Thermoregulation in leopard tortoises in the Nama-Karoo: The importance of behaviour and core body temperatures

Journal of Thermal Biology 38 (2013) 178–185

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Thermoregulation in leopard tortoises in the Nama-Karoo: The importance of behaviour and core body temperatures Megan K. McMaster, Colleen T. Downs n School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, Pietermaritzburg 3209, South Africa

a r t i c l e i n f o

a b s t r a c t

Article history: Received 15 November 2012 Accepted 4 February 2013 Available online 13 February 2013

Despite being ectotherms, reptiles have an ability to thermoregulate which is enhanced by adopting a variety of behavioural mechanisms. Different behavioural postures, the use of retreat sites and selection of microhabitats enable reptiles to maintain their core body temperatures (Tb) above that of ambient temperatures (Ta) in winter or below Ta maximum in summer. This study describes the daily activity patterns of leopard tortoises (Stigmochelys pardalis) in relation to Tb and Ta, and the extent to which leopard tortoises can manipulate their Tb in response to seasonal changes in Ta. Ten and nine leopard tortoises were radio-tracked in 2002 and 2003, respectively and cloacal Tb and behaviours observed. TM Core Tbs were measured using Thermocron iButtons surgically implanted into the body cavities of 4 and 5 adult telemetered tortoises for summer and winter 2003, respectively. There were seasonal differences in the extent to which certain behaviours were practiced and the time of day that these occurred. Leopard tortoises generally had unimodal activity patterns in winter and bimodal ones in summer. In winter tortoises were active at lower Tbs, and at lower Ta, than in summer. Tortoises maintained their core Tb well below Ta minimum profiles in summer and well above these in winter. Core Tb closely followed the increase in Ta minimum profiles in the mornings, however tortoises exhibited an extended thermal lag when Ta minimum profiles cooled overnight. By using different behavioural mechanisms in summer and winter, leopard tortoises maintained their core Tb at different levels compared with Ta minimum and maximum profiles. Consequently although they are ectotherms, they maintained their core Tb independent of Ta. & 2013 Elsevier Ltd. All rights reserved.

Keywords: Activity Behaviour Core body temperature Thermoregulation Ectotherm

1. Introduction Although ectotherms, reptiles thermoregulate using a variety of behavioural mechanisms. Stevenson (1985) calculated that a 1 kg dry-skinned ectotherm could modulate its body temperature (Tb) by 30–50 1C by changing activity time or habitat, compared to 5–15 1C using postural adjustments, and only 1–5 1C by physiological mechanisms. In particular different behavioural postures, the use of retreat sites and selection of microhabitats enable reptiles to maintain their core Tb above that of Ta (Chelazzi and Calzolai, 1986; Huey et al., 1989; Kearney, 2001; Belliure and Carrascal, 2002; Gvozdik, 2002; Kearney, 2002; Pearson et al., 2003; Downs et al., 2008; Loehr, 2012). Since the rigid shells of tortoises limit the effectiveness of postural changes during behavioural thermoregulation (Heath, 1964; White, 1973; Huey et al., 1989; Kearney, 2001; Pearson et al., 2003), one would expect the main thermoregulatory mechanism used by tortoises to be a change in daily activity period and behaviour, as was found for the tortoise Kinixys spekii

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0306-4565/$ - see front matter & 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jtherbio.2013.02.003

(Hailey and Coulson, 1996a, 1996b). Experimental investigations into the optimal Tb and activity patterns of captive tortoises are limited (Craig, 1973; Perrin and Campbell, 1981; Hailey and Loveridge, 1998). However, behavioural thermoregulation and activity have been reported in free-ranging tortoises, with behavioural patterns being compared over 24 h, between seasons, between age classes, or to environmental conditions (CloudsleyThompson, 1970; McGinnis and Voigt, 1971; Judd and Rose, 1977; Lambert, 1981; Meek, 1984; Pulford et al., 1984; Chelazzi and Calzolai, 1986; Meek, 1988; Loehr, 2002; 2012). In the few studies that have measured the Tb of tortoises, these temperatures were monitored in association with behavioural activity in the field (Lambert, 1981; Pulford et al., 1984; Wright et al., 1988; Hailey and Coulson, 1996b; Loehr 2012), without addressing whether tortoises are able to maintain stable Tb under various Tas, which this study therefore aims to do. Since behavioural thermoregulation is time-consuming and reduces energy and time that could otherwise be dedicated to foraging and social activities (Gvozdik, 2002), the ability and extent to which leopard tortoises (Stigmochelys pardalis, previously Geochelone pardalis, Fritz and Havas, 2006) are able to maintain their Tb in natural conditions and optimise the time spent at target Tbs, was investigated. We used the term target and

M.K. McMaster, C.T. Downs / Journal of Thermal Biology 38 (2013) 178–185

optimal Tb to indicate the range of Tbs at which a tortoise would pursue foraging and social behaviours rather than thermoregulatory behaviours. We hypothesised that leopard tortoises, although ectotherms, would maintain their Tb in fluctuating and extreme daily and seasonal Ta to maximise the time spent at optimal Tb. This species is relatively large and has a range of body sizes depending on age and habitat (McMaster and Downs, 2009). It was therefore expected that their large size and use of changes in daily and seasonal activity patterns, would result in a degree of thermal inertia and allow for the stability and maintenance of Tb independently of Ta. One of the major constraints in evaluating thermoregulation and behaviour of a reptile such as the leopard tortoise is that Ta is not the actual thermal regime experienced by the animal in its natural environment. Factors affecting energy flow to an animal include radiation, air temperature, wind and humidity (Porter and Gates, 1969). To define the thermal environment an animal experiences in the field, the effects of these parameters are sometimes integrated into an index value that can be directly compared to the animal’s Tb and behaviour. A commonly used index is the operative temperature (Te) (Bakken et al., 1985; Webb and Shine, 1998). Numerous physical model representations of animals have been used to measure Te, and when used correctly, operative temperature models have the potential to be a powerful tool for examining the relationship between an animal’s thermal environment and its physiology and ecology (Bakken et al., 1985; Dzialowski, 2005). However, in ectotherms the problem of thermal inertia has been highlighted, particularly in large animals that move about in a thermally heterogenous environment (Seebacher and Shine, 2004; Christian et al., 2006). In the present study, tortoises were wild and freeranging so it was difficult to determine an operative temperature profile for each. Operative temperatures are particularly affected by radiation and so change most in the heat of the day. Electronic devices have been shown to offer an alternative to models of relatively small-sized vertebrates, as size, morphology, scale architecture and colour contribute very little to temperature change (Vitt and Sartorius, 1999; Coleman and Downs, 2010). Consequently TM iButtons were used to determine a guide of the actual Ta profile experienced by leopard tortoises through the year (see below for details). An alternative way to address the problem of large body mass would have been either a randomisation method (Wills and Beaupre, 2000), or heat transfer modelling (Seebacher et al., 2003). However, here we tracked the same individuals over several seasons to determine if they showed elevated core Tb compared with Ta minimum.

2. Methods Field work was conducted on a 5500 ha area of a 26,000 ha mixed commercial sheep and game farm in the De Aar District, Nama-Karoo biome, South Africa (31104’S, 23141’E). Vegetation here is classified as grassy dwarf shrubland (Palmer and Hoffman, 1997). Average annual rainfall is low (200–400 mm) and the area has its highest rainfall in late summer and autumn (McMaster, 2001). Daily temperatures range from 5 to 39 1C in spring (Sept– Nov) and summer (Dec–Feb), and from  5 to 26 1C in autumn (Mar–May) and winter (June–Aug) (McMaster, 2001). To determine daily Ta profiles and the minimum and maximum Ta, temperatures were recorded every 20 min using Thermocron TM iButtons Temperature-Logger (Dallas Semiconductors, Dallas, TM Texas, U.S.A) accurate to 0.5 1C. iButtons were placed in the following respective positions: 20 cm above the ground in full sun, full shade and on the north, east, west and south sides of shrubs to represent positions that leopard tortoises use in the field.

179

Leopard tortoises were located by riding transects on horseback through the study area. In total, four males and six females in summer 2002, and four males and five females in summer 2003 were fitted with unique-frequency radio transmitters (Dearden, Pietermaritzburg). These were 60 g (o1% body mass) and powered by a lithium battery (AA), with a 3/4 wavelength stainless steel tracer wire antenna, potted in moulded PVC tubing and attached to the carapace with dental acrylic. For both telemetered tortoises and for any other tortoises sighted, the date, time, Ta, sex, individual marking, morphometrics, body mass (measured using a spring balance accurate to 500 g) (See Appendix). Type of activity and cloacal Tbs were recorded; the latter were taken by inserting a fine-gauge thermocouple thermometer (Cole-Palmer Digi-Senses) 50 mm into the cloaca of adult tortoises. All temperature recording equipment was calibrated comparatively against an Ever Ready electronic reference thermometer using thermally stabilised liquid baths and a calibration curve generated. The correction values were calculated for the observed temperatures using the generated calibration curve, and the temperature values corrected numerically (following Nicholas and White, 2001). Upon sighting, leopard tortoises were classified either as inactive or active. Inactive tortoises were those found in a refuge with their head and legs retracted into their shells. Refuges were used overnight or for protection from cold weather or sun. Those tortoises that were active were performing one of seven types of activity (following Els, 1989): (i) alert: tortoise was in, or just out of its form (refuge used overnight, McMaster and Downs, 2006) with its head and/or legs out of its shell; (ii) basking: tortoise orientated to expose the maximum shell surface area to the sun, often with limbs and neck extended; (iii) walking: tortoise actively walking in the open; (iv) feeding; (v) drinking; (vi) shading: tortoise is in the shade of a bush or other shelter, often with head and limbs extended; and (vii) courtship and mating. Telemetered leopard tortoises were located at least twice daily for a one month period in February 2002, 2003 and July 2002, 2003. In addition, at least two of these tortoises (of each gender) were followed for a continuous 12 h period once every month, and behaviour and cloacal Tbs were recorded every 20 min. For each telemetered tortoise in each month of field sampling, TM iButtons were attached (using dental acrylic) to the ventral surface of the upper carapace inside the rear leg cavity and programmed to take a temperature recording every 20 min as an additional measure of Tb and these recordings are hereafter referred to as ‘‘external’’ Tbs. TM To measure core Tb, iButtons (recording temperature every 20 min) were surgically implanted into the body cavities of 2 male and 2 female, and 3 male and 2 female telemetered tortoises for summer and winter 2003, respectively. Tortoises were anaestheTM tised using Fluorothane gas and iButton s surgically implanted by a qualified veterinary surgeon. Data were analysed using STATISTICA software (Statsoft, USA). Descriptive statistics, frequency summaries and regression plots were done. As part of the temperature profile, minimum and TM maximum temperatures recorded using the iButton s were used in analyses and are referred to as Ta minimum and Ta maximum.

3. Results 3.1. Body mass Body mass of tortoises showed a range of body size between individuals but did not differ significantly when years and seasons

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were considered (RMANOVA, F(3,15) ¼ 1.88, P ¼0.18). Mean body massþSD of all tortoises in summer 2002 was 13.59þ 2.86 kg (n¼10, min¼9, max¼19); winter 2002 was 12.32þ2.28 kg (n¼10; min¼8.8, max¼16.8); summer 2003 was 12.34 þ 4.00 kg (n¼9, min¼4.8, max¼ 19.8); and winter 2003 was 13.18 þ2.33 kg (n ¼9, min¼9.4, max¼18.2). Tortoises with iButTM ton s implanted did not differ significantly between season in body mass (T-test, t ¼1.104, df ¼4, P¼0.33) with summer mean body mass 11.98þ 1.69 kg (n¼5, min¼9.4, max¼13.4) compared with winter mean body mass 12.36þ1.80 kg (n ¼5, min¼ 9.4, max¼13.8).

3.2. Core body temperature Core Tbs of tortoises were plotted against the daily Ta minimum (shade) and maximum (sun) profiles in summer and winter (Fig. 1). In summer, core Tbs of all tortoises oscillated on a daily basis between 25 1C and 35 1C, with a minimum of 17.0 1C and a maximum of 38.0 1C, independent of Ta minimum and maximum profiles (Fig. 1). In the morning, the tortoises were thermoconformers and their Tb and Ta minimum profiles rose similarly until Tb reached around 35–36 1C (Fig. 1). At this temperature the tortoise Tb became independent of Ta maximum profile, which could rise to over 50 1C. As Ta cooled in the afternoon and overnight, the Tb of the tortoise lagged against Ta minimum and maximum profile, such that the tortoise became a thermoregulator; although the Ta minimum profile reached below 10 1C, the tortoise Tb never reached below 22 1C (Fig. 1). In winter, core Tb of all tortoises oscillated above Ta minimum profiles on a daily basis between 8 1C and 30 1C on most days, with a minimum recorded Tb of 3 1C and a maximum of 32 1C (Fig. 1). In winter, leopard tortoises exhibited little thermal inertia when heating, with core Tb following the increase in Ta minimum profiles closely, and continuing to rise above Ta minimum profiles at midday (Fig. 1). As in summer, the tortoises exhibited an extended thermal lag when Ta minimum profiles cooled from midday and overnight. The core Tb cooled more slowly than Ta minimum profiles, and never decreased to the minimum Ta (Fig. 1).

Ta Shade

3.3. Behaviour and body temperature The Ta minimum and Ta maximum profiles, the cloacal Tbs, and respective observed behaviours for each tortoise are shown in Figs. 3 and 4 for summer 2002 and 2003, and winter 2002 and 2003. During the summer, the most common behaviour at low Tbs was basking (Fig. 2). As Ta and cloacal Tb increased, tortoises discontinued basking in favour of walking (Fig. 2). At cloacal Tbs between 25 and 35 1C, with corresponding Ta minimum profiles of 25–35 1C and Ta maximum profiles of 30–45 1C, the majority of tortoises observed were walking (Fig. 2). Most tortoises were observed seeking refuge in shaded areas when Ta was high (Fig. 2). The behavioural response of tortoises occurred over a much broader temperature range in winter than in summer. For instance, tortoises were observed as being in shelter (either inactive or alert) at a range of cloacal Tbs from 2 to 25 1C, and at Ta minimum and maximum profiles of 5–20 1C (Fig. 3). Basking in winter 2002 was observed over a lower absolute range of Ta profiles (3–20 1C) as opposed to winter 2003 (15–30 1C) (Fig. 3). Observations of tortoises walking were limited; however, all tortoises observed walking had cloacal Tbs over 20 and 25 1C in winter 2002 and 2003, respectively and were walking at Ta profiles of 15–20 1C in winter 2002, and over 25 1C in winter 2003 (Fig. 3). Mean ( 7S.E.), minimum and maximum cloacal Tbs of leopard tortoises and Tas associated with behavioural activity types, are presented in Tables 1 and 2 for summer and winter, respectively. In summer, leopard tortoises were alert in 54% of observations at cloacal Tbs between 15 and 25 1C, with a mean cloacal Tb of 24.7270.81 (Table 1). Summer Tas were between 20 and 30 1C when 62.9% of leopard tortoises were alert, with a mean Ta of 24.3470.61 (Table 1), with tortoises becoming inactive below these Tas. In contrast, 61% of leopard tortoises in winter were alert when their cloacal Tbs were between 5 and 15 1C with a low mean cloacal Tb of 11.9370.62 (Table 1). Winter Tas were between 10 and 15 1C when 77.9% of tortoises were observed to be alert, with a mean Ta of 12.51 70.42 1C (Table 1).

Ta Sun

Tb Core

Temperature (°C)

50 40 30 20 10 0 -10 1

2

3

4

5

6

7

8

9

10

11

12

13

14

11

12

13

14

Time (Days) Ta Shade

Ta Sun

Tb Core

Temperature (°C)

50 40 30 20 10 0 -10 1

2

3

4

5

6

7

8

9

10

Time (Days) Fig. 1. Representative plot of ambient temperature (Ta) profiles against internal core body temperatures (Tb) of individual leopard tortoise, T9, over the A. Winter and B. Summer sampling period in 2003.

M.K. McMaster, C.T. Downs / Journal of Thermal Biology 38 (2013) 178–185

= Animal in shade, = Animal walking

= Animal basking and

Tb cloacal

Behavioural activities represented:

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Ta Minimum (°C)

Ta Minimum (°C)

Fig. 2. Representative plot of behavioural activity of individual leopard tortoise at various cloacal body temperatures (Tb) against ambient temperature (Ta) (1C) maximum and minimum profiles for summer 2003.

= Animal in shade, = Animal walking

= Animal basking and

Tb cloacal (°°C)

Behavioural activities represented:

Ta Minimum (°C)

Ta Minimum (°C)

Fig. 3. Representative plot of behavioural activity of individual leopard tortoise at various cloacal body temperatures (Tb) against ambient temperature (Ta) maximum and minimum profiles for winter 2003.

A

I

B

I S

IB IS I

B I S I W I

A

I

Table 1 Summer mean (7 S.E.), minimum and maximum cloacal body temperatures and ambient temperatures (1C) for each behavioural activity observed in free-ranging leopard tortoises. Behaviour

Alert Basking Walking Shade Feeding Drinking Mating Inactive Fig. 4. Representative plot of Ta maximum and minimum profiles (shaded) and external body temperatures (Tb) (dotted) of an individual leopard tortoise, with focal samples of cloacal (Tb) (solid squares), against time of day during summer 2002. Types of behavioural activity by individual tortoises are A ¼alert; B¼ basking; W¼ walking; F¼ feeding; S ¼shade.

Basking in summer was observed in 59.7% of leopard tortoises at cloacal Tbs between 15 and 25 1C, and in 74% of tortoises at Tas between 20 and 30 1C, with basking occurring at mean cloacal Tbs

Tb (1C)

TA (1C)

Mean 7S.E.

Min

Max

Mean 7S.E.

Min

Max

24.72 7 0.81 23.077 0.57 29.057 0.53 29.207 0.29 28.72 7 1.39 26.73 7 1.69 30.057 1.02 30.727 0.76

14.1 15.3 17.3 22.8 20.7 22.3 26.2 28.2

34.5 30.3 36.3 33.3 35.3 34.4 33.4 33.3

24.34 7 0.61 26.23 7 0.63 29.37 7 0.50 31.91 7 0.29 29.037 0.89 30.007 1.15 30.927 1.33 26.67 7 0.95

15.5 18.0 21.0 22.0 23.8 26.0 25.0 23.0

32.5 35.0 36.0 40.4 32.0 35.0 33.5 29.0

of 23.07 70.57 1C and mean Ta of 26.2370.63 1C (Table 1). However, in winter basking was observed in 43% of leopard tortoises at Tas of 10–15 1C, with 68.8% of tortoises observed basking having cloacal Tbs of 5–15 1C (mean of 12.26 71.38 1C; Table 2). In summer, 83% of leopard tortoises were observed walking at Tas of 25–35 1C, when 80% had cloacal Tbs between 25 and 35 1C,

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with a mean cloacal Tbs of 29.05 70.53 1C (Table 1). Tortoises in winter walked at far lower Tas and cloacal Tbs than in summer, with 60% of tortoises observed walking at Tas between 15 and 20 1C, 80% of those tortoises having cloacal Tbs of 20–24 1C, with a mean cloacal Tbs of 21.67 70.71 1C (Table 2). Other behavioural activities in summer were observed at Tas of 25–35 1C, at higher cloacal Tbs of 30–35 1C (Table 1). It is notable that 89% of tortoises sought shade at Tas over 30 1C and 91% of the tortoises had cloacal Tbs between 25 and 35 1C, with a mean cloacal Tbs of 31.91 70.29 1C. (Table 1). An individual analysis of daily behaviour for the respective tortoises in summer 2002 and 2003, and winter 2002 and 2003 are shown in Figs. 4–7. Individual leopard tortoises were alert in the early morning when Ta minimum profiles approximated Ta maximum profiles (Figs. 4–7) as did the cloacal Tbs. As Ta minimum and maximum profiles began to deviate, tortoises left overnight shelters and began periods of basking (Figs. 4–7). In summer, tortoises started to actively bask from 09 h00 for a short period, and then became fully active, walking and feeding, before midday (Figs. 4 and 5). However, they all sought shade by 12 h00, and remained in shade until late afternoon, when activity was once again resumed (Figs. 4 and 5). As such, the summer activity pattern shown by leopard tortoises was bimodal. During winter, activity patterns of leopard tortoises were limited to short bouts of walking after midday, with tortoises staying alert in their overnight refuges for most of the morning and basking over the middle of the day and into the early afternoon (Figs. 6 and 7). Consequently, during winter leopard tortoises showed a unimodal pattern of activity.

Fig. 6. Representative plot of Ta maximum and minimum profiles (shaded) and external body temperatures (Tb) (dotted) of an individual leopard tortoise, with focal samples of cloacal Tb (solid squares), against time of day during winter 2002. Types of behavioural activity by individual tortoises are A ¼ alert; B¼basking; W¼ walking; F ¼ feeding; S ¼shade; I ¼inactive.

Table 2 Winter mean (7 S.E.), minimum and maximum cloacal body temperatures and ambient temperatures (1C) for each behavioural activity observed in free-ranging leopard tortoises. Behaviour

Alert Basking Walking Inactive

Tb (1C)

TA (1C)

Mean7 S.E.

Min

Max

Mean7 S.E.

Min

Max

11.93 7 0.62 12.26 7 1.38 21.67 7 0.71 12.97 2.44

1.8 2.2 18.1 4.1

25.7 21.6 25.5 21.5

12.51 7 0.42 12.25 7 1.07 18.007 0.67 7.947 1.29

3.0 3.5 14.5 2.0

20.5 20.5 20.5 13.0

Fig. 5. Representative plot of Ta maximum and minimum profiles (shaded) and external body temperatures (Tb) (dotted) of an individual leopard tortoise, with focal samples of cloacal (Tb) (solid squares), against time of day during summer 2003. Types of behavioural activity by individual tortoises are A ¼alert; B¼ basking; I¼ inactive.

Fig. 7. Representative plot of Ta maximum and minimum profiles (shaded), external body temperatures (Tb) (dotted) and internal core Tb (dot-dash) of an individual leopard tortoise, with focal samples of cloacal Tb (solid squares), against time of day during winter 2003. Types of behavioural activity by individual tortoises are A ¼ alert; B¼ basking; W ¼ walking; F¼ feeding; S ¼shade; I¼ inactive.

In general, all individually monitored leopard tortoises in summer 2002 and 2003 had cloacal Tbs lower than their external Tbs, and lower than that of the Ta maximum profile over the course of a day (Table 1, Figs. 4 and 5). External Tbs were similar to Ta maximum and minimum in the early morning, with temperatures increasing steadily towards midday. Towards late afternoon, Ta maximum and external Tbs decreased, but cloacal Tb decreased more slowly resulting in the cloacal Tbs of tortoises being higher than Ta maximum profiles for the early part of the night (Figs. 4 and 5). In winter, the cloacal Tb of individually identified tortoises was generally higher than Ta minimum profiles but as in summer it was consistently lower than their external Tb (Table 2, Figs. 6 and 7). Cloacal Tbs were closely correlated to the internal core Tb in the morning and early afternoon; although cloacal Tbs were lower than internal in the late afternoon for all tortoises. Internal core Tb of tortoises in July 2003 (winter) were consistently higher than Ta before 09 h00 in the morning. Tas then rose more sharply than internal core Tbs over the course of the morning, but by midday, internal core Tbs had again risen above Ta and remained higher throughout the afternoon and into the evening (Figs. 6 and 7).

M.K. McMaster, C.T. Downs / Journal of Thermal Biology 38 (2013) 178–185

4. Discussion Leopard tortoises followed the classic daily pattern of chelonian thermoregulatory behaviour (Cloudsley-Thompson, 1970; McGinnis and Voigt, 1971; Lambert, 1981; Meek, 1984; Loehr, 2002), exhibiting more bimodal activity patterns in summer and unimodal activity patterns in winter. The switch from bimodal activity in summer to unimodal activity under cooler conditions has been widely reported in many reptiles including chelonians (Lambert, 1981; Meek, 1988; Geffen and Mendelssohn, 1989; Foa‘ et al., 1992, 1994; Innocenti et al., 1994; Hailey and Coulson, 1996b; Hailey and Loveridge, 1998; Loehr, 2002; Ramsay et al., 2002). Higher summer Tas consequently allow for a reduction in basking time and an increase in the amount of time available for locomotory activity, however tortoises must seek shade at midday to avoid internal Tbs reaching critical thermal maxima. Swingland and Frazier (1979) found that heat-death, as a result of over-exposure to midday temperatures, was a major cause of death in the Aldabran giant tortoise (Geochelone gigantea). Other tortoise species living in hot climates seek shade over midday, and thus exhibit a bimodal activity pattern in summer (CloudsleyThompson, 1970; McGinnis and Voigt, 1971; Rose and Judd, 1975; Lambert, 1981; Meek, 1984, 1988). In this study it was not uncommon for midday temperatures to exceed 40 1C. In winter, basking for several hours was required by the tortoises until Tbs were sufficiently elevated to support activity. As such, activity behaviour was typically unimodal and towards midday, as found in other tortoise species when under cooler conditions (Hailey et al., 1984; Meek, 1984, 1988; Geffen and Mendelssohn, 1989; Hailey and Loveridge, 1998; Loehr, 2002; Ramsay et al., 2002). In addition, if Ta maximum and minimum profiles remain low during the day, minimum optimal Tb may not necessarily be reached by tortoises, in which case they remain basking or alert in their refuges for the entire day, as was found in other tortoises at lower ambient temperatures (Lambert, 1981; Hailey et al., 1984; Meek, 1988; Loehr, 2002). Leopard tortoises in summer had lower Tbs than Ta maximum profiles over the course of a day. Tbs were similar to Tas in the early morning, while towards late afternoon Tb decreased at a slower rate than Ta minimum profiles resulting in Tbs of tortoises being higher than Ta minimum or maximum profiles overnight. In winter, the core Tb of tortoises were generally higher than Ta minimum and maximum profiles showing facultative homeothermy. In winter Leopard tortoises were active at lower Tb, and at lower Ta maximum and minimum profiles, than in summer. Leopard tortoises would become alert and start basking and walking when their Tbs were 10–15 1C lower in winter than in summer. It has been widely reported that locomotory activity in tortoises is not supported until the tortoise has reached its optimal Tb and that tortoises will remain inactive or continue basking until these Tbs have been reached (Branch, 1984; Pulford et al., 1984; Meek, 1988; Geffen and Mendelssohn, 1989; Hailey and Coulson, 1996b; Loehr, 2002; Ramsay et al., 2002). Other studies have verified this figure. Perrin and Campbell (1981) have suggested 28.7 1C as a preferred temperature for leopard tortoises, while Hailey and Loveridge (1998) reported that leopard tortoises had a preferred Tb of 32.6 1C in a warm climate and 29.1 1C in a cooler high altitude climate. However, in this study, it was found that Leopard tortoises began locomotory activity at a range of temperatures which were dependant on the ambient temperature available in a particular season. This is similar to the conclusions of Meek (1988) who argued that seasonal changes in recorded Tbs of T. hermanni are unlikely to indicate seasonal differences in optimal means or ranges, but more probably reflect the Tbs tolerated for activity. Therefore, in a climate where environmental temperatures fluctuate widely, they represent a compromise between physiological optima and ecological reality.

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High Tas have a large and often primary influence on the activity patterns of tortoises (Rose and Judd, 1975). Various tortoise species seek shade above a range of upper limits of Ta, (e.g. Ramsay et al., 2002; Hailey and Coulson, 1996a, 1996b; Geffen and Mendelssohn, 1989; Lambert, 1981; Meek, 1988; Cloudsley-Thompson, 1971). In this study, it was found that leopard tortoises began to move to shade when Ta minimum profiles approached 30 1C in summer in 2002 but in 2003 tortoises were sometimes in shade at Ta minimum below 30. Thermal homeostasis has been recorded in tortoise species and is usually achieved through behavioural means (CloudsleyThompson, 1971; McGinnis and Voigt, 1971; Cloudsley-Thompson, 1972). However, in this study, leopard tortoises did not maintain or attempt to defend a particular Tb. Instead, leopard tortoises oscillated between a narrow range of Tb using different behaviour in summer and winter. In summer these behaviours included seeking shade when it became too hot, while in winter extended periods of basking and passive thermoregulation were used to maintain Tb (McMaster and Downs, 2006). In conjunction with behaviour, some physiological mechanisms such as vascular shunting, vasoconstriction and vasodilatation, can be used to manipulate Tbs to a greater extent allowing for further Tb stability, as shown in other tortoise species (Lambert, 1981). The adoption of these mechanisms maximizes the time the tortoise is within its optimal Tb, while avoiding exposure to ecologically lethal temperatures (Swingland and Frazier, 1979; Lambert, 1981; Meek, 1984). An additional adaptation towards Tb maintenance is the thermal lag illustrated in Fig. 1. Although, heating is closely correlated with rising Ta maximum and minimum profiles in the morning, this correlation is broken as Ta minimum profiles decreased. It appears that thermal inertia aided by the selection of overnight refuges and tortoises’ orientation within the refuges (McMaster and Downs, 2006), and by physiological mechanisms such as vasoconstriction (Lambert, 1981), prevented the tortoises’ Tbs from decreasing to the extent of Ta maximum and minimum profiles. Leopard tortoises in this study showed seasonal differences in their daily activity patterns, the Ta minimum profile and core Tb at which certain behaviours can be performed, and the ability to cope with large variations in daily and seasonal Tas. For example, at very low Tas in winter, leopard tortoises showed tolerance of low Tb by becoming active at lower Tb, and therefore were able to increase the period over which walking and feeding could take place. In addition, through thermoregulatory behaviour, tortoises were able to maintain core Tbs that were independent of extreme Tas in summer and winter, thus maximizing the time spent at their target Tb range and allowing for longer daily activity periods. In conclusion leopard tortoises can maintain their core Tb independent of Ta, and alter their daily and seasonal activity patterns to do so. They used different behavioural mechanisms in summer and winter to maintain their core Tb at different levels compared with Ta minimum and maximum profiles, and consequently although considered ectotherms, they maintained their core Tb independent of Ta. This was in conjunction with a degree of thermal inertia because of their relatively large size as shown in other relatively large chelonians (Frair et al., 1972).

Acknowledgments We are grateful to D. and C. Theron of Wonderboom, De Aar for allowing us to work on their farm; C. Dearden for the design, construction and maintenance of transmitters; Dr. D. Anderson TM for anaesthetising and implanting iButtons into tortoises, Sarah Pryke for field assistance, Stuart Taylor for assistance with data

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Table A1 TM Morphological characteristics of individual free-ranging leopard tortoises over a two-year period in the Nama-Karoo. Leopard tortoises that had ‘‘internal’’ iButton surgically implanted in 2003 are indicated with an asterisk. Abbreviations: No ¼Identification number; S ¼Sex; CCL ¼ Curved Carapace Length; CCW¼ Curved Carapace Width; CCS¼Carapace Side; SCL ¼Straight Carapace Length; SCW¼ Straight Carapace Width; FMSG¼ Front Marginal Shield Gap; SCH ¼Straight Carapace Height; PLL ¼Plastron length; PLW¼ Plastron width. Date

No

S

CCL

CCW

CCS

SCL

SCW

FMSG

SCH

PLL

PLW

Mass (kg)

Feb ‘02 Feb ‘02 Feb ‘02 Feb ‘02 Feb ‘02 Feb ‘02 Feb ‘02 Feb ‘02 Feb ‘02 Feb ‘02 July ‘02 July ‘02 July ‘02 July ‘02 July ‘02 July ‘02 July ‘02 July ‘02 July ‘02 July ‘02 Feb ‘03 Feb ‘03 Feb ‘03 Feb ‘03 Feb ‘03 Feb ‘03 Feb ‘03 Feb ‘03 Feb ‘03 July ‘03 July ‘03 July ‘03 July ‘03 July ‘03 July ‘03 July ‘03

9 17 40 64 11 15 22 57 111 112 9 17 40 64 22 11 15 57 111 112 9n 13 17 64n 113 11 15 22n 111n 9n 17n 64n 15 22n 57 62

M M M M F F F F F F M M M M F F F F F F M M M M M F F F F M M M F F F F

52.0 58.0 46.0 56.0 61.0 64.0 57.0 59.0 51.0 52.0 56.0 60.0 54.0 58.0 65.0 64.0 66.0 58.0 52.0 55.0 58.0 57.0 59.0 59.0 40.0 61.0 64.0 58.0 53.0 58.0 60.0 61.0 66.0 58.5 60.5 56.0

50.0 53.0 52.0 53.0 62.0 61.0 57.0 56.0 50.0 55.0 53.0 57.0 51.0 53.0 59.0 62.0 65.0 56.0 52.0 55.0 51.0 53.0 57.0 54.0 39.0 61.0 65.0 57.5 51.0 53.0 54.0 56.0 64.0 57.5 56.0 58.0

53.0 59.0 53.0 57.0 59.0 63.0 56.0 60.0 52.0 55.0 59.0 64.0 56.0 58.0 58.0 64.0 70.0 63.0 52.0 59.0 56.0 57.0 61.0 61.0 39.0 64.0 67.0 61.0 50.0 59.5 63.0 58.0 66.0 61.5 61.0 59.0

42.0 48.0 42.0 46.0 48.0 51.0 45.0 46.0 39.0 43.0 47.0 50.0 41.0 47.0 52.0 52.0 51.0 43.0 38.0 45.0 44.0 45.0 49.0 52.0 32.0 49.0 48.0 46.0 41.0 47.0 53.0 46.0 52.0 45.0 46.0 45.0

27.0 30.0 28.0 29.0 32.0 34.0 30.0 31.0 26.0 29.0 32.0 32.0 28.0 30.0 32.0 35.0 36.0 30.0 26.0 30.0 28.0 28.0 32.0 29.0 22.0 34.0 36.0 32.0 27.0 31.0 53.0 30.5 38.0 33.0 34.0 31.5

7.3 11.0 9.0 12.0 10.0 11.0 9.0 8.0 9.0 9.0 10.0 11.0 9.0 12.0 10.5 10.0 11.5 8.0 9.0 8.0 11.0 10.0 11.0 12.0 7.0 10.0 11.0 9.5 9.0 10.0 12.0 11.0 11.0 10.0 9.0 10.0

20.0 21.0 19.0 21.0 22.0 21.0 20.0 21.0 16.0 19.0 21.0 21.0 19.0 21.0 20.0 22.0 21.0 21.0 16.0 19.0 20.0 22.0 21.5 21.0 17.0 22.0 25.0 22.0 19.0 22.0 25.0 24.0 23.0 23.0 22.0 23.0

37.0 39.0 33.0 38.0 37.0 41.0 39.0 38.0 32.0 34.0 39.0 40.0 34.5 38.0 39.0 37.0 42.0 39.0 32.5 35.0 39.0 37.0 39.5 38.5 27.0 37.0 42.0 39.5 33.0 40.0 42.0 39.5 42.5 40.0 39.0 37.0

28.0 29.0 26.0 29.0 34.0 35.0 31.0 30.0 25.0 30.0 30.0 31.0 27.0 29.0 30.0 32.0 34.0 33.0 25.0 29.0 30.0 31.0 29.5 28.0 20.0 32.0 35.0 31.0 27.0 29.0 32.0 30.0 36.0 32.0 30.0 30.0

12.0 14.5 9.0 12.6 15.0 19.0 14.5 15.5 10.0 13.8 11.9 12.4 9.2 13.1 13.4 13.6 16.8 12.6 8.8 11.4 11.2 12.4 12.6 13.4 4.8 14.2 19.8 13.3 9.4 12.2 13.8 13.8 18.2 12.6 13.8 12.8

analysis; and the National Research Foundation (GUN 2053510) for financial assistance. The research had University of KwaZuluNatal ethics approval and conformed to provincial and national guidelines.

Appendix A See Appendix Table A1.

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