Head-Body Temperature Differences in Free-Ranging Rubber Boas

00530 (paratype of A. komaii); Chiaoliping, Chiai Pref.:
KUZ 32954-955; Tamaopu, Chiai. Pref.: NMNS 01480;
Kuantzuling, Tainan Pref.: CAS 18006 00530 (paratype of A. komaii); Chiaoliping, Chiai Pref.:
KUZ 32954-955; Tamaopu, Chiai. Pref.: NMNS 01480;
Kuantzuling, (holotype of A.
formosensis), KUZ 19386; Chipen Wenchuan, Taitung
Pref.: NMNS 01609; Chufengshan, Pingtung Pref.:
NMNS 00685; detailed loc. unknown: TM RS0053,
Tainan Pref.: CAS 18006 (holotype of A.
formosensis), KUZ 19386; Chipen Wenchuan, Taitung
Pref.: NMNS 01609; Chufengshan, Pingtung Pref.:
NMNS 00685; detailed loc. unknown: TM RS0053,
Journal of Herpetology, Vol. 31, No. 1, pp. 87-93, 1997
Copyright 1997 Society for the Journal of Herpetology,
Study of Amphibians and Reptiles
Vol. 31, No. 1, pp. 87-93, 1997
Copyright 1997 Society for the Study of Amphibians and Reptiles
SYSTEMATICS OF EAST ASIAN PAREAS
0127. P. iwasakii-Ishigakijima I., Yaeyama Group:
KUZ 28133-134*, 28446, 28448, 28450, 32933-934,
33107, NTNU B-201290, OMNH R2323; Iriomotejima
I., Yaeyama Is. Group: KUZ 21304*, 32932, 0127. P. iwasakii-Ishigakijima I., Yaeyama Group:
KUZ 28133-134*, 28446, 28448, 28450, 32933-934,
33107, NTNU B-201290, OMNH R2323; Iriomotejima
I., Yaeyama Is. Group: MUR 1954-
1-08-1; Yaeyama Group (detailed locality unknown):
OPM one uncatalogued specimen.
KUZ 21304*, 32932, MUR 1954-
1-08-1; Yaeyama Group (detailed locality unknown):
OPM one uncatalogued specimen.
Head-body Temperature Differences in Head-body Temperature Free-ranging Rubber Boas
Differences in Free-ranging Rubber Boas
MICHAEL E. DORCAS1 AND CHARLES R. PETERSON
Department of Biological Sciences Idaho State University, Pocatello, Idaho 83209, USA
ABSTRACT.-Although most studies of reptilian thermal biology have measured body temperature from a
single location in an animal, the presence of regional temperature differences within the bodies of reptiles
should be considered when conducting detailed studies of their thermal biology. As part of an extensive
study of rubber boa (Charina bottae) thermal biology, we measured the oral and cloacal temperatures of 45
free-ranging rubber boas from June 1990 to August 1995. We used oral temperature as an indicator of head
temperature and cloacal temperature as an indicator of body temperature. Oral temperatures ranged from
13.8 C to 32.2 C and cloacal temperatures ranged from 11.5 C to 34.5 C. During the daytime, rubber boas gen-
erally exhibited warmer heads at average body temperatures below their thermal preference (thermal pref-
erence = 27.4 C) and cooler heads at average body temperatures above their thermal preference. At night, ac-
tive rubber boas exhibited significantly higher head temperatures than body temperatures (mean differ-
ence = 2.0 C). This study represents the first report of regional body temperature differences exhibited by
a reptile during nocturnal activity and supports the generalization that head temperature in rep-
tiles is maintained within more narrow limits than body temperature during the day. Further studies are
required to fully understand both the causes and consequences of regional temperature differences in free-
ranging reptiles.
Studies of the causes and consequences of
body temperature variation in reptiles can lead
to a better understanding of their overall ecology
in addition to augmenting our general
knowledge of thermal biology (Huey, 1982; Lillywhite,
1987; Peterson et al., 1993). Although
most studies of reptilian thermal biology have
measured body temperature from a single location
in an animal, usually cloacal or core temperature,
the existence of regional temperature
differences within the bodies of reptiles should
be considered when conducting detailed studies
of their thermal biology (Dill, 1972; Peterson
et al., 1993). Determining the underlying mecha-
Studies of the causes and consequences of
body temperature
nisms responsible for regional temperature differences
in reptiles is often difficult. Regional
temperature differences have been attributed to
several nonexclusive factors, including physical
differences among body regions (e.g., surface
variation in reptiles can lead
to a better understanding of their overall ecology
in addition to augmenting our general
knowledge of thermal biology (Huey, 1982; Lillywhite,
1987; Peterson et al., 1993). Although
most studies of reptilian thermal biology have
measured body temperature from a single location
in an animal, usually cloacal or core temperature,
the existence of regional temperature
differences within the bodies of reptiles should
be considered when conducting detailed studies
of their thermal biology (Dill, 1972; Peterson
et al., 1993). Determining the underlying mecha-
nisms responsible for regional temperature differences
in reptiles is often difficult. Regional
temperature differences have been attributed to
several nonexclusive factors, including physical
differences among body regions (e.g., surface
Present Address: Savannah River Ecology Labo-
ratory, Drawer E, Aiken, South Carolina 29802, USA.
87
area to volume ratios; Pough and McFarland,1976),
behavioral thermoregulation (e.g.,
differential exposure to solar radiation; Heath,
1964; Hammerson, 1977; Gregory, 1990), and
physiological mechanisms (e.g., blood shunts or
countercurrent heat exchangers; Heath, 1966;
Webb and Heatwole, 1971).
Several studies of head-body temperature differences
in reptiles indicate that head temperature
is maintained within more narrow limits
than body temperature (Heath, 1964; Webb et
al., 1972; Johnson, 1973; Peterson, 1982; 1987).
Maintenance of head temperature within more
narrow limits than body temperature may be
due to the fact that the thermoregulatory control
center is located in the brain of reptiles (Berk
and Heath, 1975). Additionally, precise regulation
of head temperature may help to optimize
central nervous system function (Block and
Carey, 1985). Precise regulation of head temperature
may be related to the propensity of
area to volume ratios; Pough and McFarland,1976),
behavioral thermoregulation (e.g.,
differential exposure to solar radiation; Heath,
1964; Hammerson, 1977; Gregory, 1990), and
physiological
many diurnal reptiles to allow the head to warm
before they fully emerge from nighttime retreats
mechanisms (e.g., blood shunts or
countercurrent heat exchangers; Heath, 1966;
Webb and Heatwole, 1971).
Several studies of head-body temperature differences
in reptiles indicate that head temperature
is maintained within more narrow limits
than body temperature (Heath, 1964; Webb et
al., 1972; Johnson, 1973; Peterson, 1982; 1987).
Maintenance of head temperature within more
narrow limits than body temperature may be
due to the fact that the thermoregulatory control
center is located in the brain of reptiles (Berk
and Heath, 1975). Additionally, precise regulation
of head temperature may help to optimize
central nervous system function (Block and
Carey, 1985). Precise regulation of head temperature
may be related to the propensity of
many diurnal reptiles to allow the head to warm
before they fully emerge from nighttime retreats

88
M. E. DORCAS AND C. R. PETERSON
(Fitch, 1960; Heath, 1964; Hammerson, 1977;
Gregory, 1990).
Because of their elongate form, snakes can
exhibit considerable regional differences in
body temperature (Fitch, 1960; Lillywhite, 1987;
Peterson et al., 1993). Consequently, snakes
offer an excellent opportunity to examine regional
temperature differences in detail. Numerous
reports exist describing regional temperature
differences in snakes under laboratory
or semi-natural conditions (Regal, 1966; Webb
and Heatwole, 1971; Dill, 1972; Johnson, 1973,
1975a, b; Hammerson, 1977) whereas fewer
reports exist for free-ranging snakes (Vincent,
1975; Peterson, 1987; Gregory, 1990). No study
has examined, in detail, regional temperature
differences in free-ranging nocturnal snakes.
Studies of regional temperature differences in
snakes active at night, when they do not have
access to solar radiation, will help us to further
understand both the behavioral and physiological
mechanisms by which snakes maintain
regional temperature differences and potentially
shed light on the functional and ecological
effects of regional temperature differences
in reptiles.
As part of an extensive study of rubber boa
(Charina bottae) thermal biology, we examined
differences in the head and body temperatures
of free-ranging rubber boas in southeastern
Idaho. Rubber boas are ideal subjects for studies
of regional temperature differences because
they are extremely docile. Thus, measurement of
their temperature is relatively easy and involves
minimal handling. Additionally, rubber boas are
often nocturnal, frequently at very low body
temperatures (Dorcas, 1995), and thus provide
an interesting comparison to studies of regional
temperature differences in diurnal species.
In this study, we compare our results with
previous research, propose possible mecha-
nisms to explain the existence of regional temperature
differences in rubber boas, and discuss
what is needed to further understand both the
causes and consequences of regional temperature
differences in reptiles.
MATERIALS AND METHODS
We determined the thermal preference (= selected
temperature; Pough and Gans, 1982) of
rubber boas by measuring the cloacal temperatures
of 19 rubber boas in a laboratory thermal
gradient. Snakes were collected from eastern
Washington and southeastern Idaho. We housed
snakes individually in 37.8 L aquaria with a substrate
of 3-5 cm of aspen bedding covered with
two layers of newspaper. All snakes had been
in captivity at least one month before thermal
preference experiments began. Using fluores-
matched that of southeastern Idaho. During the
active season (May through October), the ambient
room temperature was kept at approximately
18 C. One end of each cage was placed
on heat tapes to raise the operative temperature
(Bakken, 1992) at that end of the cage to 38 C.
To produce a relatively linear thermal gradient
between the front and rear of each cage, we
glued
cent lighting, we provided a photoperiod that
two layers of tin to the cage bottoms to
conduct heat to the cooler end. This arrangement
allowed the snakes to select body temperatures
between 18 C and 38 C. All body temperature
measurements were made during the summers
(1 June-31 August) of 1990 and 1991 between
1100 and 1400 h. To make the
measurements, we carefully lifted the tips of the
snakes' tails with one hand and inserted a thermocouple
approximately 1 cm into their cloacas,
disturbing the snakes as little as possible. We
used a thermocouple thermometer (Model
HH23, Omega, Stamford, CT) with a type T thermocouple
(36 gauge). To reduce irritation to the
snakes, the tip of the thermocouple was coated
with paraffin and petroleum jelly was used as a
lubricant. To determine the thermal preference
of rubber boas, we used only temperatures
taken from nongravid, nondigesting snakes to
calculate each snake's mean body temperature
and a single grand mean for all snakes. We used
the grand mean as the thermal preference.
To investigate head and body temperature
differences in free-ranging rubber boas, we measured
the oral and cloacal temperatures of rubber
boas when encountered in the field from
June 1990 to August 1995. Oral temperatures
were taken by grasping the snake behind the
head and inserting the bulb of a quick-reading
thermometer (model T-6000, Miller and Weber
Inc., Queens, NY) approximately 2 cm into the
mouth and anterior esophagus. Cloacal temperatures
were taken by carefully lifting the tail
and inserting the bulb of the thermometer approximately
2 cm into the cloaca and rectum. We
wiped the bulb of the thermometer with a dry
cloth between measurements. Both oral and
cloacal temperatures were measured to the nearest
0.1 C within 20 sec of each other and within
30 sec of capture. Care was taken to touch the
snakes as little as possible so as to minimize the
effects on their body temperatures. When possible,
snakes were left on the ground while temperatures
were taken. On five of the eleven occasions
on which we measured the temperatures
of snakes at night, we also measured soil surface
and 1 cm air temperatures.
Measurements were not taken in a fixed order.
Instead, we arbitrarily took either the cloacal
or oral temperature first (oral temperatures
were taken first for about 1/2 of the measurements).
On a few occasions we remeasured

HEAD AND BODY TEMPERATURES OF RUBBER BOAS
TABLE 1. Descriptive statistics summarizing the measurements of oral and cloacal temperatures of rubber
boas (Charina bottae) during the day and at night. The mean difference is presented as the mean absolute value
of the differences between oral and cloacal temperatures.
Oral temperature (C) Cloacal temperature (C) Mean (C)
N Minimum Maximum Minimum Maximum 1Oral-Cloacall
Day 34 15.2 32.2 13.8 34.5 2.0
Night 11 13.8 28.2 11.5 25.8 2.0
snakes' cloacal temperatures after first taking
their cloacal and oral temperatures (in that order)
and observed no change from the first cloacal
temperature taken.
The oral and cloacal temperatures of 45 different
snakes were measured. Some snakes were
encountered more than once during the course
of the study (e.g., telemetered snakes) and we
measured their temperatures each time. To
avoid problems of nonindependence, we randomly
selected one pair of measurements to use
in the analyses for each snake that had multiple
measurements.
We used oral temperature as an indicator of
head temperature and cloacal temperature as an
indicator of body temperature. We examined the
relationship between oral and cloacal temperatures
using linear regression and interpreted a
slope -71 as an indication of regional temperature
differences. For further statistical analysis,
we considered snakes measured during daytime
separately from those measured at night. The
daytime measurements were taken between
0831 and 1952 MST and were analyzed by examining
the relationship between 13.8 C to 32.2 C and cloacal temperatures ranged
from 11.5 C to 34.5 C (Table 1). The relationship
between oral and cloacal temperature had a
slope significantly
average body
temperature (calculated as the mean of oral and
cloacal temperature) and the difference between
oral and cloacal temperatures using linear regression.
We considered the mean of oral and
cloacal temperatures to be a better indicator of
overall body temperature than either oral or
cloacal temperature alone. For the 11 snakes
measured at night (taken between 2010 and 0136
MST), we tested for a difference in oral and cloacal
temperatures using a paired t-test. All statistical
tests were conducted using SYSTAT
(Wilkinson, 1990) with a rejection level of a
0.05.
RESULTS
different than one (upper and
lower 95% confidence intervals equal 0.69 and
0.81 respectively), thus indicating the presence
of regional temperature differences (Fig. 1). During
the day, at average body temperatures be-
low their thermal preference, snakes tended to
have oral temperatures considerably higher
than their cloacal temperatures. During the day,
at average body temperatures above their thermal
preference, snakes tended to have oral temperatures
lower than their cloacal temperatures
(R2 = 0.60, F = 47.6, df = 32, P < 0.001; Fig.
2A). At night, snakes were active at relatively
low body temperatures (Dorcas, 1995) and had
oral temperatures that averaged 2.0 C higher
than their cloacal temperatures (t < 9.8, df = 10,
P < 0.001; Table 1 and Fig. 2A and B). In all five
instances in which we measured soil surface and
1 cm air temperatures (in conjunction with oral
and cloacal temperatures) at night, the oral and
cloacal temperatures were lower than the soil
35 -
30 -
- 25
Cu
a)
. 20-
I-
2 15 -
0
O Day
.1
* * -
Night
0
.1
I
10
I *
* ?
10 15 20 25 30 35
Cloacal Temperature (?C)
The thermal preference of rubber boas was
determined from 942 temperature measure-
ments made on 19 snakes in the laboratory ther-
mal gradient. Snake temperatures ranged from
20 C to 36 C and the individual mean tempera-
tures for the snakes varied from 25.6 C to 29.0
C. The grand mean (thermal preference) was
27.4 C.
In the field, oral temperatures ranged from
89
FIG. 1. The relationship between oral and cloacal
body temperatures in rubber boas (Charina bottae).
Open symbols represent measurements made during
the daytime and filled symbols represent measurements
made at night. The dashed line represents a
1:1 relationship between oral and cloacal temperatures
(i.e., no regional temperature differences). The
solid line is the regression representing the relationship
between oral and cloacal temperature in rubber
boas (v = (0.75)x + 6.86).

90
A
a
-
Q. a)
o E
(U
8
6-
4-
2
B
I0
0
a v
..- -
-2
1
M. E. DORCAS AND C. R. PETERSON
tion from predation (Dorcas, 1995). When males
or nongravid females were found during the
daytime, they were usually inactive (not moving)
and partially or completely covered warmer
head
by
dead leaves, which allowed them to maintain
relatively high body temperatures without being
completely exposed.
-_ _ _,...
DISCUSSION
-Cs- oral = coacal
| '~ ~ | warmer
8 <
II
body
"'"
Thermal
Preference
O Day
* Night
10 15 20 25 30 35
Average Body Temperature (C)
B
Air Temperature = 13.0?C
\ \\\\E ..Substrate . Temperature 16.5C
FIG. 2. A) The relationship of average body temperature
(calculated as the mean of the head and cloacal
temperature) and the difference between head
and cloacal temperature in rubber boas (Charina bottae).
The data points in the upper half of part A represent
snakes with warmer heads and data points in
the lower half of the figure represent snakes with
warmer cloacas. Open symbols represent measurements
made during the daytime and filled symbols
represent measurements made at night. The measurements
resulting in the data point labeled "B" are illustrated
in part B of the figure. The regression line is
generated from daytime measurements only (y =
(-0.34)x + 9.53, R2 = 0.60, df = 33, P < 0.001). Note
that the point at which the regression line crosses the
line representing equal head and cloacal temperatures
coincides with the thermal preference of rubber boas.
See text for further discussion. B) A diagram representing
one example of a set of environmental (soil surface
and 1 cm air) and snake oral and cloacal temperatures
taken at night. Note that substrate temperature
was higher than either oral or cloacal temperature but
both oral and cloacal temperatures were higher than
the air temperature. This snake was an adult female
and was captured and its temperatures measured on
11 July 1991 at 2154 MST (data point labeled "B" in
part A).
surface temperature but higher than the air temperature
(Fig. 2B).
During the day, snakes were usually encountered
while basking, sometimes only partially
exposed under dead leaves or in rock crevices
(Dorcas, 1995). Most of the high temperature
readings (i.e., >30 C) were of gravid females using
a large rock Two main points arise from this study. First,
during the daytime, rubber boas exhibited
warmer heads at temperatures below their thermal
preference and warmer bodies at temperatures
above their thermal preference. Second,
rubber boas active at night exhibited significantly
higher
outcropping as a "rookery"
(Klauber, 1972; Graves and Duvall, 1993; Cobb,
1994) which allowed thermoregulation at high,
stable body temperatures and apparent protec-
head temperatures than body tem-
peratures.
The observation that rubber boas appear to
regulate their head temperature more precisely
than their body temperature during the daytime
is consistent with the findings of previous
researchers (Webb and Heatwole, 1971; Hammerson,
1977; Johnson, 1973; Peterson, 1982,
1987). The differences observed in head and
body temperatures may be due to several nonexclusive
factors. Pough and McFarland (1976)
showed that substantial differences in head and
body temperatures can be found in dead, as well
as live, green iguanas (Iguana iguana), thus indicating
a passive mechanism for the maintenance
of regional temperature differences. They attributed
the temperature differences observed to
differences in the surface area to volume ratios,
and thus heating and cooling rates, of the iguanas'
heads and bodies. Because the heads of rubber
boas are not well differentiated from their
bodies, it is unlikely that the differences observed
during the daytime are due to such passive,
physical mechanisms. We believe that an
active, rather than passive, mechanism is the
most likely cause of regional temperature differences
in rubber boas during the daytime.
Active maintenance of regional temperature
differences can involve behavioral mechanisms,
physiological mechanisms, or both. Physiological
mechanisms (blood shunts or countercurrent
heat exchangers) responsible for regional
temperature differences have been described
for several species of reptiles, including
some pythons (Webb and Heatwole, 1971; Johnson,
1973) and lizards (Heath, 1966; Webb et al.,
1972; Spray and Belkin, 1973; Crawford et al.,
1977). However, the role of physiological mechanisms
in maintaining regional temperature differences
in rubber boas during the daytime is
unknown.
It is clear that, during the daytime, behavioral
o u 0
m
0
-4-
-6-
-8
I * I I I I
mechanisms play an important role in the maintenance
of regional temperature differences by
rubber boas. Gravid rubber boas frequently

HEAD AND BODY TEMPERATURES OF RUBBER BOAS
warm their developing embryos by exposing
only the posterior portion of their body to solar
radiation, which likely is important for accelerating
embryonic developmental rate (Dorcas,
1995). Accelerating embryonic developmental
rate may be especially important during cool
years at northern latitudes and/or high alti-
know if regional temperature differences persist
in the early morning hours.
Whereas the exact mechanism is unknown,
warming of the head during nocturnal activity
likely occurs via heat transfer from the substrate.
Whether physiological (e.g., blood
shunts or counter-current exchangers) or behavioral
activities (e.g., periodically burying
tudes, if the snakes are to give birth before time
for hibernation (Dorcas, 1995). While warming
the posterior portion of their body to high temperatures
(maximum recorded = 36 C), the
snakes maintain considerably lower head temperatures
(maximum recorded = 32.5 C). This
is apparently done by shielding their head from
direct solar radiation, although physiological
processes cannot be ruled out. Likewise, the
maintenance of higher head temperatures at
lower average body temperatures (below their
thermal preference) may be the result of behavioral
processes (e.g., heliothermal and/or thigmothermal
activities), physiological processes,
or both. However, during this study, we did not
observe head basking, a behavior apparently
common in some diurnal snakes (Hammerson,
1977,1979,1987,1989; Gregory, 1990). Whatever
the mechanism, the maintenance of head temperatures
within more narrow limits than body
temperatures during the daytime supports the
premise that their head in loose soil) contribute to maintaining
temperature control of the central
nervous system is a primary factor influencing
the observed patterns of regional temperature
differences in reptiles.
This study is the first to demonstrate the pres-
warmer head temperatures is unknown. A
physiologically-based hypothesis is that, as a
snake crawls along the ground, heat is transferred
from the warmer ground to the snake's
body via its ventral surface. By restricting blood
flow to the dorsum and allowing warm blood
from the venter to flow anteriorly toward the
head, the snake might maintain head temperatures
a few degrees higher than the rest of its
body. Whatever the mechanism, the presence of
warmer head temperatures during activity at
low overall body temperatures further supports
the view that regional temperature differences
may play an important role in optimizing cen-
tral nervous system function (Heath, 1964;
Campbell, 1969; Webb et al., 1972; J. Kauffman
and A. Bennett, pers. comm.). However, the
functional consequences of maintaining head
temperature 2-3 C above body temperature
have yet to be determined.
Further studies are needed to examine both
the causes and consequences of regional temperature
differences in reptiles. Detailed studies
ence of regional temperature differences (i.e.,
higher head temperatures) in a reptile while active
at night. All of the nighttime measurements
were made on active snakes, mostly from snakes
found crossing dirt roads (using rectilinear locomotion)
while we were road cruising. While
the thermal environment above ground is typically
assumed to be spatially homogeneous at
night, our results indicate that this is not necessarily
the case. On the five occasions on which
we took environmental measurements in conjunction
with snake body temperatures at night,
we found a temperature difference of several degrees
between the soil surface and the cooler air
1 cm above it. This temperature difference between
the soil and the air just above it would
allow rubber boas to maintain head temperatures
2-3 C higher than their body temperatures
while they are active at night (Fig. 2A). It should
be noted that the gradient between air and soil
temperatures should decrease throughout the
night as the soil temperature cools, thus reducing
the opportunities for generating regional
temperature differences. We did not record using temperature sensitive radiotelemetry and
automated telemetric monitoring (Peterson and
Dorcas, 1992) should improve our ability to describe
regional temperature differences in freeranging
any
temperatures of snakes between 0136 and 0831
MST, even though rubber boas are active at
those times (Dorcas, 1995), and thus we do not
animals. Laboratory or field enclosure
studies using radiotelemetry, temperature sensitive
PIT (passive integrated transponder) tags,
and infrared video-photography coupled with
detailed physiological studies (e.g., blood flow
experiments) should greatly enhance our understanding
of how regional temperature differ-
ences are maintained.
Whereas examination of the causes of regional
body temperature variation in reptiles will certainly
be enlightening, studies of the consequences
of regional temperature differences are
needed to further understand its adaptive significance
in reptiles. Although precise maintenance
of head temperatures is presumably important
for central nervous system function in
reptiles, tests of this assumption are required.
Investigations should include experiments to
determine the functional consequences of regional
temperature differences for processes
such as crawling, swimming, and tongue flicking
and experiments examining the ecological
consequences of regional temperature differ-
ences for behaviors such as prey detection, prey
91

92
M. E. DORCAS AND C. R. PETERSON
capture, and escape from predators. Given the
physical characteristics of snakes and the tractability
of many species for conducting both
laboratory and field investigations, it is clear
that studies of snakes can play an important role
in developing a deeper understanding of the
causes and consequences of regional temperature
differences in reptiles.
Acknowledgments.-We thank Jim Strawn and
Patty Strawn for allowing us to conduct much
of this research on their property and for
directly assisting us with many logistic details.
Michael McDonald assisted with making temperature
measurements of some snakes. Mark
Gerber allowed us to use his data on three
snakes measured while he was road cruising.
We thank J. Whitfield Gibbons, Justin D. Congdon,
John R. Lee, Jane K. Distler, Julian C. Lee,
and two anonymous reviewers for providing
useful comments on the manuscript. This research
was supported by awards from Sigma Xi,
the American Museum (Theodore Roosevelt
Memorial Fund), the Gaige Award of the American
Society of Ichthyologists and Herpetologists,
the Northwest Science Association, the
Chicago Herpetological Society, the Graduate
School and the Department of Biological Sciences
at Idaho State University, and a National
Science Foundation Doctoral Dissertation Grant
IBN-9224230 to M. E. Dorcas (C. R. Peterson,
sponsor). Data analysis and manuscript preparation
were supported by Contract DE-AC09-
76SR00819 between the U.S. Department of Energy
and the University of Georgia's Savannah
River Ecology Laboratory.
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Journal of Herpetology, Vol. 31, 31, No. 1, 1, pp. 93-98, 93-98, 1997
Copyright 1997 Society for the Study of Amphibians and Reptiles
Postmetamorphic Development of
Supernumerary Thyroid Glands in
Pleurodeles waltl
STEFANO GOZZO,1'4 ALESSANDRA TAGLIONI,' RITA CASET-
TI,1 CLAUDIO BAGNOLI,2 AND VINCENZO MONACO,3 'IS-
tituto di Medicina Sperimentale, Consiglio Nazionale delle
Ricerche (CNR), 2Laboratorio di Parassitologia, Istituto
Superiore di Sanita, and 3Dipartimento Ambiente, ENEA,
Rome, Italy.
During a study of histological material obtained
from Pleurodeles waltl, our group observed an unexpected
subdivision of thyroid tissue into more masses
than has generally been reported for other species of
amphibians (Gorbman, 1959; Gorbman and Bern,
1962; Gorbman, 1964; Norris, 1985a). In the present
study, a description of these supernumerary thyroid
aggregations of Pleurodeles waltl in various developmental
stages is given. Moreover, the histological reaction
of these structures to thiourea, a substance inhibiting
thyroid hormones, was investigated to verify
their reciprocal biochemical affinity in postmetamorphic
animals.
All the animals used in this study were collected
from a breeding stock of Pleurodeles waltl maintained
at the ENEA-Casaccia Center in Rome. The artificial
breeding of this species began with the importation
into Italy of 20 specimens from a locality near Granada
in Spain in 1985.
The larval stages were reared in an outdoor artificial
pond (8 x 6 x 1 m). They were extensively ex-
posed to sunlight and fed on Hyla tadpoles, insects,
worms, daphnia, and other crustaceans. After metamorphosis,
four During
groups of five animals each were
a study of histological material obtained
from Pleurodeles waltl, our group observed an unexpected
subdivision of thyroid tissue into more masses
than has generally been reported for other species of
amphibians (Gorbman, 1959; Gorbman and Bern,
1962; Gorbman, 1964; Norris, 1985a). In the present
study, a description of these supernumerary thyroid
aggregations of Pleurodeles waltl in various developmental
stages is given. Moreover, the histological reaction
of these structures to thiourea, a substance inhibiting
thyroid hormones, was investigated to verify
their reciprocal biochemical affinity in postmetamorphic
animals.
All the animals used in this study were collected
from a breeding stock of Pleurodeles waltl maintained
at the ENEA-Casaccia Center in Rome. The artificial
breeding of this species began with the importation
into Italy of 20 specimens from a locality near Granada
in Spain in 1985.
The larval stages were reared in an outdoor artificial
pond (8 x 6 x 1 m). They were extensively ex-
posed to sunlight and fed on Hyla tadpoles, insects,
worms, daphnia, and other crustaceans. After metamorphosis,
four groups of five animals each were
4
Present Address: Istituto di Medicina Sperimentale,
CNR c/o AMB-PRO-TOSS, ENEA Casaccia, S. P.
Anguillarese km 4
Present Address: Istituto di Medicina Sperimentale,
CNR c/o AMB-PRO-TOSS, ENEA Casaccia, S. P.
Anguillarese 1.3, 00060, Rome, Italy.
km 1.3, 00060, Rome, Italy.
and Ctenosaura hemilopha. Comp. Biochem. Physiol.
44A:881-892.
VINCENT, T. 1975. Body temperatures of Thamnophis
sirtalis parietalis at the den site. J. Herpetol. 9:252-
and Ctenosaura hemilopha. Comp. Biochem. Physiol.
44A:881-892.
VINCENT, T. 1975. Body temperatures of Thamnophis
sirtalis parietalis at the den site. J. Herpetol.
254.
WEBB, G. J. W., AND H. HEATWOLE. 1971. Patterns of
heat distribution within the bodies of some Australian
pythons. Copeia 1971:209-220.
C. R. JOHNSON, AND B. T. FIRTH. 1972. Headbody
temperature differences in lizards. Physiol.
Zool. 45:130-142.
WILKINSON, L. 1990. SYSTAT: the system for statistics.
Systat, Inc., Evanston, Illinois.
9:252-
254.
WEBB, G. J. W., AND H. HEATWOLE. 1971. Patterns of
heat distribution within the bodies of some Australian
pythons. Copeia 1971:209-220.
C. R. JOHNSON, AND B. T. FIRTH. 1972. Headbody
temperature differences in lizards. Physiol.
Zool. 45:130-142.
WILKINSON, L. 1990. SYSTAT: the system for statistics.
Systat, Inc., Evanston, Illinois.
Accepted: 30 October 1996.
SHORTER COMMUNICATIONS
93
placed in separate aquaria (40 x 30 x 20 cm) containing
10 L of water, renewed weekly, and through which
air bubbled. Two of the aquaria contained 0.16% of
thiourea, also renewed weekly; the remaining aquaria
were used for the controls. The animals were fed ad
libitum on strips of beef twice weekly. After one year,
these animals were killed and subjected to histological
analysis.
Ten newly hatched larvae, ten larvae aged 30 d, five
specimens at metamorphic climax, ten control postmetamorphic
specimens, and ten thiourea-exposed
postmetamorphic specimens were used for histological
studies. All the animals were anaesthetized in a humid,
ether-saturated box and fixed for ten days in
Dubosq-Brazil containing 37% formalin (Beccari and
Mazzi, 1972). Body weight, total body length, snout-
vent length, and the widest head size were measured
after fixation. The anterior regions of the body were
then removed, washed for two hours in tap water, and
decalcified for two days in a solution composed of 85
parts distilled H20, 10 parts 37% formalin, and 5 parts
formic acid. After decalcification, the pieces were
again washed for six hours in running tap water and
the picric acid was removed using a solution of 80%
alcohol and 10% ammonium acetate. The samples
were then dehydrated in alcohol, embedded in a mixture
of 80% paraffin, 16% stearic acid, and 4% white
beeswax, and sliced orthogonally to the animal's longitudinal
axis into 15 ,um serial sections. All serial sections
were stained with hematoxylin-eosin.
The control group and the thiourea-exposed animals,
one year after the metamorphosis, were compared
in order to identify differences due to the treatment
between body weight, total body length, snoutvent
length, and widest head size. Data were subjected
to one-way analysis of variance (ANOVA) to determine
significant differences between group values.
A differentiation of thyroid tissue into follicles was
not observed in the newly-hatched larvae of Pleurodeles
waltl. At the age of 30 d the larvae revealed two
large pyriform thyroid organs located in the lower jaw,
to the left and the right of the central musculature.
They displayed wide follicles mostly containing col-
placed
loid with vacuoles, and a high density of red blood
cells was observed within the interfollicular spaces.
in separate aquaria (40 x 30 x 20 cm) containing
10 L of water, renewed weekly, and through which
air bubbled. Two of the aquaria contained 0.16% of
thiourea, also renewed weekly; the remaining aquaria
were used for the controls. The animals were fed ad
libitum on strips of beef twice weekly. After one year,
these animals were killed and subjected to histological
analysis.
Ten newly hatched larvae, ten larvae aged 30 d, five
specimens at metamorphic climax, ten control postmetamorphic
specimens, and ten thiourea-exposed
postmetamorphic specimens were used for histological
studies. All the animals were anaesthetized in a humid,
ether-saturated box and fixed for ten days in
Dubosq-Brazil containing 37% formalin (Beccari and
Mazzi, 1972). Body weight, total body length, snout-
vent length, and the widest head size were measured
after fixation. The anterior regions of the body were
then removed, washed for two hours in tap water, and
decalcified for two days in a solution composed of 85
parts distilled H20, 10 parts 37% formalin, and 5 parts
formic acid. After decalcification, the pieces were
again washed for six hours in running tap water and
the picric acid was removed using a solution of 80%
alcohol and 10% ammonium acetate. The samples
were then dehydrated in alcohol, embedded in a mixture
of 80% paraffin, 16% stearic acid, and 4% white
beeswax, and sliced orthogonally to the animal's longitudinal
axis into 15 ,um serial sections. All serial sections
were stained with hematoxylin-eosin.
The control group and the thiourea-exposed animals,
one year after the metamorphosis, were compared
in order to identify differences due to the treatment
between body weight, total body length, snoutvent
length, and widest head size. Data were subjected
to one-way analysis of variance (ANOVA) to determine
significant differences between group values.
A differentiation of thyroid tissue into follicles was
not observed in the newly-hatched larvae of Pleurodeles
waltl. At the age of 30 d the larvae revealed two
large pyriform thyroid organs located in the lower jaw,
to the left and the right of the central musculature.
They displayed wide follicles mostly containing col-
loid with vacuoles, and a high density of red blood
cells was observed within the interfollicular spaces.