Thermal responses to feeding in a secretive and specialized predator (Gila monster, Heloderma suspectum)

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Thermal responses to feeding in a secretive and specialized
predator (Gila monster, Heloderma suspectum)
C.M. Gienger
n
, C. Richard Tracy, Linda C. Zimmerman
Department of Biology and Program in Ecology, Evolution and Conservation Biology, University of Nevada, Reno, MS-314, Reno, NV, 89557, USA
article info
Article history:
Received 21 August 2012
Accepted 20 December 2012
Available online 2 January 2013
Keywords:
Thermoregulation
Body temperature
Lizard
Digestion
abstract
We investigate how a unique dietary specialist, the Gila monster (Heloderma suspectum), uses
behavioral thermoregulation to elevate body temperature (T
b
) after feeding. Lizards in a laboratory
thermal gradient were fed rodent meals of three different sizes (5, 10, or 20% of body mass), or sham fed
(meal of 0% body mass), and T
b
s were recorded for three days before feeding and seven days after
feeding. Gila monsters selected a mean T
b
of 25.2 1C while fasting (set-point range 23.6–27.1), and
increased T
b
s after feeding. The magnitude and duration of post-prandial T
b
increases are positively
related to meal size, and Gila monsters selected mean T
b
s up to 3.0 1C higher and maintain elevated T
b
s
for 3–6 days after feeding. Selection of T
b
does not appear to differ between day and night time periods,
and because the lizards are both diurnal and nocturnal (at different times of year), photoperiod may not
be an important influence on T
b
selection.
&2012 Elsevier Ltd. All rights reserved.
1. Introduction
The thermal biology of reclusive species is often difficult to
evaluate because individuals are hard to observe directly engaging
in thermoregulation, and because thermal trade-offs among different
behaviors (e.g., foraging, refuge-site selection, predator avoidance, and
reproductive activities) are usually intertwined (Blouin-Demers and
Weatherhead, 2001;Downes and Shine, 1998). Reclusive lizards can
often be dietary specialists (Huey et al., 2001;Pianka and Pianka,
1976) and specialized diets can lead to specific patterns of body
temperature (T
b
)variation(Pianka and Parker, 1975;Zimmerman and
Tracy, 1989). Species that are both reclusive and dietary specialists
might, therefore, be expected to have T
b
patterns that are influenced
by diet, as well as by the ecological and environmental factors that
dictate a reclusive and specialized lifestyle.
Gila monsters (Heloderma suspectum) are especially reclusive
lizards that spend nearly all the time hidden in underground refugia
(495% of time in some populations; Beck, 1990), even when
environmental conditions are suitable for above-ground activity. They
also occupy an unique dietary niche, and almost exclusively binge
feed on the eggs and altricial nestlings of ground-nesting vertebrates,
especially rodents and lagomorphs. Because of their specialized ‘nest-
predator’ diet, meals consumed by Gila monsters can be as large as
one-third of their body mass (Beck, 2005;Stahnke, 1950,1952), and
3 to 4 large meals may fulfill an individual’s entire annual energetic
needs (Beck, 1986;Beck and Lowe, 1994).
Here, we investigate how patterns of T
b
selection in Gila
monsters can be influenced by specialized diet and the consump-
tion of large vertebrate prey (relative to body size). Few lizard
species are able to specialize on vertebrate prey, and those that
do, such as some large varanids (Losos and Greene, 1988), tend to
be highly active and thermoregulate at a high and constant T
b
that
allows them to actively pursue, capture, and subdue prey
(Christian and Bedford, 1996;Christian and Weavers, 1996). Gila
monsters are therefore unique in that they are neither highly
active, nor particularly thermophilic (Beck, 2005).
However, after feeding, Gila monsters may become temporarily
thermophilic and increase T
b
to facilitate digestion. Feeding on in-tact
vertebrate prey, such as that observed in most snakes, is often
associated with a dramatic digestive response that includes increased
rates of post-prandial metabolism, protein synthesis, and nutrient
absorption (Secor, 2005,2009); all of these temperature-dependent
digestive processes likely function at a higher level with increased
body temperature (Karasov and Martı
´nez del Rio, 2007;Wang et al.,
2002). We therefore test the predictions that Gila monsters should
elevate T
b
after feeding, and that the magnitude and duration of
elevated post-prandial T
b
should be related to meal size, as larger
meals likely take longer to digest and pass through the body.
2. Materials and methods
2.1. Laboratory thermal gradient
Experiments to assess T
b
selection were conducted in a
thigmothermal gradient. An aluminum sheet (1 cm thick) was
fastened to a plywood box frame (6.1 1.2 0.6 m) from below,
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journal homepage: www.elsevier.com/locate/jtherbio
Journal of Thermal Biology
0306-4565/$ - see front matter &2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.jtherbio.2012.12.004
n
Corresponding author. Present address: Department of Biology and Center of
Excellence for Field Biology, Austin Peay State University, Clarksville, TN 37044,
USA. Tel.: þ1 9312217076.
E-mail address: giengerc@apsu.edu (C.M. Gienger).
Journal of Thermal Biology 38 (2013) 143–147

and divided into four lanes by three plywood dividers (61 cm
high 1.5 cm thick). All plywood surfaces were coated with
marine resin and sealed at joints with silicon sealant. A layer of
sand covering the aluminum base provided a substratum that was
changed between trials.
The gradient was cooled at one end by a recirculating chiller
pumping a 5 1C ethylene glycol solution through 0.75 cm dia-
meter copper tubing taped to the aluminum base along one-third
of the length of the gradient. The gradient was warmed at the
other end by heating strips (Omega Flexible Heaters SRFG-148/5)
taped to the underside of the aluminum base and spaced
at30 cm intervals. Each heat strip was wired to a solid-state
relay and temperature was maintained at þ/0.1 1C of a given
set-point by a feedback program written for a computer controller
datalogger (Campbell Scientific CR10X). Temperatures ranged
from 10 to 50 1C and changed linearly along the length of the
gradient at 11C per 16 cm.
Lighting was provided by overhead fixtures suspended 1.2 m
above the gradient surface. Ten 125 W (6400 K) full spectrum
light bulbs (Hydrofarm Inc., Petaluma, CA.) were evenly spaced in
two parallel rows of five bulbs. This arrangement provided an
average illumination of 1894 candella (SD7248) on the gradient
surface. Lighting was controlled to provide a 12:12 photophase:
scotophase cycle, which matched the photoperiods provided to
individuals in their cages between trials.
2.2. T
b
sampling
Body temperatures (T
b
) of 10 adult Gila monsters (mean
mass¼479 7115 g; 8 male and 2 non-gravid female) were
recorded using Thermochron ibutton dataloggers (Dallas Semi-
conductor). Each ibutton was calibrated against a NIST traceable
standard thermometer, and was attached to the chest of the lizard
directly over the heart using a 4 3 cm strip of 0.5 cm thick foam
insulation (Frost King, Thermwell Products, Sparks, NV). The
insulated datalogger package was further secured using medical
tape (Nexcare Absolute Waterproof tape, 3 M, St. Paul, MN)
wrapped around the circumference of the chest. The entire
datalogger package had a mass of 5 g, which was less than 2%
of the mass of each lizard.
To ensure that temperatures measured by ibuttons matched
internal T
b
, we compared ibutton recordings against cloacal
temperatures. We placed one Gila monster (with attached ibut-
ton) in each of the four lanes of the thermal gradient. A clear
plastic box (inverted) was placed over each lizard and T
b
was
allowed to equilibrate for 15 min. We then recorded internal T
b
using a Schultheis rapid-reading thermometer inserted 1.5 cm
into the cloaca. This procedure was repeated at different positions
in the gradient with substratum temperatures of 15, 20, 25, 30,
and 35 1C. The correlation coefficient between cloacal and ibutton
temperature was greater than 0.995 for each lizard (mean
slope¼1.0), indicating that ibuttons attached to the chest of Gila
monsters gave very close estimates of T
b
. In all experiments, T
b
s
were recorded every 15 min.
2.3. Feeding effects on preferred T
b
Food was withheld from lizards for two weeks prior to
initiating each experiment. After introducing individuals onto
the thermal gradient, they typically paced the entire length for
1–4 h before becoming settled and adopting a thermoregulatory
posture in which the ventral body surface was pressed against the
substrate. We considered that an individual was habituated to the
gradient after it was observed either sleeping or resting for six
consecutive hours without the exploratory pacing seen in newly
introduced individuals.
Once lizards habituated, we logged T
b
s for 72 h and then
randomly assigned each to one of four feeding treatments that
differed in meal size. Lizards were fed a meal of rat pups (Rattus
norvegicus) equivalent to 5, 10, or 20% of body mass (treatment
group), or were fed nothing (0% meal, sham control group). To
administer meals, each lizard was removed from the gradient,
placed in a clear plastic box, and fed (or sham fed) by hand. All
meals were initiated at 12 pm local time and all were completed
within one hour. After completing the meal (or sham), lizards
were placed back on the gradient and T
b
s continued to be
recorded for seven days. Lizards were then returned to their
home cages and allowed to rest for a minimum of two weeks
before repeating the procedure for each of the other feeding
treatments. The thermal gradient was cleaned between trials by
replacing the sand substrate and by wiping down gradient wall
surfaces with a dilute 5% bleach solution.
Daily means and standard deviations of selected T
b
s were
calculated for each individual in each combination of feeding
period (pre and post-feeding), meal size (sham, 5, 10, or 20%
of body mass), and photoperiod (photophase or scotophase).
We then used the general procedures of Hertz et al. (1993)
to estimate the preferred T
b
set point range as the bounds of
the central 50% of observed T
b
s for each individual in each
treatment combination. Thus, the lower and upper set points of
the preferred T
b
range are estimated by the 75% and 25% quartiles
of the distribution (respectively). Typically, the framework of
Hertz et al. (1993) is used to evaluate the preferred T
b
of
individuals in a laboratory thermal gradient where environmental
constraints on thermoregulation are assumed to be absent.
2.4. Statistical analyses
Because T
b
data often exhibit a skewed distribution (Dewitt
and Friedman, 1979), and fail to meet the assumptions
of parametric testing, we transformed data prior to analyses.
We attempted several data transformations (log, square-root,
inverse), but none yielded normal distributions. We, therefore,
conducted analyses on untransformed data, and because the
experiments were perfectly balanced (identical sample sizes
among treatments), violation of the normality and homogeneity
assumptions should have a small effect on the probability of Type
1 error (Refinetti, 1996). Repeated measures analysis of variance
(RM ANOVA) was used to determine differences in mean T
b
selection and thermoregulatory set-points as a function of feeding
state (pre- or post-feeding), meal size (sham, 5, 10 or 20%), and
time of day (photo- or scotophase). Post-hoc comparisons were
conducted using Fisher’s LSD.
3. Results
3.1. Effect of photoperiod on preferred T
b
Photoperiod did not affect T
b
regulation of animals maintained
on a 12:12 light:dark cycle. There was neither an overall effect of
photoperiod as a factor on mean T
b
in the full model (meal
size feeding state photoperiod; F
1,9
¼0.22, P¼0.65), nor was
photoperiod significant in the interactions with meal size
(F
3,27
¼0.29, P¼0.83), with feeding state (F
1,9
¼1.16, P¼0.31), or
with both (F
3,27
¼0.60, P¼0.44). Photoperiod was also not sig-
nificant as a main or interaction effect for T
set
lower or T
set
upper,
and was therefore excluded from all further analyses.
C.M. Gienger et al. / Journal of Thermal Biology 38 (2013) 143–147144

3.2. Effect of feeding and meal size on preferred T
b
While in a fasting (post-absorptive) state, Gila monsters on the
thermal gradient selected a mean T
b
of 25.270.6 1C and had a
set-point range of 23.670.9 to 27.170.4 1C (mean of individual
means for all lizards). There was a strong effect of both feeding
and meal size on all T
b
metrics used to compare 72 h pre-feeding
and 72 h post-feeding periods. Mean T
b
was significantly higher
after feeding than before (F
1,9
¼63.9, Po0.0001; Fig. 1) and it was
also significantly affected by meal size (F
3,27
¼9.39, Po0.0001);
the results are nearly identical for T
set
lower (F
1,9
¼30.3,
P¼0.0004; F
3,27
¼12.9, Po0.0001; Fig. 1) and T
set
upper
(F
1,9
¼32.2, P¼0.0003; F
3,27
¼4.2, P¼0.01; Fig. 1), for tests of
feeding state and meal size, respectively. The standard deviation
of T
b
was significantly lower after feeding than before (F
1,9
¼6.8,
P¼0.028; Fig. 2) and it was also significantly affected by meal size
(F
3,27
¼5.42, P¼0.005).
Interaction terms for feeding state meal size were significant
only for mean T
b
(F
3,27
¼3.3, P¼0.04) and T
set
lower (F
3,27
¼4.3,
P¼0.01), but the magnitude of the interaction effect was low for
both. Partial
o
2
, a measure of explained variance (Graham and
Edwards, 2001;Keren and Lewis, 1979), was 0.068 for mean T
b
and 0.079 for T
set
lower, indicating that each interaction
explained less than 8% of the variance in their respective models.
The duration that post-prandial Gila monsters maintained T
b
above the pre-feeding level varied with meal size (Fig. 3). The
sham treatment (0% meal) did not elicit an elevated T
b
response
(F
7,63
¼1.7, P¼0.13), and mean T
b
actually declined to the lowest
level of the experiment on day 7 post-sham, corresponding to the
cumulative period of three weeks since lizards had eaten a meal.
The 5% meal treatment gave a significant increase in T
b
overall
(F
7,63
¼3.12, P¼0.007), and T
b
was significantly higher for three
days post-feeding. Larger meals led to longer periods of elevated
T
b
post-feeding; both the 10% and 20% feeding treatments gave
significant overall responses (F
7,63
¼4.7, Po0.001; F
7,63
¼11.8,
Po0.001, respectively) and T
b
s were significantly higher for five
and six days after feeding, respectively (Fig. 3).
4. Discussion
4.1. Behavioral thermoregulation and influences on T
b
selection
Our goal was to investigate how the specialized feeding strategy of
Gila monsters, namely binge-feeding on large meals of vertebrate
prey, influences patterns of selected body temperature. After feeding,
22
24
26
28
30
Mean Tb
pre-feeding
post-feeding
22
24
26
28
30
0 5 10 20
Meal Size (% of Body Mass)
22
24
26
28
30
Tset
**
***
**
Tset
Fig. 1. Body temperature (T
b
) and thermoregulatory set-point responses to
feeding in Heloderma suspectum over four feeding levels (meal size as % of lizard
body mass) for 72 h pre-feeding and 72 h post-feeding. There is a significant effect
of both feeding and meal size on mean T
b
, as well as thermoregulatory set-points
(T
set
lower, and T
set
upper). Stars above pairs indicate significant differences
between pre and post-feeding (Fisher’s LSD). Values are mean of individual
means71 SE; N¼10 individuals for all.
1.0
1.5
2.0
2.5
3.0
3.5
Standard Deviation of Tb (°C)
0 5 10 20
Meal Size (% of Body Mass)
pre-feeding
post-feeding
*
Fig. 2. Standard deviation of body temperature (T
b
) in response to feeding in
Heloderma suspectum over four feeding levels (meal size as % of lizard body mass)
for 72 h pre-feeding and 72 h post-feeding. There is a significant effect of both
feeding and meal size on standard deviation of T
b
. Stars above pairs indicate
significant differences between pre and post-feeding (Fisher’s LSD). Values are
mean of individual means71 SE; N¼10 individuals for all.
C.M. Gienger et al. / Journal of Thermal Biology 38 (2013) 143–147 145

Gila monsters selected higher and less variable T
b
s than when fasting.
Presumably, selecting higher T
b
s allows lizards to improve digestion
by reducing passage time of the meal through the gut (Waldschmidt
et al., 1986), or by increasing digestive efficiency (Beaupre et al., 1993;
Harlow et al., 1976). Digestive efficiency of Gila monsters has been
reported to be 76.5% at constant T
b
of 27 1C(Beck, 1986)and90.6%at
29 1C(Wegscheider, 1998), suggesting that even modest increases in
T
b
, such as those observed in this study, could improve digestive
performance.
Although Gila monsters likely elevate T
b
following feeding to
improve digestion, they can also regulate digestive function
without changing T
b
. While being maintained at a constant T
b
of
30 1C, Gila monsters increase metabolism up to 4.9 times basal
levels after consuming rat meals equivalent to 10% of body mass
(Christel et al., 2007). Selecting elevated T
b
s, therefore, could work
interactively with physiological processes to optimize digestion
(Dorcas et al., 1997;Tracy et al., 2005). However, the benefit of
elevating T
b
to up-regulate digestive machinery after feeding is
likely governed by the size of the meal. A large meal (either 10 or
20% of body mass) was generally required to evoke a significant
increase in upper or lower thermoregulatory set-points (Fig. 1).
This suggests that selecting higher T
b
s after eating small meals
may not be necessary, because digestion can take place effectively
in the absence of a post-prandial T
b
increase, or that the metabolic
costs of elevating T
b
(Q
10
effects), may be more than the value of
the meal.
Digestive costs for Gila monsters, calculated as specific
dynamic action (SDA; Secor et al., 1994), are roughly 18% of the
energetic value of a meal when meal size is equivalent to 10% of
body mass (Christel et al., 2007). Research from other carnivorous
reptiles has shown that digestive costs can be considerable even
for small meals, and that digestive costs increase with meal size
(Secor and Diamond, 1997a,b). To process a meal, the digestive
organs and cellular machinery must be up-regulated from a
quiescent state when the gut is empty to a functioning state
when the gut is full. If the metabolic costs of a post-prandial T
b
increase are added to the SDA costs, along with the pre-feeding
costs of prey pursuit and consumption (Cruz-Neto et al., 2001;
Pough and Andrews, 1985), it could mean that eating small meals
would yield little net energy gain. This may partially explain why
Gila monsters are adapted to consume large meals, such as the
entire contents of prey nests. By consuming large meals, the
energetic return to Gila monsters may be large relative to the
digestive costs.
The T
b
selection of Gila monsters did not appear to be
influenced by time of day. Photoperiod is an important factor
influencing temperature selection in other lizard species
(Ballinger et al., 1969;Sievert and Hutchison, 1991;Tracy et al.,
2005), and this is likely related to voluntary ‘hypothermia’ (Regal,
1967). To save energy, some lizards seek cooler T
b
s at night when
predation risk is putatively lower, and there is less need to
maintain a high and constant T
b
for predator avoidance or escape
(Dawson, 1975). Digestion likely poses a limit to any voluntary
reduction in T
b
(Tracy et al., 2005), and with large meals, the
benefit of increasing digestive function by selecting warmer T
b
may outweigh the potential energy savings of reducing T
b
during
the night.
An alternative explanation might be that photoperiod is simply
not a strong environmental cue for temperature regulation in
nocturnal and secretive species, such as Gila monsters. Some species
of nocturnal geckos have little or no diel variation in preferred T
b
(Angilletta and Werner, 1998), yet other diurnal species routinely
show strong day and night differences (Firth and Belan, 1998;Firth
et al., 1989;Tracy et al., 2005). While diurnal species may translate
photoperiodic cues using the pineal complex and its regulatory effects
onmelatoninproductionandT
b
selection (Lutterschmidtetal.,2003;
Ralph et al., 1979), nocturnal and crepuscular species may not be as
sensitive to cues from photoperiod in regulating circadian processes
(Ellis et al., 2006;Hyde and Underwood, 2000). This hypothesis is
supported by the observation that Gila monsters are ‘‘poor time-
keepers’’ (referencing their circadian patterns) and show no differ-
ences in activity under constant light or constant dark conditions
(Lowe et al., 1967).
While Gila monsters select higher T
b
s after feeding, many
reptiles do not. Preliminary reviews by Sievert (1989) and
Touzeau and Sievert (1993) suggest that only about half of the
species tested show significant elevation of T
b
after feeding. Many
factors may obfuscate the ability to detect a significant post-
prandial thermophilic response, including meal size, meal com-
position, and feeding frequency. Clearly, more work is needed to
01234567
Time Post-Feeding (days)
22
24
26
28
30
22
24
26
28
30
22
24
26
28
30
22
24
26
28
30
0%
5%
10%
20%
***
*****
******
Tb(°C)
Fig. 3. Mean body temperatures (T
b
)ofHeloderma suspectum prior to (day 0) and
following feeding for each of four meal size treatments; meals equal to 0 (sham
treatment), 5, 10, or 20% of lizard body mass. Values are mean of individual means
(71 SE) for each combination of meal size and day post-feeding. N¼10
individuals for all. Dashed line is grand mean of pre-feeding T
b
s. Stars indicate
days in which T
b
was significantly elevated (Fisher’s LSD) above the pre-feeding
baseline.
C.M. Gienger et al. / Journal of Thermal Biology 38 (2013) 143–147146

explain patterns of postprandial thermophily in the context of
variation in species’ diets.
We have shown how the specialized feeding strategy of Gila
monsters, binge-feeding on large meals of vertebrate prey, can
lead to shifts in patterns of preferred T
b
. Gila monsters use
behavioral thermoregulation to regulate T
b
, and preferred T
b
changes with digestive state and meal size. By selecting higher
T
b
after feeding, both gut passage rate and digestive efficiency
could be increased, thereby reducing the time in which Gila
monsters would be physically encumbered by a digestive tract
full of food and more vulnerable to predation.
Acknowledgments
Research was supported by the Biological Resources Research
Center, Department of Biology, and Program in Ecology, Evolution
and Conservation Biology at the University of Nevada, Reno. Care
of animals and experimental procedures were approved by
the UNR Institutional Animal Care and Use Committee (protocol
A06/07-34). We thank the Zoological Society of San Diego for
providing experimental animals used in feeding trials. Dan Beck
provided useful advice and discussion on the thermal biology of
Gila monsters. John Gray, Scott Hampton, and Ken Nussear
provided logistic and technical support in the lab. An early draft
of the manuscript was improved by comments from Dan Beck,
Jack Hayes, Jill Heaton, and Scott Mensing.
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