Low Cost of Locomotion Increases Performance at Low Temperature in a Nocturnal Lizard Author(S): Kellar Autumn, Randi B

Division of Comparative Physiology and Biochemistry, Society for Integrative and Comparative Biology

Low Cost of Locomotion Increases Performance at Low Temperature in a Nocturnal Lizard Author(s): Kellar Autumn, Randi B. Weinstein and Robert J. Full Source: Physiological Zoology, Vol. 67, No. 1 (Jan. - Feb., 1994), pp. 238-262 Published by: The University of Chicago Press. Sponsored by the Division of Comparative Physiology and Biochemistry, Society for Integrative and Comparative Biology Stable URL: http://www.jstor.org/stable/30163845 Accessed: 12-06-2017 13:18 UTC

REFERENCES Linked references are available on JSTOR for this article: http://www.jstor.org/stable/30163845?seq=1&cid=pdf-reference#references_tab_contents You may need to log in to JSTOR to access the linked references.

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected].

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://about.jstor.org/terms

Division of Comparative Physiology and Biochemistry, Society for Integrative and Comparative Biology, The University of Chicago Press are collaborating with JSTOR to digitize, preserve and extend access to Physiological Zoology

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms 238

Low Cost of Locomotion Increases Performance at Low Temperature in a Nocturnal Lizard

Kellar Autumn1,2 Randi B. Weinstein2

Robert J. Full2 1Museum of Vertebrate Zoology and 2Department of Integrative Biology, University of California at Berkeley, Berkeley, California 94720

Accepted 8/16/93

Abstract Thermal optima for physiological processes are generally high (300 -400 C) in lizards. Performance decreases substantially at low temperatures, yet some lizards are nocturnal and are active with body temperatures below 150 C. We corrobo- rated three hypotheses about the ecophysiological consequences of the evolution of nocturnality in lizards: (I) nocturnality requires activity at low temperature; (2) activity at low temperature imposes a thermal handicap that constrains performance capacity; (3) nocturnal species have higherperformance capacity at low temperature than do comparable diurnal species. Field body temperatures during activity averaged i5.30C in Teratoscincus przewalskii, a nocturnal, terrestrial gecko from northwestern China. Individuals of T. przewalskii sustained

exercise at 150 C on a treadmill for more than 60 min at 0.18 km s h-1. However, 15a C was suboptimalfor sustained locomotion. Resting and maximum oxygen consumption at 15a and 250 C were similar to predicted values for diurnal lizards, supporting the hypothesis that much of thermalphysiology in lizards is evo- lutionarily conservative. The minimum cost of transport (C,,,i, O. 73 mL 02 g-1 km-1) for T. przewalskii was only 34% of the predicted value for a diurnal lizard of the same mass. This low cost yielded a maximum aerobic speed (MAS) of 0.27 km h-1' at 15 C, which is 2.5 times the predicted MASfor a diurnal lizard of the same mass. In comparison with predicted values for diurnal lizards, T. przewalskii showed increased but thermally submaximal locomotor performance capacity at nighttime temperatures.

Introduction

Lizards are ancestrally diurnal, and the thermal optima for physiological processes are generally high (300-400C; Dawson 1975; Huey 1982; Avery

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms Locomotion at Low Temperature in a Nocturnal Lizard 239

1984). Similarly, most lizards are active at these high body temperatures (T,'s) (Brattstrom 1965; Pianka 1986; Huey et al. 1989) and are capable of performance at near thermally maximal levels (Hertz, Huey, and Garland 1988). (For a discussion of the terms maximal and submaximal, see the Appendix.) Because of the limited potential for thermoregulation at night, nocturnal ectotherms often experience low body temperatures during activity (Cowles and Bogert 1944; Brattstrom 1965; Bustard 1967; Porter and Gates 1969; Pianka 1986; Huey et al. 1989). Performance decreases substantially at low temperatures, yet some lizards are nocturnal and are active with body temperatures below 150C (Thomas 1981; Valakos 1989; Henle 1990; K. Autumn, personal observation). Nocturnal lizards may have derived features that permit activity at low temperatures. Optimality theory predicts coadaptation of (physiological) thermal optima and activity temperatures (Huey and Slatkin 1976; Huey and Bennett 1987; Hailey and Davies 1988; Huey and Kingsolver 1989; Huey et al. 1989). Whereas this is generally true for diurnal lizards (Bennett 1982; Werner 1983), Huey et al. (1989) reported that there is little difference between the thermal optima for sprinting in diurnal and nocturnal species. This finding is important because it implies that performance in nocturnal lizards is thermally submaximal at night (Dial 1978; Huey et al. 1989) and contradicts the notion that it is possible to predict the evolution of physiology from ecology alone (also see Garland, Huey, and Bennett 1991). If performance in nocturnal lizards is constrained to submaximal levels at night, it is possible that increased performance at low temperature has evolved within a context of evolutionary stasis (fig. 1). We propose a general set of hypotheses to address this question.

1. Nocturnality Requires Activity at Low Temperature. As a preliminary test of this hypothesis, we determined the thermal consequences of nocturnal activity by measuring field-active body temperatures in a nocturnal lizard, Teratoscincus przewalskii, the frog-eyed gecko. We chose a lizard that is found at high latitudes because the thermal effects of nocturnality should be exaggerated at latitudinal and altitudinal limits of the biogeo- graphic distributions of nocturnal species. Frog-eyed geckos are found as far north as 470N latitude. Contrary to Pianka's (1986) prediction that these lizards must be diurnal at such high latitudes, T przewalskii is entirely nocturnal (Autumn and Han 1989; Semenov and Borkin 1992), is active at very low temperatures (Semenov and Borkin 1992; see Results), and has a foraging mode that requires sustained locomotion (Semenov and Borkin 1992; Y. L. Werner, personal communication).

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms 240 K. Autumn, R. B. Weinstein, and R. J. Full

Thermal Optimum

>e S Nocturnal-- ..a. * ...Diurnal

Critical Thermal Critical Thermal Minimum Maximum

5 15 25 35 45

Body Temperature ()Diurnal Body Temperature (0C)

Fig. 1. Hypothesis of differences in thermal sensitivity ofperformance in nocturnal and diurnal lizards. Thermal optima (To), critical thermal maxima (CTmax), and critical thermal minima (CT,,,) are similar in nocturnal and diurnal lizards. Performance capacity in nocturnal and diurnal lizards is thermally submaximal at low temperatures. Perfor- mance at low temperatures is higher in nocturnal lizards.

2. Activity at Low Temperature Imposes a Thermal Handicap That Con- strains Performance Capacity. We define a handicap as an acute physiological response that occurs when an animal is operating under suboptimal conditions. A handicap constrains performance to submaximal levels. In order to test this hypothesis, we determined the thermal sensitivity of performance capacity by measuring sustained locomotion (endurance) at temperatures equal to and greater than those measured in active geckos. En- durance is a good measure of an animal's ability to perform daily tasks (Garland and Bennett 1990), is sensitive to temperature (Bennett 1982), and is repeatable and measurable in the laboratory (Huey and Dunham 1987; Arnold and Bennett 1988; Garland 1988).

3. Nocturnal Species Have Higher Performance Capacity at Low Temper- ature than Do Comparable Diurnal Species. In testing this hypothesis, we investigated three possible mechanisms for increased endurance at low temperatures by comparing our experimental data with predicted values for physiological variables affecting sustained locomotor performance in diurnal lizards.

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms Locomotion at Low Temperature in a Nocturnal Lizard 241

a) Teratoscincusprzewalskii could have a lower CTmin in comparison to diurnal lizards. Since the CTmin is the temperature at which the animal be- comes immobile, a lower CTmi, would allow T. przewalskii to be active at lower body temperatures. b) Teratoscincusprzewalskii could have a higher maximal rate of oxygen consumption (Vo2 ,ax) at low temperature than a diurnal lizard of the same body mass. A higher Vo2 max would increase the range of sustainable locomotor speeds by increasing the maximum aerobic speed (MAS). Compar- isons of Vo2 max among species must account for temperature, body mass, and type of exercise (Gatten, Miller, and Full 1992). c) Teratoscincus przewalskii could have a lower minimum cost of locomotion (Cmin) than diurnal lizards. A lower Cmin would also increase the range of sustainable speeds by increasing the MAS without increasing Vo2 max (Full 1991; Gatten et al. 1992). The latter two possibilities follow from the equations

V02 - )0 + Cmin " Speed, (1) Vo2max Y0 +Cmin " MAS, (2) and

MAS = (VO2max - yo)/Cmin, (3) where 3y (the y-intercept of the Vo2 VS. speed function; Gatten et al. 1992) is assumed to be constant. Comparisons of Cmin among species may be independent of temperature (John-Alder and Bennett 1981; John-Alder, Lowe, and Bennett 1983; Bennett and John-Alder 1984; Lighton and Feener 1989; Full, Zuccarello, and Tullis 1990) but must account for body mass and type of exercise (Gatten et al. 1992). Increased endurance capacity at low temperature exhibited by T przewalskii, relative to diurnal lizards, should cor- relate with a greater MAS (John-Alder and Bennett 1981) because exercise at speeds below MAS can be sustained by energy derived primarily from aerobic metabolism. At speeds above MAS, fatigue occurs more rapidly since much of the energy for muscular activity must come from anaerobic sources. The thermal sensitivity of endurance capacity is largely due to the thermal sensitivity of the MAS, which in turn is a consequence of the thermal sensitivity of the Vo2max (Bennett 1982; Gatten et al. 1992). Because of the solid understanding of the physiology underlying sustained (aerobic) locomotion, we are able to not only measure performance, but also determine performance capacity.

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms 242 K. Autumn, R. B. Weinstein, and R. J. Full

In testing the mechanisms of our third hypothesis, it is important to determine what are comparable diurnal species. Body mass and temperature explain much of the variation in physiological variables affecting endurance (Full 1991) and must be considered when making comparisons among species. Allometric comparisons may include or exclude phylogeny (see Harvey and Pagel [1991] for review). If phylogeny is ignored in allometric comparisons, the implicit assumption is that the allometry represents a functional dependence that transcends phylogeny. We used both standard allometric comparisons and phylogenetically independent contrasts (Felsenstein 1985) in this study.

Material and Methods

Field Observations

The field site was 3 km south of Dunhuang (40010'N, 94050'E), on the road to Dunhuang Sand Dunes, Jiuquan Prefecture, Gansu Province, People's Republic of China. This region lies along the Silk Road and forms an inter- mediate zone between the Gobi Desert to the northeast and the Taklimakan Desert to the west. The area is known for its low rainfall and extreme temperatures. The habitat was flat, sandy desert with sparse vegetation-primarily small, spiny Alhagi sparsiflora (Leguminosae) bushes. Field observations were made from September 19, 1990, to September 25, 1990. Sunrise was at 0700 hours Beijing time (0300 hours GMT). Sunset was at 1930 hours Beijing time (1530 hours GMT). Field body temperatures in Teratoscincus przewalskii were sampled by radiotelemetry and a cloacal thermocouple. To determine Tb's Of geckos in their burrows, transmitters (Minimitter, model T) were surgically implanted into the body cavities of three large adult lizards (one male, two female; mean body mass, 15 g). Prior to surgery, lizards were placed in a sealed enclosure and anesthetized with a few drops of liquid Metafane on a cotton ball. The transmitters weighed 3.5 g and measured 25 mm in length and 10 mm in diameter, approximately the size of a typical clutch of two T. przewalskii eggs. The transmitters did not appear to cause abnormal behavior or discomfort or to hinder locomotion. While this procedure was sufficient to determine the Tb's of geckos in burrows, these radiotelemetry data prob- ably do not reflect typical field-active Tb's since aboveground activity may have been reduced in telemetered geckos. For this reason, we used only cloacal temperatures in nontelemetered geckos to determine Tb during activity. A least-squares exponential regression of temperature on time per 100 transmitter pulses yielded r2 values greater than 0.99 for calibration

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms Locomotion at Low Temperature in a Nocturnal Lizard 243

temperatures of 15a-35oC in all three transmitters. Drift in calibration after the study did not exceed 1C. Substrate temperature and air temperature (10 cm aboveground) were monitored with a thermocouple reader (Bailey BAT-12) over a period of 2 d. Cloacal temperatures in nontelemetered, nocturnally active geckos were sampled with a thermocouple thermometer (Bailey BAT-12). Geckos were located by flashlight, captured by hand, and grasped by the head and hind leg to minimize conduction. All cloacal temperatures were taken within 15 s of capture. Substrate temperature and air temperature (10 cm above ground) were measured at the spot where the lizard was captured.

Laboratory Maintenance ofAnimals

Live adult specimens of T. przewalskiiwere collected under the 1987-1991 cooperative agreement among the Chengdu Institute of Biology, Academia Sinica, the University of California, and the California Academy of Sciences. The geckos were transported to the University of California, Berkeley, where the laboratory experiments were performed. Pairs of geckos were housed in 16-L plastic terraria with a moist hide box and metal screen top. Each cage had direct UV lighting from a fluorescent tanning lamp and a heat strip to allow behavioral thermoregulation over a gradient of 25a-40aC. Tech- nicians and researchers wore protective goggles to avoid the UV radiation. The animals were kept in an environmental room on a 13L:11D photoperiod at 240C. The UV light and heat strip were on a 13:11-h on-off cycle corresponding to the photoperiod. The geckos were fed a diet of mealworms, crickets, and vitamin/mineral supplement and were watered daily. Any animal that was in questionable condition or had recently autotomized its tail was excluded from experiments. Only adult geckos were used. Each experimental group contained a nearly even sex ratio. Experiments were con- ducted within 8 mo of capture.

Critical Thermal Minima

Geckos were rapidly cooled in a walk-in freezer (-50C). Critical thermal minima were determined by measuring the cloacal temperature when the gecko was no longer able to right itself (Spellerberg 1972).

Aerobic Metabolism

Oxygen Consumption Measurements. Individuals were exercised in a miniature treadmill respirometer (Herreid, Full, and Prawel 1981). Air leaving the chainm-

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms 244 K. Autumn, R. B. Weinstein, and R. J. Full

ber was dried with Drierite, and CO2 was removed with Ascarite. The oxygen concentration was monitored with an 02 analyzer (Ametek S3A) interfaced with a personal computer (Macintosh II) and data acquisition hardware (NBMIO-16 Board, National Instruments) and software (LabView, National Instruments). Mass-specific, steady-state oxygen consumption (Vo2) was calculated from the 02 concentration (Withers 1977). Calculations of instantaneous Vo2 (Herreid et al. 1981) were identical to steady-state rates. The treadmill respirometer was placed in an environmental chamber (Fisher Low Temper- ature model 146) to control ambient temperature at either 150 or 250C.

Resting Metabolic Rate and Maximal Vo2. Geckos (mean mass + SE = 11.2 g a 0.7 g, N [individuals] = 7) were placed in the treadmill chamber for a 30-min equilibration period at either 150 or 250C, which was sufficient for Tb to reach the ambient temperature. All individuals were tested at both 150 and 25aC, although the order of experiments was randomized. After equilibration, measurements of the resting rate of oxygen consumption (Vo2 rest) were taken for 10 min while the lizards rested quietly. The submaximal and maximal rates of oxygen consumption were determined by a multiple speed, or step, treadmill test (Full and Herreid 1983). After the 10-min rest period, lizards were exercised at a slow speed. The slowest speed used at each temperature was the minimum speed at which the lizards

could run consistently (0.14 km * h-' at 150C and 0.18 km s h-' at 250C). On attaining a steady-state oxygen consumption (Vo2 s) for 3 min, the speed of the treadmill belt was increased to a higher speed until a new higher steady state was attained. Three minutes after a new steady state had been reached, speed was increased again. At 250C, Vo2 max was defined as the

Vo2 s attained when two consecutive incremental increases in speed resulted in no further increase in Vo2. At 150C, animals fatigued before reaching Vo2 s at speeds greater than 0.29 km * h-', even when exercised at a single speed. Each animal exercised at only three or four speeds per day. Animals rested for at least 5 d between trials.

Endurance Capacity

Geckos (mean mass a SE = 9.06 g + 0.52 g, N[individuals] = 25), including the seven individuals from the aerobic metabolism experiment (above), were exercised in a miniature treadmill respirometer (Full 1987). The treadmill respirometer was placed in an environmental chamber (Fisher Low Temper- ature model 146) to control ambient temperature at either 150 or 250C. After 30 min of temperature equilibration in the treadmill chamber, individuals were exercised to fatigue at a single speed. The nine speeds used ranged from 0.18

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms Locomotion at Low Temperature in a Nocturnal Lizard 245

to 1.08 km s hV at both 250C (N= 25) and 150C (N= 24). Three individuals exercised at each speed, except only one individual ran at 0.65 km s h-' at 250C. Geckos maintained a consistent pace without prodding until just before fatigue. An animal was considered fatigued when it failed to keep pace with the treadmill belt or did not respond to three successive prodding attempts. The experiment was halted if endurance time exceeded 30 min (John-Alder et al. 1983; Bennett and John-Alder 1984), and these values were not used in calculating the endurance versus speed function. Experiments during which geckos walked erratically or struggled were discarded.

Phylogenetic Analysis

Regressions using standardized, phylogenetically independent contrasts of

Cmi on body mass followed the protocol of Felsenstein (1985) and Garland, Harvey, and Ives (1992). We used the computer program C.A.I.C., version 1.2 (Purvis 1991), to calculate independent contrasts. Phylogenetic relationships for independent contrasts were taken from Estes, de Queiroz, and Gauthier (1988). Branch lengths were estimated from fossil records (Estes 1983). We used Gim,, and body mass values for species from seven lizard families as reported by John-Alder et al. (1986). For some species, John- Alder et al. (1986) report C,,i from both large and small individuals. We excluded the measurements with low mass if they differed by more than 10-fold from the measurements with the higher mass(es). Values for taxa containing more than one species (e.g., Iguanidae, Lacerta, Varanus) were estimated from mean log-transformed species values. We used a model of gradual evolution (Brownian motion) and regression through the origin (Garland et al. 1992) to calculate allometries of standardized independent contrasts (IC) of log rin (Y) versus log body mass (X). We calculated the allometries once for all taxa and once excluding our data for T. przewalskii. To check the assumptions of independent contrasts and linear regression, we searched for correlations and patterns in plots of ICX, and IC Y versus estimated nodal values and variances, and in plots of residuals versus ICX, and IC 1. There was no significant correlation (P>> 0.05) or pattern evident in any of these plots, and the residuals were symmetrically distributed about zero, which indicates that the assumptions were supported.

Results

Field Body Temperature

Body temperatures in three telemetered geckos in burrows varied with surface substrate temperature and ranged from 4.4aC at 0545 hours to 36.80C

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms 246 K. Autumn, R. B. Weinstein, and R. J. Full

at 1607 hours (fig. 2). The exact position of individuals in burrows was sometimes evident by differences in signal strength. These observations suggest that geckos actively thermoregulate during the day in the burrow by moving closer to the burrow mouth as the ground cooled and further from the burrow mouth as the ground warmed. Burrows of Teratoscincus przewalskii are generally more than 1 m long and extend 0.5 m below the surface. The maximum daytime substrate temperature on the surface was 52.10C at 1600 hours, while maximum Tb was only 36.80C (fig. 2). Deep- burrow temperatures measured at midday did not exceed 25aC. Cloacal temperatures in nocturnally active nontelemetered geckos ranged from 9.90 to 21.5aC and averaged 15.30C a 0.87 SE (N = 13). The geckos seemed to be thermoconformers during the night: Tb was directly proportional to

nighttime ground temperature (T,; Tb = -1.01 + 1.08 s Tg, r2 = 0.79, P < 0.001). Geckos were active above ground from sunset to sunrise. Peak aboveground activity lasted for 2 h after full darkness after sunset.

Critical Thermal Minimum

Mean CTmin was 8.90C (SD = 1.26, range 6.50-12.20C, N= 11), only 1aC below the lowest field-active body temperature recorded in the field (fig. 2).

Oxygen Consumption

Rate of Consumption at Rest. The rate of oxygen consumption during the 10 min prior to exercise was averaged to obtain Vo2 rest. Mass-specific Vo2 rest was strongly influenced by the ambient temperature (fig. 3; table 1). Geckos

resting at 25aC had a significantly higher Vo2 rest than those at 15"C (paired t-test, P< 0.001; table 1).

Steady-State Oxygen Consumption versus Speed. Steady-state oxygen consumption was calculated as the mean Vo2 for the last 2-3 min of exercise

at(fig. each 3; tablespeed. 1). AtAt eachboth temperature,150 and 25"C, theVo2iss y-intercepts increased of linearly the regression with speed equations (y0) were elevated above Vo2 rest (fig. 3; table 1).

Maximum Rate of Oxygen Consumption. At 15aC, Vo2 max was attained at 0.29 + 0.001 km h-V1 (mean + SE). Animals exercising at faster speeds

fatigued in less than 4 min, and Vo2 swas WS not attained. At 250C, Vo2 max was attained at the three fastest speeds tested (range 0.36-0.57 km h-l). The

slope of the regression equation describing Vo2 ss versus speed within this

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms Locomotion at Low Temperature in a Nocturnal Lizard 247

60 Night - ,-+ * Day - *---- Night 50

S40 / / . \

S3030 /- / . .s s

S 20 /H5 d.t 10 .

0 4 8 12 16 20 24 Time of Day (h)

Fig. 2. Body temperature cycle in Teratoscincus przewalskii. Body temperatures in nontelemetered (triangles) field-active geckos were as low as 100 C during the night. Geckos were only active above ground at night. Body temperatures during activity were similar to ground (dashed line) and air (dotted line) temperatures. Telemetered (circles and solid line) geckos in burrows actitvel- thermoregulated during the day. Day- time ground temperatures reached 52. G C, while the maximum recorded body temperature was 368. 8C Deep burrow temperatures measured at midday did not exceed 250 C.

range did not test significantly different from zero (P = 0.34), and these Vo2s values have been pooled to calculate mean Vo2 max. Mass-specific Vo2 max was significantly higher at 25oC than at 15aC (paired t-test, P< 0.001; fig. 3; table 1).

Maximum Aerobic Speed. The speed at which Vo2 max was attained was calculated from the intersection of the Vo2 s versus speed regression equation (table 1) and a horizontal line representing Vo2 max as indicated in figure 3.

Cost of Locomotion

At both 150 and 25aC, the total cost of locomotion, defined as the amount of 02 used per gram to travel 1 km, decreased with increasing speed. The

slope of the regression equation describing submaximal Vo2 ss s a function of speed (at constant temperature) represents Cmin (Taylor, Schmidt-Nielsen,

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms 248 K. Autumn, R. B. Weinstein, and R. J. Full

0.6

0.5

0.4 E- 0.3 -~ 250CI-- , --- S0.2 O 15aC "" 0.1 . MAS

0.0,, .. . . 3 . , s . s , 0.0 0.1 0.2 0.3 0.4 0.5 0.6

Speed (km h-1)

Fig. 3. Steady-state oxygen consumption during exercise at 15 C (closed circles) and 250 C (open circles). The slopes of the lines relating aerobi- cally submaximal Vo2s and speed at a constant temperature represent Cmn. Resting rates are shown at zero speed.

and Raab 1970). The values for Cmin at 150 and 25"C did not test significantly different (ANCOVA, P= 0.18; fig. 3; table 1).

Endurance

Endurance capacity (time to fatigue) decreased exponentially as exercise speed increased at each ambient temperature tested (fig. 4) and was strongly influenced by temperature. At 250C, geckos showed a greater endurance capacity (tend) over the range of speeds tested (tend = 0.030v-207, where tend is in hours and vis in km h-a; r2 = 0.87; P= 1 X 10-4) than geckos exercised at 15aC (tend = 0.013v1.70; r2 = 0.83; P = 1 X 10-4). Endurance at both temperatures was correlated with the MAS.

Discussion

Frog-eyed geckos (Teratoscincus przewalskii) are nocturnally active with Tb'S roughly 200C below the thermal optima of diurnal lizards. The method of parsimony establishes a diurnal ancestor for all lizards. The Iguania (sister taxon to the larger group to which geckos belong) is almost entirely diurnal,

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms (r2=0.52;P<0.001) (r2=0.59;P<0.001)

Vo2,(mLO2g--h1)

(oC)(mL02g-'sh-1')0O2g--h-')(kmVo2rest(V,kmh-1)VO2 15.036(a.006).300(a.009).2688.33.73(+.14)V+.0631.75 Aerobicmetabolismandthermaldependenceofactivitycapacityat15025aCinTeratoscincusprzewalskii 25.102(a.010).518(+.08).3335.081.06(+.20)V+.1651.62 Note.ValuesforVo2restandmaxrepresentmeana1SE(inparentheses).The95,confidencelimitstheslopeofVS.speedregression TABLE 1 equationsareindicatedinparentheses. aAt150-250C,QG0ofvo2ret=2.83. bAt150-250C,QioofVo2..=1.74. 7 Vo2 resta Vo2 m3xo MASc Vo2 m.x/ versus Speed y-Intercept/ Speed versus m.x/ Vo2 MASc m3xo Vo2 resta Vo2 7 cAt150-250C,QioofMAS=1.21.

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms 250 K. Autumn, R. B. Weinstein, and R. J. Full and the strong phylogenetic pattern of nocturnality (99% of nocturnal lizards are geckos, and 99% of geckos are nocturnal) indicates a single evolution of nocturnality for the Gekkota (see Estes et al. [1988] for phylogeny). An- cestral diurnality in lizards is further supported by functional evidence (Walls 1942). Because lizards are ancestrally diurnal and are generally active at temperatures near optimum (Avery 1982; Bennett 1982; Werner 1983), the mean activity temperature of 15.3aC in T. przewalskii represents a substantial evolutionary shift. One might expect a corresponding shift in physiology to accompany this new selective regime (Huey and Slatkin 1976; Huey and Bennett 1987; Hailey and Davies 1988; Huey and Kingsolver 1989; Huey et al. 1989; Baum and Larson 1991). Since the velocity of physiological rate processes decreases exponentially with temperature below the thermal optimum, a diurnal lizard would experience a severe handicap in performance capacity at 150C. Assuming a Qio of 2.5, a 200C drop in body temperature would result in an 84% decrease in performance capacity. Optimality theory predicts that nocturnal lizards should have derived adaptations that fully compensate for low body temperature. Ideally, performance capacity should be thermally maximal at the temperatures that the lizard experiences during activity (Huey and Slatkin 1976; Huey and Bennett 1987; Huey and King- solver 1989; Huey et al. 1989). If thermally maximal performance capacity

0.5 -

150C 250C 0.4 iI. a

o 0.3- ie 0

d)I 0 o 0.2

0.1 O

MAS 00 M 0.0 0.2 0.4 0.6 0.8 1.0 1.2

Speed (km h-1) Fig. 4. Endurance time as a function of speed at 150 C (closed circles) and 250 C (open circles). Endurance was correlated with MAS. Experi- ments were terminated after 30 min if the animal had not yet become fatigued and were not included in the curve fitted to the data.

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms Locomotion at Low Temperature in a Nocturnal Lizard 251

at low temperature has not evolved in T przewalskii, perhaps performance capacity at low temperature has increased to a satisfactory level (Stearns 1982). In the following sections we show that nocturnal activity imposes a thermal handicap on locomotor performance (see Introduction) and that, while T. przewalskii retains the thermal sensitivity typical of lizards, it differs from diurnal lizards in being capable of greater sustained locomotor performance at low temperature (150 C).

Locomotor Performance at Low Temperature

Critical Thermal Minimum. Increased sustained locomotor performance in T. przewalskii cannot be explained by a difference in the CTmin. The CTmin (8.90 C) in T przewalskii is at the high end of the range of CTmin recorded for diurnal lizards (2.5a-9.8aC) reported by Spellerberg (1972) and is similar to the mean CTmin of 13 species of diurnal (10.10C) and nocturnal (10.00C) lizards reported by Huey et al. (1989). While it is likely that low-temperature acclimation could lower the CTmin in T przewalskii (Spellerberg 1972; Kaufmann and Bennett 1989), our results indicate that its CTmin is not exceptionally low for a lizard. It is surprising that mean Tb during activity was only 1C above CTmin,. However, there was a fair range of CTmin measured for our laboratory population (6.50-12.20C). It is not as surprising then to find some individuals active in the field at Tb'S of 100C. Individuals of T przewalskii may operate closer to their lower critical thermal limits than do diurnal lizards or nocturnal lizards from warmer habitats (see Huey 1982).

Resting Rate of Oxygen Consumption. The resting metabolic rate of T przewalskii at 150 and 25aC is similar to values predicted for diurnal lizards of the same body mass. Allometric equations for Vo2 rest in lizards (Andrews and Pough 1985) predict values for Vo2 rest that are similar to the observed values for Vo2 rest in T przewalskii at 15" and 25oC (table 2). In addition, the degree of thermal dependence found for Vo2 rest in T. przewalskii (Qo10 = 2.83) is similar to those reported for several species of lizards over the

200-300C interval (Q10 range = 1.7-5.4; Bennett and Dawson 1976).

Maximal Oxygen Consumption. The Vo2 max'S observed for T przewalskii are not exceptionally high for a lizard of its size. On the basis of allometric equations for several (12-15) species of lizards (Vo2 max at 200C = 0.69m-o19,

Vo2 max at 300C = 1.96m0-24, Vo2 max in mL 02. - h- ' and m in grams; Bennett 1982), the predicted Vo2 max values for an 11.2-g lizard at 200 and

30oC are 0.44 and 1.10 mL 02 s g-1 , h-', respectively. To our knowledge, no other lizard has been exercised on a treadmill at a body temperature of

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms (mL02,-h-)02g-1h-l)km1)(kmhI) Vo2restmaxCminMAS

T,, (oC)MeasuredPredictedaPredictedbPredictedePredicted 15.04.30.28.732.13.27.11"(.10)e ComparisonoftheenergeticsandperformanceTeratoscincusprzewalskiiahypotheticaldiurnallizard ofthesamebodymass 25.10.52.691.062.13.33.17d(.25)e g-'km-1;John-Alderetal.1986). TABLE2 aValuebasedonAndrewsandPough1985. bValueassumesaQioof2.5(Bennett1982). cValuebasedonJohn-Alderetal.1986. dValueassumesthey-intercept(seetable1)andVo2maxmeasuredforT.przewalskiiCminpredictedalizardofsamebodymass(2.13mL02 eValueassumesthey-interceptmeasuredforT.przewalskiiandVo2maxCminpredictedalizardofsamebodymass.

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms Locomotion at Low Temperature in a Nocturnal Lizard 253

15aC, limiting comparisons of our observed data to predicted values. The Vo2 max observed for T. przewalskii at 150C is similar to the predicted value (table 2), and the Vo2 max observed at 250C is 25% lower than the predicted value (table 2), assuming a Qio at 200-300C of 2.5. Thermal dependence for Vo, max in T. przewalskii (table 1) is similar to Qio's reported for lizards over the 200-300C interval (Qio range = 1.7-2.9; Bennett 1982) and the 250-350C interval (Qio range = 1.3-2.8; John-Alder et al. 1983).

Minimum Cost of Transport. The mass-specific Cmin observed for T. przewalskii is less than half the Cmi,, predicted for a terrestrial animal of comparable mass. Full (1989) plotted Cmin as a function of body mass for 153

species of terrestrial animals (Cmin = 10.92 m-030, Cmin in mL 02 . g-1 * km-1 and m in grams; fig. 5A). Mass-specific Cmin decreases with an increase in body mass so that larger animals require less energy to move 1 g over 1 km. The observed Cmi,, for T przewalskii is 36%-52% of the predicted value for an 11.2-g terrestrial animal (2.03 mL 02 g -' km-1'; 95%o confidence limits = 0.84-4.92; calculated from data presented in Full 1989). When compared with lizards alone, the Cmin observed for T przewalskii is 34%-50% of the Cmi predicted for a lizard of its body size. The predicted Cmin for an 11.2-g lizard is 2.13 mL O s g-' , km-' (95% confidence limits = 1.26-3.58; calculated from data presented in John-Alder et al. 1986; table 2). The observed values for T przewalskii at both 150 and 250C fall below the 95% confidence limits for an 11.2-g lizard (fig. 5B). Felsenstein (1985) identified potential problems in the use of standard regression with species as observations and outlined a method to compare characters among species or higher taxa using phylogenetically independent contrasts (also see Garland et al. 1993). The advantage to using independent contrasts (instead of species) as observations is that phylogeny is taken into account in the determination the regression and its confidence limits. If species are treated as independent observations, it is possible that degrees of freedom could be overestimated and that conclusions could be biased by the overrepresentation of speciose taxa (Harvey and Pagel 1991). Our results showed little difference between standard and IC regressions for lizard body mass and Cmi. The gecko-Autarchoglossa contrast fell well outside the 95% confidence interval of the IC allometry (fig. 5 C). The concor- dance of standard regression and IC regression provides further evidence that Cmi in the gecko is unusually low. There are several factors that may cause a low Cmin. One is simply a low cost of muscular force production (Kram and Taylor 1989). Another is an unusually high Yo due to elevated cost at low speeds. If Cmin is low because y0 is unusually high, the MAS will not be increased (see Introduction,

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms A 2.53 a U, oyp Mammals Birds

1 + 2Frogs 4aL2 aL l0 ASalamanders Lizards 1 Crustaceans 2. -6 5 - - 2 - 1 Insects as( .5 [] Myriapods S G Gecko Q

- 2 - S1.8 1.6 s

1.4 AG25~~ ..a A

1.2 G. G1 ""0

-2.5 -2 -1.5 -1 -.5 0 .5 log Mass (kg) .05 C

.04 -

aa .02 .01 -

-.12 -.1 -.08 -.06 -.04 -.02 0 .0 , , , G-A Alog ,Mass " Fig. 5. A, Minimum cost of transport as a function of body mass for a broad sample of terrestrial animals (see text). Geometric symbols represent values for terrestrial animals (Full 1989); G represents values for the gecko Teratoscincus przewalskii. Minimum cost of transport for T. przewalskii falls below the 95% forecast confidence limits (dashed lines) of the allometry. B, Minimum cost of transport as a function of body mass for lizards (see text). The triangles represent values for diurnal lizards (Uohn-Alder et al. 1986); G represents values for the gecko T. przewalskii. Minimum cost of transportfor T. przewalskii falls below the 95% forecast confidence limits (dashed lines) of the allometry. C, Phylo- genetically independent contrasts (IC) in minimum cost of transport (ACmin) versus IC in body mass (Am)for lizards. The triangles represent contrasts among diurnal lizards (John-Alder et al. 1986); G-A represents the contrast between T. przewalskii and autarchoglossan lizards. This contrast falls outside the 95% confidence limits (dashed lines) of the allometry (r2 = 0.70;F = 13.7; P = .01; n = 7; A log Cmn = -0.25 s A log

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms Locomotion at Low Temperature in a Nocturnal Lizard 255

eq. [3]). An elevated yo could be due to erratic locomotion or extraneous behavior at low speeds. To minimize this possibility, the slowest treadmill speeds used in this study were chosen to reduce extraneous locomotor movement. The ratio of y-intercept to Vo2 rest measured for T przewalskii (table 1) was comparable to that of other vertebrates (Paladino and King 1979; John-Alder and Bennett 1981) and invertebrates (Herreid 1981; Full and Herreid 1983; Full 1987). Moreover, our conclusions are not sensitive to changes in yo: even for a Yo equal to zero, given the MAS measured for the gecko, the Cmin,, would still fall below the 95% forecast confidence limits of the predicted Cmin for diurnal lizards. The relatively low Cmin observed for T. przewalskii may partially compensate for a thermally reduced Vo2 max by increasing MAS above predicted values and therefore increasing the range of sustainable speeds at low temperature. This pattern is similar to that found for lungless salamanders (Full et al. 1988, 1990) and sidewinders (Secor, Jayne, and Bennett 1992). Gila monsters also have a relatively low Cmin, but they have a relatively high Vo2 max (John-Alder et al. 1986). If T. przewalskii had the Cmin predicted for a lizard of the same body mass, then the MAS at 15aC would be only 0.11 km h-' rather than the observed 0.27 km s h-1 (table 2). Therefore, as a result of a relatively low Cmin, the MAS for T. przewalskii is increased by 2.5-fold above predicted values (fig. 6). An increased MAS translates into increased endurance capacity for T przewalskii. Since T przewalskii is an active forager (Semenov and Borkin 1992; Y. L. Werner, personal communication), sustained locomotion is likely to be a particularly important aspect of its ecology. These results support our third hypothesis (see Introduction; fig. 1) of increased performance at low temperatures in nocturnal lizards. Unlike most diurnal lizards (see Bennett 1982; Werner 1983), individuals of T. przewalskii are not capable of thermally maximal sustained locomotor performance in the field because they are nocturnal and their range of activity temperatures is suboptimal (endurance at 25aC was greater than at 150C; fig. 4). These results support our first and second hypotheses (see Intro- duction) that nocturnality represents a thermal handicap that constrains performance capacity. It is very interesting that a low Cmin is the only physiological difference we found between T przewalskiiand diurnal lizards. The

m), which indicates that T. przewalskii has a low Cmn in comparison to its sister taxon, once the effect of mass has been removed. Excluding the gecko data, the IC allometry was highly significant (r2 = 0.89; F = 37.8; P < 0.002; n = 6) and had a slope of- 0.30, which is similar to the slope of -0.28 reported by John-Alder et al. (1986).

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms 256 K. Autumn, R. B. Weinstein, and R. J. Full physiological similarity of nocturnal and diurnal lizards despite their ecological dissimilarity requires further explanation (see Huey et al. 1989). Evolutionary stasis of thermal optima in nocturnal lizards has been attributed to balancing selection on the need for a high CTmax (Huey et al. 1989; R. B. Huey, personal communication). However, we have no evidence that maximum daytime temperatures in these deep (0.5-m) burrows are potentially lethal or stressful to T. przewalskii. On the contrary, these lizards may have the advantage of protected basking (Bustard 1967; Huey et al. 1989) in a thermally buffered microhabitat that is both refuge and thermal gradient.

Nocturnality and Activity Temperature

Nocturnality in T. przewalskii represents an evolutionary shift in daily activity cycle (Huey et al. 1989). It is illuminating that nocturnality in these geckos does not involve a shift in daily temperature cycle. By observing how Tb fluctuates during a 24-h period (fig. 2), it would be difficult to discern whether

o.3 - . . . .-

-r 0.2 -

g ,

O o.1 / MAS MAS Predicted Gecko

0.0 0.0 0.1, a0.2 , 0.3i '0.4

Speed (km h-')

Fig. 6. Effect of low Cmin on MAS in Teratoscincus przewalskii. The dashed line represents the predicted relationship of Vo2s and running speed (John-Alder et al. 1986). The solid line shows the relationship determined in this study for T. przewalskii at 15a C (closed circles). The slopes of the lines relating Vo2, and speed represent Cmn. The dashed arrow represents the predicted MAS for a diurnal lizard of the same body mass (see text and table 2). The solid arrow represents the MAS determined in this study for T. przewalskii at 150 C. The low Cm,,n in T. przewalskii increases the range of sustainable speeds by a factor of 2.5 times the predicted value.

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms Locomotion at Low Temperature in a Nocturnal Lizard 257

these lizards were in fact nocturnal or diurnal. Our field data show a pattern typical of a diurnal lizard: high Tb during the day and low Tb at night (Regal 1967, 1974; Stebbins and Barwick 1968; Avery 1985). It is likely that the minimum Tb in the gecko would be lower than the minimum Tb in most diurnal lizards because of thermal buffering in the burrow against extreme nocturnal temperatures. The difference between the behavior of T. przewalskii and that of a diurnal lizard is that activity and thermoregulation do not occur coincidentally. It has long been known that nocturnal lizards choose a higher Tb on a laboratory thermal gradient than they experience during field activity (Licht et al. 1966; Huey 1982; Arad, Raber, and Werner 1989). Our radiotelemetry data indicate that this is not an artifact of laboratory conditions and that nocturnal and diurnal lizards have similar thermal re- quirements (Bustard 1967) despite substantial differences (of up to 350C) in field-active Tb. The meaning of activity in nocturnal lizards should be reevaluated. During the day individuals of T przewalskii are physiologically active because Tb is high. At night, Tb, is low and suboptimal, yet this is the time when locomotor activity takes place. To understand the ecology and evolution of nocturnal lizards, it is necessary to consider other activities as well as foraging. Digestion, growth, and reproduction in lizards require products of rate- processes that may be sufficiently rapid only at high temperature (Cowles and Bogert 1944; Dawson 1975; Andrews 1982; Avery 1984; Stevenson, Pe- terson, and Tsuji 1985; Hailey and Davies 1987; Troyer 1987). In other words, the heat sum necessary for a complete lizard life cycle may not be available at night. Thus, nocturnal lizards may require a high Tb during the day (Bustard 1967; Saint Girons 1980) because much of their physiology is ancestrally optimal at high temperatures. From this perspective, it is not surprising that performance capacity in nocturnal lizards is thermally submaximal at low temperature.

Acknowledgments

We thank the following for their help on this project: A. Bennett, E. Brodie III, D. de Nardo, X.-L. Fang, C. Farley, T. Garland, H. Greene, R. Huey, P. Licht, R. Macey, T. Papenfuss, J. Segal, B. Shoplock, S. Thoms, D. Wake, Y.-Z. Wang, E. Zhao, the staff of the University of California, Berkeley (UCB), Office of Laboratory Animal Care, and two anonymous reviewers. This project was supported by a National Geographic research grant to T. Papenfuss, R. Macey, and K. Autumn, National Science Foundation (NSF) grants PYI: DCB 90-58138 and IBN-9205844 (to R.J.F.), NSF graduate fellowship (to R.B.W),

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms 258 K. Autumn, R. B. Weinstein, and R. J. Full

Sigma Xi grant (to K.A.), the Museum of Vertebrate Zoology Karl B. Koford Fund (to K.A.), UCB Integrative Biology Department grant-in-aid (to K.A.), the California Academy of Sciences, and the Patagonia Corporation.

Appendix Discussion of Terminology

Ambiguity arises over the terms maximal and submaximal because they can refer to performance capacity in general or to aerobic metabolism. We use thermally maximalperformance capacity to refer to the highest level of performance possible at any temperature. Optimal conditions permit maximal performance. At temperatures below the thermal optimum, performance is constrained to thermally submaximal levels. When referring to aerobic metabolism, we specifically state that it is the rate of aerobic metabolism that is maximal or submaximal (relative to Vo2 max) and that temperature is held constant. It is important to distinguish between performance and performance capacity. Performance refers to a measured value of a performance variable (e.g., sprint speed = 0.8 m * s-I), while performance capacity is the maximum potential value of the performance variable in an individual or species. Performance maxima can be inferred by a large sample of performance measurements (e.g., maximum sprint speed in John-Alder, Garland, and Bennett [1986]); however, direct measurement of performance capacity is preferable since factors such as behavior are less likely to be important. Performance capacity can be determined by using physiological measurements to verify that performance is maximal (e.g., endurance capacity is verified by measuring the maximum aerobic speed).

Literature Cited

ANDREWS, R. M. 1982. Patterns of growth in reptiles. Pages 273-320 in C. GANS and F. H. POUGH, eds. Biology of the Reptilia. Vol 13. Academic Press, London. ANDREWS, R. M., and F. H. POUGH. 1985. Metabolism of squamate reptiles: allometric and ecological relationships. Physiol. Zool. 58:214-231. ARAD, Z., P. RABER, and Y. L. WERNER. 1989. Selected body temperature in diurnal and nocturnal forms of Ptyodactylus (Reptilia: Gekkonidae) in a photothermal gradient. J. Herpetol. 23:103-108. ARNOLD, S. J., and A. F. BENNETT. 1988. Behavioural variation in natural populations. V. Morphological correlates of locomotion in the garter snake (Thamnophis radix). Biol. J. Linnean Soc. 34:175-190. AUTUMN, K., and B. HAN. 1989. Mimicry of scorpions by juvenile lizards, Teratoscincus roborowskii (Gekkonidae). Chinese Herpetol. Res. 2:60-64. AVERY, R. A. 1982. Field studies of body temperatures and thermoregulation. Pages 93-166 in C. GANS and F. H. POUGH, eds. Biology of the Reptilia. Vol 12. Academic Press, London.

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms Locomotion at Low Temperature in a Nocturnal Lizard 259

-. 1984. Physiological aspects of lizard growth: the role of thermoregulation. Pages 407-424 in M. W. J. FERGUSON, ed. The structure, development, and evolution of reptiles. Symp. Zoological Soc. Lond. 52. -. 1985. Thermoregulatory behaviour of reptiles in the field and in captivity. Pages 45-60 in S. TowNsoN and K. LAWRENCE, eds. Reptiles: breeding, behaviour and veterinary aspects. British Herpetological Society, London. BAUM, D. A., and A. LARSON. 1991. Adaptation reviewed: a phylogenetic methodology for studying character macroevolution. Syst. Zool. 40:1-18. BENNETT, A. F. 1982. The energetics of reptilian activity. Pages 155-199 in C. GANS and F. H. POUGH, eds. Biology of the Reptilia. Vol 12. Academic Press, London. BENNETT, A. F., and W. R. DAWSON. 1976. Metabolism. Pages 127-223 in C. Gans and F. H. Pough, eds. Biology of the Reptilia. Vol 12. Academic Press, London. BENNETT, A. F., and H. B. JOHN-ALDER. 1984. The effect of body temperature on the locomotory energetics of lizards. J. Comp. Physiol. 155B:21-27. BRATTSTROM, B. H. 1965. Body temperatures of reptiles. Am. Midland Nat. 73:376- 422. BUSTARD, H. R. 1967. Activity cycle and thermoregulation in the Australian gecko, Gehyra variegata. Copeia 1967:753-758. COWLES, R. B., and C. M. BOGERT. 1944. A preliminary study of the thermal require- ments of desert reptiles. Bull. Am. Museum Nat. Hist. 83:265-296. DAWSON, W. R. 1975. On the physiological significance of the preferred body temperatures of reptiles. Pages 443-473 in D. M. GATES and R. SCHMERL, eds. Per- spectives of biophysical ecology. Springer, New York. DIAL, B. E. 1978. The thermal ecology of two sympatric, nocturnal Coleonyx (Lac- ertilia: Gekkonidae). Herpetologica 34:194-201. ESTES, R. 1983. The fossil and early distribution of lizards. Pages 365-398 in A. G. J. RHODIN and K. MIYATA, eds. Advances in herpetology and evolutionary biology: essays in honor of Ernest E. Williams. Museum of Comparative Zoology, Cambridge, Mass. ESTES, R., K. DE QUEIROZ, and J. GAUTHIER. 1988. Phylogenetic relationships within Squamata. Pages 119-281 in R. ESTES and G. PREGILL, eds. Phylogenetic relationships of the lizard families: essays commemorating Charles L. Camp. Stanford University Press, Stanford, Calif. FELSENSTEIN, J. 1985. Phylogenies and the comparative method. Am. Nat. 125:1-15. FULL, R. J. 1987. Locomotion energetics of the ghost crab. I. Metabolic cost and endurance. J. Exp. Biol. 130:137-153. -. 1989. Mechanics and energetics of terrestrial locomotion: from bipeds to polypeds. Pages 175-182 in W. WIESER and E. GNAIGER, eds. Energy transformation in cells and animals. Thieme, Stuttgart. - 1991. The concepts of efficiency and economy in land locomotion. Pages 97-131 in R. W. BLAKE, ed. Efficiency and economy in animal physiology. Cambridge University Press, Cambridge. FULL, R. J., B. D. ANDERSON, C. M. FINNERTY, and M. E. FEDER. 1988. Exercising with and without lungs. I. The effects of metabolic cost, maximal oxygen transport and body size on terrestrial locomotion in salamander species. J. Exp. Biol. 138:471- 485. FULL, R. J., and C. F. HERREID. 1983. The aerobic response to exercise of the fastest land crab. Am. J. Physiol. 244:R530-R536.

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms 260 K. Autumn, R. B. Weinstein, and R. J. Full

FULL, R. J., D. A. ZUCCARELLO, and A. TULLIS. 1990. Effect of variation in form on the cost of terrestrial locomotion. J. Exp. Biol. 150:233-246. GARLAND, T., JR. 1988. Genetic basis of activity metabolism. I. Inheritance of speed, stamina, and antipredator displays in the garter snake Thamnophissirtalis. Evolution 42:335-350. GARLAND, T., JR., and A. F. BENNETT. 1990. Quantitative genetics of maximal oxygen consumption in a garter snake. Am. J. Physiol. 259:R986-R992. GARLAND, T., JR., A. W. DICKERMAN, C. M. JANIS, and J. A. JONES. 1993. Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42:265-292. GARLAND, T., JR., P. H. HARVEY, and A. R. IVES. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41:18- 32. GARLAND, T., JR., R. B. HUEY, and A. F. BENNETT. 1991. Phylogeny and thermal physiology in lizards: a reanalysis. Evolution 45:1969-1975. GATTEN, R., K. MILLER, and R. J. FULL. 1992. Locomotion energetics at rest and during exercise. Pages 314-377 in M. E. FEDER and W. BURGGREN, eds. Environmental physiology of the amphibians. Cambridge University Press, New York. HAILEY, A., and P. M. C. DAVIES. 1987. Digestion, specific dynamic action, and ecological energetics of Natrix maura. Herpetological J. 1:159-166. - . 1988. Activity and thermoregulation of the snake Natrix maura. II. A synoptic model of thermal biology and the physiological ecology of performance. J. Zool. Lond. 214:325-342. HARVEY, P. H., and M. D. PAGEL. 1991. The comparative method in evolutionary biology. Oxford University Press, Oxford. HENLE, K. 1990. Population ecology and life history of the arboreal gecko Gehyra variegata in arid Australia. Herpetological Monogr. 4:30-60. HERREID, C. F. 1981. Energetics of pedestrian arthropods. Pages 491-526 in C. F. HERREID and C. R. FOURTNER, eds. Locomotion and energetics in arthropods. Plenum, New York. HERREID, C. F., R.J. FULL, and D. A. PRAWEL. 1981. Energetics of running cockroaches. Science 292:331-333. HERTZ, P. E., R. B. HUEY, and T. GARLAND, JR. 1988. Time budgets, thermoregulation, and maximal locomotor performance: are reptiles olympians or boy scouts? Am. Zool. 28:927-938. HUEY, R. B. 1982. Temperature, physiology, and the ecology of reptiles. Pages 25- 91 in C. GANS and F. H. POUGH, eds. Biology of the Reptilia. Vol. 12. Academic Press, London. HUEY, R. B., and A. F. BENNETT. 1987. Phylogenetic studies of coadaptation: preferred temperatures versus optimal performance of lizards. Evolution 41:1098-1115. HUEY, R. B., and A. E. DUNHAM. 1987. Repeatability of locomotor performance in natural populations of the lizard Sceloporus merriami. Evolution 41:1116-1120. HUEY, R. B., and J. G. KINGSOLVER. 1989. Evolution of thermal sensitivity of ectotherm performance. Trends Ecol. Evol. 4:131-135. HUEY, R. B., P. H. NIEWIAROWSKI, J. KAUFMANN, and J. C. HERRON. 1989. Thermal biology of nocturnal ectotherms: is sprint performance of geckos maximal at low body temperatures? Physiol. Zool. 62:488-504. HUEY, R. B., and M. SLATKIN. 1976. COsts and benefits of lizard thermoregulation. Q. Rev. Biol. 51:363-384.

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms Locomotion at Low Temperature in a Nocturnal Lizard 261

JOHN-ALDER, H. B., and A. F. BENNETT. 1981. Thermal dependence of endurance and locomotory energetics in a lizard. Am. J. Physiol. 241:R342-R349. JOHN-ALDER, H. B., T. GARLAND, JR., and A. F. BENNETT. 1986. Locomotory capacities, oxygen consumption, and the cost of locomotion of the shingle-back lizard (Trachydosaurus rugosus). Physiol. Zool. 59:523-531. JOHN-ALDER, H. B., D. H. LOWE, and A. F. BENNETT. 1983. Thermal dependence of locomotory energetics and aerobic capacity of the Gila monster (Heloderma sus- pectum). J. Comp. Physiol. 151:119-126. KAUFMANN, J. S., and A. F. BENNETT. 1989. The effect of temperature and thermal acclimation on locomotor performance in Xantusia vigilis, the desert night lizard. Physiol. Zool. 62:1047-1058.

KRAM, R., and C. R. TAYLOR. 1989. Why does metabolic rate increase with running speed? Proc. Int. Union Physiol. Sci. 17:430-431. LICHT, P., W. R. DAWSON, V. H. SHOEMAKER, and A. R. MAIN. 1966. Observations on the thermal relations of western Australian lizards. Copeia 1966:97-110. LIGHTON, J. R. B., and D. H. FEENER, JR. 1989. A comparison of energetics and ven- tilation of desert ants during voluntary and forced locomotion. Nature 342:174- 175. PALADINO, F. V., and J. R. KING. 1979. Energetic cost of terrestrial locomotion: biped and quadruped runners compared. Can. Rev. Biol. 38:321-323. PIANKA, E. R. 1986. Ecology and natural history of desert lizards. Princeton University Press, Princeton, N.J. PORTER, W. P., and D. M. GATES. 1969. Thermal equilibria of animals with environment. Ecol. Monogr. 39:227-244. PURVIs, A. 1991. Comparative analysis by independent contrasts, version 1.2: user's guide. Oxford University, Oxford. REGAL, P. J. 1967. Voluntary hypothermia in reptiles. Science 155:1551-1553. S1974. Circadian and low frequency rhythms in the temperature preference of a lizard. Pages 709-711 in L. E. SCHEVING, F. HALBERG, and J. E. PAULY, eds. Chronobiology. Igaku Shoin, Tokyo. SAINT GIRONS, H. 1980. Thermoregulation in reptiles with special reference to th< tuatara and its ecophysiology. Tuatara 24:59-80. SECOR, S. M., B. C. JAYNE, and A. F. BENNETT. 1992. Locomotor performance and energetic cost of sidewinding by the snake Crotalus cerastes. J. Exp. Biol. 163:1- 14. SEMENOV, D. V., and L. J. BORKIN. 1992. On the ecology of Przewalsky's gecko (Ter- atoscincusprzewalskii) in the Transaltai Gobi, Mongolia. Asiatic Herpetological Res. 4:99-112. SPELLERBERG, I. F. 1972. Temperature tolerances of southeast Australian reptiles ex- amined in relation to reptile thermoregulatory behaviour and distribution. Oec- ologia 9:23-46. STEARNS, S. C. 1982. On fitness. Pages 3-17 in D. MOSSAKOWSKI and G. ROTH, eds. Environmental adaptation and evolution. Fischer, Stuttgart. STEBBINS, R. C., and R. E. BARWICK. 1968. Radiotelemetric study of thermoregulation in a lace monitor. Copeia 1968:541-547. STEVENSON, R. D., C. R. PETERSON, and J. S. TsuJI. 1985. The thermal dependence of locomotion, tongue flicking, digestion, and oxygen consumption in the wandering garter snake. Physiol. Zool. 58:46-57.

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms 262 K. Autumn, R. B. Weinstein, and R. J. Full

TAYLOR, C. R., K. SCHMIDT-NIELSEN, and J. L. RAAB. 1970. Scaling of energetic cost to body size in mammals. Am. J. Physiol. 219:1104-1107. THOMAS, B. W. 1981. Hoplodactylus rakiurae n. sp. (Reptilia: Gekkonidae) from Stewart Island, New Zealand, and comments on the taxonomic status of Hetero- pholis nebulosus McCann. N.Z. J. Zool. 8:33-47. TROYER, K. 1987. Small differences in daytime body temperature affect digestion of natural food in a herbivorous lizard (Iguana iguana). Comp. Biochem. Physiol. 87A:623-626. VALAKOS, E. D. 1989. Thermal ecology of Cyrtodactylus kotschyi (Steindacher, 1870) (Sauria-Gekkonidae) in the insular ecosystems of the aegean. Herpetological J. 1:396-399. WALLS, G. L. 1942. The vertebrate eye and its adaptive radiation. Cranbrook, Bloomfield Hills, Mich. WERNER, Y. L. 1983. Temperature effects on cochlear function in reptiles: a personal review incorporating new data. Pages 149-174 in R. R. FAY and G. GOUREVITCH, eds. Hearing and other senses: presentations in honor of E. G. Wever. Amphora, Groton, Conn. WITHERS, P. C. 1977. Measurement of V02, Vco2 and evaporative water loss with a flow-through mask. J. Appl. Physiol. 42:120-123.

This content downloaded from 128.32.10.164 on Mon, 12 Jun 2017 13:18:09 UTC All use subject to http://about.jstor.org/terms