TheEffectofAdaptiveEvolutionandEcologyonThermoregulatory BehaviorinHolbrookiamaculata(LesserEarlessLizard)

IsaiahHoyer 08134886 hoye6378@vandals.uidaho.edu 2082158841

Adaptive Evolutionary Ecology

Isaiah Hoyer

Abstract
White Sands, New Mexico, is a site of recent evolutionary divergence in three lizard species. I will examine how previous evolutionary adaptation of Holbrookia maculata (Lesser Earless Lizard) in White Sands has affected thermoregulatory behavior. I hypothesize that there is a difference in preferred relative body temperature in Holbrookia maculata in White Sands from their dark soils conspecifics. I will work with two undergraduates and three doctoral students in White Sands, New Mexico, for approximately one-month. I will capture lizards by hand and measure traits such as body size, body temperature, and operative temperature (surface and air). The divergence of the two lizards has shown cascading affects on phenotype (Des Roches et al. 2011). The thermoregulatory behavior of ectotherms is greatly affected by their environment. The changes in coloration among H. maculata in respect to their surrounding environment must have influenced change in their thermoregulatory behavior. I predict that the white morph H. maculata has evolved an overall lower body temperature due to their degraded ability of solar radiated heat absorption in respect to the dark morph H. maculata. I predict that the white morph H. maculata differs in habitat use and are able to travel further from cover because they are less likely to reach their thermal maximum than their dark soil conspecifics.

Introduction
White Sands National Monument, New Mexico (Figure 1), is a site of recent evolutionary divergence in three lizard species. The unique geology of the White Sands gives scientists a remarkable chance to study evolutionary ecology. Over thousands of years, the inland of Lake Otero receded to a temporal shallow basin that is now called Lake Lucero, reveling approximately 275 square miles of white gypsum. The dunes are a dynamic and growing habitat that is largely shaped by the consistent eastwardly blowing winds (Kocurek 2007). The gypsum dune field is the largest of its kind on Earth! In the last 6000 years, several of the plants and animals in the neighboring dark soiled habitat have had the opportunity to colonize White Sands and adapt to its dynamic environment. There is potential for adaptation by organisms inhabiting any newly formed, recently devastated or isolated habitats. The exploitation of White Sands by the lizard species is shaped by evolutionary driving forces. In comparison to the surrounding dark soils, White sands has

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reduced species richness and species abundance for potential competitors and predators (Des Roches et al. 2010). The available habitat of the newly formed gypsum dunes resulted in feats of adaptation in both plants and animals. The plants that persist in White Sands must be hardy enough to withstand being buried and survive in the prevailing winds that shape the dynamic habitat. Much of the wildlife in the White Sands environment has evolved cryptic coloration to match their surroundings (Harmon and Rosenblum 2010). It is likely that preferential predation on mismatched lizards has selected for this cryptic coloration (Rosenblum 2005). The selective forces acting upon cryptic coloration may affect the thermal regulatory behavior of ectotherms, organisms that allow their body temperature to fluctuate relative to their environment, e.g. alligators, frogs and lizards (Tucker et al. 1963). Thermoregulation is the ability of an organism to maintain its body temperature within certain limits. Background color matching and color change affect rates of bodily warming in lizards (Norris 1967). A lizard will regulate its body temperature behaviorally (Stevenson 1979). Many lizards can increase or decrease heat absorption by changing their color (Cole 1943); however, color also has a genetic basis. Most lizards, including individuals that persist in White Sands, are unable to change their color entirely to match their neighboring habitat (i.e., the white lizards cannot be as darkly colored as their dark conspecifics and the dark lizards cannot be as white as their white conspecific; Rosenblum 2005). Norris observed that in early mornings some lizards were darker in color, presumptively facilitating warming, than throughout the day when they were more faithfully matching the substrate. Three species of lizards have a white and dark morphs associated to the color of their habitat; Holbrookia maculata, Aspidoscelis inornata, and Sceloporus undulata (Harmon and Rosenblum 2010). The lesser earless lizard, H. maculata, is a species of interest for the Figure 1. White Sands National Monument, New Mexico

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thermoregulatory study because it is more conspicuous than the other lizards, and it shows the most dramatic change in color (Harmon and Rosenblum 2010)(See Figure 2). There is little to no gene flow between the populations in White Sands and dark soils habitats (Rosenblum et al. 2007). The isolation of H. maculata gives the greatest expected difference in thermoregulatory behavior. The other lizard species show more interaction among color morphs due to overlapping ranges. Also, H. maculata evolved its skin color differently than A. inornata and S. undulatus. The mechanisms for the blanched phenotype in H. maculata are unknown although it is speculated that a mutation in the Melancortin-1 receptor gene (Mc1r) is responsible as documented in A. inornata and S. undulates (Rosenblum 2005). There are many potential differences among the color morphs of H. maculata that I might find. Due to the reduced efficiency of solar radiated heat absorbance, the white morph may have evolved a different behavior or phenotypic than the dark morph to maximize its heat gain and compensate for its color loss. Lizards receive their energy in the form of direct sunlight, reflected sunlight, erratically scattered skylight, thermal radiation from the atmosphere, conduction from the ground, and surrounding vegetation. The amount of energy absorbed depends on the lizards surface area exposed, the angles of the surfaces, and the absorptivity of the surface to the quality of incident radiation (Bartlette and Gates 1966). Interestingly the gypsum that makes up White Sands has less conductive properties (retains less heat) than the darker surroundings soils (Scheidt et al. 2010). Therefore, it is possible that the White Sand morphs could have evolved an overall lower body temperature. Another interesting difference between the color morphs could be distance from cover. It is possible that the white color of a lizard will allow it to spend more time in the open due to its reflectivity and inferior sun absorption capability. A white object is less efficient at sun absorption than a darker object. As a result from the evolved color change, the white morph H. maculata is potentially able to spend more time foraging and exhibit increased activity further from cover. It takes the white morph H. maculata longer to reach their thermal maximum than Figure 2. H. maculata (white morph left), and H. maculata (dark morph right).

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dark morph H. maculata. Thermoregulation has been correlated to fitness through costs and benefits associated to environmental factors (Slatkin 1976). Lizards become thermoconformers when costs of thermoregulation outweigh the potential benefits. There is an opportunity cost to a lizard spending time thermoregulating. A lizard that spends less time thermoregulating is able to engage in other important activities such as foraging or mate searching (Nadeau 2005). Examples of lizard behaviors that affect body temperature are perch choice, time in shade, and the time in sun. Morphological examples in lizards that affect body temperature are dorsal skin brightness, proximity of blood vessels to the surface of the skin, body size and body surface area. With my research, I will examine how previous evolutionary adaptation of Holbrookia maculata to White Sands has affected thermoregulatory behavior. I hypothesize that there is a difference in preferred relative body temperature in Holbrookia maculata in White Sands from their dark soils conspecifics. Specifically, I predict: a) the overall body temperature is lower in White Sand H. maculata due to divergent evolution, b) the white morph H. maculata are able to travel further from cover because they are less likely to reach their thermal maximum than their dark soil conspecifics. I will determine the relationships among morphology, habitat use, and thermal behavior to elucidate differences in evolutionary ecology between White Sands and dark soils lizards. There are three possible outcomes of my study on thermal preference. My hypothesis is number three, predicting different preferred body temperature. 1. H0 Lizards use habitat randomly. --- Use = Availability. No matter the temperature, stimuli, or other factors the lizards have no preference of temperature. 2. H1 Lizards use habitat non-randomly. --- Shared preference. Lizards prefer the same temperature. Lizards prefer different temperatures. 3. H2 Non-random habitat use. --- Unique thermal preference. For one month during the summer 2012, I will travel to White Sands, New Mexico, to study how past adaptation and current ecological surroundings affect thermoregulatory behavior of the two color morphs of Holbrookia maculata. Furthermore, I will compare habitat use (perch selection, temperature selection) by the two color morphs in their separate habitats to determine divergence in thermoregulatory behavior. The research will contribute to a larger pool of

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evolutionary ecology work of the White Sand lizards. Dr. Erica Bree Rosenblums lab has performed research on colonization, genetics of adaptation, and ecologically relevant morphological traits, sexual communication and functional morphology. Ongoing research includes several experiments and studies exploring ongoing natural selection on color in White Sands. My own research will help determine whether this selection on color change also influences thermoregulatory behavior.

Research Objectives
For my project, I will gather evidence about changes in thermoregulatory behavior of H. maculata. Specifically, I will determine whether previous adaptation in color to different ecological surroundings has influenced the thermoregulatory behavior of the two divergent populations of Holbrookia maculata occupying White Sands and the surrounding dark soils scrubland of the Chihuahuan Desert. I aim answer questions such as: What influential factors affect thermoregulation in H. maculata? Does the mean body temperature vary between the light and dark color morphs of H. maculata? Is there differences in use of thermal microhabitat in H. maculata color morphs? To do this, I will capture individuals of both dark and light color morphs of different age and sex classes and collect data on morphological measurements, brightness measurements, distance from cover, and approximate vegetation density.

Methods and Analysis

I will spend approximately one-month in White Sands, New Mexico in collaboration with three doctoral and two undergraduate students. The necessary Institutional Animal Care and Use Committee (IACUC) protocol forms have been submitted and approved for University of Idaho and University of California Berkeley (Protocol # 2010-48). I will capture lizards by hand and by noose. Upon capture I will randomly generate a coordinate of 0.5 meters to 10 meters radius where I will place two null lizards (Figure 3). Null lizards are often copper models of lizards (non-regulating) that will accurately measure the available temperatures (Bakken 1992). I will also place two null lizards in the approximate origin of capture to measure the available temperature (Figure 3). The null lizard models will be painted to mimic lizard dorsal surface color. I will also translocate substrate mismatched lizard models to simulate the available temperature for H. maculata conspecifics. Measuring the a black model on white substrate will

Adaptive Evolutionary Ecology be equivocal to available temperature for a dark morph lizards and visa versa for a white model on dark substrate. I will measure traits that will allow me to document variation in the wild: Body size or Snout-vent- length (SVL), weight, body or cloacal temperature, environmental temperature (surface and air). I will also measure distance from cover, percent vegetation, and perch choice. I will measure the nearest distance from cover to the nearest ten centimeters. Percent vegetation will be calculated using a visual index of vegetation in a 3 meter radius around the lizard. The majority of vegetation in the

Isaiah Hoyer

Figure 3. Sampling Method.

White Sands and dark soil habitats are approximately reach no greater height than 1.5 meters. I will only count vegetation that is serves as cover to lizards such as shrubs and bushes, not grasses. Percent vegetation will be subject to 10 categories (1: 0-10 % vegetation, 11-20 %, 2130 %). Perch choice will be identified as ground (not associated with vegetation), tree/shrub. Perch height and diameter will be estimated by eye to nearest centimeter. Percent vegetation and perch choice is comparable and repeatable from Des Roches 2010 ecological release in the White Sands study. The thermal and morphological data will be analyzed using R statistical program (R Development Core Team 2012). To infer differences in thermal preference I will be compare the lizard body temperature (use) versus the null model temperature (available). Among the color morphs, if there is a large difference between used and available temperature then there is distinct preference for temperature. Figuring differences in field temperatures of the lizards is an important step to identifying actual thermal preference. By making an effort to identify differences in thermal use vs. available of the two color morphs, I will support the need for an experiment in a controlled environment, where the substrate structure, temperature, and color can be manipulated on a spectrum. I will quantify multiple characters simultaneously including body temperature and distance to cover that directly affect thermoregulation. I will use a conditional logistic regression

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to compare used and available temperature. I will also be able to see how body temperature is affected by color, size and an interaction between size and color. E.g. linear regression: body temperature ~ null model origin temperature. E.g. linear regression: body temperature = color ~ size ~ size*color.

I might also to use analysis of variance (ANOVA), analysis of covariance (ANCOVA), or multivariate analysis of variance MANOVA (R Development Core Team 2012) with an alpha value of P=0.05. Des Roches 2010 commonly used 2-way ANOVA to infer significance in body size ~ sex. The H. maculata home range size has not been well evaluated in White Sands, nevertheless this species generally has a small home range (Hulse 1985). H. maculata is a conspicuous species and individuals will usually bask on the same perch throughout a field season (Des Roches, personal observation). Hager 2001 microhabitat study found that there are about 8.5 H. maculata per hectare within the White Sands interdunes (between dune areas that contain most of the vegetation and animal life). Based on these observations, I plan to conduct sampling within in several small (1 km2) interdunes. My sample size goal is to collect at least 40 lizards, 20 white and 20 dark. However, I will continue to capture lizards past my goal throughout the field season. I will mark each individual with a sharpie streak on its tail, which will avoid any duplicate data. The sharpie will not harm the lizard and will wash off in a few days. Upon capture I will first measure the lizards body temperature with a Carolina cloacal thermometer and then subsequently measure the air, substrate or perch temperature with a general purpose thermometer. Difficulties and Possible Resolutions There are many difficulties that I might encounter during my research in the field. The entirety of my study depends upon accurate measurements on relative body temperature of H. maculata. H. maculata is more conspicuous than the other lizards of the White Sands, making it a good candidate for study. However, we still have to be able to catch the lizards in a safe and timely manner. The lizards must be caught with in a minimal time frame to ensure accurate results. A stressed or winded lizard may have a different body temperature than a resting lizard. Therefore I will not insists in chasing a lizard for more than 10 meters (Hager 200). I approximate that from the time the lizard is disturbed by my presence, I have about ten seconds

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to capture and measure their body temperature (Hager 2000). The nooses have been quite effective in the past as have the durable Carolina cloacal thermometers. Also, spotting the lizards may prove to be a difficult task in its self due to the brightness and reflectivity of the gypsum in the sun. Therefore, to counteract the bright gypsum dunes, I will wear polarized sunglasses and carry binoculars to spot lizards in the distance.

Relevance of Research to Profession and Society

Investigator As an undergraduate, I will learn firsthand what is involved in ecological field research. I will gain experience in experimental design, collecting and analyzing data, as well as working cooperatively towards a common goal with other scientists. During my time in White Sands, I will be involved with an outreach project with local students. In past field seasons, the lab team designated a full day field course open to all local residents and students in the area. I will gain qualification in explaining my research and involvement in White Sands to many different age groups and backgrounds. Working with two other undergraduates and two graduate doctorial students will prepare me for graduate school, pursuing a career as a field technician and/or researching positions. The interactions with the community will give me experience in understanding the publics desires and curiosities. The research I will conduct this summer and the analysis afterwards will fulfill my senior thesis requirement for my major in Ecology and Conservation Biology. The knowledge I have gained over my undergraduate career will be greatly exercised during this project. Ecology and Biology White Sands, New Mexico gives visitors and students a great opportunity to experience the recent evolutionary ecology of its inhabitants. As a federally protected national monument it is protected from human disturbance. The interactions among the wildlife are greatly apparent. As in many desert environments there is low relative diversity in plants and animals when compared the tropic regions of the world. The ecotone, transition areas from White Sands to dark soils, is a very busy place for natural selection to act on the lizards. There is high selection of mismatch prey from avian predators (Rosenblum 2005).

Adaptive Evolutionary Ecology

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Studying the thermal ecology of the H. maculata in White Sands will add knowledge of what traits have been affected by their evolution. The unique habitat of White Sands can clearly show what major forces act upon adaptive evolution. The White Sand system is rare window in time of a stage in speciation. Understanding how selection leads to evolution in new environments is key to understanding biological diversity. Conservation implications can be addressed from better understanding of how traits are affected by colonization. Studying the influences that the environment poses on a species provides more accurate predictions for the future health of colonization populations. Understanding the constraints and benefits for species divergence will support conservation efforts of endangered/threatened species of similar habitats. White Sands is one of the most recent sights to see vertebrate adaptive evolution in North America. White Sands gives Biologists a rare opportunity to study real time evolution on traits of known functional significance in the field. University of Idaho Dr. Rosenblum and Dr. Harmon have had many publications and study opportunities that have risen from the evolutionary work in the White Sands. Many papers have been published since, as well as funding. The outreach to the worlds biggest gypsum dune holds fast to University of Idahos spirit in leadership and discovery. Research in White Sands, New Mexico, adds to the diversity and elasticity of this great University. Supporting my research sheds light on the fact that Idaho has interest outside the Northwest.

Implications for Management

Studying the thermal ecology of the Holbrookia maculata in White Sands will add knowledge about traits that have been affected by their divergence. Conservation implications can be addressed from better understanding of how traits are affected by colonization. Studying the influences that the environment poses on a species provides more accurate predictions for the future health of colonizing populations. Understanding the constraints and benefits for species divergence will support conservation efforts of endangered and threatened species under future scenarios of climate and related habitat change. Understanding how varying temperatures regimes have affected the thermoregulatory behavior of H. maculata will translate to the implications of climate change. Habitats are changing due to shifts in climate, understanding how ectotherms adapt relative to their 10

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environment will provide managers with foresight on how to better protect similar species. My study facilitates better understanding and management of other species by identifying the mechanisms of adaptation that correlate to changing thermal environments. If the lizards of the White Sands become endangered, the studied adaptive traits will become invaluable tools when zoning habitat. Certain habitats can be classified with more ecological importance such as the ecotone (Des Roches et al. 2010). If the lizards of the White Sands become a significant interest, my behavior studies will help future investigators form predictions and methods for their experiments. My study and past Rosenblum/Harmon studies are steps to figuring the source and sink dynamics of the White Sands. GPS coordinates, orientation of sexes on the landscape, and mark-recapture data contributes to a future source/sink study. The source/sink dynamics will attribute to managers for figuring the health of the populations. Understanding how selection leads to evolution in new environments is key to understanding biological diversity.

Discussion
The White Sands system has much to offer to evolutionary biologists. The unique adjacent environments of White Sands and the dark soils give implications on divergence of the lizards. Holbrookia maculata color morphs are relatively isolated from each other suggesting the most extreme differences in morphology compared to A. inornata and S. undulates which exhibit overlapping home ranges. Climate and phenotype affect associative costs of maintenance and activity i.e. foraging, time basking, growth, reproduction and space utilization (Tracy et al. 1983). The thermal environment has potential to influence the physiology and behavior of lizards (Hager 2000). The evolution of H. maculata has many factors that could affect their thermoregulatory behavior. In all organisms there are many environmental factors that affect body temperature. Poikilotherms generally depend on absorption of solar radiation for their heat gain, and conduction from warmed surroundings. Interestingly the gypsum that makes up White Sands has less conductive properties (retains less heat) than the darker surroundings soils (Scheidt et al. 2010). Therefore, it is possible that the White Sand morphs could have evolved an overall lower body temperature. Another interesting difference between the color morphs could be distance from cover. It is possible that the white color of a lizard will allow it to spend more time in the open due to its reflectivity and inferior sun absorption capability. A white object is less efficient 11

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at sun absorption than a darker object. As a result from the evolved color change, the white morph H. maculata is potentially able to spend more time foraging and increased activity further from cover. It takes the white morph H. maculata longer to reach their thermal maximum than dark morph H. maculata. There are many potential differences in the color morphs of H. maculata that I might find. Due to the reduced efficiency of solar radiated heat absorbance, the white morph may have evolved a larger dorsal surface area to maximize its heat gain and compensate for its color loss. The divergence of H. maculata has led to many changes in traits and adaptations (Des Roches et al. 2010). My research will contribute to past studies on thermoregulation, physiology, and evolution. If thermal differences in the conspecific lizards are significant, than morphological studies on their absorption of heat would prove interesting. Do they absorb solar radiation or conduction heat differently? Are there differences in the proximity of blood vessels to the surface of their skin? Are White Sand H. maculata more efficient at oxygen consumption than the dark morphs i.e. estimation by heart rate during heating (Tucker 1964). A more thorough study on thermal preference could determine if the lizards vary in their thermal maximum and thermal minimum. We could test whether a white lizard prefers a lower temperature on dark soils and visa versa for the dark lizard on white sands. Dr. Rosenblum also suggested that we test whether a lizard is able to distinguish color, Do they know their white? Do the lizards know when they are matching or mismatching their surroundings? Has the White Sand H. maculata evolved a larger in body size to ensure less fluctuation in their body temperature (Stevenson 1985), allowing them to increase their activity further from cover? As in many research projects, the questions and correlations are endless. The recent colonization of the White Sands gives biologist a rare opportunity to study the effects of evolution. The University of Idaho, the field of evolutionary ecology and biology, and me will benefit from the research conducted in White Sands, New Mexico. After all Theodosius Dobzhansky says it best, nothing in biology makes sense except in the light of evolution.

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Adaptive Evolutionary Ecology

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Timeline
May 2012: Meet with other student field assistants; learn on field protocols. May 15 2012: Depart for NM by car. May-June 2012: Collect, mark and measure 40 Holbrookia maculata (20 in the White Sands and 20 in adjacent dark soils habitat). June 20 2012: Depart from NM by plane. August 1 2012: Depart for NM by plane. August 2012: Fulfill responsibilities as field assistant in the dark soils and White Sands. August 20 2012: Depart from NM by car. September 2012-April 2013: Analyze behavior and morphology over one field season. April 2013: Present results of ECB Senior Thesis to the College of Natural Resources

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References
Andrews, Robin M. "Geographic Variation in Field Body Temperature of Sceloporus Lizards." Thermal Biology 23.6 (1998): 329. Print. Bakken, G. S. 1992. Measurement and application of operative and standard operative temperatures in ecology. American Zoologist 32:194216. Barlett, Peter N., and David M. Gates. "The Energy Budget of a Lizard on a Tree Trunk." Ecology 48.2 (1967): 315-22. Print. Cole, LaMont C. "Experiments on Toleration of High Temperature in Lizards with Reference to Adaptive Coloration." Ecology 24.1 (1943): 94-108. Print. Des Roches, S., Robertson, J. M., Harmon, L. J. & Rosenblum, E. B. 2010. Evidence for ecological release in White Sands lizards. For Proc. Roy. Soc. B. Hager, Stephen B. "Variation in Body Temperature and Thermoregulatory Behavior between Two Populations of the Lesser Earless Lizard, Holbrookia Maculata." Contemporary Herpetology (2000). Print. Hager, S. B. 2001 "Microhabitat Use and Activity Patterns of Holbrookia Maculata and Sceloporus undulatus at White Sands National Monument, New Mexico." Journal of Herpetology 35.2 (2001): 326-30. Print. Hulse, Arthur C. "Home Range Size in Holbrookia Maculata (Iguanidae) from Southeastern Arizona." The Southwestern Naturalist 30.4 (1985): 608-10. Print. Kocurek, G., M. Carr, R. Ewing, K. G. Havholm, Y. C. Nagar, and A. K. Singhvi. "White Sands Dune Field, New Mexico: Age, Dune Dynamics and Recent Accumulations." Sedimentary Geology 197 (2007): 313-31. Print. Nadeau, Gabriel Blouin-Demers And Patrick. "The Cost-Benefit Model of Thermoregulation Does Not Predict Lizard Thermoregulatory Behavior." Ecology 86.3 (2005): 560-66. Print. Norris, K. S. "Color Adaptation in Desert Reptiles and Its Thermal Relationships." Ecology (1967): 162-229. Print. Rosenblum, Erica Bree. "The Role of Phenotypic Plasticity in Color Variation of Tularosa Basin Lizards." Copeia 3 (2005): 586-96. Print. Rosenblum, E. B., Hickerson, M. J. & Moritz, C. 2007 A multilocus perspective on colonization accompanied by selection and gene flow. Evolution 61, 2971-2985. Rosenblum, Erica Bree and Harmon, Luke J. "Same Same but Different: Replicated Ecological Speciation at White Sands." Evolution (2010). Print.

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Rosenblum, E. B. (2006). "Convergent Evolution and Divergent Selection: Lizards at the White Sands Ecotone." The American Naturalist 167(1): 1-15. Slatkin, Raymond B. Huey and Montgomery. "Cost and Benefit of Lizard Thermoregulation." The Quarterly Review of Biology 51.3 (1976): 363-84. Print. Stephen Scheidt, Michael Ramsey, and Nicholas Lancaster. "Determining Soil Moisture and Sediment Availability at White Sands Dune Field, New Mexico, from Apparent Thermal Inertia Data." Journal of Geophysical Research 115.F02019 (2010): 1-23. Print. Stevenson, Raymond B. Huey and R. D. "Integrating Thermal Physiology and Ecology of Ectotherms: A Discussion of Approaches." American Zoologist 19.1 (1979): 357-66. Print. Stevenson, R. D. "Body Size and Limits to the Daily Range of Body Temperature in Terrestrial Ectotherms." The American Naturalist 125.1 (1985): 102-17. Print. Tracy, Warren P. Porter and C. Richard. "Biophysical Analyses of Energetic, Time-Space Utilization, and Distributional Limits." Lizard Ecology. Ed. Raymond B. Huey, Eric R. Pianka, and Thomas W. Shoener. Cambridge and London: Harvard University Press, 1983. 55-83. Print. Tucker, George A. Bartholomew and Vance A. "Control of Changes in Body Temperature, Metabolism, and Circulation by the Agamid Lizard, Amphibolurus Barbatus." Physiological Zoology 36.3 (1963): 199-218. Print. Tucker, George A. Bartholomew and Vance A. "Size, Body Temperature, Thermal Conductance, Oxygen Consumption, and Heart Rate in Australian Varanid Lizards." Physiological Zoology 37.4 (1964): 341-54. Print. Figure 1 <http://maps.google.com/> Figure 2 photo by Simone Des Roches

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