What factors allow opportunistic nocturnal activity in a primarily diurnal desert lizard (Ctenotus pantherinus)?

Comparative Biochemistry and Physiology, Part A 156 (2010) 255–261

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What factors allow opportunistic nocturnal activity in a primarily diurnal desert lizard (Ctenotus pantherinus)? Chris E. Gordon, Christopher R. Dickman, Michael B. Thompson ⁎ Institute of Wildlife Research, School of Biological Sciences, Heydon-Laurence Building (A08), University of Sydney, NSW 2006, Australia

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Article history: Received 15 June 2009 Received in revised form 8 February 2010 Accepted 11 February 2010 Available online 17 February 2010 Keywords: Arid zone Diel activity Mean selected temperature Metabolic rate Prey sensory perception Skink Termite

a b s t r a c t Most animals show strong 24-h patterns of activity, usually being diurnal or nocturnal. An Australian desert skink, Ctenotus pantherinus, is unusual in being active day and night when all other Ctenotus species are diurnal, making it an excellent model to explore factors that promote night-time activity. We tested whether C. pantherinus 1) selects cooler temperatures than diurnal skinks, 2) shows no difference in mean selected temperature between day and night, 3) has the same metabolic rate during the day and night, 4) selects termites over other prey types, 5) can detect prey using only auditory or olfactory senses, and 6) experiences lower predation risk at night than during the day. C. pantherinus shows many features of diurnal skink species, with a high mean selected temperature (36.1 ± 1.6 °C) that is the same night and day, and a 32% lower metabolic rate at night than during the day. C. pantherinus selects termite prey over other insects and can detect prey using only auditory and olfactory senses; models of C. pantherinus experienced less predation at night than during the day. Preference for termites and reduced predation risk at night favour opportunistic nocturnal activity in this predominantly diurnal lizard and may contribute to its wide geographic distribution in arid Australia. © 2010 Elsevier Inc. All rights reserved.

1. Introduction Animals generally show predictable 24-h patterns of activity, being strictly diurnal, nocturnal or crepuscular (Takahashi et al., 2001). Circadian rhythms allow animals to anticipate imminent changes in their social and physical environment and to prepare appropriate responses (Aronson et al., 1993). The ecological consequences of such rhythms may be profound. For example, differences in the daily time of activity allow species to avoid interspecific competition and to partition shared resources, resulting in increased local species diversity (Carothers and Jaksic, 1984; Werner and Anholt, 1993; Pinter-Wollman et al., 2006). Shifts in daily activity also can occur between trophic levels, with predators and prey influencing each others' activity (Halle, 1993; Kramer and Birney, 2001). Circadian rhythms are mostly ubiquitous and important for individuals and ecological communities. Once established, the rhythms are often constrained within lineages (Daan, 1981) and are costly or difficult to change (Kronfeld-Schor and Dayan, 2003). Species that can be either nocturnal or diurnal offer unique opportunities to identify factors that influence diel activity. For example, some species of fish can be active either by day or night, and shift their daily activity in response to the presence of competitors, predators, nutritional status, or environmental factors such as temperature and light intensity ⁎ Corresponding author. School of Biological Sciences, Heydon-Laurence Building (A08), University of Sydney, NSW 2006, Australia. Tel.: +61 2 9351 3989; fax: +61 2 9351 4119. E-mail address: [email protected] (M.B. Thompson). 1095-6433/$ – see front matter © 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.cbpa.2010.02.007

(Fraser and Metcalfe, 1997; Metcalfe and Steele, 2001). Foraging ants and termites change their daily activity according to air humidity and temperature (Abensperg-Traun, 1994; Reid, 1995). Our aim is to identify factors that determine daily activity in an Australian desert lizard, the panther skink, Ctenotus pantherinus (Peters) in the Simpson Desert. C. pantherinus is a Spinifex specialist that is unique within its genus of otherwise diurnal lizards in being active during the day and at night. Night activity occurs throughout the night from sunset till after midnight (Pianka, 1986; Gordon et al., 2009). It has the largest geographical range of any species of Ctenotus (Cogger, 2002), and is one of the most frequently captured skinks in field surveys (Downey and Dickman, 1993; James, 1994; Rotsaert, 2008). Thus, C. pantherinus is an unusually good model to test hypotheses about mechanisms that shape diel activity patterns. Specifically, we test hypotheses about thermal physiology, prey preferences and detection, and predator avoidance in C. pantherinus. Both diurnal and nocturnal reptiles often select cooler temperatures at night than during the day (Rismiller and Heldmaier, 1982; Innocenti et al., 1993; Refinetti and Susalka, 1997; Ellis et al., 2006). Selection of cool temperatures at night by diurnal lizards represents a voluntary hypothermia that reduces energy costs (Regal, 1967). In contrast, selection of cool temperatures by nocturnal lizards at night may allow exploitation of resources of food and space unavailable to diurnal species (Werner and Anholt, 1993), or reflect a common evolutionary constraint imposed by the correlation of high sunlight levels with high temperature (Refinetti and Susalka, 1997, Autumn et al., 1999a,b). Similarly, metabolic rate generally is lower at night

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than during the day in diurnal lizards, but is often not different or is higher at night in many nocturnal lizards (Hare et al., 2006). For C. pantherinus, we tested the hypotheses that mean selected temperature and metabolic rates are the same by day and by night, and that its mean selected temperature is not different from diurnally active congeneric skinks. Like many other night-active lizards in arid Australia, C. pantherinus includes large numbers of termites (70–90%) in its diet of invertebrates (Pianka, 1969; James 1991a; Twigg et al., 1996). As termites are primarily nocturnal, the nocturnal predators of termites may be expected to have enhanced sensory perception for night hunting, such as low-light vision (Röll, 2000) or heightened senses of smell or hearing (Webb and Shine, 1992). We tested the hypotheses that termites are selected over other species as prey by C. pantherinus, and that, despite being in a group of diurnal lizards that rely on sight for predation, C. pantherinus can detect prey using senses other than sight. To assess whether preference is based on nutritional gains, we measured the energy density and water contents of termites and other prey. Predation risk may also change patterns of daily activity in reptiles (Webb and Whiting, 2005; Daly et al. 2007, 2008). For example, predation by birds influences activity in open habitats by day in the central-netted dragon, Ctenophorus nuchalis (Daly et al., 2007, 2008). We tested the hypothesis that predation on models of C. pantherinus is greater during the day than at night. 2. Methods 2.1. Lizard capture and husbandry Lizards (n = 15) were captured from 12 to 23 September 2007 in the Simpson Desert, Queensland, Australia (see Dickman et al., 1999, 2001 for site descriptions). Lizards were transported to the University of Sydney within a week of capture and housed in individual glass aquaria (for juvenile lizards, 240 × 410 × 200 mm high; for adults, 370 × 460 × 210 mm high) containing sand, a basking rock and a shelter. A 60-W light bulb provided a thermally heterogeneous environment in each aquarium, with temperatures ranging from 26 to 45 °C, and a photoperiod of 12 h light/12 h dark. Captured lizards varied from 47 to 89 mm snout–vent–length (SVL) and 2.6 to 14.2 g body mass. As C. pantherinus matures at approximately 77 mm SVL (James, 1991b), lizards were separated into juveniles (b77 mm SVL, n = 7) and adults (N77 mm SVL, n = 8) for some experiments. Thirteen of the lizards used in experiments were non-gravid females, two were mature males. Lizards were housed for 1–2 months before experiments commenced, and were fed twice weekly between 1300 and 1800 h on crickets (dusted in multivitamin powder), with water provided ad lib. 2.2. Mean selected temperature Mean selected temperature (MST) was measured using four thermal gradients (aquaria, 280 mm × 840 mm) with temperatures spread evenly from 15 to 50 °C using heat tape. The gradients were in a temperature-controlled room at 10 °C with a 12:12 light cycle. A 40 × 40 mm square grid was placed under each thermal gradient, segregating each aquarium into 147 squares. Substrate temperature (glass) within each square was measured using a calibrated ‘Ray tek®’ infrared thermometer. Substrate temperature was measured four times during the two-week experimental period; twice before, once during, and once after experimentation, to allow calculation of a spatially and temporally independent substrate temperature for each grid square. Lizards (n = 15) were placed singly into thermal gradients for three consecutive days; the first day allowed for habituation to the new environment, with measurement of MST on the second and third days (experimental days 1 and 2). Lizards were

two days post-absorptive (Robert and Thompson 2000) before entering the thermal gradient and were filmed continually during both experimental days. A dim red light allowed night observations. Lizard temperature (n = 15, male: 2, 1 juvenile; female: 13, 6 juvenile) was estimated hourly by assuming that a lizard's body temperature (Tb) was equal to the average substrate temperature (Ts) of all 40 × 40 mm squares on which it had been lying for more than 10 min. MST was calculated within four six-hour time periods: 0800–1400 h (light), 1400–2000 h (light), 2000–0200 h (dark) and 0200–0800 h (dark). Ten minutes was long enough for the temperature of lizards in the gradient to equilibrate because lizards were found on squares with a difference in temperature of N10 °C between time periods only 2.4% of the time and the average rate of temperature change in C. pantherinus is 1.01 °C (±SE 0.04) per min. Heating and cooling rates in C. pantherinus (n = 8, female: 8, 4 juvenile) were measured using thermocouples (0.1 mm) attached to a temperature logger (data-tech) calibrated to 0.1 °C in a water bath. External body temperature was measured with a copper-constantan thermocouple taped to the dorsal body surface, and internal body temperature by taping another thermocouple into the cloaca (∼10 mm). Lizards were placed in an incubator at either 15 or 35 °C for 30 min, or until body temperature (Tb) equalled ambient temperature (Ta). 15 and 35 °C were selected to represent a realistic range of temperatures experienced by C. pantherinus in the field between day and night. Lizards with a Tb of 35 °C were then placed in an incubator at 15 °C, and lizards with a Tb of 15 °C were placed at 35 °C. Temperature was logged every minute, with time for Tb = Ta compared between heating and cooling of lizards. The order in which lizards were heated and cooled was randomised. 2.3. Resting metabolic rate Rate of oxygen consumption (V̇ O2) was used as an index of resting metabolic rate in C. pantherinus (n = 12, females: 12, 6 juvenile). Rate of oxygen consumption (ml g− 1 h− 1) was measured at 15, 25 and 30 °C during the day (0900–700 h) and night (1900–0200 h,) using flowthrough respirometry (Withers 1977). 15 and 30 °C were chosen because they represent typical upper and lower temperatures of C. pantherinus during summer nights in the Simpson Desert, with 25 °C representing the mean night-time temperatures in November (Gordon et al., 2009). Measurements were made in clear perspex chambers (75 ml, 100 mm× 35 mm for juveniles; 95 ml, 170 mm× 35 mm for adults) that allowed external light to enter during the day and which were shielded from light at night. Lizards were conditioned to the experimental protocol for two weeks before experiments (Hare et al., 2004) and were three days post-absorptive at the time of the measurements (Roberts, 1968; Robert and Thompson, 2000). Two juvenile and one adult lizard never settled during the experiment so their data were omitted. Oxygen consumption was measured using a two channel Sable Systems Oxilla 2 oxygen analyser coupled with Sable Systems gas analyser sub-samplers with a constant flow of 6.5 ml min− 1. Samples were stripped of water vapour and carbon dioxide before entering the oxygen analyser using a drierite–carb-absorb–drierite series. Air was drawn through the three experimental chambers in a controlled temperature cabinet. One chamber contained a lizard, and two were empty to act as blank controls. Lizards were allowed to settle for 15 min, during which time oxygen concentrations were measured in the control blank chambers. After 15 min, one of the control chambers was replaced with the sample lizard. Rate of oxygen consumption of each lizard was measured for 90 min, or until it reached a steady reading for 30 min. The order in which lizards were sampled was randomised between temperature treatments, and atmospheric air was constantly pumped into the temperature chamber. V̇ O2 was calculated as the difference in oxygen content between the control blank chamber and the experimental lizard chamber using

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the equation of Withers (1977). Barometric pressure was measured during all trials, and incorporated into calculations of V̇O2. If any trace failed to reach a steady state within 90 min, the measurement was repeated on another day.

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scored if a lizard was stationary and with its head oriented towards and within 10 mm of a vial. Lizards were four days post-absorptive for each trial. 2.6. Predation risk

2.4. Food preference and nutrition Cafeteria trials were conducted in large aquaria (140 mm ×230 mm × 70 mm, sand substrate) between 1400 and 1800 h at 26 °C to determine food preferences. Lizards were given a choice of four food sources per trial; one cockroach (Nauphoeta cinerea, 20 mm long), one mealworm (Tenebrio molitor, 20 mm long), ∼ 10 termites (Coptotermes lacteus, 3 mm long) and three seeds (Trachymene glaucifolia, 5 mm circumference). Each offering was of approximately equal volume. The invertebrates were chosen as they belong to Orders that are part of the diet of C. pantherinus and were within their normal prey size range (Pianka, 1969; James, 1991b; Twigg et al., 1996). Termites collected from a location near Sydney and commercially available mealworms and cockroaches were used in all experiments. Seeds from a common annual plant in the Simpson Desert acted as a control that we expected to be ignored. Each food type was offered in a separate Petri dish, with the arrangement of food items randomised between trials. Lizards (n = 15, male: 2, 1 juvenile; female: 13, 6 juvenile) were placed individually under a small holding container in the experimental aquarium for 15 min, then released and their feeding activities were filmed for one hour. The food type eaten first by each lizard was scored, with trials repeated four times per individual to assess repeatability of results. Only trials in which the prey item was eaten were used in the analyses. Lizards were three days post-absorptive for each trial and sand was mix between trials to remove scent. Energy densities of cockroaches, mealworms and termites were determined using bomb calorimetry (Gallenkamp Autobomb, CBA-305; Chen et al., 2004). Dried samples of each invertebrate (n = 3, ∼0.4 g) were combusted completely and energy density calculated as described by Gorecki (1975). The calorimeter was calibrated by combusting three benzoic acid samples. 2.5. Foraging mode The importance of olfactory, auditory and visual cues in prey detection was assessed using small plastic vials (50 mm × 15 mm diameter) as experimental units. Vials were treated to provide them with either a single sensory cue, all three cues together, or with no cues that lizards might use for foraging. Clear vials were imbued with olfactory cues by placement in an aquarium containing mealworms for 30 min before experimentation; auditory cues were provided by placing live mealworms in black vials containing sand and crushed dry leaves; and visual cues were provided by placing freshly killed mealworms (via pin into head) in clear vials. All sensory cues combined were provided by placing live mealworms into perforated clear vials containing sand and dry leaves, and clean vials, acting as controls, were used to provide no cues. Mealworms (Tenebrio molitor) were chosen as a food source as they were readily available and the lizards were habituated to feed on mealworms before experimentation as a supplement to their normal diet. Experiments were conducted from 1400 to 1800 h at 26 °C in large aquaria (370 × 600 × 260 mm high, sand substrate only). Aquaria contained four vials with a sensory cue (either olfactory, auditory or visual, or all cues together) and four vials without sensory cues, or eight clean vials to act as procedural controls, in which case, four were randomly designated as + cue and four as −cue. Lizards (n = 15, male: 2, 1 juvenile; female: 13, 6 juvenile) were placed individually in small holding containers in the aquaria and allowed to settle for 10 min before being released. Exploration of vials by lizards (n = 15) was filmed for 30 min and all visits to vials were scored. A visit was

Predation risk during the day and at night was assessed using adult lizard-sized plasticine models painted with water based acrylic paint to resemble C. pantherinus (Webb and Whiting, 2005; Daly et al., 2008, Fig. 1). One model was placed every 10 m along a 650 m long transect during July 2008. Lizard models were placed in microhabitats where C. pantherinus was seen during field surveys in the Simpson Desert, with 60% of models placed within 20 mm of a spinifex hummock, 20% placed under a hummock, and 20% placed on open sand 500 mm from spinifex. Models were checked for signs of predation at dusk (day period) and dawn (night period) for five consecutive days. A predation attempt was defined as a noticeable depression in the plasticine model that ruptured the paint coating. Position on the model of the attack was noted, with identification of the predator (bird or dasyurid marsupial) assessed by direct observations in the field or using reference collections of bird beaks and talons and dasyurid marsupial jaws kept at the University of Sydney. 2.7. Data analysis Mean selected temperature was compared between time treatments using a one factor repeated measures ANOVA, with MST dependent on time period during experimental day one and two. Preliminary analysis showed no difference in MST between juvenile and adult lizards (size) or time period using a two factor repeated measures ANOVA (day 1: size: F(1,12) = 0.27 P 0.61, time period: F(3,36) = 2.16 P 0.11, size ⁎ time period: F(3,36) = 1.12 P 0.35; day 2: size: F(1,12) = 0.23 P 0.65, time period: F(3,36) = 1.44 P 0.25, size ⁎ time period: F(3,36) = 1.54 P 0.22), so data were pooled between size classes. Differences in rates of oxygen consumption between temperature treatment and day and night sampling were compared using a two factor repeated measures ANOVA, with rate of oxygen consumption dependent on temperature treatment and time (day or night). Preliminary analysis showed no difference in oxygen consumption between juvenile and adult lizards at the three experimental temperatures, so data were pooled between size classes (day: size: F(1,10) = 0.01 P 0.91, temperature: F(2,20) = 10.57 P 0.01, size ⁎ temperature: F(2,20) = 0.51 P 0.61; night: size: F(1,10) = 0.30 P 0.60, temperature: F(2,20) = 13.14 P b 0.001, size ⁎ temperature: F(2,20) = 0.09 P 0.91). Oxygen consumption data were log transformed for analysis. Predicted metabolic rate was calculated at each temperature using the equation of Andrews and Pough (1985) to allow comparison of observed metabolic rate with predicted metabolic rate at a specific temperature (day treatment only). Observed and predicted metabolic rates were compared at each temperature using independent Mann Whitney U-tests. Q10 values were calculated between 15–25 °C and 25–30 °C separately for day and night periods to assess the metabolic sensitivity to increasing temperature (Schmidt-Nielsen, 1990). In the heat retention / loss experiments, the time taken for Tb = Ta was analysed using a one-way repeated measures ANOVA, with internal heating, internal cooling, external heating and external cooling as factors. Frequency of food types eaten first was compared for trial one using χ2. If a lizard did not eat in the first trial, its food choice in the second trial was used. When χ2 was applied in trials two, three and four, an unacceptable number of cells with expected values less than five occurred, so statistical comparisons were not further considered (Quinn and Keough, 2002). In the foraging mode experiment, mean frequencies of explorations of treatment and control vials were compared using a separate paired t-test for each of the five treatments.

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Fig. 1. Plasticine models of Ctenotus pantherinus showing predatory attacks by birds. Photographs show (A, B) deep beak marks on the head of adult lizard models, (C) small beak marks on the head and front left limb of juvenile lizard model, and (D) beak marks on the head, torso, all limbs and tail of adult lizard model. Models were spray painted brownmaroon with white spots to mirror natural colouration.

Comparisons between treatments were not made as the scale at which each sensory cue operates was not comparable. Predation risk was analysed using a χ2, with total frequency of attacks during the five day and night periods compared. Micro habitat was not analysed as a variable. In all statistical comparisons α is set at 0.05, a non-significant result is denoted as NS, and ± denotes one standard error. 3. Results 3.1. Mean selected temperature and metabolic rate Mean selected temperature did not differ between time periods (F(7,91) = 1.45; P 0.19), averaging 36.1 °C ± 1.6 °C overall. V̇ O2 increased with temperature during the day and at night (F(2,44) = 29.643; P b 0.0005), and was greater during the day than at night (F(2,44) = 6.635; P b 0.05; Fig. 2). No interaction occurred between temperature and day / night treatment (F(1,22) = 0.067; P 0.94). The difference in V̇O2 between day and night increased with rising temperature (0.04 ml g− 1 h− 1 greater at 15 °C, 0.10 ml g− 1 h− 1 greater at 25 °C and 0.14 ml g− 1 h− 1 greater at 30 °C). Q10 values were all 2–3, except for 25–30 °C at night (Table 1). V̇ O2 was 0.049 ml g− 1 h− 1 lower at 15 °C than would be predicted using Andrews and Pough (1985) equation (Z = − 2.340; P b 0.05; Fig. 2).

Observed and predicted V̇ O2 were not significantly different at 25 °C (Z = −1.457; P 0.16) or 30 °C (Z = − 1.280; P 0.22). Cooling rates of C. pantherinus (1.01 ± 0.04 °C/min) were slower than heating rates (1.3 ± 0.07 °C/min; Fig. 3). On average, it took 26.6 ± 2.2 min (external temperature) and 27.0 ± 1.9 min (internal temperature) for Tb to equal Ta when cooling, compared to 19.5 ± 1.4 min (external temperature) and 20.8 ± 0.9 min (internal temperature) when heating. A statistical difference occurred in time taken for Tb = Ta (F(3,21) = 9.829; P b 0.0001), with pair-wise comparisons using t-tests with Bonferroni correction showing a difference between external (skin) heating and external (skin) cooling, and external (skin) heating and internal (cloaca) cooling only. 3.2. Food preference, nutrition, foraging mode and predation risk C. pantherinus repeatedly chose to eat termites first in 80%, 58%, 64% and 47% of the four food preference trials (for trial one: χ2(2) = 27.999; P b 0.0001, n = 15, seeds omitted) (Fig. 4). Cockroaches were always the least preferred invertebrate food type, and seeds were never eaten. Mealworms had the highest energy density followed by cockroaches then termites, with termites having the highest water content (Table 2). Animals visited vials with only auditory (t = 2.267; P b 0.05), olfactory (t = 7.267, P b 0.0001) or visual cues (t = 7.483, P b 0.0001; Fig. 5) more than their respective controls. The differential was greatest for olfactory cues, with a 7.7 fold difference recorded between treatment and control vials, followed by visual cues (4.4 fold difference), then auditory cues (2.7 fold difference). The differential was greater still when vials combined all sensory cues (16.1 more treatment than control vials were explored, t = 10.202 P b 0.0001). Similar, low numbers of visits were made to the two sets of clean control vials (t = 0.574, P 0.58). Plasticine models of C. pantherinus were attacked at a greater frequency in the day (40, 12.3% of models) than at night (3, 0.9% of models) (χ2(1) = 34.093; P b 0.0001). Only birds attacked models during the day and only dasyurid marsupials attacked them at night. Half the attacks by birds occurred on the head area of the models, with the remaining attacks on the body, limbs and tail (Fig. 1). Direct

Table 1 Q10 values (± SE) calculated for rates of oxygen consumption of Ctenotus pantherinus measured between 15–25 °C and 25–30 °C during the day (n = 9) and at night (n = 11). Fig. 2. Rate of oxygen consumption (mean ± SE, ml g− 1 h− 1) of Ctenotus pantherinus during the day (0900–1700 h, n = 12, white) and night (1900–0200 h, n = 12, black), as well as predicted day metabolic rate (Andrew and Pough, 1985, grey).

Day Night

15 °C–25 °C

25 °C–30 °C

2.4 ± 0.3 2.0 ± 0.4

2.8 ± 0.8 1.6 ± 0.2

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Table 2 Energy density (J mg− 1) of termite (Coptotermes lacteus, n = 3), cockroach (Nauphoeta cinerea, n = 3) and mealworm(Tenebrio molitor, n = 3) samples used in food preference experiments for Ctenotus pantherinus. The numbers of each type of invertebrate required to equal 1 g of sample dry weight, as well as the percentage water content of each invertebrate, are also shown.

J mg− 1 Number g− 1 % water

Termites

Cockroach

Mealworm

23.21 1053 59%

25.34 18 53%

29.56 22 45%

4. Discussion

Fig. 3. Average time taken for external (skin; black square) and internal (cloaca; white circle) body temperature (°C) of Ctenotus pantherinus (n = 8) to equal ambient temperature (dashed line). In A) lizards with a body temperature at 15 °C were placed at 35 °C until their body temperate equalled ambient temperature, and in B) lizards with a body temperature of 35 °C were placed at 15 °C until their body temperature equalled ambient temperature.

observations confirmed that at least some small pecks were inflicted by willie wagtails Rhipidura leucophrys, while deeper pecks (including some that decapitated the models) were inflicted by Australian ravens Corvus coronoides. Bite marks were made by a dunnart, most likely Sminthopsis youngsoni.

Fig. 4. Percentage of times that termite (Coptotermes lacteus), cockroach (Nauphoeta cinerea), mealworm (Tenebrio molitor) and seed (Trachymene glaucifolia) food sources were eaten first by Ctenotus pantherinus in food preference trials. Four consecutive trials were conducted to assess repeatability of results (trial 1: n = 10, black, trial 2: n = 11, dark grey, trial 3: n = 14, light grey, trial 4: n = 15, white).

C. pantherinus shows many traits typical of diurnal lizards, with the same high mean selected temperature day and night (Rismiller and Heldmaier, 1982; Bennett and John-Adler, 1986; Innocenti et al., 1993; Refinetti and Susalka, 1997; Ellis et al., 2006), metabolic depression during the night (Hare et al., 2006), and a metabolic rate that is lower than predicted at 15 °C, but not 25 °C and 30 °C (Andrews and Pough, 1985). The high mean selected temperature of C. pantherinus is similar to the preferred body temperatures of other arid Australian Ctenotus skinks (Bennett and John-Adler, 1986). A preference for activity at high temperatures in nature is supported for C. pantherinus because 1) arid Australian Ctenotus skinks generally have high field-active body temperatures and are active during hot days (Bennett and John-Adler, 1986; Cogger, 2002), and 2) C. pantherinus has a lower than predicted daytime metabolic rate at 15 °C, but not 25 °C and 30 °C, which indicates optimal activity at hot temperatures and impeded activity at cold temperatures (Andrews and Pough, 1985). Circadian cycling in mean selected temperature is common in lizards, with cooler temperatures selected at night in both diurnal and nocturnal species (Innocenti et al., 1993; Ellis et al., 2006). Lack of a difference in selected temperatures between day and night in C. pantherinus in a laboratory thermal gradient correlates with its being active both day and night in the field in spring (Gordon et al., 2009). Lack of a circadian cycle may support opportunistic activity irrespective of time of day when thermal conditions are conducive to activity. If so, a seasonal shift in activity is likely to occur, with night activity restricted to hot summer months when temperatures are generally 20–30 °C within six hours after sunset, but not during cold

Fig. 5. Mean numbers of visits (± SE) by Ctenotus pantherinus (n = 15) to experimental vials impregnated with a sensory cue (grey) and to control vials with no sensory cue (white). Auditory, visual, olfactory, all senses combined and control treatments were manipulated using small plastic vials as experimental units.

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winter months when evening temperatures typically reach 0 °C. Temperature-driven seasonal shifts in activity time occur in other nocturnal lizards (Pianka and Pianka, 1976; Autumn et al., 1999). As metabolic rate is depressed at night in C. pantherinus, a trait shared with other diurnal lizards (Hare et al., 2006), opportunistic night activity would have to override this metabolic depression. C. pantherinus has a more robust and stocky body form than most of its congeners (Cogger, 2002), thus giving it a relatively lower surface area to volume ratio which may facilitate heat retention into cool evening periods, as in other reptiles (Avery, 1982; Ayers and Shine, 1997), and extend its activity into the night. Slower cooling rates than heating rates provides further evidence for the importance of heat retention in allowing night activity in C. pantherinus. C. pantherinus is a termite specialist (Pianka, 1969; James, 1991a; Twigg et al., 1996) and it prefers termites over other prey tested, even though termites have lower energy densities than cockroaches and mealworms. Being a dependable and abundant nocturnal food source across much of arid Australia (Morton and James, 1988), a preference for termites as prey correlates well with the nocturnal activity of C. pantherinus. Despite their abundance, however, spatial and temporal variability in termite activity may constrain selection for termite specialisation, with termite specialists often having a higher incidence of empty stomachs than species with more generalist diets (Pianka, 1986; Abensperg-Traun, 1994; Huey et al., 2001). Nocturnal lizards, being ectotherms, seemingly overcome such problems by having low energy requirements, and the ability to detect prey at night (AbenspergTraun, 1994). Termites have a higher water content than the other invertebrate prey that we tested, and we did not analyse the susceptibility of C. pantherinus to rates of water loss compared to other lizards. Analysis of the water relations and food preference for termites in relation to other prey items (i.e. grasshoppers or beetles) in C. pantherinus may provide further understanding of the unusual diel activity of this species. C. pantherinus has small eyes, and is nested phylogenetically within a group of diurnally active lizards (Greer, 1989), which makes it unlikely that vision is of particular importance in detecting prey during nocturnal foraging, as occurs in many nocturnal geckos (Röll, 2000). As C. pantherinus can detect prey using olfactory and auditory cues independent of vision, trails left by termites (Moore, 1966) may be detected using olfactory cues at night, with fine scale termite acquisition reliant on a combination of auditory, olfactory, and possibly visual cues. Predation by birds restricts basking times in many reptiles (e.g., the elapid snake Hoplocephalus bungaroides; Webb and Shine, 1992), which support the hypothesis that predation on C. pantherinus by avian predators is a factor selecting for nocturnal activity. The high incidence of diurnal attacks on models of C. pantherinus (62% showed signs of bird attack during the day) compared to nocturnal attacks by marsupials (5%), suggest that nights are less dangerous than days for C. pantherinus to be active. Estimates of night predation by nocturnal marsupials may be conservative as many nocturnal marsupials rely on olfactory cues for predation at night. 5. Conclusion Thermal and metabolic responses of C. pantherinus are characteristic of a diurnal lizard, but it is often active at night. It has overcome the physiological constraints imposed by low night time temperatures to exploit an abundant, water-rich food source, termites. Although generally reliant on visual cues for prey capture as a diurnal species, the ability to detect prey using auditory or scent cues alone allows C. pantherinus to successfully forage at night. Being able to extend its foraging into the night allows C. pantherinus to avoid common diurnal predators. An assessment of seasonal shifts in time of activity during summer and winter, as well as of temperature-dependent locomotor performance, water relations, would help to determine if C. pantherinus

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