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BODY TEMPERATURES OF SELECTED AMPHIBIAN ANDREPTILE SPECIESAuthor(s): Matthew Raske, D.V.M., Gregory A. Lewbart, M.S., V.M.D., Dipl.A.C.Z.M., Daniel S. Dombrowski, M.S., D.V.M., Peyton Hale, B.S., MariaCorrea, Ph.D., and Larry S. Christian, B.S.Source: Journal of Zoo and Wildlife Medicine, 43(3):517-521. 2012.Published By: American Association of Zoo VeterinariansDOI: http://dx.doi.org/10.1638/2011-0244R.1URL: http://www.bioone.org/doi/full/10.1638/2011-0244R.1
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Journal of Zoo and Wildlife Medicine 43(3): 517–521, 2012
Copyright 2012 by American Association of Zoo Veterinarians
BODY TEMPERATURES OF SELECTED AMPHIBIAN AND
REPTILE SPECIES
Matthew Raske, D.V.M., Gregory A. Lewbart, M.S., V.M.D., Dipl. A.C.Z.M., Daniel S. Dombrowski,
M.S., D.V.M., Peyton Hale, B.S., Maria Correa, Ph.D., and Larry S. Christian, B.S.
Abstract: Ectothermic vertebrates are a diverse group of animals that rely on external sources to maintain a
preferred body temperature. Amphibians and reptiles have a preferred optimal temperature zone that allows for
optimal biological function. Physiologic processes in ectotherms are influenced by temperature; these animals
have capabilities in which they make use of behavioral and physiologic mechanisms to thermoregulate. Core body,
ambient air, body surface, and surface/water temperatures were obtained from six ectothermic species including
one anuran, two snakes, two turtles, and one alligator. Clinically significant differences between core body
temperature and ambient temperature were noted in the black rat snake, corn snake, and eastern box turtle. No
significant differences were found between core body and ambient temperature for the American alligator,
bullfrog, mata mata turtle, dead spotted turtle, or dead mole king snake. This study indicates some ectotherms are
able to regulate their body temperatures independent of their environment. Body temperature of ectotherms is an
important component that clinicians should consider when selecting and providing therapeutic care. Investigation
of basic physiologic parameters (heart rate, respiratory rate, and body temperature) from a diverse population of
healthy ectothermic vertebrates may provide baseline data for a systematic health care approach.
Key words: Amphibians, reptiles, ectotherm, body temperature
INTRODUCTION
Amphibians and reptiles are popular private
household pets, animal models in biomedical
research, and part of public educational exhibits
worldwide. As ectotherms, these animals rely on
external sources, such as environmental heat and
adaptive behavior,16 to maintain a preferred body
temperature (PBT). Ectothermic vertebrates are a
diverse, complex, group of animals. Knowing the
animal’s unique anatomic and physiologic char-
acteristics, as well as its environmental require-
ments, is extremely important when working with
these exotic species.15,19 Amphibians and reptiles
have a preferred optimal temperature zone
(POTZ), which is a species-specific temperature
range that allows for optimal metabolism, effec-
tive immune function, and reproduction. There-
fore, it is essential for these ectotherms to stay
within their POTZ, in order to achieve a PBT and
remain in good health.13
All physiologic processes in ectotherms are
influenced by temperature in some way.2,28 In
order to regulate body temperature, reptiles have
notable thermoregulatory capabilities in which
they make use of behavioral and physiologic
mechanisms, including basking, postural changes,
heart rate hysteresis, peripheral circulation, and
even various levels of metabolic heat produc-
tion.21,25 Another critical component of ectother-
mic thermoregulation is the cardiovascular
system. Reptiles increase the rate of heat absorp-
tion by increasing heart rate, whereas during
cooling, reptiles decrease heart rate to conserve
body heat.10 Heart rate during heating is signifi-
cantly faster than during cooling, regardless of the
body temperature, and is known as heart rate
hysteresis.5
Some reptiles use metabolic heat production to
increase the rate of heating and decrease the rate
of cooling, or to sustain their body temperature
above ambient temperatures. It has been found
that rubber boas (Charina sp.) are able to control
their rates of heating and cooling and that they
heat faster than they cool.27 Pure endothermy and
pure ectothermy are the ends of a spectrum of
thermoregulatory patterns and most species fall
somewhere in between.18 The best examples of
metabolic heat production are in leatherback sea
turtles, Dermochelys coriacea,9 and several species
of female pythons during incubation of their
From the Department of Clinical Sciences, North
Carolina State University College of Veterinary Medi-
cine, 1060 William Moore Drive, Raleigh, North
Carolina 27607, USA (Raske, Lewbart, Dombrowski,
Christian); Department of Population Health and
Pathobiology, North Carolina State University College
of Veterinary Medicine, 1060 William Moore Drive,
Raleigh, North Carolina 27607, USA (Correa); and
North Carolina State Museum of Natural Sciences, 11
West Jones Street, Raleigh, North Carolina 27601, USA
(Christian, Dombrowski, Hale). Present address (Raske):
The Animal Medical Center, 510 E. 62nd Street, New
York, New York 10065. Correspondence should be
directed to Dr. Lewbart ([email protected]).
517
eggs.8 Other examples of species that are able to
raise their body temperatures considerably above
the air temperature are the lizard Liolaemus and
the toad Bufo spinulosus that were studied at
altitude in the Andes.17 Diamond pythons (Mor-
elia spilota) are able to keep their body tempera-
tures slightly warmer than ambient conditions.23
It is known that recently fed Python molurus have
the ability to raise their body temperatures above
the ambient temperature without external heat
sources11 and corn snakes (Elaphe guttata) are able
to increase their body temperature during diges-
tion.20
Previous studies have investigated the differ-
ences between core body temperature and ambi-
ent temperature of ectotherms;3,7,24 a study has
also examined differentials between body surface
temperature and ambient temperature.6
In contrast to the previous studies that investi-
gated differences between core body or body
surface temperatures and ambient temperatures
of ectotherms under natural environmental con-
ditions, our study investigates whether various
ectotherms have the ability to sustain their body
temperature above ambient after removal from
their heat source and examines heart rate in
relation to body temperature and ambient tem-
perature.
MATERIALS AND METHODS
Core body, ambient air, body surface, and
surface or water temperatures were obtained from
six species of ectotherms including one species of
anuran, two species of snakes, two species of
turtles, and one species of alligator, specifically
American bullfrog (Rana catesbeiana), six black
rat snakes (Elaphe obsoleta obsoleta), five corn
snakes (Elaphe guttata), six Eastern box turtles
(Terrapene carolina), seven mata mata turtles
(Chelus fimbriatus), and five American alligators
(Alligator mississippiensis). All the subjects were
housed indoors at the North Carolina Museum of
Natural Sciences (NCMNS) in Raleigh, North
Carolina (USA) under artificial conditions. Heat
sources and photoperiods were regulated and all
subjects used had been housed at the NCMNS
for a minimum of 6 mo to ensure an adequate
acclimatization had occurred. Data acquisition
took place in July 2008.
An EBROt Compact J/K/T/E thermocouple
thermometer was used to obtain all temperature
readings (model EW-91210-40; Cole-Parmer, Ver-
non Hills, Illinois 60061, USA). Core body
temperatures were recorded from the cloaca using
the Oaliton Type T polyvinyl chloride epoxy tip
24 gauge 3 152.4 cm probe (08505-90). When
obtaining body temperatures, caution was taken
not to allow heat exchange from the handler to the
body of the ectotherm. Ambient air temperature
was taken approximately 10 cm from the ecto-
therm using Oaliton type T Air probe 21.6 cm
(08500-75). Body surface temperatures were ob-
tained via the Type T low-cost Surface 12.1 cm
(08525-66) probe. For all animals, except the two
species of turtles, the probe was placed midbody
on the dorsal surface. For the turtles, the surface
probe was placed on the following five areas: left
front, right front, left hind, right hind, and
midcarapace. Surface temperature was obtained
via the type T low-cost surface 12.1 cm probe on
the temporary enclosure surface. Water tempera-
ture was obtained via the type T small-diameter
10.2 cm probe (08505-57). The probe was placed
halfway in the water to obtain the reading.
In the morning, the respiratory rate and
attitude of each ectotherm was observed to
determine health status. The attitude scale used
was bright, alert, responsive (BAR); quiet, alert,
responsive (QAR); depressed; or comatose. Each
subject was then taken from its enclosure,
weighed, and placed into an individual portable
container. They were then placed in a separate
room at room temperature with no primary heat
sources, the lights off, and no access to food. Four
hours later core body, ambient air, body surface,
and surface or water temperatures readings were
recorded. All temperatures are in degrees Centi-
grade to the nearest 0.18C. Five consecutive
readings of each type of temperature were taken.
There was approximately a 10-sec delay between
each reading. After temperature readings were
recorded, a heart rate reading was recorded for
each ectotherm. Heart rate was measured using a
Doppler blood flow detector (Parks Medical
Electronics, Inc, Aloha, Oregon 97007, USA) at
the level of the heart in all species, except the
turtles, where the carotid artery was utilized.
The same procedure was used to collect and
record temperatures from three dead ectotherms
including a tiger salamander (Ambystoma tigri-
num), mole king snake (Lampropeltis calligaster),
and a spotted turtle (Clemmys guttata).
Statistical methods
One-way analysis of variance (ANOVA) was
used to analyze differentials between Tb, Ta, Tbs,
and Ts/w. Significance of statistical analyses was
accepted at P � 0.05.
518 JOURNAL OF ZOO AND WILDLIFE MEDICINE
RESULTS
Clinical significance to some degree was found
in the difference between core body temperature
and ambient temperature in the black rat snake
(ANOVA, P ¼ 0.030), corn snake (ANOVA, P ¼0.003), and Eastern box turtle (ANOVA, P ¼0.004). No clinical significance was found in the
difference between core body temperature and
ambient temperature for the American alligator
(ANOVA, P ¼ 0.006), bullfrog (ANOVA, P ¼0.000), mata mata turtle (ANOVA, P ¼ 0.127),
dead spotted turtle (ANOVA, P¼ 0.531), or dead
mole king snake (ANOVA, P¼ 0.060). A correla-
tion between heart rate and differences in core
body temperature and ambient temperature was
not observed.
The following are the temperature ranges and
heart rate ranges for each species used in the
study.
Black rat snake (Elaphe obsoleta obsoleta):
Temperatures were taken from six black rat
snakes. Core body temperatures ranged from
25.68C to 30.18C. Ambient air temperatures
ranged from 25.28C to 25.78C. The body surface
temperatures ranged from 25.28C to 25.88C. The
surface temperatures ranged from 25.68C to
26.78C. The heart rates ranged from 58 to 68
beats/min.
Corn snake (Elaphe guttata): Temperatures
were taken from five corn snakes. Core body
temperatures ranged from 25.48C to 27.78C.
Ambient air temperatures ranged from 24.48C to
25.38C. The body surface temperatures ranged
from 25.48C to 26.18C. The surface temperature
readings ranged from 25.98C to 28.18C. The heart
rates ranged from 54 to 68 beats/min.
Eastern box turtle (Terrapene carolina): Tem-
peratures were taken from six Eastern box turtles.
Core body temperatures ranged from 24.88C to
26.48C. Ambient air temperatures ranged 24.78C
to 26.08C. The body surface temperatures ranged
from 25.78C to 26.78C. The surface temperature
readings ranged from 24.98C to 27.18C. The heart
rates ranged from 36 to 72 beats/min.
Mata mata turtle (Chelus fimbriatus): Temper-
atures were taken from seven mata matas. Core
body temperatures ranged from 24.58C to 25.38C.
Ambient air temperatures ranged from 24.48C to
25.58C. The body surface temperature ranged
from 24.38C to 25.98C. The water temperature
readings ranged from 24.68C to 25.58C. The heart
rates ranged from 16 to 32 beats/min.
American bullfrog (Rana catesbeiana): Tem-
peratures were taken from five bullfrogs. Core
body temperatures ranged from 22.18C to 25.48C.
Ambient air temperatures ranged from 24.58C to
25.48C. The body surface temperature ranged
from 22.78C to 23.68C. The water temperature
readings ranged from 21.18C to 22.38C. The heart
rates ranged from 56 to 64 beats/min.
American alligator (Alligator mississippiensis):
Temperatures were taken from five American
alligators. Core body temperatures ranged from
24.58C to 25.08C. Ambient air temperatures
ranged from 24.48C to 25.28C. The body surface
temperatures ranged from 24.58C to 25.58C. The
surface temperature readings ranged from 24.38C
to 24.68C. The heart rates ranged from 36 to 44
beats/min.
Mole king snake (Lampropeltis calligaster): Tem-
peratures were taken from a dead mole king snake.
Core body temperatures ranged from 24.68C to
Table 1. The six species in this study with ranges of the core body, ambient, body surface, and surface/watertemperatures, along with ranges of heart rate, mean core body temperature, and mean ambient temperaturedifferentials.
Common name Scientific nameRanges ofTb
a (8C)Ranges ofTa (8C)
Ranges ofTbs (8C)
Ranges ofTs/w (8C)
Ranges ofheart rate(beats/min) MTb/MTa
Black rat snake Elaphe obsoleta obsoleta 25.6–30.1 25.2–25.7 25.2–25.8 25.6–26.7 58–68 þ1.50Corn snake Elaphe guttata 25.4–27.7 24.4–25.3 25.4–26.1 25.9–28.1 54–68 þ1.10Eastern box turtle Terrapene carolina 24.8–26.4 24.7–26.0 25.7–26.7 24.9–27.1 36–72 þ0.12Mata mata Chelus fimbriatus 24.5–25.3 24.4–25.5 24.3–25.9 24.6–25.5 16–32 –0.01
Bullfrog Rana catesbeiana 22.1–25.4 24.5–25.4 22.7–23.6 21.1–22.3 56–64 �1.64American alligator Alligator mississippiensis 24.5–25.0 24.4–25.2 24.5–25.5 24.3–24.6 36–44 �0.04Mole king snake (dead) Lampropeltis calligaster 24.6–25.0 24.4–25.2 25.0–25.8 24.8–26.0 N/A �0.175Tiger salamander (dead) Ambystoma tigrinum 24.8–25.3 24.4–25.7 24.8–26.5 25.1–27.6 N/A þ0.075Spotted turtle (dead) Clemmys guttata 24.7–25.4 24.6–25.7 24.8–26.6 24.9–26.6 N/A �0.175
a Tb, core body temperature; Ta, ambient air temperature; Tbs, body surface temperature; Ts/w, surface or water temperature;
MTb, mean core body temperature; MTa, mean ambient air temperature; N/A, not applicable.
RASKE ET AL.—AMPHIBIAN AND REPTILE BODY TEMPERATURES 519
25.08C. Ambient air temperatures ranged from
24.48C to 25.28C. The body surface temperatures
ranged from 25.08C to 25.88C. The surface temper-
ature readings ranged from 24.88C to 26.08C.
Tiger salamander (Ambystoma tigrinum): Tem-
peratures were taken from a dead tiger salamander.
Core body temperatures ranged from 24.88C to
25.38C. Ambient air temperatures ranged from
24.48C to 25.78C. The body surface temperature
ranged from 24.88C to 26.58C. The surface tem-
perature readings ranged from 25.18C to 27.68C.
Spotted turtle (Clemmys guttata): Tempera-
aken from a dead spotted turtle. Core body
temperatures ranged from 24.78C to 25.48C.
Ambient air temperatures ranged from 24.68C to
25.88C. The body surface temperatures ranged
from 24.98C to 26.68C. The surface temperature
readings ranged from 24.88C to 26.68C.
DISCUSSION
The purpose of this experiment was to study
whether various ectotherms are able to sustain body
temperatures above that of their surroundings in the
absence of an external heat source. Elaphe obsoleta
obsoleta, E. guttata, and T. carolina displayed clinical
significance in differences between core body temper-
ature and ambient air temperature. This indicates
these ectotherms are able to regulate, to some extent,
their body temperatures independent from the ambi-
ent temperature they are exposed to. Research has
shown that when a reptile or amphibian is in an
environment with decreasing temperatures, the body
temperature of that ectotherm will drop accordingly,
usually with a slight lag, due to conduction rates, skin
thickness, and vasomotor responses.4 In studies
involving the agamid lizard, Amphibolurus barbatus, it
was determined that the animal was able to maintain
core body temperatures higher than the air tempera-
tures, and was able to control rates of heating and
cooling, which is a condition typical of heliothermic
reptiles. This led A. barbatus to be considered a model
to highlight evolution in the spectrum of thermoreg-
ulation patterns from ectothermy to endothermy.1,4
Further research should be conducted to determine
if there are other ectotherms that exhibit the ability to
regulate body temperature.
The insignificant differences between core body
temperature and ambient air temperature shown
by dead L. calligaster and C. guttata, compared
with the live ectotherms, indicates heat transfer
depends somewhat on blood circulation.
Veterinary clinicians working with ectotherms,
such as reptiles and amphibians, need to be
familiar with the specific requirements of various
species in order to provide optimal patient care.
The body temperature of ectotherms is an impor-
tant component that clinicians need to consider
when selecting and providing therapeutic care.14
Heart rate, respiratory rate, and core body
temperature measurements are basic components
of a physical examination of domestic animals.
However, in exotic animals, not all clinicians
utilize such physiologic parameters in their deci-
sion-making processes regarding appropriate
treatment and care, which may reflect the lack of
species-specific research on reptiles and amphib-
ians.12,19 Furthermore, in reptiles and amphibians,
signs of disease are usually not evident until late
in the disease process.22,26 As a result, any
methods that are safe and inexpensive and still
provide an accurate health status assessment have
an application in exotic animal medicine. Investi-
gation of these basic physiologic parameters
(heart rate, respiratory rate, and body tempera-
ture) from a diverse population of healthy ecto-
thermic vertebrates may provide a more
systematic approach to the health care of these
animals and provide a baseline model for future
studies.
Acknowledgments: This study was supported in
part by the Robert J. Koller Aquatic Animal
Medicine Research Endowment.
LITERATURE CITED
1. Bartholomew, G. A., and Tucker, V. A. 1963.
Control of changes in body temperature, metabolism,
and circulation by the agamid lizard, Amphibolurus
barbatus. Physiol. Zool. 36: 199–218.
2. Bicego, K., R. Barros, and L. Branco. 2006.
Physiology of temperature regulation: comparative
aspects. Comp. Biochem. Physiol. A 147: 616–639.
3. Brattstrom, B. 1965. Body temperatures of rep-
tiles. Am. Midl. Nat. 73: 376–422.
4. Brattstrom, B. 1971. Social and thermoregulatory
behavior of the bearded dragon, Amphibolurus barbatus.
Copeia 3:484–497.
5. Franklin, C., and F. Seebacher. 2003. The effect of
heat transfer mode on heart rate responses and hyster-
esis during heating and cooling in the estuarine crocodile
Crocodylus porosus. J. Exp. Biol. 206: 1143–1151.
6. Garrick, D. 2008. Body surface temperature and
length in relation to the thermal biology of lizards.
Biosci. Horizons 1: 136–142.
7. Huey, R., and T. Webster. 1975. Thermal biology
of a solitary lizard: Anolis marmoratus of Guadeloupe,
Lesser Antilles. Ecology 56: 445–452.
8. HutchisonV., H. Dowling, and A. Vinegar. 1966.
Thermoregulation in a brooding female Indian python,
Python molurus bivittatus. Science 151: 694–695.
9. James, M., and N. Mrosovsky. 2004. Body tem-
peratures of leatherback turtles (Dermochelys coriacea)
520 JOURNAL OF ZOO AND WILDLIFE MEDICINE
in temperate waters off Nova Scotia, Canada. Can. J.
Zool. 82: 1302–1306.
10. Kik, M., and M. Mitchell. 2005. Reptile cardiol-
ogy: a review of anatomy and physiology, diagnostic
approaches, and clinical disease. Semin. Avian Exotic
Pet Med. 14: 52–60.
11. Marcellini, D., and A. Peters. 1982. Preliminary
observations on endogenous heat production after
feeding in Python molurus. J. Herpetol. 16: 92–95.
12. Martinez-Jimenez, D., and S. Hernandez-Divers.
2007. Emergency care of reptiles. Vet. Clin. N. Am.
Exotic Anim. Pract. 10: 557–585.
13. McBride, M., and S. Hernandez-Divers. 2004.
Nursing care of lizards. Vet. Clin. N. Am. Exotic Anim.
Pract. 7: 375–396.
14. Mitchell, M. 2006. Therapeutics, In: Mader, D.
(ed). Reptile Medicine and Surgery, 2nd ed. W. B.
Saunders, Philadelphia, Pennsylvania. Pp. 631–664.
15. Mosley, C. 2005. Anesthesia and analgesia in
reptiles. Semin. Avian Exotic Pet Med. 14: 243–262.
16. O’Malley, B. 2005. Clinical Anatomy and Phys-
iology of Exotic Species. W. B. Saunders, London,
United Kingdom.
17. Pearson, O., and D. Bradford. 1976. Thermoreg-
ulation of lizards and toads at high altitudes in Peru.
Copeia 1: 155–169.
18. Pough, H., R. Andrews, J. Cadle, M. Crump, A.
Savitzky, and K. Wells. 2004. Herpetology, 3rd ed.
Pearson Education, Inc., Cranbuny, New Jersey.
19. Read, M. 2004. Evaluation of the use of anes-
thesia and analgesia in reptiles. J. Am. Vet. Med.
Assoc. 224: 547–552.
20. Roark, A., and M. Dorcas. 2000. Regional body
temperature variation in corn snakes measured using
temperature-sensitive passive integrated transponders.
J. Herpetol. 34: 481–485.
21. Seebacher, F., and C. Franklin. 2005. Physiolog-
ical mechanisms of thermoregulation in reptiles: a
review. J. Comp. Physiol. B 175: 533–541.
22. Selleri, P., and S. Hernandez-Divers. 2006. Renal
diseases of reptiles. Vet. Clin. N. Am. Exotic Anim.
Pract. 9: 161–174.
23. Slip, D., and Shine, R. 1988. Thermoregulation
of free-ranging diamond pythons, Morelia spilora (Ser-
pentes, Boidae). Copeia 4: 984–995.
24. Stevenson, R. 1985. Body size and limits to the
daily range of body temperature in terrestial ecto-
therms. Am. Nat. 125: 102–117.
25. Tattersall, G., V. Cadenav, and M. Skinner. 2006.
Respiratory cooling and thermoregulatory coupling in
reptiles. Respir. Physiol. Neurol. 154: 302–318.
26. Walton, R. 2001. Establishing reference inter-
vals: health as a relative concept. Semin. Avian Exotic
Pet Med. 10: 66–71.
27. Zhang, Y., M. Westfall, K. Hermes, and M.
Dorcas. 2008. Physiological and behavioral control of
heating and cooling rates in rubber boas, Charina
bottae. J. Therm. Biol. 33: 7–11.
28. Zug, G., L. Vitt, and J. Caldwell. 2001. Herpe-
tology: An Introductory Biology of Amphibians and
Reptiles, 2nd ed. Academic Press, San Diego, Califor-
nia.
Received for publication 8 November 2011
RASKE ET AL.—AMPHIBIAN AND REPTILE BODY TEMPERATURES 521
