ARTICLE IN PRESS

Journal of Thermal Biology 28 (2003) 385–391

Influence of body temperature on food assimilation and locomotor performance in white-striped grass , wolteri () Xue-Jun Chena, Xue-Feng Xub, Xiang Jia,*

a School of Life Sciences, Hangzhou Normal College, Hangzhou, Zhejiang 310036, China b Department of Biochemistry, Chuzhou Normal College, Chuzhou, Anhui 239012, China

Received 23 May 2002; accepted 14 February 2003

Abstract

Influence of body temperature on food assimilation and locomotor performance was studied in adult white-striped grass lizards (Takydromus wolteri) from a population in Chuzhou (Anhui, Eastern China). Food passage time dramatically decreased with increase in body temperature within the range from 26Cto34C, and then nearly levelled at higher body temperatures. Lizards overall gained net mass at 26C, 28C and 30C and lostmass at32 C and 34C. Daily production of faeces (mass-specific) was affected by body temperature and, when influence of variation in the total food energy intake was removed by an ANCOVA, lizards at 26C were found to produce faeces that contained significantly lower energy as compared with those at higher body temperatures. The total energy of urates was affected by the total food energy intake, but an ANCOVA with the total food energy intake as the covariate showed that lizards at different body temperatures did not produce urates that differed in energy. Within the temperature range considered, daily production of urates (mass-specific), apparent digestive coefficient (ADC) and assimilation efficiency (AE) were not affected by body temperature, although both ADC and AE were apparently greater in lizards at 26C. Both locomotor stamina and sprint speed increased with increase in body temperature within the range from 18Cto30C, and then decreased at higher temperatures. Inter-individual differences were a significant source of variation in locomotor performance. Except for ADC and AE, all traits examined were significantly affected by body temperature, although thermal sensitivities differed considerably among traits. Within the body temperature range considered, 26C was the most suitable body temperature for somatic tissue growth, and 30C was an optimal body temperature for locomotor performance. r 2003 Elsevier Science Ltd. All rights reserved.

Keywords: Reptilia; Lacertidae; Takydromus wolteri; Food passage time; Apparent digestive coefficient; Assimilation efficiency; Locomotor stamina; Sprint speed

1. Introduction however, within a certain range, moderate to relatively high body temperatures usually maximize performances Body temperature may profoundly affect physiologi- (Huey, 1982; Huey and Kingsolver, 1989; Ji etal., 1995, cal and behavioural performances of . Extreme 1996, 1997; Xu etal., 1999, 2001 ; Du etal., 2000 ). Reptiles body temperatures are harmful and potentially lethal; that are active in the field tend to maintain relatively high and constant body temperatures mainly through *Corresponding author. Tel.: +86-571-88082506; fax: +86- behavioural thermoregulation, so that their performances 571-88804145. can be expressed athigh levels. However, for reptiles E-mail addresses: [email protected] (X.-J. Chen), living in the environments lacking thermal gradients, [email protected] (X.-F. Xu), [email protected] (X. Ji). behavioural thermoregulation is rather constricted,

0306-4565/03/$ - see front matter r 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0306-4565(03)00022-6 ARTICLE IN PRESS 386 X.-J. Chen et al. / Journal of Thermal Biology 28 (2003) 385–391 and variation in body temperature may largely mirror pliable-shelled eggs each per breeding season lasting variation in ambient temperature (Wang and Xu, 1987). from May to July (Chen, 1991; Pan and Ji, 2001). The thermally homogeneous environments where the The captured lizards were transported to our labora- temperature is uniform usually do not occur in nature tory at Hangzhou Normal College, where sex was but can be established in the laboratory by using determined and mass and length were recorded to the constant temperature rooms, inside which a ’s nearest 1 mg and 0.01 mm, respectively. Prior to and body temperatures can be controlled precisely at between trials, lizards were randomly maintained 8–10 expected levels so that its behavioural and physiological in each 600 400 300 mm3 (length width height) performances corresponding to any given body tem- glass terrarium, of which the bottom was filled with perature can be examined (Wang and Xu, 1987; Ji and moistsoil, grasses and debris. We fed lizards with Wang, 1990; Ji etal., 1993, 1995, 1996, 1997 ; Xu etal., mealworms (larvae of Tenebrio molitor) and water 1999, 2001; Du etal., 2000 ). enriched with vitamins and minerals. We exposed lizards In reptiles, food assimilation and locomotor abilities to a natural light cycle. The supplementary heating was have clear ecological relevance: netenergy gains through provided by a 100 W lightbulb suspended 15 cm above feeding mean somatic tissue growth and/or offspring the terrarium floor, so that lizards had ample opportu- production (Nagy, 1983), whereas locomotor abilities nities to regulate body temperatures within their may be associated with individual fitness because of its voluntary range during the photophase and cool to air importance for avoiding predators and enhancing temperature when the lights were switched off. Indivi- foraging success (Pough, 1989; Bauwens etal., 1995 ; dual lizards were measured only at a single temperature. Miles etal., 1995 ; Bran˜ a and Ji, 2000; Ji etal., 2002 ). Excepting for competing occasionally for food, we did Thus, quantifying the thermal dependence of food not find any antagonistic interactions among lizards in assimilation and locomotor abilities is important. In the terraria. Body temperatures (cloacal, Tb) were taken this study, we investigate Takydromus wolteri, a small using a WMZ-03 electronic thermometer (Shanghai multiple-clutched oviparous insectivorous lacertid Medical Instruments, China), which was calibrated with mainly living in hilly areas covered by grasses and a standard thermometer. To improve the reliability of bushes (Chen, 1991). The is geographically our measurements, we measured each lizard twice and widespread; its distributional range covers some pro- considered the mean of the two readings as a lizard’s vinces in eastern (Jiangsu, Anhui and Jiangxi) and body temperature. central (Hubei and Sichuan) China, north to the northeastern provinces of China, Korea and Russia 2.1. Food passage time (Southern Primorskiy Territory) (Chen, 1991; Zhao and Adler, 1993). We present data on several traits that are The trials at 26C, 28C, 30C, 32C, 34C, and 36C relevant to food assimilation and locomotor abilities and were conducted in May 2000 and 2001, and the trial at supposed to be influenced by body temperature, includ- 38C was conducted in May 2001. All trials were ing: (1) food intake, (2) food passage time, (3) apparent conducted in a constant temperature room inside which digestive coefficient (ADC), (4) assimilation efficiency the fluorescent tubes were on a 12 light: 12 dark cycle; (AE), (5) locomotor stamina and (6) sprint speed. Our lights were automatically switched on at 07:00 (Beijing purposes are to contribute further data to the thermal time). Lizards were individually housed in a biology of lizards in eastern China and to compare data 200 150 250 mm3 glass terrarium. We starved lizards generated from this study with those collected in other at the test body temperature for 3 d prior to feeding, and parallel studies. then fed each lizard with two mealworms of which each had been marked by inserting a 3 mm blue plastic thread (diameter 0.2 mm) into the abdomen. We started trials at 2. Materials and methods different temperatures at the same time (17:00) of day, and allowed all lizards to eat voluntarily marked Adult T. wolteri, with snout-vent length (SVL) mealworms, thereby avoiding force-feeding. All plastic ranging from 44 to 61 mm, were collected by hand or threads were collected within a few minutes after being noose in early May 2000 and 2001 from a population in expelled, and the food passage time was defined as the Chuzhou (Anhui, Eastern China), where is the southern lapsed time from swallowing to the first appearance of limit of its distributional range. The mean temperatures plastic threads. of the whole year, the hottest month (July) and the coldest month (January) in Chuzhou are approximately 2.2. Food intake and food assimilation 14.5C, 28.5C and 1.8C, respectively; the active season of T. wolteri there begins in late March and The trials at 28C, 30C, 32C and 34C were ends in early November (Chen, 1991). In the laboratory, conducted between May and July in 2000 and 2001, large females are able to lay up to 4 clutches with 1–4 and the trial at 26C was conducted in the same season ARTICLE IN PRESS X.-J. Chen et al. / Journal of Thermal Biology 28 (2003) 385–391 387 of 2001. All trials were conducted in constant tempera- 2.4. Statistical analyses ture rooms as described above. Lizards were also individually housed in a 200 150 250 mm3 glass Individuals that refused to run or died during the terrarium. We starved lizards at the test body tempera- course of trials were excluded from analysis. All data ture for 3 d to insure uniform post-absorptive states, and were tested for normality (Kolmogorov–Smirnov test) then fed them with mealworms and water ad libitum.We and homogeneity of variances (F-max test), and Arc-sine collected faeces and urates at least 5 times daily. Trials (for ADC and AE) and Loge (for other traits when lasted for a minimum of 24 days to allow the necessary) transformations were performed to achieve to accumulation of sufficient faeces and urates for accurate the conditions for using parametric tests. Because calorimetry. Initial body mass was recorded at the end preliminary analyses showed that there were no sig- of 3 d fastprior tofeeding, and final body mass was nificant differences in all examined traits between both recorded at the end of a 3 d fast which terminated each sexes and among individuals examined in differentyears, trial. we pooled data for both sexes and for individuals Faeces, urates and mealworms for each lizard were examined in differentyears. We used one-way ANOVA dried to constant mass at 65C and weighed. Dried to determine whether there were differences in food samples were burned in a WGR-1 adiabatic calorimeter passage time, ADC and AE among temperature treat- (Changsha Instruments, China) and data were auto- ments. The same analysis was also used to determine matically recorded in a computer. The assimilation whether there were differences in daily food intake, efficiency was calculated as AE ¼ 100ðI À F À UÞ=I changes in body mass, daily production of faeces, daily (Kepenis and McManus, 1974; Ji and Wang, 1990; Ji production of urates, locomotor stamina and sprint etal., 1993 ), where I is the total energy consumed, F the speed among temperature treatments, because no linear energy in faeces and U the energy in urates. The relationships existed between these variable and indivi- apparent digestive coefficient was calculated as ADC ¼ dual size (mass). We used one-way ANCOVA (with 100ðI À FÞ=I (Harwood, 1979; Ballinger and Holscher, total food energy intake as the covariate, thereby 1983; Waldschmidtetal., 1986 ). removing influence of variation in this variable) to determine whether lizards at different body temperature 2.3. Locomotor performance would differ in energy contents of faece and urates produced. We used two-way ANOVA (with body Locomotor stamina was examined in May 2000 and temperature and individual as the factors) to determine at 9 body temperatures ranging from 18Cto38C whether there were inter-individual differences in (18C, 23C, 26C, 29C, 30C, 32C, 34C, 36C and locomotor stamina and sprint speed. Descriptive statis- 38C). All trials were conducted in a 600 400 tics are presented as mean 71 standard error, and the 300 mm3 glass terrarium which was placed in a constant significance level is setat a=0.05. temperature room, and the sequence was randomized. We housed lizards ðN ¼ 11Þ in the room for 2 h prior to each trial, thereby insuring their body temperatures to 3. Results be controlled at the test level. We kept chasing lizards until they refused to move because of fatigue. Loco- 3.1. Food passage time and food assimilation motor stamina was defined as the lapsed time from being chased to refusing to move. Food passage time was significantly affected by body Sprint speed, which was defined as the speed in the temperature (F6,135=48.91, Po0:0001), and itdecreased fastest 50 cm interval selected by a computer software dramatically with increase in body temperature within (see below), was examined in May 2001 and at11 body the range from 26Cto34C and then nearly levelled temperatures ranging from 18Cto38C (18C, 20C, within the range from 34Cto38C(Fig. 1). 22C, 24C, 26C, 28C, 30C, 32C, 33C, 35C and Lizards used for determination of food assimilation 38C), the sequence being also randomized. All trials did not differ in initial body mass among temperature were conducted in a constant temperature room, and treatments (F4,71=2.06, P ¼ 0:096). Mass changes were body temperatures were controlled in the same way as affected by body temperature (F4,71=4.20, Po0:004), described above. We chased lizards ðN ¼ 12Þ down a with lizards overall gaining net mass at 26C, 28C and 2000 100 150 mm3 racetrack with one side transpar- 30C and losing mass at32 C and 34C(Table 1). Daily ent, which allow lateral filmation with a Panasonic food intake (mass-specific) was affected by body NV-DS77 digital video camera (Panasonic Co., Japan). temperature (F4,71=5.19, Po0:001), with lizards taking Each lizard was run two times at each temperature with a apparently more food at 26C and 34C than at the minimum of 30 min rest between trials, and the tapes three intermediate body temperatures (Table 1). Daily were later examined with a computer using MGI production of faeces (mass-specific) was affected by VideoWave III software (MGI Software Corp., Canada). body temperature (F4,71=2.76, P ¼ 0:034), but this trait ARTICLE IN PRESS 388 X.-J. Chen et al. / Journal of Thermal Biology 28 (2003) 385–391 was significantly affected by food intake at each test P ¼ 0:064) were not significantly affected by body temperature (Table 1). An ANCOVA with the total food temperature (Table 1), although both ADC and AE energy intake as the covariate showed that lizards at were apparently greater in lizards at 26CTb(Table 1). different body temperatures produced faeces that The total energy of urates was also affected by the total differed in energy (F4,70=3.07, P ¼ 0:022), with lizards food energy intake at each test temperature, but an at26 C producing faeces that contained significantly ANCOVA with the total food energy intake as the lower energy as compared with those at other four covariate showed that lizards at different body tempera- higher body temperatures (Tukey’s test, all Po0:04). tures did not produce urates that differed in energy Within the temperature range examined, daily produc- (F4,70=1.81, P ¼ 0:136). tion of urates (mass-specific) (F4,71=1.99, P ¼ 0:105), ADC (F =2.09, P ¼ 0:091) and AE (F =2.33, 4,71 4,71 3.2. Locomotor performance

Body temperature significantly affected locomotor stamina (F8,90=5.36, Po0:0001) and sprintspeed 60 (F10,121=15.00, Po0:0001). Locomotor stamina in- a creased with body temperature within the range from 23 18 C to around 30 C, and then decreased at higher 50 ab temperatures (Fig. 2). Sprintspeed also increased with 21 body temperature within the range from 18Cto30C, 40 bc and then decreased at higher temperatures (Fig. 3). 24 A two-way ANOVA confirmed that body temperature c significantly affected locomotor stamina (F8,80=12.59, 26 30 Po0:0001) and sprintspeed ( F10,110=19.34, Po d 0.0001), and it also revealed that inter-individual d 18 Food passage time (min) d differences were a significant source of variation in both 20 21 9 traits (locomotor stamina: F10,80=13.14, Po0:0001; spring speed: F11,110=15.00, Po0:0001).

24 26 28 30 32 34 36 38 40 Body temperature (°C) 4. Discussion Fig. 1. Food passage time of Takydromus wolteri atdifferent body temperatures. Data are expressed as mean 71 standard The mean values of food passage time corresponding error. Sample sizes are indicated in the figure. Means with to a given body temperature and the thermal sensitivity different superscripts differ significantly (Tukey’s test, a ¼ 0:05; of the trait may differ considerably among species a > b > c > d). (Waldschmidtetal., 1986 ; Van Damme etal., 1991 ;

Table 1 Initial body mass, changes in body mass, daily food intake, daily production of faeces, daily production of urates, ADC and AE of adult Takydromus wolteri

Temperature N Initial body Changes in Daily food Daily Daily ADC (%) AE (%) (C) mass (g) body mass intake production production (mg dÀ1) (J gÀ1 dÀ1) of faeces of urates (J gÀ1 dÀ1) (J gÀ1 dÀ1)

26 7 2.170.0.1 11.0a72.3 509.6a733.5 33.9b72.9 23.172.6 93.370.5 88.870.8 (1.9–2.4) (2.7–28.3) (368.0–602.9) (27.8–49.5) (15.6–34.5) (91.8–94.8) (86.1–91.7) 28 22 2.570.1 3.7b72.1 451.3ab722.8 42.2ab73.1 26.271.7 90.570.6 84.671.0 (1.9–3.3) (À14.0–22.4) (288.1–777.1) (21.4–76.2) (13.7–46.0) (85.4–94.5) (76.8–91.1) 30 17 2.670.1 3.6b71.8 398.5b719.0 36.8ab72.9 21.471.5 90.770.5 85.270.7 (1.9–3.6) (À14.8–15.8) (244.4–583.3) (13.7–65.7) (10.6–30.8) (87.2–94.5) (79.6–89.3) 32 14 2.770.1 À1.0bc72.6 367.3b723.0 32.8b72.8 19.971.7 90.570.5 84.470.8 (2.2–3.8) (À18.7–13.8) (233.3–548.2) (14.2–52.2) (10.8–32.3) (87.5–94.9) (79.7–89.8) 34 16 2.470.1 À3.8c72.0 515.7a738.8 45.4a73.1 25.372.4 90.770.6 85.870.7 (1.9À3.0) (À24.1–10.0) (339.3–818.5) (22.8–68.2) (11.7–45.9) (85.9–94.6) (79.9–90.6)

Data are expressed as mean 71 standard error (range). ANOVA for all traits, and mean with different superscripts differ significantly (Tukey’s test, a ¼ 0:05; a > b > c). ARTICLE IN PRESS X.-J. Chen et al. / Journal of Thermal Biology 28 (2003) 385–391 389

160 [Eumeces chinensis (Ji etal., 1995 ; Xu etal., 1999 ); a a Sphenomorphus indicus (Ji etal., 1997 )]; (3) decreasing a 140 a with increase in body temperature at lower temperatures ) a a and increasing at higher temperatures [Lacerta vivipara (Van Damme etal., 1991 ); Sceloporus merriami (Beau- 120 ab pre etal., 1993 ); Eumeces elegans (Du etal., 2000 ); Eremias brenchleyi (Xu etal., 2001 )]. The thermal 100 b dependence of food passage time in T. wolteri seems to belong to Pattern 2, although food passage time of the 80 b species levels at a body temperature (34 C) higher that that reported for E. chinensis [adults: 30C(Ji etal., Locomotor stamina (min 60 1995); juveniles: 26 C(Xu etal., 1999 )] and S. indicus [adults: 30C(Ji etal., 1997 )]. The three patterns are evident, although they seem to be the same one (Pattern 18 20 22 24 26 28 30 32 34 36 38 40 1) within the range from low to moderate body Body temperature (°C) temperatures. Patterns 2 and 3 show up in some species when lizards are tested at very warm temperatures (Van Fig. 2. Locomotor stamina of Takydromus wolteri ðN ¼ 11Þ at Damme etal., 1991 ; Beaupre etal., 1993 ; Ji etal., 1995, 7 different body temperatures. Data are expressed as mean 1 1997; Xu etal., 1999, 2001 ; Du etal., 2000 ). standard error. Means with different superscripts differ In this study, lizards at body temperatures ranging significantly (Tukey’s test, a ¼ 0:05; a > b). from 26Cto30C gained netmass, whereas lizards at body temperature higher than 32C lostmass. This implies that there might be a pivotal point between 30C 1200 and 32C for energy balance in T. wolteri: lizards at a ab body temperatures lower than this point are overall in a ab ab positive energy balance, and lizards at body tempera- 1000

) tures higher than this point are in a negative energy -1 bc abc balance. Among individuals whose body temperatures 800 were lower than this point, lizards at 26 C gained much cd cd more mass than did those at 28C and 30C, largely because of their greater daily food intake, lower 600 metabolic rate and apparently higher ADC and AE. d d d This observation indicates that, similar to what observed

Sprint speed (mm. sec (mm. Sprint speed in other lizards (e.g., Ji etal., 1993, 1995 ; Xu etal., 1999 ; 400 Du etal., 2000 ), growth can be maximized in T. wolteri by shifting body temperatures to moderate levels. Lizards at34 C, although took significantly more food 18 20 22 24 26 28 30 32 34 36 38 40 daily than did those at 30C and 32C, lostmore mass, Body temperature (°C) largely because of their higher metabolic rates. It is well known that the values of ADC and AE are Fig. 3. Sprintspeed of Takydromus wolteri ðN ¼ 12Þ at influenced by activities of digestive enzymes, food different body temperatures. Data are expressed as mean 71 standard error. Means with different superscripts differ passage time and type and amounts of food consumed significantly (Tukey’s test, a ¼ 0:05; a > b > c > d). (Andrews and Asato, 1977; Harwood, 1979; Beaupre etal., 1993 ; Witz and Lawrence, 1993). Within a certain range, increasing body temperature may increase activ- ities of digestive enzymes but reduce exposure of food to Beaupre etal., 1993 ; Ji etal., 1995, 1996, 1997 ; Xu etal., enzymatic action because of the shortened food passage 1999, 2001; Du etal., 2000 ), but no general patterns can time (Harwood, 1979). It is this unique mechanism that be drawn at the time because of lack of data from more results in thermal insensitivity of ADC and AE in many species. However, based on available data, three studied lizards, although the amount of unavailable patterns of thermal dependence of food passage time energy in food, which is dependenton theamountand can be drawn in lizards: (1) decreasing with increase in type of food consumed, may also appreciably modify the body temperature [Uta stansburiana (Waldschmidtetal., values of ADC and AE. In this study, influence of body 1986); Takydromus septentrionalis (Ji etal., 1996 )]; (2) temperature on ADC and AE was not statistically decreasing with increase in body temperature at lower significant, but lizards at 26C had noticeably greater temperatures and being levelled at higher temperatures values of ADC and AE (Table 1), largely because they ARTICLE IN PRESS 390 X.-J. Chen et al. / Journal of Thermal Biology 28 (2003) 385–391 produced faeces that contained lower energy as com- of T. septentrioanlis, but the range of body temperatures pared with those at other body temperatures. Lizards at over which lizards were able to express over 90% other four higher body temperatures had almost the potential of maximum sprint speed is very similar in same ADC and AE (Table 1), suggesting that T. wolteri both species [T. wolteri: 26–32C; T. septentrioanlis: be still among the species of which ADC and/or AE are 27–33C(Ji etal., 1996 )]. relatively less sensitive to variation in body temperature Overall, except for ADC and AE, all traits examined (Dutton et al., 1975; Waldschmidtetal., 1986 ; Ji and in this study were significantly affected by body Wang, 1990; van Damme etal., 1991 ; Beaupre etal., temperature, although thermal sensitivities differed 1993; Ji etal., 1993, 1995, 1996, 1997 ; Xu etal., 1999, considerably among traits. Within the temperature 2001; Du etal., 2000 ). Moreover, T. wolteri is also range considered, 26C was the most suitable body similar to other typical insectivorous lizards in that temperature for somatic tissue growth and 30C was an ADC and AE are both much greater than those reported optimal body temperature for locomotor performance. for herbivorous lizards (see Andrews and Asato, 1977). Thus, our data add some evidence supporting the As in other studied lizards [L. vivipara (van Damme multiple optima hypothesis for the thermal dependence etal., 1991 ); E. chinensis (Ji etal., 1995 ); E. elegans of behavioural and physiological performances in (Du etal., 2000 ); E. brenchleyi (Xu etal., 2001 ); reptiles. T. septentrionalis (Ji etal., 1996 )], T. wolteri exhibited great inter-individual differences in locomotor perfor- mance across the test body temperatures. The optimal Acknowledgements body temperatures for locomotor stamina and sprint speed in T. wolteri are much consistent, because the This research could not have been completed without maximum values of both traits occurred at nearly the the tireless laboratory efforts of Yi Shi, Hua-Song Zhou, same body temperature (30C). Unfortunately, no Xiao-Zhong Hu and Guo-Qiao Wang, nor without the comparable data on locomotor stamina are available field efforts of the students in the Department of for other species, so inter-specific comparisons cannot be Biochemistry at Chuzhou Normal College. Comments made at this time. However, it seemed that locomotor from two anonymous reviewers were very helpful for stamina in T. wolter was not as thermally sensitive as improving the manuscript. Funds for this research were expected, because lizards were able to express over 90% provided by the local governments of Zhejiang Province potential of this ability over a wide range of body and Hangzhou City and the Zhejiang Provincial Natural temperatures (23–34C; Fig. 2). Science Foundation (RC97019) to XJ. Compared with locomotor stamina, sprint speed was more thermally sensitive, because the body temperature range (26–32C) over which lizards were able to express over 90% potential of this ability was narrower (Fig. 3). References Our data show that the optimal body temperature for sprintspeed is lower in T. wolteri (30C) than in Andrews, R.M., Asato, T., 1977. Energy and utilization of a E. chinensis (34C; Ji etal., 1995 ), E. elegans (34C; Du tropical lizard. Comp. Biochem. Physiol. 58A, 57–62. etal., 2000 ), E. brenchleyi (32C; Xu etal., 2001 ) and Ballinger, R.E., Holscher, V.L., 1983. Assimilation efficiency T. septentrionalis (32C; Ji etal., 1996 ), butwe are and nutritive state in the striped plateau lizard, Sceloporus presently unable to give explanations for these differ- virgatus. (Sauria, lguanidae). Copeia 1983, 838–839. Bauwens, D., Garland Jr., T., Castilla, A.M., Van Damme, R., ences. All of these species are very common in eastern 1995. Evolution of sprint speed in lacertid lizards: morpho- China, but they differ, in various degrees, in habitat use, logical, physiological, and behavioral covariation. Evolu- selected body temperature and thermal tolerance. The tion 49, 848–863. maximum sprintspeed also differs considerably among Beaupre, S.J., Dunham, A.E., Overall, K.L., 1993. The effects species and, in our experience, lizards that differ in size, of consumption rate and temperature on apparent digest- mass, morphology (and body shape), selected body ibility coefficient, urate production, metabolizable energy temperature and habitat use may differ considerably in coefficientand passage timein canyon ( Sceloporus merria- this trait (Ji etal., 1995, 1996 ; Du etal., 2000 ; Xu etal., mi) from two populations. Func. Ecol. 7, 272–280. 2001). In Chuzhou, T. wolteri and T. septentrioanlis are Bran˜ a, F., Ji, X., 2000. The influence of incubation temperature largely sympatric species that use similar habitats, on morphology, locomotor performance, and early growth of hatchling wall lizards (Podarcis muralis). J. Exp. Zool. although lizards of both species rarely appear simulta- 286, 422–433. neously in the same perch and lizards of the former Chen, B.H., 1991. Lacertidae. In: Chen, B.H. (Ed.), The species are more often found in slightly wetter and Amphibian and Reptilian Fauna of Anhui. Anhui Science shadier microhabitats (Chen, 1991). The maximum and Technology Publishing House, Hefei, pp. 219–230. À1 sprintspeed (1057 mm s /30C Tb) of T. wolteri is Du, W.-G., Yan, S.-J., Ji, X., 2000. Selected body tempe- greater that that (approximately 800 mm sÀ1/32C Tb) rature, thermal tolerance and thermal dependence of food ARTICLE IN PRESS X.-J. Chen et al. / Journal of Thermal Biology 28 (2003) 385–391 391

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