Stigmochelys pardalis Bell, 1828 - IngentaConnect

Seasonal and daily activity patterns of leopard tortoises (Stigmochelys pardalis Bell, 1828) on farmland in the Nama-Karoo, South Africa M.K. McMaster & C.T. Downs* School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, Pietermaritzburg, 3209 South Africa Received 16 November 2012. Accepted 20 March 2013

The leopard tortoise (Stigmochelys pardalis) is the largest of southern Africa’s 13 tortoise species, and occurs in a variety of habitats from arid and semi-arid areas to mesic grassveld, savanna and bushveld. Seasonal activity patterns of S. pardalis were investigated as a function of rainfall, sex, time of day, temperature and time after sunrise on farmland in the semi-arid Nama-Karoo, South Africa. We predicted that because of seasonal rainfall, and subsequent increase in the food available, activity patterns of leopard tortoises would vary greatly among seasons, but that the primary constraint on activity levels within a season would be ambient temperature. Type of activity, time of day that the activity was performed, and the frequency that each activity was performed, differed among seasons. There was no overall seasonal difference in the level of activity with sex, but in certain seasons and with regard to specific activities, there were significant differences between the sexes. Diel activity was primarily bimodal in summer and autumn, and unimodal in winter and spring, with nonthermoregulatory activities being performed primarily in the afternoon. There was a positive correlation between number of tortoises caught and rainfall per season, but activity levels and number of tortoises walking and feeding was not correlated with seasonal rainfall. Leopard tortoise activity behaviours responded to ambient temperature, but results indicate that activity is also initiated by the time since sunrise. Key words: Stigmochelys pardalis, leopard tortoise, activity patterns, activity behaviour, Nama-Karoo Biome, time of day, season.

INTRODUCTION The leopard tortoise (Stigmochelys pardalis Bell, 1828; previously Geochelone pardalis Fritz and HavaÓ 2006) is found in parts of central and southern Africa in a variety of habitats including arid Karoo, Kalahari thornveld, grassveld, savanna and tropical bushveld (Boycott & Bourquin 2000). It is the largest of southern Africa’s 13 tortoise species (Van Dijk et al. 2011). Despite its large size and wide distribution, there is relatively little published information regarding its ecology, physiology and behaviour, particularly in more xeric areas, with most of the studies being taxonomic, anecdotal or relating to captive individuals (Branch 1988; Lombard 1995; Kabigumila 1998; Boycott & Bourquin 2000; McMaster & Downs 2006a,b, 2008, 2009; Wimberger et al. 2009). There are some studies of the food habits, size composition and sex ratio in the wild (Milton 1992; Rall & Fairall 1993; Mason et al. 1999; Kabigumila 2001a,b,c). Preliminary observations of field activity behaviour of leopard tortoises during the day (Rall 1985; Kabigumila *Author for correspondence. E-mail: [email protected]

2001a,b; Douglas & Rall 2006; McMaster & Downs 2006b) and over seasons (Jacobsen 1978; Grobler 1982; Patterson et al. 1989; Hailey & Coulson, 1996a; Kabigumila 2001a,b; McMaster & Downs 2006a,b) have been made, as well as in terms of habitat selection and refuge use (Douglas & Rall 2006; McMaster & Downs 2006a,b). Thermoregulatory behaviour in this species was investigated by Perrin & Campbell (1981) and McMaster (2007). Tortoises (family Testudinidae) are ectothermic and therefore their temporal and spatial activity and behavioural patterns depend on environmental constraints (Rose & Judd 1975; Meek 1984; Hailey & Coulson 1996b; Kazmaier et al. 2001). The relative importance of each of these environmental factors, particularly temperature and rainfall, in determining activity patterns of tortoises varies between species and between areas. Ambient temperature is the most well-documented environmental factor influencing both the period and type of activity of tortoises, for example, the Mediterranean Testudo spp. (Lambert 1981; Meek 1984, 1988; Geffen & Mendelssohn 1989) and Gopherus berlandieri in

African Zoology 48(1): 72–83 (April 2013)

McMaster & Downs: Seasonal and daily activity patterns of leopard tortoises

Texas (Rose & Judd 1975; Kazmaier et al. 2001). However, rainfall was the primary influence on activity of leopard tortoises in the Serengeti, and was significantly correlated with the activity of Kinixys spekii in Zimbabwe (Bertram 1979a,b). However, occurrence of rainfall in a season can be disjunct to the activity observed. For instance, if rain falls on day one or week one of a season, but the rest of the season is dry, activity for the season might seem elevated even though there was no further rain; that is, the tortoises may replenish water reserves (Nagy & Medica 1986) and have little need for further drinking. An opposite result may occur if the season is dry until the last few days or weeks, so that tortoise activity is low during the season, but high immediately after the rain. Reduced activity during the dry season or a drought may be correlated with the availability of food and water, rather than directly to rainfall or temperature (Lambiris et al. 1987; Hailey 1989; Peterson 1996). Cloudsley-Thompson (1970) showed a distinct ‘temperature-independent circadian rhythm of activity’ in Geochelone (or Centrochelys) sulcata that was unaffected by photoperiod, while the primary influence on daily activity in T. hermanni was habitat type (Wright et al. 1988). Hailey & Coulson (1996b) concluded that seasonal activity for Kinixys spekii in Zimbabwe was positively correlated with rainfall, but during a specific season, level and pattern of activity was positively correlated with temperature (see also Nagy & Medica 1986). Further influences on the type of activity and activity pattern are wind speed, cloud cover, humidity, age and sex (see Lambert 1981; Meek 1984; Els 1989; Diemer 1992). We investigated activity patterns and behaviour of leopard tortoises on farmland in the semi-arid Nama-Karoo, South Africa, as a function of temperature, time of day, season and sex. We predicted that because of seasonal rainfall and temperature changes, activity patterns of leopard tortoises would vary greatly among seasons, but that the primary environmental constraint on activity levels within a season would be ambient temperature. MATERIALS & METHODS Our study area was in the De Aar District, NamaKaroo biome, South Africa (31°04’S, 23°41’E) as detailed in McMaster & Downs (2006a,b, 2009) where a weather station (South African Weather Bureau) at the site collects daily minimum and maximum ambient temperatures and rainfall. Mean minimum and maximum ambient tempera-

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tures (±S.E.) and total rainfall per season at the study site from summer 1997 to autumn 1999 are shown in Fig. 1. Although the area has its highest rainfall in late summer and autumn, the average annual rainfall is low (200–400 mm). Temperatures ranged from 5°C to 39°C in spring (September– November) and summer (December–February), and from –5°C to 26°C in autumn (March–May) and winter (June–August). We located leopard tortoises by riding transects on horseback across the study area twice daily (McMaster & Downs 2006a,b, 2009). Individual tortoises were marked using a coded sequence of notches filed into their marginal scutes following Branch (1984). All tortoises were sexed, weighed and various morphometric characteristics were recorded when first encountered (McMaster & Downs 2006a,b). Date, time, individual marking, body mass, sex and type of activity were recorded for all tortoises observed. Geographical positions of all tortoises located were recorded using a handheld Trimble Navigation GeoExplorer II Geographical Position System unit. In addition to opportunistic sightings, adult females (n = 8) and males (n = 6) were radio-tracked (McMaster & Downs 2006a,b). Telemetered leopard tortoises were located twice daily from October 1997 to April 1999 and their geographic location and behaviour recorded. In addition, each individual telemetered tortoise was followed for a continuous 18 h period (from 04:00 to 22:00) once every three months, and its behaviour and location recorded every 15 min. Data of activity from all these observations were used in the analyses as described below. We classified leopard tortoises as inactive or active. Inactive tortoises were those found with their head and legs retracted into their shells. Active tortoises were identified as performing one of seven behavioural activities (following Els 1989): i) alert: tortoise was in, or just out of its form, with its head and/or legs out of its shell; ii) basking: a tortoise orientated to expose the maximum shell surface area to the sun, often with limbs and neck extended; iii) walking; iv) feeding; v) drinking; vi) shading: tortoise was in the shade of a bush or other shelter, often with head and limbs extended; and vii) courtship and mating. All ambient temperatures (Ta) were expressed as means (±S.E.) and were measured to the nearest 0.5°C using a handheld thermometer in the shade 1 m above the ground. All statistical tests were calculated using STATISTICA software (Statsoft, Tulsa, Oklahoma, U.S.A.). Generalized linear models (GLIM) were

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African Zoology Vol. 48, No. 1, April 2013

Fig. 1. Seasonal minimum and maximum temperatures (mean ± S.E.) and total rainfall from January 1997 to May 1999 at the study site, De Aar district, Nama-Karoo, South Africa.

used to investigate the relationship between temperature and rainfall and behaviour of all tortoises observed. Repeated measures analysis of variance (RMANOVA) was used to compare the marked tortoises’ behaviour between seasons. Independent t-tests were used to compare differences between sexes in each season. The frequency (%) of each active behaviour was calculated as the number of observations over total observations for the season. RESULTS Data on number of leopard tortoises (n = 92) located, their body mass and sex ratio are presented elsewhere (McMaster & Downs 2006a,b, 2009). Daily activity and inactivity Leopard tortoise activity was observed on 3955 occasions over the total search time of 2615 person-hours. There was no significant correlation between the number of tortoises observed per month and the total rainfall per month (GLIM, R² = 0.05, F(1,16) = 0.84, P = 0.37), the mean minimum daily temperature per month (GLIM, R² = 0.14, F(1,16) = 2.63, P = 0.12) or the mean maximum daily temperature per month (GLIM R² = 0.07, F(1,16) = 1.17, P = 0.30). In addition, there was no

correlation between total rainfall per season and the number of active tortoises (GLIM, R² = 0.59, F(1,2) = 2.84, P = 0.23) or of inactive tortoises (GLIM, R² = 0.59, F(1, 2) = 2.87, P = 0.23) observed per season. Throughout the year, leopard tortoises were inactive overnight (pers. obs.), and generally became active after sunrise for the duration of the day, and became inactive in the late afternoon. In winter and spring tortoises became active later in the day and became inactive earlier in the afternoon, so overall remained active for shorter periods than in summer and autumn (Fig. 2). There was a significant difference in the number of active to inactive tortoises among seasons (RMANOVA, F(3,39) = 5.16, P = 0.004). Furthermore, a post hoc Sheffe test showed there was a significant difference within each season for spring, summer and autumn in the number of inactive to active tortoises (Sheffe test: P < 0.001). Initiation of leopard tortoise activity differed among seasons. The earliest time of day that at least 75% of the tortoises were active (usually alert), was 08:00 in spring (2.5 h after mean sunrise), 06:00 in summer (57 min after mean sunrise), 07:00 in autumn (46 min after mean sunrise) and 10:00 in winter (3.3 h after mean sunrise)


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Fig. 2. Number of inactive and active leopard tortoises of total observed over the hours of the day (06:00–19:00) for (a) spring, (b) summer, (c) autumn, and (d) winter with mean sunrise and sunset times. Black = inactive; grey = active.

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Table 1. Mean ± S.E. ambient temperatures for each hour of the day (06:00–19:00) for all the seasons. Hour of day

Spring

Summer

06:00 07:00 08:00 09:00 10:00 11:00 12:00 13:00 14:00 15:00 16:00 17:00 18:00 19:00

5.9 ± 0.8°C 12.8 ± 0.7°C 15.5 ± 0.7°C 19.4 ± 0.6°C 20.9 ± 0.4°C 22.8 ± 0.5°C 24.2 ± 0.5°C 23.6 ± 0.4°C 25.0 ± 0.4°C 26.2 ± 0.4°C 25.3 ± 0.4°C 23.5 ± 0.6°C 21.4 ± 1.3°C 19.0 ± 0.8°C

19.7 ± 1.3°C 23.5 ± 0.6°C 25.8 ± 0.3°C 28.3 ± 0.3°C 30.5 ± 0.4°C 32.0 ± 0.3°C 32.6 ± 0.7°C 34.0 ± 1.1°C 34.4 ± 0.9°C 34.5 ± 0.6°C 32.9 ± 0.3°C 31.7 ± 0.3°C 30.4 ± 0.3°C 30.1 ± 0.7°C

(Fig. 2). Mean Ta ± S.E. (Table 1) for summer and autumn were similar at these hours (19.7 ± 1.3°C and 19.5 ± 1.3°C, respectively), and were lower in spring (15.5 ± 0.7°C) and winter (13.6 ± 0.4°C). This shows that tortoises initiated activity at lower Tas in spring and winter. However, the period between sunrise and activity was 1–2 h longer in winter and spring than in summer. Sixty to 100% of the leopard tortoises observed on any day in summer were active by 08:00–09:00 (Ta = 25.8 ± 0.3–28.3 ± 0.3°C), while in spring, autumn and winter by 12:00 (Ta = 24.2 ± 0.5°C, Ta = 30.6 ± 1.1°C and Ta = 18.8 ± 0.3°C, respectively) (Table 1, Fig. 2). In autumn, 92–98% of tortoises were active from 08:00 (Ta = 23.6 ± 0.6°C), until all were found active at 12:00 (Ta = 30.6 ± 1.1°C) (Table 1, Fig. 2). Thus the temperature range at which most tortoises were active differed among seasons (Table 1, Fig. 2). Time and temperatures at which leopard tortoises returned to an inactive state showed great seasonal variation (Table 1, Fig. 2). While tortoises first became inactive at 15:00 in autumn and winter, 16:00 in spring, and only at 18:00 in summer (Fig. 2), mean ambient temperatures at these times ranged with spring (25.3 ± 0.4°C), summer (30.4 ± 0.3°C) and autumn (27.8 ± 1.2°C), but were lower for winter (Ta = 20.2 ± 0.4°C) (Table 1, Fig. 2). Most (>75%) tortoises were inactive in winter by 18:00 (Ta = 11.0 ± 0.7°C), an hour later at 19:00 in spring and autumn, (Ta = 19.0 ± 0.8°C and 21.5 ± 0.7°C, respectively), and a 20:00 in summer (Ta = 26.1 ± 0.7°C) (Table 1). These times

Autumn 16.6 ± 1.0° C 19.5 ± 1.3° C 23.6 ± 0.7° C 25.8 ± 0.7° C 26.0 ± 0.6° C 28.8 ± 0.8° C 30.6 ± 1.1° C 30.9 ± 0.4° C 28.5 ± 0.2° C 27.8 ± 1.2° C 27.0 ± 0.9° C 25.8 ± 0.7° C 23.7 ± 0.7° C 21.5 ± 0.7° C

Winter 2.7 ± 0.5°C 5.8 ± 0.4°C 9.3 ± 0.3°C 11.4 ± 0.3°C 13.6 ± 0.4°C 16.9 ± 0.5°C 18.8 ± 0.3°C 19.4 ± 0.3°C 19.8 ± 0.3°C 20.2 ± 0.4°C 17.0 ± 0.4°C 15.6 ± 0.4°C 11.0 ± 0.7°C 9.1 ± 0.7°C

corresponded with 30 min, 1.5 h, 45 min and 1 h after mean sunset in spring, autumn, winter and summer, respectively (Fig. 2). Active behaviour The percentage of leopard tortoises performing different activities varied daily and seasonally. Frequencies of the various active behaviours performed by tortoises per hour per season are shown in Fig. 3. Frequency of tortoises performing certain activities differed significantly with season: feeding (F(3,39) = 8.06, P = 0.0002, post hoc Scheffe tests show summer significantly higher than spring and winter, P < 0.05), drinking (F(3,39) = 8.48, P = 0.0002, winter significantly lower than other seasons, P < 0.05), walking (F(3,39) = 3.37, P = 0.028, winter significantly lower than other seasons, P < 0.05), mating (F(3,39) = 11.36, P = 0.00002, spring and summer significantly higher than autumn and winter, P < 0.05), alert (F(3 39) = 4.84, P = 0.006, winter significantly higher compared with other seasons P < 0.05), shading (F(3,39) = 9.89, P = 0.00006, summer significantly higher than other seasons P < 0.05), and inactive (F(3,39) = 12.30, P = 0.000008, winter significantly greater than other seasons P < 0.05). However, there was no significant seasonal difference in the frequency of tortoises found basking (F(3,39) = 2.46, P = 0.07). In order to compare seasonal frequency of certain activities between the sexes, the results were combined. In spring, males walked significantly more than females (t-test, t = 3.23, d.f. = 11, P = 0.008) and showed more non-thermoregulatory

Fig. 3. Percentages of total leopard tortoises observed performing the various active behaviours over the hours of the day (06:00–19:00) for (a) spring, (b) summer, (c) autumn, and (d) winter.

McMaster & Downs: Seasonal and daily activity patterns of leopard tortoises 77

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Table 2. Percentage (%) of leopard tortoises observed per season as inactive or performing one of the seven active behaviours when initially encountered during the daytime. Activity

Spring 1208

n: Active

Inactive

Feeding Drinking Basking Walking Mating Alert Shading

Summer 1239

Autumn 637

Winter 871

7.1 2.5 15.8 17.8 4.1 7.0 31.5

28.7 4.0 5.7 15.0 3.6 17.0 25.2

19.0 1.9 12.6 13.2 1.7 26.8 19.2

0.8 0.0 14.6 3.0 0.0 43.5 0.0

14.1

0.7

5.7

38.1

activities than females (walking, feeding, mating, drinking) (t = 3.066, d.f. = 27, P = 0.005). In contrast in spring females were significantly more alert (t = –3.07, d.f. = 12, P = 0.009) and performed more thermoregulatory activities (basking and shading) (t = –2.76, d.f. = 42, P = 0.008) than males. In summer, there was a significant difference between sexes in the number of tortoises observed alert with females being alert more frequently (t = 2.70, d.f. = 13, P = 0.018), and in winter, in the frequency of female tortoises observed basking more often than males (t = –8.49, d.f. = 8, P = 0.000028). There were no significant differences between sexes in autumn activities. Frequency and patterns of certain behaviours differed among the seasons in leopard tortoises. In spring, most were alert (31.5%), walking (17.8%), basking (15.8%) or inactive (14.1%) (Table 2). An unimodal pattern of activity was observed in spring, with tortoises basking in the morning, walking from late morning into the late afternoon, and feeding, drinking and mating throughout the day (Fig. 3a). Although mating was not observed often, the highest frequency of mating was observed in spring and none in winter (Table 2). In summer and autumn, more leopard tortoises were observed feeding (28.7% and 19.0%, respectively) and walking (15.0% and 13.2%, respectively) (Table 2) than the in other seasons. Both of these were particularly evident after seasonal rainfall. However, there was no significant correlation between total rainfall per season and frequency of tortoises observed walking (GLIM R² = 0.16, F(1,2) = 0.386, P = 0.597) or feeding (GLIM R² = 0.46, F(1,2) = 1.704, P = 0.322). In summer and autumn, tortoises appear to have increased walking and feeding activity because of other factors, possibly

increased food availability or higher Ta, rather than as a response to rain itself. In summer, higher Ta resulted in a low occurrence of basking activity (5.7%) compared with the other seasons, and a large occurrence of tortoises seeking shade (25.2%) compared with other seasons (Table 2). In winter, most tortoises were found either inactive (38.1%) or alert (43.5%), while basking was displayed by 14.6% of the tortoises and walking by only 3.0% (Table 2). There was a distinct bimodal pattern of nonthermoregulatory activity in leopard tortoises during the day in summer and autumn (Fig. 3b,c). In summer, tortoises were observed feeding and walking for a limited period in the morning, sought shade from as early as 08:00 until as late as 18:00, and would usually resume feeding and walking only after 15:00 (Fig. 3b). Most walking and feeding activity took place in the afternoon (Fig. 3b). Similarly, in autumn, tortoises were primarily found alert or basking in the morning, were observed walking and feeding in the late morning and sought shade from 09:00 over midday (some staying in the shade until as late as 17:00), with most walking and feeding to a greater extent after 15:00 (Fig. 3c). Drinking was observed primarily in summer, occurring throughout the day and being more frequent from midday into the late afternoon. Mating was observed in the morning and late afternoon (Fig. 3b). In winter, tortoises were unimodal in activity and mainly performed thermoregulatory activity, being found inactive until midday, and alert or basking throughout the day (Fig. 3d). No tortoises were observed mating, drinking or seeking shade in winter.


DISCUSSION Seasonal activity In the Serengeti, 91% of all leopard tortoises were observed during the wet season, although this was partly due to tortoises being more visible and easier to find when walking (Bertram 1979a). In the present study, visibility was not a major factor as the vegetation cover was low and sparse and visual observations were done from horseback. Furthermore, there was no correlation between the number of leopard tortoises observed per month and monthly rainfall, monthly minimum or monthly maximum temperatures. Similarly, Geffen & Mendelssohn (1989) found no correlation existed between the number of Testudo kleinmanni caught per month and either monthly rainfall, rainfall from the previous month or humidity. In addition, Bertram (1979b) found no correlation between mean daily distance travelled per month (a measure of activity) by Kinixys belliana, and total rainfall in that month, mean maximum temperatures, humidity levels, number of rainy days or rainfall from previous months. Monthly sightings of K. spekii were correlated with rainfall, but not temperature or humidity (Hailey & Coulson 1996b). Leopard tortoise activity was thought by Hailey & Coulson (1996b) to be significantly related to both rainfall and temperature, and Bertram (1979a) found that 91% of all movements by leopard tortoises in the Serengeti were made after rain. Similarly, desert tortoises G. agassizii showed large seasonal changes in activity, influenced by rainfall and temperature (Nagy & Medica 1986). While rain caused an increase in the activity of K. spekii, it was the plant growth following rainfall that was the primary cause of increased tortoise activity (Lambiris et al. 1987). Similarly, the Aldabra giant tortoise (Aldabrachelys gigantea) showed seasonal changes in activity in response to changes in food availability (Gibson & Hamilton 1983). There was no correlation between seasonal rainfall and either activity or inactivity of leopard tortoises in the Nama-Karoo. Increased activity at the actual time of rainfall and within the same month of rainfall, has been recorded in many tortoise species, for example, T. kleinmanni (Geffen & Mendelssohn 1989), G. agassizii (Nagy & Medica 1986), K. spekii (Lambiris et al. 1987) and leopard tortoises (Patterson et al. 1989). However, Hailey & Coulson (1996b) proposed that changes in activity associated with rainfall may also be accounted for

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by the lower maximum temperatures occurring during rain. In the present study though, daily activity of leopard tortoises increased in summer and autumn compared with winter and spring. There was a significant increase in summer and autumn in the frequency of some active behaviours. Similarly many other tortoise species, for example, K. belliana, G. berlandieri and T. kleinmanni, alter their daily activity periods in response to seasonal changes, becoming active earlier, reducing midday activity, staying active later in the day under hot conditions (Rose & Judd 1975; Bertram 1979b; Meek 1988; Geffen & Mendelssohn 1989; Kazmaier et al. 2001), and showing a reduction in activity during winter months (Hailey et al. 1984; Els 1989; Diemer 1992; Hailey & Coulson 1996b). Testudo hermanni showed great variation in activity among months (Hailey, 1989), while K. spekii used changes in daily activity patterns as a primary thermoregulatory mechanism (Hailey & Coulson 1996c). The activity of another southern African tortoise Chersina angulata also varies with season, temperature and time of day (Ramsay et al. 2002; Keswick et al. 2006) but this may be affected by the island habitat where they were observed. Only in spring were there significant sex differences in leopard tortoises’ activity with males more frequently active than inactive, highlighting that generally sexes behave similarly. Chersina angulata also show sexual disparity in activity patterns and time budgets during spring (Keswick et al. 2006) but again this may be affected by the island habitat where they were observed. In comparison T. hermanni showed no difference in activity levels between the sexes in any month (Hailey 1989), however sex ratios at two different study sites varied seasonally, suggesting that seasonal differences in activity of the sexes may occur (Hailey et al. 1984). Environmental cues and activity Environmental cues that initiated activity appear complex in leopard tortoises. Ta appears an important factor influencing the onset of activity and yet tortoises were active at lower Tas in spring and winter, when activity began later (1–2 h) after sunrise, than in summer or autumn. While time of day is useful as a measure of daily activity change, other factors that are related to time of day, such as Ta and length of photophase which affects light intensity, may be the primary factors that initiate tortoise activity. In spring and summer, T. graeca

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Table 3. Tortoise species that show a bimodal and a unimodal pattern of activity, as observed in leopard tortoises. Generally, bimodal activity occurs under warm conditions, and unimodal activity occurs in cooler seasons. Species

Reference

Chersina angulata Dipsochelys dussumieri Geochelone nigra Geochelone sulcata Geochelone yniphora Gopherus agassiziI Gopherus berlandieri Gopherus polyphemus Kinixys spekii Psammobates geometricus Stigmochelys pardalis Testudo hermanni Testudo graeca

Els 1989; Ramsay et al. 2002 Bourn & Coe 1978 Rodhouse et al. 1975 Cloudsley-Thompson 1970 Juvik et al. 1981 McGinnis & Voigt 1971; Zimmerman et al. 1994 Rose & Judd 1975 Douglass & Layne 1978 Hailey & Coulson 1996 Baard 1990 Rall 1985; Kabigumila 2001b; present study Hailey et al. 1984; Mazzotti et al. 2002* Lambert 1981; Wright et al. 1988

*Unimodal activity in summer because of cooler conditions.

were active at Tas of 18–32°C, primarily between 12:00 and 16:00, with activity being initiated below 23°C and before 12:00 (Lambert, 1981). Despite differences in actual time (before 12:00) at which most leopard tortoises were active, Tas were between 18°C and 26°C. Similarly, T. kleinmanni were found active at a wide range of Tas from 17–45°C, but 52% were active between 21°C and 24°C (Geffen & Mendelssohn 1989). Interestingly Chersina angulata can be active at Ta = 9°C (Keswick et al. 2006) which is far lower but this may be affected by the island habitat where they were observed. Similarly, environmental cues that terminated activity of leopard tortoises were complex, as tortoises did not seem to respond exclusively to either decreasing Tas or reduced photophase affecting light intensity, but rather the combination of both. Similarly, T. graeca were active at Tas of 18–32°C between 08:34 and 18:31, however, few tortoises were still active during the 1.5 hours before sunset, and their activity depended not only on Ta, but also time of day at which Ta was reached (Lambert 1981). Active behaviours There were notable differences among seasons in type, duration and time of day that the activities were performed by leopard tortoises. Frequency of the activity differed among some seasons. Similarly other tortoise species have been widely reported to show a high seasonal variation in activity patterns (Lambiris et al. 1987; Geffen & Mendelssohn 1989; Hailey 1989). Psammobates geometricus are active throughout the year but

with higher activity in autumn and spring (van Blomestein 2005). Temperature has been widely recorded in association with tortoise activity as an indication of daily activity patterns (Lambert 1981; Gibson & Hamilton 1983; Hailey et al. 1984; Meek 1984; Samour et al. 1987). Geffen & Mendelssohn (1989) found that T. kleinmanni were active between 17°C and 28°C, with 52% active within a range of 21–24°C. The daily activity pattern of K. spekii differed if the maximum Ta was above or below 29°C (Hailey & Coulson 1996b). When Tas were below 29°C, K. spekii showed a unimodal activity pattern and above it, a bimodal. Similarly, in spring and summer, T. graeca was active between 18°C and 32°C, with a switch from unimodal to bimodal activity patterns occurring at 28°C, and tortoises becoming inactive below 18°C (Lambert 1981). Activity in these cases was clearly temperature dependent. Basking by leopard tortoises was at a similar frequency in spring, autumn and winter, but at a lower frequency in summer. Similarly high summer Ta reduced the basking activity of T. hermanni, allowing for increased time available for locomotory activity and feeding (Meek 1984, 1988). A bimodal pattern of activity under warm conditions, and a switch to a unimodal activity pattern in cooler seasons, as we observed in leopard tortoises, is well-documented for tortoises (see Table 3 for summary). It would suggest this is to avoid extreme temperatures during the midday in summer. However, high Tas restricted the activity period of T. kleinmanni before shade had to be sought (Geffen & Mendelssohn 1989). Meek (1984)


noted that the Ta range over which locomotion, feeding and mating occurred was very narrow compared with the temperature window over which basking, shading and other thermoregulatory activities were performed. Thus while leopard tortoises may be alert or basking at low Tas, some of their further activity requires a higher Ta while even higher Tas will cause tortoises to seek shade to avoid overheating. When daily Tas are consistently high for the whole season, for example in the Nevada and Negev deserts, tortoises G. agassizii and Testudo spp., respectively, changed their activity patterns seasonally and had their main activity period during spring, while reducing and limiting activity to avoid midday heat in summer (Nagy & Medica 1986; Geffen & Mendelssohn 1989). Similarly, leopard tortoises in the semi-arid Nama-Karoo show a similar pattern. However, following rainfall in summer, G. agassizii were active despite high Tas (Nagy & Medica 1986). Aestivation was initiated in K. belliana during dry conditions and in T. hermanni due to a digestive bottleneck (Hailey 1989). Generally tortoises appear to respond to a combination of environmental and physiological stimuli and show plasticity in their behaviour and activity patterns (Kazmaier et al. 2001). Leopard tortoises’ activity and behaviour seem to agree with this statement. In summary, time of day, ambient temperature and time after sunrise, affect initiation of activity in leopard tortoises. They showed a response to temperature with regard to activity. Activities in summer and autumn were performed at the same Tas, despite the difference in the time of day at which these temperatures were reached. Tortoises commenced activity at lower Tas in winter and spring, however, the time of day in spring at which these were observed were the same as in summer. Low seasonal variation in the time after sunrise at which activity commenced indicated that after a certain time after sunrise, leopard tortoises became alert, basked, walked and fed, irrespective of the Tas at that time (which in spring and winter, was still very low). While tortoises are generally reported to stay inactive until Tas rise above a certain limit, for example, in T. graeca Ta = 18°C (Lambert 1981), tortoises in winter and spring in this study were walking and feeding below 18°C. Therefore, Tas appear to be one of the main influences on activity and active behaviours of leopard tortoises, and together with time after sunrise also appears to initiate tortoise activity.

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