Seasonal Thermoregulation of the Introduced Wall Lizard,

Podaris muralis

Mara Leyendecker
Mentor: J. Pedro do Amaral
Science and Health Department, Clermont College
McMicken College of Arts and Sciences
University of Cincinnati
WISE
July 31, 2014

TABLE OF CONTENTS

Pages
Abstract

Introduction

35

Methods

56

Results

67

Discussion

78

Acknowledgements-WISE Impact

Literature Cited

1012

List of Figures

1324

ABSTRACT
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Thermoregulation is vital for the survival of ectotherms. Without proper thermoregulation, an

ectotherms enzymes may likely overheat and denature, or freeze and stop functioning.
Throughout this experiment, I tested how thermoregulatory effectiveness of Podarcis muralis
changed as the seasons progressed from spring to summer. Each lizard was individually noosed
in Prospect Hill near Cincinnati, Ohio. It was hypothesized that the lizards need to
thermoregulate more carefully increases as the seasons progress, because the environmental
temperatures become less favorable. The results showed that the thermoregulatory effectiveness
varied as the seasons progressed. From May to June the mean thermoregulatory effectiveness
decreased, when from June to July the mean thermoregulatory effectiveness increased.
Furthermore, it was shown that when the thermal quality of the environment was less favorable
the lizards did thermoregulate more effectively. Therefore, the hypothesis was supported. It was
concluded that as the weather worsened, the lizards became more accurate and effective at
thermoregulating. For the future, it would be interesting to measure the lizards temperatures
using both an infrared thermometer and noosing them in the field. I would also like to study the
lizards in their native land and compare those results to the ones studied in Cincinnati.

INTRODUCTION
Temperature is considered one of the most pervasive physiological parameters (Hutchinson and
Dupr 1992, Ragland and Kingsolver 2008). It affects the kinetic energy of the reactants
involved in enzymatic activities, thus it affects nearly every physiological process that occurs
within an organism (Hutchinson and Dupr, 1992). Furthermore, an organisms internal body
temperature (Tb) has a direct effect on internal body processes, including locomotion, digestion,
and growth (Waldschmidt and Tracy 1983, Stevenson et al. 1985, Huey and Bennett 1987, Huey
et al. 1989, Huey and Kingsolver 1989, Dorcas et al. 1997, Brett 1971, Grant 1990, Christian and
Weavers 1994, Avery 1984, Bronikowski et al. 2001). Consequently, proper temperature
maintenance is vital for organisms to carry out metabolic processes. Understanding how an
organism responds to different environmental temperatures is necessary in understanding the
biological processes that occur within the organism. Furthermore, thermoregulation is
particularly important for ectotherms organisms that are unable to regulate a stable internal
body temperature without external heat sources.
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Ectotherms rely on external heat sources to maintain a stable internal body temperature
(International Union of Physiological Sciences 2003). Some ectotherms are active under a
narrow range of temperatures, whereas others are active over a broader range (Blouin-Demers
and Weatherhead, 2001). Various heat transfer processes occur between the animal and its
environment, including radiation, convection, convection, and evaporation (Stevenson, 1985).
Ectotherms also use different behavioral mechanisms that include shuttling between hot and cold
areas, such as from basking in the sun to hiding in the shade (Stevenson, 1985). Moreover,
ectotherms use different body postures, like facing towards or away from the sun and moving on
top of rocks or under them (Sartorius et al. 2002). Thermoregulation is especially important in
the winter when many ectotherms are exposed to environmental temperatures lower than the
freezing point of their body fluids (Claussen et al. 1990). This process of thermoregulation
allows ectotherms to regulate their internal body temperature and thus be able to carry out
important physiological processes even in harsh environments.
Podarcis muralis, a wall lizard species native to Europe, is an example of an organism
that must thermoregulate to survive. The species was introduced in Cincinnati between the years
19511952 by a little boy named George Rau (Deichsel and Gist, 2001). He brought about 10 of
these lizards from their native land in northern Italy (Lake Garda near Milan) to Cincinnati, and
from those ten lizards there are now thousands in the Cincinnati area (Deichsel and Gist, 2001).
Potentially, these lizards have thrived in Cincinnati due to putative similarities between it and
their native habitat. These similarities include climate and structures, such as the buildings and
cracked walls of the city. Podarcis muralis are ideal for studying thermoregulation as they are so
abundant and must thermoregulate to survive.
Thermoregulatory effectiveness (E') describes numerically how body temperature is
maintained close to a preferred range against an environment that might not be favorable. To
measure E', three temperatures must be measured: body temperature of lizards (Tb), their
preferred body temperature (Tsel), and the operative temperatures (available temperatures in the
environment Te) (Hertz et al.1993). Once these three temperatures are measured, three indices
can be calculated: the accuracy of thermoregulation (db); the thermal quality of the habitat (de);
and the effectiveness of thermoregulation (E') (Hertz et al.1993, Blouin-Demers and
Weatherhead 2001) .
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The purpose of this experiment was to measure how thermoregulatory effectiveness

changes as the seasons progress from spring to summer. It was hypothesized that the lizards
need to thermoregulate more carefully increases as the seasons progress because the
environmental temperatures become less favorable. To compensate for a less favorable
environment, the organisms must thermoregulate more effectively to survive, thus an expected
increase in the E' index as the seasons progressed.

METHODS
The lizards, Podarcis muralis, used in this experiment were captured near Prospect Hill in
Cincinnati, Ohio, USA between the months of MayJuly 2014. Three days out of each of the
three months were field days. During each field day, lizards were captured by noosing between
the times of 08001800. Immediately after their capture, their internal body temperature (Tb) was
measured using a Schultheis quick-reading cloacal thermometer (Miller & Weber, New York).
Each lizard was also weighed and sexed. Their time of capture, the air temperature of the site of
capture measured at waist-height in the shade, and their exact location, using GPS, were also
recorded. Additionally, during each field day, sixteen programmable thermometers were placed
in an area representative of the environment where the lizards were noosed to measure the
operative temperatures (Te). To properly measure the lizards preferred temperature (Tsel), the
lizards were placed singly in an environment where there would be no thermoregulatory costs
(Blouin-Demers and Weatherhead, 2001). Tsel was thus measured from lizards tested in a lab
circular thermal gradient (DeWitt, 1967). Before placing the lizards in the gradient, a
thermocouple probe was placed in their cloacae. Once in the gradient, each lizard was then tested
for three hours. Data obtained during the first hour of the trial were not used to calculate Tsel. I
followed Christian and Weavers (1996) in using the interquartile range of all temperatures
selected in the thermal gradient to represent Tsel. Ten lizards were tested in the thermal gradient
throughout the duration of the study.
After measuring Tb, Tsel, and Te, three indices were calculated: thermoregulatory accuracy
(db), environment thermal quality (de), and thermoregulatory effectiveness (E') (Hertz 1993,
Blouin-Demers and Weatherhead 2001). In the case of db, values closer to 0 will signify higher
5

thermoregulatory accuracy. This is because as the animal's internal body temperature in the
environment matches that in the lab, a db value of 0 will be calculated showing that the animal is
very accurate at thermoregulating. In the case of de, values that are closer to 0 will signify
environments that are more favorable for these lizards. The last index that was calculated was E'.
E' was calculated by subtracting db from de. Large E' value will mean that the effectiveness of
thermoregulation is higher.
Thermoregulatory indices:
The accuracy of thermoregulation (db); better accuracy will have values that are closer to zero
db = Tsel - Tb
The thermal quality of the habitat (de); better environments will have values that are closer to
zero
de= Tsel - Te
The effectiveness of thermoregulation (E'); higher effectiveness will have higher values
E' = de - db

RESULTS
By and large, Podarcis muralis kept their Tb within Tsel (Figs. 1, 2, 3). Moreover, from May to
June db grew to a higher value than 0 meaning that the lizards became slightly less accurate at
thermoregulating (Figs. 4,5,6). The mean value of the thermoregulatory accuracy changed from
0 to 0.02, a difference of 0.02. The increase in the mean indicates that the lizards did become
slightly less accurate at thermoregulating from May to June. From June to July however, average
db values remained constant. The mean did not change. This indicates that the lizards' accuracy
remained constant during this period. On average, from May to June, de increased as the seasons
progressed (Figs. 7,8,9). The index de became progressively closer to 0 as the thermal quality of
the environment increased or became more favorable as the season progressed from May to June.
The mean values changed from 4.30 to 1.23, a difference of 3.07. However, from June to July the
6

mean values of the thermal quality of the environment decreased. The means changed from 1.23
to 4.73, a difference of 3.50. The decrease in means indicates that the environment was more
favorable for the lizards between June and July. E' decreased on average from May to June (Figs.
10,11,12). The mean value for May was 2.17 while that for June was 0.68, thus a decrease in the
thermoregulatory effectiveness during this time period. However, between June and July the
mean values increased from 0.68 to 3.18. This indicates that thermoregulatory effectiveness
increased during this time period.

DISCUSSION
The hypothesis was supported. The lizards thermoregulated more effectively and accurately
when the environment was less favorable. The mean Tsel values stayed within the mean Tb values
likely as a result of adjustments in lizard behavioral thermoregulation. This is because the lizards
were able to shuttle between warmer and cooler areas, which allowed them to thermoregulate
even in extreme conditions. Moreover, the varying weather conditions on the days of the
samplings played a role in the results. The third sample was taken when the area being studied
was much cooler and cloudier than the first two samplings. As the weather oscillated between
both warm and cool temperatures, the lizards thermoregulatory accuracy stayed fairly constant
and maximal. Because db stayed essentially unchanged at 0, E' values were directly affected by
the de values. Therefore, increases to E' were mostly caused by increases in de.
This particular summer was fairly atypical. The study period in June were the warmest
out of the three study periods. During a typical summer the environmental temperatures are
expected to increase from May to July. The increase in temperature from the first to the second
samplings resulted in a low thermoregulatory effectiveness (E'). The decrease in temperature
from the second to the third sampling resulted in a much higher E'. The environment did become
less favorable for the lizards from June to July as shown by a higher thermal quality of the
environment (de). Because the lizards thermoregulatory accuracy (db) remained relatively
constant and maximal throughout the study periods, E' values were directly dependent on de
values. Therefore, as de values increased, E' values consequently increased.

For further research I would like to use an infrared thermometer in addition to noosing
the lizards in the field. This would provide a means of comparison between the two methods to
see which one is more accurate. Using an infrared thermometer would also eliminate any lost
time between when the lizard was captured and when its temperature was measured. I would also
like to compare the effects of color on thermoregulation. I would want to test how a lizard with a
yellow belly thermoregulates in comparison to one with an orange body. Finally, it would be
interesting to test this same species of lizard in their native land and compare those results to
those from those living in Cincinnati.

ACKNOWLEDGEMENTS and WISE IMPACT

I would like to thank the following people and institutions because without their help none of this
research would have been possible. Thank you to the University of Cincinnati and the McMicken
College of Arts and Sciences, the current institution where I am studying. Thanks to the
University of Cincinnati Clermont College Department of Science and Health, the institution in
which this research was conducted. Also, a special thanks to Dr. Ghia, the director of the WISE
program, and the WISE program itself for funding. I would also like to thank my mentor, Dr. J.
Pedro do Amaral for all of his patience and time in helping me throughout the research process.
Thank you to the IACUC who approved the animal use protocol so that this research could be
conducted. Finally I would like to thank Burl Holbrook Trestleview Farm for the lab tabletop that
was used throughout this study. WISE has allowed me to be exposed to the application side of
science rather than just the classroom setting. It has allowed me to network with many other
women and helped me to become a more confident public speaker. WISE has also given me first
time hand on research experience that is very valuable for my future career. In the future I hope
to obtain a BS in Biology and then go onto Medical School to become a dermatopathologist. I
hope to be able to do research in the future on certain skin conditions and diseases where not
much is known and this project has helped me to solidify my future career choice and realize that
research is something that I hope to continue to pursue in the future.
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(Elaphe obsoleta) in a Thermally Challenging Environment. Ecology 82:3025-3043.
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Bronikowski, A. M., A. F. Bennett, and R. E. Lenski. 2001. Evolutionary adaptation to
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Claussen, D. L., M. D. Townsley, and R. G. Bausch. 1990. Supercooling and freeze-tolerance in
the European wall lizards, Podarcis muralis, with a revisional history of the discovery of
freeze-tolerance in vertebrates. Journal of Comparative Physiology B 160: 137-143.
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Christian, K. A. and B. W. Weavers. 1996. Thermoregulation of monitor lizards in Australia: An
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Deichsel, G. and D. H. Gist. 2001. On the origin of the common wall lizards Podarcis muralis
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(Charina bottae): physiology, behavior, and environmental constraints. Physiological
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Grant, B. 1990. Trade-offs in activity time and physiological performance for thermoregulating
desert lizards, Sceloporus merriami. Ecology 71:2323 2333.
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Huey, R. B. and A. F. Bennett. 1987. Phylogenetic studies of coadaptation: preferred
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performance. Trends in Ecology and Evolution 4:131135.
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
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Hutchison, V. H. and R. K. Dupr, 1992. Thermoregulation. Pages 206249 in M. E. Feder and
W. Burgren, editors. Environmental Physiology of the Amphibia. University of Chicago
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for Thermal Physiology. 2d ed. Pflug Arch Eur J Physiol 28:75-106.
Ragland, G. J. and J. G. Kingsolver. 2008. The effect of fluctuating temperatures on ectotherm
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LIST OF FIGURES

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Figure 1: Results for spring 2014 (May) for all three temperatures. The blue dots show mean Tb values. The black
whisks represent the 95% confidence interval of the means. The grey bar shows the range of Tsel values. The red dots
show the Te values and the dashed lines show the Te max and Te min values. The black bars represent the scotophase
of the photoperiod while the white between them represents the photophase of the photo period.

12

Figure 2: Results for summer 01 2014 (June) for all three temperatures. The blue dots show mean Tb values. The
black whisks represent the 95% confidence interval of the means. The grey bar shows the range of Tsel values. The
red dots show the Te values and the dashed lines show the Te max and Te min values. The black bars represent the
scotophase of the photoperiod while the white between them represents the photophase of the photoperiod.

13

Figure 3: Results for summer 02 2014 (July) for all three temperatures. The blue dots show mean Tb values. The
black whisks represent the 95% confidence interval of the means. The grey bar shows the range of Tsel values. The
red dots show the Te values and the dashed lines show the Te max and Te min values. The black bars represent the
scotophase of the photoperiod while the white between them represents the photophase of the photoperiod.

14

Figure 4: Spring 2014 (May) thermoregulatory accuracy (db) values. The black bars represent
the scotophase of the photoperiod.

15

Figure 5: Summer 01 2014 (June) thermoregulatory accuracy (db) values. The black bars
represent the scotophase of the photoperiod.

16

Figure 6: Summer 02 2014 (July) thermoregulatory accuracy (db) values. The black bars
represent the scotophase of the photoperiod.

17

Figure 7: Spring 2014 (May) thermal quality of the environment values (de). Black bars
represent the scotophase of the photoperiod.

18

Figure 8: Summer 01 2014 (June) thermal quality of the environment values (de). Black bars
represent the scotophase of the photoperiod.

19

Figure 9: Summer 02 2014 (July) thermal quality of the environment values (de). Black bars
represent the scotophase of the photoperiod.
20

Figure 10: Spring 2014 (May) thermoregulatory effectiveness values (E'). Black bars represent
the scotophase of the photoperiod.
21

Figure 11: Summer 01 2014 (June) thermoregulatory effectiveness values (E'). Black bars
represent the scotophase of the photoperiod.

22

Figure 12: Summer 02 2014 (July) thermoregulatory effectiveness values (E'). Black bars
represent the scotophase of the photoperiod.

23