J. therm. Biol. Vol. 13, No. 3, pp. 135-142, 1988
0306-4565/88 $3.00 + 0.00
Copyright © 1988 Pergamon Press plc
Printed in Great Britain. All rights reserved
TEMPERATURE EFFECTS D U R I N G GESTATION
IN A VIVIPAROUS LIZARD
CAROL A . BEUCHAT
Department of Physiology, College of Medicine, University of Arizona, Tucson, AZ 85724, U.S.A.
(Received 22 August 1986; accepted in revised form 12 November 1987)
Abstract--1. The length of gestation of the viviparous lizard Sceloporusjarrovi is strongly dependent upon
the body temperature of the pregnant female.
2. Significantly more abnormal or dead offspring were born of pregnant females maintained at constant
temperatures of 26, 36 and 38°C than in the control group that was allowed to behaviourally
thermoregulate for 8 h'd -1 or in animals maintained at constant temperatures between 28 and 34°C.
3. Pregnant females allowed to thermoregnlate for 8 h. d-i had larger young than lizards maintained
at constant temperatures. Among animals kept at constant temperatures, neonate size declined with
temperature between 28 and 36°C.
4. Survivorship of adults did not vary among animals maintained at constant temperatures of 26-36°C
or in the control group, but animals that eventually died survived longer at cooler temperatures. No adult
animals survived constant exposure to 38°C.
5. Adult lizards at 28, 30 and 32°C and in the control group were able to maintain body mass, but those
at higher temperatures lost weight.
Key Word Index--Lizard; reptile; incubation; embryonic development; gestation; optimal temperature;
sex ratio; viviparity; development rate; incubation temperature; Scleporus jarrovi.
INTRODUCTION
The temperature at which reptilian embryos are
incubated can influence many aspects of development. Gestation generally proceeds more rapidly
at higher temperatures (Fox et al., 1961; Licht and
Moberly, 1965; Bustard and Greenham, 1968;
Vinegar, 1974; Sexton and Marion, 1974; Muth,
1980), but incubation temperatures that are too high
or too low can result in reduced viability of the young
(Blanchard and Blanchard, 1941; Licht and Moberly,
1965; Goode, 1966; Goode and Russell, 1968; Platt,
1969; Sexton and Marion, 1974) or abnormal morphologies (Fox et al., 1961; Fitch, 1964; Bustard,
1969; Vinegar, 1974; Burger et al., 1987). In several
groups of reptiles, even sex ratio can be highly
temperature dependent (see Bull, 1980 for review).
Because fecundity is a major fitness component,
natural selection should favour adaptations by female
lizards to ensure that the embryos are exposed to a
suitable range of temperatures during development.
In oviparous species, the thermal requirements of the
embryos, together with requirements for appropriate
soil water potential, should play a major role in nest
site selection (Muth, 1980). During incubation, it is
likely that microclimatic conditions will vary such
that the eggs are not exposed constantly to the
optimal temperature for development, but rather to
a range of temperatures that bound this value. The
timing of reproduction of a species, and even its
geographical limits of distribution, may ultimately be
determined by daily and seasonal variations in the
physical environment that might only transiently
exceed the limits of thermal tolerance of the eggs
(Muth, 1980).
135
In live-bearing reptiles, the impact of the thermal
environment on the embryos can be buffered by the
thermoregulatory behaviour of the pregnant female,
who should maintain a body temperature during
pregnancy that is not only appropriate for her own
physiological functions and ecological circumstances,
but is also as close as possible to that which will
produce the largest number of viable young in the
least amount of time. It would be ideal if the pregnant
female could behaviourally maintain a body temperature during pregnancy that is optimal for both
her own physiology and that of her embryos. However, numerous studies of adult reptiles have demonstrated that, within species, the optimal temperatures
for various physiological functions (e.g. digestion,
locomotion, etc.) can vary widely (Dawson, 1975;
Huey, 1982). As a consequence, reptiles may be
forced to maintain a body temperature that compromises among these multiple and conflicting optima.
During pregnancy in viviparous species, the thermal
requirements of the embryos are superimposed on the
multiple optima of the adult; if the optimum temperature for the embryos is not coincident with the
preferred body temperature of the pregnant female,
it could result in the need for additional compromise.
In numerous species of viviparous reptiles, females
maintain different body temperatures during pregnancy than at other times (Beuchat, 1986), suggesting
that the optimal temperature for development of the
embryos in these species is indeed different than the
body temperature normally preferred by adults
(Garrick, 1974; Ellner and Beuchat, 1984; Beuchat,
1986; Beuchat and Ellner, 1987). If this is the case,
these separate thermal optima for embryo and adult
should be demonstrable experimentally, and the tem-
CAROLA. BEUCHAT
136
perature maintained by a female during pregnancy
should be a compromise that maximizes fitness
(Ellner and Beuchat, 1984; Beuchat and Ellner, 1987).
This study examines the effects of temperature
during gestation on the embryos and adults of the
viviparous lizard Sceloporus jarrovi. The preferred
body temperature of non-pregnant adults of this
species is 34.5°C, but females maintain a temperature
of 32.0°C during pregnancy (Beuchat, 1986). This
shift in thermal preferendum during pregnancy
presumably reflects the presence of non-coincident
thermal optima for embryos and adult (Ellner and
Beuchat, 1984; Beuchat, 1986; Beuchat and Ellner,
1987). The temperature range most suitable for embryonic development is determined here by quantifying the effects of incubation temperatures between
26 and 38°C on the length of gestation, size of the
young, and their viability. The effects of temperature
are examined in the adults as well, in terms of their
survivorship and change in body mass. The data
obtained in this study have subsequently been used in
a quantitative test of the hypothesis that the body
temperature regulated by pregnant S. jarrovi is a
fitness-maximizing compromise between separate,
conflicting optimal temperatures for embryo and
adult (Beuchat and Ellner, 1987).
METHODS
Sceloporus jarrovi were collected in the Pinalefio
mountains of southeastern Arizona between 14
March and 15 April. Because this species is a fall
breeder, all adult females were pregnant at this time.
Mass, snout-vent length, and elevation of capture
were recorded for each lizard, and all individuals
were toe-clipped for identification. The animals were
divided into eight groups that randomly and evenly
distributed the three classes of animals (pregnant
females, adult males, and juveniles, both male and
female) and the six collection sites (at elevations of
1707, 1738, 1860, 2165, 2180 and 2895m) across
groups. Altitudinal differences in the timing of birth
(Ballinger, 1973) were compensated for by maintaining animals captured from low altitudes in March
and early April in a refrigerator until the start of the
experiment. Laparotomy of several animals from
each site verified that developmental stage was
reasonably uniform across all groups at the onset of
the experiment.
On 20 April, one of the eight groups was placed in
a large terrarium (60 × 60 × 130 cm) equipped with a
heat lamp on an 8L:I 6D photoperiod that permitted
behavioural thermoregulation. These conditions provide an approximation to those encountered by the
lizards in nature and, consequently, this group was
designated as the control. The animals in the remaining seven groups were placed in multiple 10 gallon
aquaria in constant-temperature cabinets maintained
( + 0.3°C) at one of seven temperatures: 26, 28, 30, 32,
34, 36 or 38°C. Crickets and water were provided ad
libitum, and the photoperiod was maintained at
8L: 16D. The animals were checked daily for deaths
and were weighed at weekly intervals. The aquaria
were inspected at frequent intervals each day for the
appearance of newborns, which were then immedi-
ately removed. For each of the offspring, the date of
birth, body mass, sex (males were distinguished by
the presence of a pair of enlarged post-anal scales),
and identification of parent when known were
recorded (the identity of the mother was known for
335 of the 521 young born in the experiment). In
addition, each newborn was categorized as: (1) alive
and normal, (2) alive but not normal, or (3) dead.
"Not normal" offspring included those that suffered
from obvious morphological abnormalities that most
commonly included lateral or vertical spinal
curvature, limb paralysis, or kinked tails. Some newborns, although appearing morphologically normal,
exhibited bizarre behaviour such as turning in circles,
and these were likewise classified as abnormal.
Midway through the experiment, the 36°C environmental chamber malfunctioned and all the animals at
this temperature died. Because data at this temperature were critical, additional animals were collected from the field between 15--20 June and divided
among the 32, 34 and 36°C boxes on 29 June. The
former two temperatures were included to provide a
basis of comparison against 36°C, as well as to check
for any differences between lizards collected in June
and those obtained earlier in the year. Because these
animals were only under the experimental regimen
for a few weeks before parturition occurred, they are
included only in the computations involving viability
of the embryos.
Statistical significance of discrete variables (e.g. sex
ratio, offspring viability) was determined using a
Chi-square; continuous variables (e.g. body mass,
length of gestation) were examined first using Analysis of Variance (ANOVA) followed, if significant, by
Tukey's multiple comparison test. For all tests,
differences among groups were judged to be significant at an alpha level of 0.05 or less. For discrete
variables that showed significant overall effects, pairwise comparisons were performed with the alpha
level adjusted using the Bonferroni technique. In
addition, contributions of individual cells to the total
Chi-square were determined by examining the adjusted residual associated with each cell.
Because the identity of the mother of approximately 35% of the newborn lizards was not known
(see above), it was necessary to determine if any of
the variables of interest varied among clutches in
order to use the offspring of unknown parentage in
the analyses. For offspring of known parentage, there
were no differences between clutches in sex, fate, or
body mass at birth. Therefore, all newborns, of both
known and unknown parentage, were pooled for
analysis.
RESULTS
Length of gestation
Among animals collected in March and April, date
of parturition was not affected by either site or date
of capture (excluding animals collected between 15
and 20 June, see "Methods"; one-way ANOVA,
P > 0.05), allowing pooling of these groups for the
subsequent analyses. The length of gestation (from
the beginning of the experiment until parturition),
Temperature effects during gestation in a lizard
1 0 0 -go
17 H e a t t h y
-
80
-
70
-
60
-
50
-
40
-
137
100
-~
o
w
86
~ Abnormat
40
38
80
110
[ ] Deed
100
53
O
34
36
38
I
I
I
eo
60
40
=.
30
=17~,
Centre[
-
26
28
30
32
T e m p e r a t u r e (*C)
Conlro("
26
2s
3o
~z
5~,
36
Fig. 2. Viability of S. jarrovi offspring as a function of
incubation temperature. At birth, the young were categorized as healthy (open bars), alive but apparently abnormal
(shaded bars), or dead (hatched bars). The graph depicts the
percentage of the total number of offspring at each temperature (indicated above each set of bars) that fell into each
category at birth. Only one female gave birth to an unknown
number of young (all stillborn) at 38°C.
3a
T e m p e r a t u r e (*C}
F i g . 1, T h e effect o f i n c u b a t i o n t e m p e r a t u r e o n l e n g t h o f
g e s t a t i o n in S. jarrovi. G e s t a t i o n l e n g t h w a s c o m p u t e d as t h e
number of days from 20 April, when the experiment was
started, to the day of birth. No data were available at 36°C
due to an equipment malfunction (see "Methods"). Indicated at each temperature are the mean, 5: I SD, and the
sample size.
varied from about 30-95 days and was significantly
influenced by incubation temperature (one-way
ANOVA, F6m = 74.7, P < 0.0001; Fig. 1). The length
of gestation was significantly longer at 26°C
( 8 8 . 5 d + 6 . 2 ; m e a n + S D ) than at any other
temperature, and in fact the period of embryonic
development was almost twice as long at 26°C as it
was at 28°C, just 2°C warmer (48.3d+3.8).
Embryonic development was most rapid at 34°C: the
length of gestation at this temperature (33.9 d + 4.1)
was significantly shorter than at any of the
temperatures below 32°C. Development of the
embryos in pregnant females that were allowed to
thermoregulate behaviourally took significantly
longer (57.7 d + 6.5) than it did in lizards maintained
at constant temperatures of 30, 32 or 34°C.
N o data for length of gestation were available at
36°C due to equipment malfunction (see "Methods"),
and only one animal gave birth at 38°C (see Survivorship of adults) with a gestation period about 8
days longer than the mean at 34°C.
Offspring sex ratio
Sex ratio o f the offspring was unaffected by site o f
capture, allowing data from all sites to be pooled for
analysis. There was a significant relationship between
sex ratio and temperature (Chi-square = 14.3, df = 6,
P = 0.026), but incubation temperature did not appear to influence sex ratio in any systematic manner
(Table 1): the sex ratio differed from that expected by
chance only at 28 and 36°C, where males were in
significant excess.
Offspring viability
Viability of the offspring did not vary with either
sex or site of capture (Chi-square, P > 0.05), but was
significantly affected by incubation temperature (Chisquare = 141.5, d f = 6, P < 0.0001; Fig. 2), The viability of the offspring of pregnant females that were
allowed to regulate the temperature of choice for
8 h ' d -] was very high: 95% of the young in the
control group were born with no obvious morphological or behavioural abnormalities. Comparably high viability (88-93%) was observed in the
young of animals maintained at constant temperatures from 28 to 34°C, in which the proportion
of viable young was greater than expected by chance.
Viability dropped sharply and significantly at constant temperatures above and below this range: more
than half of the newborns at 26 and 36°C were born
either dead or with abnormalities, and all o f the
young at 38°C were stillborn (although only one
female survived to give birth at this temperature; see
Survivorship of adults).
Offspring body mass
The average mass of neonates born to females in
the control group was 0.715g (+0.096, n =83;
Fig. 3), which is in close agreement with previously
published values for this species when maintained
Table 1, The effect of temperature on sex ratio of offspring of Sceloporus jarrovi
Temperature (°C)
Total
% Male
Ratio
Control
26
28
86
51.2
1.0
38
36.8
0.6
40
70.0
2.3*
1
30
80
50.0
1.0
32
104
49.0
1.0
34
100
46,0
0,9
36
38
52
65.4
1,9"
----
The total number of lizards that were born, the percent that were male, and the overall sex ratio
(male:female) are given for each group. The animals at 38°C were all dead at birth and were
not sexed. Those groups in which the sex ratio differed significantly from that of the control
group arc indicated by an asterisk.
138
CAROL A. BEUCHAT
0.9 r~
100
0.8 l~
v 0,7
33
~5
32 J
eo
22
6o
2
E 0.6 F
m
38
-
u)
)8 i 9 4 i 27
0.51--
Control 26
28 30 32 34
Temperoture (*C)
b_
#.
36
o
Contro~" 26 28 30
under similar conditions (0.72 g ___0.08, n = 95:
Beuchat et al., 1985; 0.718g+_0.076, n = 1 4 2 :
Beuchat et aL, 1986).
A three-way A N O V A of newborn body mass on
sex, viability (normal vs abnormal or dead), and
gestation temperature revealed that there were no
significant interactions among these variables
(P >0.05). Mean body mass pooled over all
experimental groups did not vary with sex of the
offspring (male mass = 0.660 g ___0.099, n = 227;
female mass = 0.663 _ 0.092, n = 220; Fl = 0.402,
P = 0.527), but it was significantly affected by both
viability (normal vs abnormal or dead; P = 0.049)
and gestation temperature (P <0.001). Newborn
lizards that were judged to be viable (i.e. there was
no evidence of the presence of any morphological,
physiological, or behavioural abnormalities) were
significantly larger than those that were either stillborn or born live but with some apparent abnormality (body mass: viable = 0.667 g + 0.091, n = 412;
not viable = 0.600 g +_ 0.122, n = 35). Multiple comparison tests among gestation temperatures indicated
that newborns born at 36°C were significantly smaller
(body mass = 0.56 g + 0.08; n = 27) than those in
any other group, whereas the offspring from mothers
that were allowed to behaviourally thermoregulate
during gestation were significantly larger (body
mass = 0.72 g + 0.09; n = 83) than any others except
those at 28°C (Fig. 3). There was a general trend of
decreasing body mass with increasing incubation
temperatures above 28°C; this trend, however, was
significant only between the young at 28°C and those
at 34 and 36°C.
Survivorship of adults
The temperature at which male and female adult S.
jarrovi were maintained during the experiment had no
effect on either growth or survivorship that was
dependent upon sex or reproductive condition
(comparisons by temperature of pregnant females
with males and non-pregnant females: Chi-square,
P > 0.05). Consequently, males, non-pregnant
females, and pregnant females were pooled for
subsequent analyses.
Survivorship of adult S. jarrovi varied with experimental temperature regimen (Chi-square=35.4,
H 2z_
32 34 :56 38
Temperature (*C)
38
Fig. 3. Variation in the body mass of S. jarrovi at birth as
a function of incubation temperature. Indicated for each
group are the mean (_+ 1 SD) and the sample size. All young
at 38°C were dead at birth and their masses were not
recorded.
16
h h
40
2o
I
31 30
19
Fig. 4. Survivorship of adult S. jarrovi under each of the
temperature regimes. Depicted for each temperature is the
percentage of all individuals (gravid females, non-gravid
females, and males) in that group that survived for the
duration of the experiment. The sample sizes are indicated
above the bar for each group.
d f = 7, P < 0.0001; Fig. 4). The highest survivorship
was observed in the control group, in which 82%
of the animals survived for the duration of the
experiment. Survivorship of animals maintained at
experimental temperatures between 26 and 36°C was
reduced somewhat, but not significantly, below that
in the control group, and these groups did not differ
significantly from each other (Chi-square, P > 0.05).
The lizards were markedly intolerant of 38°C: all
animals in this group died within an average of 18
days from the start of the experiment (Figs 4 and 5).
Survival time of those animals that eventually died
during the experiment was itself a function of temperature regimen (one-way ANOVA, F7,79 = 28.4,
P < 0.0001). Lizards survived the longest at the coolest experimental temperature: animals at 26°C lived
significantly longer than those at any other experimental temperature or in the control group, and
animals at 28, 30°C, and in the control group lived
longer than those at 36 and 38°C. All six animals that
died at 36°C were gravid females that had been
captured and added to the experiment in June (see
"Methods"), and these died significantly sooner than
animals maintained at 34°C.
80
i
12
7o
"~ 60
I
50
E
= 4o!
I
.~ 30
m
II
20
10
I
Contro
26
28
30 32
34 36
38
Temperature (°C)
Fig. 5. Survival time (number of days to death) of adult male
and female S. jarr~i that did not survive for the duration
of the experiment (see Fig. 4). Mean, 4-1 SD, and the
number of individuals that died are indicated for each
group.
Temperature effects during gestation in a lizard
Growth of adults
The change in body mass of adult lizards in the
experiment was significantly influenced by temperature (three-way ANOVA, F7 =4.8, P < 0.001),
sex of the individual (gravid female versus male or
non-gravid female, Ft = 15.7, P < 0.001), and
whether the individual died during the course of the
experiment (Fl = 20.1, P < 0.001), but there were no
significant interactions among these variables.
All of the animals in the experiment were maintained on an ad libitum diet of crickets and water
("Methods"). Lizards in the control group increased
in mass on this regimen by an average of 0.33% .d -~
where
% mass change.d -~ = 100 x m2 - m ~
m~
where m~ = mass at start of the experiment and
m2 = mass at termination of the experiment.
The % mass change/day of lizards at 26, 28, 30
and 32°C (-0.35, -0.11, 0.13 and - 0 . 3 7 % . d -1,
respectively) did not differ from that of the control
group. However, the change in mass of lizards at 34,
36 and 38°C was significantly different from that of
the control group and was negative, indicating a loss
of mass, in all cases. The greatest mass loss was
observed in animals at 38°C, in which body mass
declined by an average of 1.8% of initial body
mass.d-l; this was significantly greater than that
observed in all other groups except 36°C.
Independent of the effect of temperature regimen,
mass loss during the experiment was significantly
influenced by sex and reproductive status. Males and
non-gravid females lost significantly more mass
( - 0 . 7 9 % . d -I, n =50) than did gravid females
( - 0 . 2 3 % . d - J , n = 111). In addition, animals that
survived for the duration of the experiment gained
mass (0.08%. d -l) while those that did not lost mass
( - 1.14%,d-~).
DISCUSSION
As in other reptile species that have been examined
(see for example Muth, 1980), the temperature at
which the embryos of Seeloporus jarrovi are maintained during gestation has a marked effect on many
aspects of development. The length of gestation is
profoundly and non-linearly sensitive to temperature,
and it can vary nearly two-fold with a change in
temperature of as little as 2°C (Fig. 1). Although
development rate generally increases with incubation
temperature in reptiles, it may not be most rapid at
the highest incubation temperature compatible with
development. Eggs of Dipsosaurus dorsalis take
slightly but significantly longer to develop at 40°C
than at 36 or 38°C (Muth, 1980), and the more
limited data in this study are suggestive of a similar
trend in S. jarrovi (Fig. 1): although all of the
newborn S. jarrovi that were maintained at 38°C
during gestation (the highest temperature in this
study) were dead at birth, the gestation period at this
temperature was longer than that at 34°C, the next
lowest temperature for which data were available
139
(but not necessarily the temperature at which
development was most rapid).
Incubation temperature also has a profound effect
on the viability of reptilian offspring. Most S. jarrovi
(88-93%) born at temperatures between 28 and 34°C
were healthy, but viability dropped dramatically
at incubation temperatures only 2°C outside of
this range (Fig. 2). Eggs of a congeneric species,
S. undulatus, are similarly sensitive to incubation
temperature (Sexton and Marion, 1974): although
67-68% of the eggs hatch at 20 and 25°C, hatching
success drops to 46% at 35°C, and no eggs hatch
at an incubation temperature of 20°C or lower. In
D. dorsalis, hatching success is high (67-100%) over
a somewhat broader range of temperatures from 28
to 38°C (Muth, 1980). Eggs of that species will not
hatch only 2°C below this range (at 26°C), and both
hatching success and hatchling viability are severely
reduced at 40°C.
These and similar data for other species suggest
that the range of temperatures suitable for development of embryos of both oviparous and viviparous
reptiles is narrowly defined by the effect of temperature on viability. The optimum gestation temperature must fall within this range and should in
theory be the temperature at which all other
temperature-sensitive parameters are optimized or,
alternatively, that which achieves the best (i.e.
fitness-maximizing) compromise among these parameters if their optima are not coincident (Huey, 1982;
Beuchat and Ellner, 1987). For example, it could be
advantageous for the period of gestation to be as
short as possible, perhaps to minimize the amount of
time the mother spends pregnant or to afford the
young the longest possible growing season. In this
case, a pregnant S. jarrovi that maintains a constant
body temperature of 34°C would maximize development rate with no loss in fecundity. Further increases in body temperature might result in even
more rapid development, but only with a substantial
reduction in the viability of the young that are born
(Fig. 2). In S. jarrovi, there is an additional effect of
temperature on body mass of the neonates (Fig. 3)
such that neonates incubated at higher temperatures
during gestation are slightly smaller than those at
lower temperatures. The effect of birth mass on
fitness in this species is not known, but if we presume
that larger young have a selective advantage over
smaller young (due, for example, to larger fat stores,
lower risk of predation, or a larger range in prey sizes
that can be eaten), then an incubation temperature of
28°C might be preferable to any higher temperature.
If both length of gestation and birth mass are important components of fitness, the optimal gestation
temperature must compromise in some way between
these.
However, a clear conflict between the thermal
optima of adult and embryonic S. jarrovi, as would
be suggested by the data for body temperature regulation of pregnant adults, is not evident from a
cursory examination of these laboratory data. Adult
S. jarrovi that are not pregnant (both males and
females) have a preferred body temperature of about
34.5°C (Beuchat, 1986). Embryos maintained at 34°C
during gestation would have very rapid development,
high viability, and a birth mass that is 88% of that
140
CAROL A. BEUCHAT
under control conditions. Yet pregnancy in S. jarrovi
is accompanied by a shift in preferred body temperature to 32°C. If this adjustment in body temperature is an accommodation to the thermal requirements of the embryos during gestation, the
magnitude of the shift should be predictable from
quantitative information on the effects of temperature on the growth, survivorship, and fecundity
of the pregnant female. That is, life history theory
should allow prediction of the body temperature that
will maximize fitness by optimally compromising
among the potentially conflicting thermal demands of
the adult and embryo (Ellner and Beuchat, 1984).
Application of mathematical modeling techniques
using the data presented here and in other studies
verifies that the optimal temperature for gestation of
S. jarrovi embryos is indeed 34°C, but only if the
female can maintain this temperature precisely (i.e.
with a standard deviation about the mean of zero;
Beuchat and Ellner, 1987). Field data, however,
indicate that daytime body temperature is regulated
with a precision (1 SD) of about +0.9°C (Beuchat,
1986). Reptilian embryos might be able to tolerate
brief exposure to temperatures that, with longer
exposure, are detrimental (Fitch, 1964; Fitch and
Fitch, 1967). However, because viability of S. jarrovi
embryos is markedly reduced at temperatures above
34°C, females must regulate a body temperature low
enough that frequent excursions to the upper set
temperature do not result in an accumulated exposure that results in reduced viability. Incorporation
of information about thermoregulatory precision into
the model results in the prediction that pregnant
female S. jarrovi should maintain a body temperature
of 32°C, verifying that the shift in body temperature
during pregnancy is indeed a compromise to
accomodate conflicting thermal requirements of the
adult and embryo (Beuchat and Eilner, 1987).
The data reported here can be used to compute
temperature-specific development rates, and to compare these rates in animals exposed to constant or
cycling temperature regimes. For example, the gestation length of pregnant S. jarrovi maintained at
32°C, the preferred body temperature of pregnant
females in the field (Beuchat, 1986), averaged
39.7 days (from the start of the experiment until
parturition). Over the period of gestation, these
embryos were exposed to 32°C for a total of
953 h (39.7 d x 2 4 h . d - t ) . Assuming that 100% of
embryonic development occurs during this 39.7 d
period, the development rate (computed as
the amount of development that occurs per hour
as a percent of total development) at 32°C is
100%/953 h = 0.10%" h- t.
Similar temperature-specific development rates can
be computed for the animals in the control group that
were able behaviourally to maintain the temperature
of choice during the 8 h daytime period but had a
body temperature equal to room temperature at
night. Pregnant lizards regulate the same daytime
body temperature in the laboratory as they do in the
field (Beuchat, personal observation). Therefore, if it is
assumed that no significant embryonic development
occurs at night, the development rate computed for
the 8 h. d - l when the animals are thermoregulating is
100/[(57.7d) x ( 8 h ' d - l ) ] = 0 . 2 1 % ' h l, which is
about twice the rate estimated for animals maintained
at a constant temperature of 32°C. This discrepancy
might suggest that the temperature dependence of
embryonic development is influenced by the nature of
the thermal regime such that embryos maintained at
32°C for only part of the day develop faster while at
that temperature than those that experience that
temperature continuously. It is more likely, however,
that some development occurred in the control animals at night when they were at room temperature,
which was probably about 24°C. There are no data
for development rate of S. jarrovi embryos at 24°C,
but the amount of night-time development can be
very roughly estimated by assuming a night-time
temperature of 26°C and using the constant temperature data at that temperature. At 26°C, gestation
took an average of 88.5 d, and the embryos were
exposed to a total of 1416 h at this temperature. As
above, development rate can be calculated as
100%/1416 h = 0.07% of total development, h-~. If
under control conditions lizards had a body temperature of 26°C for 16 h.d -l, the amount of development that occurred at night can be estimated as
(57.7 d)× (16 h. d -1 ) × (0.07%. h -1) = 64.6% of total
development. The remainder of development (35.4%)
occurred during the 8 h photophase when the animals
were behaviourally thermoregulating, so the estimated development rate during the daytime is:
(35.4%)/((57.7 d) × (8 h - d - l ) ) = 0.08% "h -l. This estimate of development rate in lizards behaviourally
maintaining an average body temperature of 32°C for
8 h . d - l is slightly less than that computed for animals maintained at this temperature continuously.
However, because night-time temperature was probably lower than 26°C, these calculations overestimate
the night-time development rate and thereby underestimate daytime development rate. Using data for
length of gestation at 24°C would no doubt bring the
estimates of development rate at a body temperature
of 32°C under cycling and constant regimes into
closer agreement. In addition, pregnant females
behaviourally thermoregulating with a mean body
temperature of 32°C will actually experience body
temperatures that range from about 30-34°C
(Beuchat, 1986). Incorporation of information about
the periodicity of the oscillations in body temperature
into these computations would result in a more
accurate estimation of development rate during the
daytime.
Although this analysis required several assumptions, it suggests that development occurs at the same
rate at a given temperature, regardless of whether
that temperature is experienced constantly or as part
of a cyclic thermal regime. It also indicates that, for
S. jarrovi in lower altitude populations where nighttime temperatures are mild, the selection of a nocturnal retreat site that cools slowly at night (such as
a sheltered crack in a large boulder) could substantially shorten the length of gestation. Although
no data on sleeping-site selection are available for
S. jarrovi, there is evidence that other lizards may
select nocturnal retreats on the basis of their thermal
characteristics (Christian and Tracy, 1984).
The data in this study were collected by maintaining the experimental groups at constant temperatures. However, body temperatures of lizards
Temperature effects during gestation in a lizard
lection of far more information on the physiological
effects of temperature on reptiles than is currently
available.
®
c
t2
141
9
0
30
--I
C
O_
.;.
Controt
26
28
30
32
34
36
3e
Temperofure (oC)
Fig. 6. Change in body mass as a percentage of mass at the
start of the experiment in adult male and female S. jarrovi.
Mean, _+1 SD, and sample size are indicated for each
temperature.
usually vary diurnally with photoperiod and are
typically maintained at the "preferred" level by behavioural thermoregulation only during the part of
the day when the animal is active. At other times (e.g.
night-time for diurnal lizards), body temperature is
presumably not actively regulated but instead varies
passively with ambient temperature (Huey, 1982).
This photoperiodic variation in body temperature
even occurs in some lizards in the laboratory that
have continuous access to a heat source (Regal,
1967), and indeed it appears to be necessary for the
maintenance of health. Lizards kept continuously at
their preferred body temperature may suffer damage
to somatic or reproductive cells, or may simply fail to
thrive for reasons that remain obscure (Wilhoft,
1958; Licht, 1965). Although survivorship of adult S.
jarrovi was highest in the control group, it was not
significantly better than that of lizards under any of
the constant temperature regimes except 38°C
(Fig. 4). However, lizards died sooner and were more
likely to suffer a significant decline in body mass at
warmer constant temperatures (Figs 5 and 6).
The deleterious effects of constant temperatures on
the health of lizards are obvious but complex, and
applying data such as that presented here to problems
of animals in the field must be done with caution.
However, collecting data under more ecologically
appropriate thermal regimes by employing cycling
temperatures instead of constant temperatures in the
laboratory may be feasible but difficult. There is, first
of all, the obvious logistic difficulty of requiring
access to a large number of constant temperature
chambers (if all experiments need to be done simultaneously, as in this study), each of which has the
capacity for regulation of photoperiod as well as
diurnal cycling of temperature. In addition, the design of the most appropriate thermal regime is not
obvious. Should night-time temperatures drop to
room temperature, or to the temperature most typically experienced by animals in the field? Night-time
temperatures during the summer at the sites of low
altitude (c. 1900 m) populations of S.jarrovi are very
mild but at 2900 m could approach freezing. For this
species, the most appropriate night-time temperature
in a laboratory situation would be arguable, and its
selection could substantially alter the results of a
study. Greater sophistication in the design of such
temperature-effect experiments must await the colT.B. 13/3~-D
Acknowledgements--I am grateful to E. Braun for logistical
support, D. Vleck for assistance in the collection of data,
and R. Hagaman (Computer Systems and Biostatistics,
College of Medicine, University of Arizona) for performing
the statistical analyses. Financial support was provided by
grants from the National Science Foundation (DEB
8202880 and DCB 8510632), a fellowshipfrom the National
Institutes of Health (National Research Service Award
AM07063-03), and the Colgate University Research
Council.
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