. 1993. Temperature, sumed more and/or different postures during activity and lizard life histories. American Naturalist the afternoon. During the hottest periods, if 142:273–295. lizards were exposed, they assumed more ADOLPH, S. C., AND W. 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