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

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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 liz- ards. 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 per- formance 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, ter- restrial 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 liz- ards, 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. przewal- skii showed increased but thermally submaximal locomotor performance capac- ity 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 Physiological Zoology 67(1):238-262. 1994. a 1994 by The University of Chicago. All rights reserved. 0031-935X/94/6701-9256$02.00 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 ac- tivity (Cowles and Bogert 1944; Brattstrom 1965; Bustard 1967; Porter and Gates 1969; Pianka 1986; Huey et al. 1989). Performance decreases sub- stantially 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 de- rived features that permit activity at low temperatures. Optimality theory predicts coadaptation of (physiological) thermal optima and activity tem- peratures (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 sub- maximal 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 noc- turnal 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 noc- turnal 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 physio- logical 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 per- formance capacity by measuring sustained locomotion (endurance) at tem- peratures 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 loco- motor 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 lo- comotion (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 in- dependent 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.
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