Cloacal evaporative cooling: a previously undescribed means of increasing evaporative water loss at higher temperatures in a desert ectotherm, the Gila monster Heloderma suspectum
Department of Biology, Arizona State University, Tempe, AZ 85287-4501, USA
* Author for correspondence (e-mail: denardo{at}asu.edu)
Accepted 31 December 2003
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Summary |
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Key words: evaporative water loss, temperature, reptile, cloaca, cutaneous evaporation, ventilatory evaporation, lizard, Gila monster, Heloderma suspectum
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Introduction |
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In addition to having limited capabilities for internal heat production,
ectotherms are thought to have limited physiological mechanisms for
significantly reducing Tb when environmental temperatures
are high (Schmidt-Nielsen,
1964). Evaporative water loss (EWL) represents the predominant
means by which any organism can cool its body when Ta
exceeds Tb. Not surprisingly, then, EWL has been shown to
be critical to thermoregulation in endotherms (for reviews, see
Dawson and Bartholomew, 1968
;
Calder and King, 1974
).
However, EWL of ectotherms is rarely investigated in terms of its potential
for suppressing body temperature. Instead, it is widely accepted that the only
means by which reptiles can lower Tb is to move to a
cooler environment such as a burrow.
While EWL could provide a means for reptiles to reduce
Tb when Ta exceeds
Tb, EWL is typically viewed merely as a detriment to water
balance (for a review, see Mautz,
1982a). Reptiles living in arid environments tend to have reduced
EWL compared to more mesic species, and this low EWL rate is considered to be
an adaptive response to xeric conditions
(Cohen, 1975
; Mautz,
1982a
,b
;
Dmi'el, 1998
,
2001
). While seldom studied,
the use of EWL for thermoregulation by ectotherms has been reported in several
species. Cicadas can effectively reduce Tb below
Ta by actively increasing cutaneous EWL
(Toolson, 1987
). Additionally,
some arid-environment lizards increase EWL by panting at thermally challenging
temperatures (Templeton, 1960
;
Dawson and Templeton, 1963
;
Warburg, 1965
;
Crawford and Kampe, 1971
).
Gila monsters Heloderma suspectum are relatively large, active
foraging lizards of the Sonoran Desert of Arizona and northern Mexico. Single
foraging bouts can cover considerable distances (in excess of 1 km) over an
extended period of time (12 h or more) in search of vertebrate nests, the
contents of which comprise their diet
(Bogert and Del Campo, 1956;
Beck, 1990
). The Sonoran Desert
summer consists of two distinct climatic seasons. From mid-April through
mid-July, the Sonoran Desert is hot (daytime high temperatures of
3545°C) and dry (no rainfall). However, a summer rainy season
commences in approximately mid-July and extends into mid-September. During
this summer rainy season, temperatures remain high but there is a relatively
reliable, albeit limited, rainfall (approximately 10 cm). While Gila monsters
are predominantly crepuscular or nocturnal during the summer to avoid peak
temperatures, air temperatures frequently exceed 40°C at sunset and remain
warm throughout much of the night. Requiring lengthy surface activity in an
environment that is hot and dry for several consecutive months suggests that
Gila monsters should have low cutaneous evaporation to benefit water balance.
Nevertheless, Gila monsters are said to have `leaky skin'
(Lowe et al., 1986
;
Brown and Carmony, 1991
),
though published data in support of this contention are lacking. From the
perspective of water balance, leaky skin in a xeric environment is maladaptive
because it increases the rate of desiccation
(Brown and Carmony, 1991
).
Consequently, the purported existence of leaky skin is used as evidence to
support the hypothesis of a tropical origin for Gila monsters
(Lowe et al., 1986
).
Since EWL rates of Gila monsters have physiological, ecological, and even
evolutionary implications, we examined evaporative water flux in this species.
In addition to measuring total EWL, we investigated the relative contribution
by the skin and other potential routes of water loss. We designed a means by
which we could partition cutaneous, ventilatory and cloacal EWL. We use the
term `ventilatory' to refer to evaporation occurring from the buccopharyngeal
epithelia, whether or not such evaporation is being enhanced by breathing.
While cloacal EWL has not previously been described, we considered it a viable
means by which water could be evaporated from the body. While usually confined
within the body cavity, the mucous membranes of the cloaca can be exposed to
the environment through the vent (with or without eversion; D. F. DeNardo,
personal observation). Furthermore, water permeability of the lizard cloaca
has been demonstrated in the context of post-renal concentration of urine
(Braysher and Green, 1970).
While previous studies of EWL in reptiles have neglected or intentionally
prevented cloacal EWL (for a review, see
Mautz, 1982a
), we chose to
examine this mucosal surface as a possible route for EWL.
We hypothesized that EWL could provide thermal advantages to an actively
foraging ectotherm that inhabits a hot, arid environment. Evaporation would be
especially advantageous if there were a fairly predictable water resource. In
fact, despite living in an arid environment, cicadas are able to invest large
volumes of water into EWL because of their high tolerance of desiccation
(Toolson, 1987) and their
ability to regularly obtain water from the xylem of bushes
(Cheung and Marshall, 1973
).
The predictable late summer rains of the Sonoran Desert provide a water
resource to replenish water expended during the dry spring and early summer
months. Additionally, the Gila monster possesses a large urinary bladder that
might serve as a water reservoir during extended dry periods, as it does in
the desert tortoise Gopherus agassizii
(Dantzler and Schmidt-Nielsen,
1966
; Minnich,
1976
). Therefore, we predicted that Gila monsters would have a
relatively high EWL rate and that elevated water flux would be especially
apparent at thermally challenging temperatures, when hyperthermia would be
more of an immediate physiological threat than dehydration. We further
predicted that, by providing a mechanism for shedding body heat, high EWL
rates would allow the animal to maintain sub-ambient Tb,
at least in the short term. Lastly, since water is especially critical during
dehydration, we predicted that dehydration would lead to a reduction in
EWL.
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Materials and methods |
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Body surface area was estimated by representing the animal as a collection of simple geometric volumes. We made actual body measurements that allowed us to calculate the surface areas of the geometric constituents: a square pyramidal frustum (the head), five right regular cylinders (the body and four limbs), and a right circular cone (the tail). Estimated whole body surface areas were between 622 and 958 cm2.
Experimental apparatus
Ambient temperature was maintained throughout trials by housing the test
chamber in an environmental chamber fitted with an electronic temperature
controller (Omega Engineering CN2011, Stamford CT, USA). The test chamber was
thus a chamber within a chamber, and it experienced very little thermal
oscillation throughout trials (Ta was maintained at
±0.2°C during a given trial and ±0.5°C among
trials).
We partitioned EWL into two components (head and body) by placing Gila monsters individually into a two-compartment test chamber fitted for separate flows of air into and out of the compartments. The test chamber was custom-made to fit the test species, thereby minimizing the time for turnover of air and maximizing the temporal resolution of our hygrometric measurements. The chamber was constructed almost entirely of borosilicate glass (Pyrex), because glass is minimally hygroscopic, and it allowed for continuous visual monitoring of the test animal using an infrared camera connected to a remote monitor. The overall geometry of the test chamber was a horizontally placed, right circular cylinder (overall length 52 cm, inside diameter 9.5 cm) with closed, flat ends. To allow for partitioning, the main cylinder consisted of two open-ended cylinders of unequal length (body compartment: 39.5 cm long, 2800 ml volume; head compartment: 12 cm long, 850 mlvolume). A two-part neck stock composed of aluminum plate was attached perpendicularly to a horizontal base and served to safely hold the venomous lizard in place while the investigator installed the compartments and thereafter during trials. Attached to the open end of the head compartment was a latex sheet (#07315 Heavy Dental Dam, Hygenic, Akron, OH, USA) perforated with an elliptical hole (17 mm x 21 mm) through which the head was passed. With the animal in place, the cylinders were clamped against the stock using a bar clamp. A closed-cell foam gasket formed a seal between the body compartment and the stock. The compliant latex sheet sealed the head compartment and prevented mixing of air between compartments even if the animal moved. The lack of mixing of air between the head and body chamber was verified during test trials that delivered 100% saturated air into one chamber without causing any change in dewpoint in the other chamber.
Each compartment was fitted with three threaded, borosilicate glass hose connectors (#7 Chem-Thread, Chemglass, Vineland, NJ, USA). Two connectors accepted non-hygroscopic tubing (Bev-A-Line, Thermoplastic Processes Inc., Stirling, NJ, USA) for both influent and effluent air. The third hose connector served as a port for passage of type T (copperconstantan) thermocouple cables, permitting continuous recording of animal temperatures and ambient temperatures. A small, outward leak at the thermocouple port, required to allow for play in the cables, allowed us to equalize pressures between compartments (a higher flow rate was used in the body compartment). The leak did not affect the sub-sampled effluent in our positive-pressure setup, and equalization of pressures further reduced the chance of mixture of air between compartments.
Influent air was first passed through an industrial purifier
(#PCDA11129022, Puregas, Denver, CO, USA) that removed carbon dioxide and
water vapor. Dried air was sent through a manifold to supply separate air
lines for each of the compartments. Mass-flow controllers (#FMA-A2406 and
#FMA-A2409, Omega Engineering, Stamford, CT, USA) were placed in the air lines
upstream of the compartments to maintain separate and constant influxes (head:
1000 ml min1; body 4000 ml min1). We
calibrated the mass-flow controllers for the experimental air mixture (dry and
CO2-free) using soap film flow meters, and we generated calibration
curves describing STP (standard temperature and pressure)
volumetric flow (ml min1) as a function of electrical
potential difference (mV). At the flow rates selected, the air in the head and
body compartments underwent 99% turnover
(Lasiewski et al., 1966) every
3.4 and 3.2 min, respectively.
Each compartment's effluent was sent to its own hygrometer (#RH100, Sable Systems, Las Vegas, NV, USA) and then vented to the room. The hygrometers were calibrated with bottled nitrogen (zero gas) and experimental air that was bubbled through three serially placed columns of distilled water, each approximately 150 cm deep, before being sent individually to the hygrometers (span gas). A copperconstantan thermocouple measured the water temperature in the columns, and each hygrometer was individually heated to be warmer than the water, thus preventing condensation. The hygrometers were set to output dewpoint and were adjusted so that the dewpoint reading equaled the water temperature. We verified the linearity of the hygrometers and the veracity of the calibrations by later sending air through the columns when the water was comparatively cooler, and the hygrometers indicated the correct (and lower) dewpoints. The hygrometers remained powered throughout the entire experiment to minimize calibration drift, and calibrations were checked occasionally and readjusted when necessary. While the hygrometers showed little or no drift, we minimized the effects of any drift by calculating evaporative fluxes based on elevations in dewpoint above separate baseline values obtained by flowing air through the sealed, empty compartments before each trial. Measurements were sampled every second and averaged every minute by a computer-interfaced datalogger (CR23x, Campbell Scientific, Logan, UT, USA) that received inputs from five thermocouples, two mass-flow controllers, and two hygrometers.
Experiment 1: Effects of Ta on EWL
In order to monitor Tb throughout the experimental
trials, each of six lizards (mean body mass 606±26.8 g) wasimplanted
with a thermocouple array. Each array consisted of three 30-gauge, type T
thermocouple cables (#TT-T-30-SLE, Omega Engineering) extending from three
(two male, one female) subminiature connectors (#SMP-W, Omega Engineering). To
prevent injury to the animal, the thermocouples terminating the long cable and
one of the short cables were thinly covered with pourable rubber coating
(Plasti-Dip, PDI Inc., Circle Pines, MN, USA).
With the animal under isoflurane anesthesia, an approximately 1 cm incision was made ventro-laterally in the abdominal region. From the incision site, a metal trocar was routed subcutaneously until it was exteriorized on the dorsum at mid-body. The two thermocouples coated with Plasti-Dip were inserted from the dorsum retrograde into the trocar. The trocar was removed, leaving the short thermocouple situated subcutaneously at the back. The body wall was punctured at the superficial ventro-lateral incision site, and the long thermocouple was placed 1 cm deep into the body cavity and sutured to the body wall. The array was triply sutured to the skin where it emerged on the dorsum to keep it in place and reduce tension at the dorsal incision site. Both the dorsal and ventro-lateral incisions were closed with everting mattress sutures (3-0 Vicryl, Ethicon, Somerville, NJ, USA). The third thermocouple was attached to the skin surface directly superficial to the subcutaneous thermocouple using cyanoacrylate glue and then covered with a thin coating of Plasti-Dip. When connected to the datalogger, these three thermocouples could provide continuous measurements of core body, subcutaneous, and skin temperatures. Because of the failure of several subcutaneous and skin thermocouples, only core Tb results are reported here. Each animal was given at least 3 days to recover from surgery prior to participating in the experiment trials.
Each Gila monster was tested once at each of five ambient temperatures
(approximately 20.5, 30.0, 35.0, 37.5 and 40.0°C). Ta
= 30°C approximates the body temperature selected by Gila monsters in a
laboratory thermogradient (29.4°C;
Bogert and del Campo, 1956) as
well as the mean Tb obtained from free-ranging Gila
monsters (29°C; Lowe et al.,
1986
; 28.5°C, Beck,
1990
), while the other temperatures lie near or beyond the
extremes of the species' active Tb range
(2437°C; Beck,
1990
). Animals were used only when they were not undergoing or
about to undergo ecdysis, as ecdysis can affect EWL. Trials for an individual
were separated by at least 24 h, and the five treatment temperatures were
randomized. Animals were moved from the housing room to the environmental
chamber and allowed at least 2 h to adjust to the trial temperature. Based on
pilot tests, this time was sufficient for Tb to stabilize
while the animal was kept in the new thermal environment. During this
stabilization time, air was flowed through the sealed but empty compartments
to obtain baseline compartment air temperatures and dewpoints. Compartment
vapor densities calculated from the baseline dewpoints were subtracted from
vapor densities calculated from dewpoints during the experimental trial, and
the resulting differences (along with flow rates and body mass) were used to
determine EWL (see `Calculations' below).
Animals were then placed in the partitioned chamber for at least 40 min to allow them to adjust to the new environment and for stabilization of dewpoints and body temperatures. The three body temperatures, ambient temperatures of the two compartments, and separate dewpoints of air flowing over the head and air flowing over the rest of the body were recorded for 20 min while the animal was at rest. Upon collection of these data, a cotton wad was placed in the cloaca, and an H-shaped piece of latex was tied around the hind limbs to cover the vent. This `diaper' prevented moisture from leaving the cloaca, while minimally impeding integumentary evaporation (the diaper covered approximately 1% of the animal's total surface area). After being fitted with the diaper, the animal was returned to the test chamber and a second set of data was collected in the same fashion as the original set. For any trial in which moisture (e.g. urine) was visible on the animal or the walls of the chamber during or at the end of the trial, the data were discarded and the trial was repeated at a later time. The presence of such liquid was also easily detectable as a rapid rise on the plot of body chamber dewpoint.
Experiment 2: Effects of dehydration on EWL
We recorded the mass of six adult Gila monsters not used in experiment 1
(mean body mass=520±27.9 g) and then deprived them of food and water
for 610 weeks, until they reached approximately 80% of initial mass.
Six additional adult Gila monsters (mean body mass=523±29.5 g) were
provided water ad libitum but no food for 10 weeks. We were thereby
able to assess the fraction of mass-loss attributable to energetic demands
(catabolism), rather than to dehydration. To assess the effect of dehydration
on serum osmolality, a blood sample was collected from the caudal vein of each
animal after the 610 week period. We centrifuged the samples and stored
the serum in sealed tubes at 80°C for later analysis. We measured
serum osmolality twice for each sample with a vapor pressure osmometer (#5500,
Wescor, Logan, UT, USA) that we calibrated immediately prior to measurements
using standard solutions (290 mmol kg1 and 1000 mmol
kg1; Wescor).
The six dehydrated Gila monsters underwent experimental trials similar to that of experiment 1, except that animals were not implanted with thermocouple arrays, and trials were limited to 37.5°C and 40°C. Imposing these limitations allowed for much faster completion of the trials (to minimize the duration of the dehydrated state) while still providing valuable data for assessing the effect of dehydration on EWL at the most thermally challenging temperatures.
Calculations
For each trial, we determined values for dewpoint and temperature by
calculating the mean values over a 5 min period near the end of the trial when
values were nearly constant. We used dewpoints to calculate
ambient-temperature vapor pressures using an eighth order polynomial
describing saturation vapor pressure as a function of air temperature
(Flatau et al., 1992). Vapor
pressures were used to calculate ambient-temperature vapor densities using the
Ideal Gas Law (Campbell and Norman,
1998
). Finally, evaporative fluxes (mg min1)
were calculated by multiplying vapor density (mg ml1) by ATP
(ambient temperature and pressure) rate of flow of air (ml
min1) for each of the two compartments. We calculated
absolute evaporative flux (mg H2O h1) as well as
fluxes relative to both mass (mg H2O g1
h1) and surface area (mg H2O
cm2 h1) to account for variation in size
between individuals. We assumed that a portion of the water vapor appearing in
the head compartment was attributable to evaporation from the cranial
integument (skin and conjunctivae) and that evaporative flux from the skin of
the head equaled that from the skin of the body. We further assumed that,
despite the probably greater evaporative flux from the moist eyes than from
the dry skin, the small size of the eyes compared to the head made the
absolute increase negligible. We therefore estimated the non-ventilatory
component of the flux occurring in the head chamber based on the surface area
of the head and on the area-specific value for evaporative flux from the skin
in the body compartment during the diapered trial. The resulting
non-ventilatory, head-chamber component was then subtracted from the total
head-chamber flux to yield ventilatory flux, and it was added to the
body-chamber flux to yield non-ventilatory flux. Finally, non-ventilatory flux
during the diapered trial was subtracted from non-ventilatory flux during the
non-diapered trial to yield cloacal flux, and non-ventilatory flux during the
diapered trial was taken to be cutaneous flux. Lastly, for experiment 1 we
assessed the ability of Gila monsters to physiologically thermoregulate by
subtracting the mean air temperature of the body compartment from the mean
core Tb during each trial.
Statistical analysis
We used StatView (version 5, SAS Institute, Cary, NC, USA) for all
statistical analyses. For experiments 1 and 2, we used repeated-measures
analyses of variance (R-M ANOVA), with Ta and cloacal
patency as within-subjects factors, and either Tb or water
flux as the dependent variable. To compare EWL rates of hydrated animals in
experiment 1 with dehydrated animals in experiment 2, we used R-M ANOVA with
hydration as the between-subjects factor, Ta as the
within-subjects factor, and water flux as the dependent variable.
Post-hoc comparisons were made using paired Student's
t-tests adjusted for an experimentwise Type 1 error rate of 0.05. The
adjusted alpha for controlling Type 1 experimentwise error was
0.05/N, where N = the number of sampling periods (i.e.
=0.01 and
=0.025 for experiments 1 and 2, respectively).
Osmolality results were analyzed using a Student's t-test. All values
are presented as means ± S.E.M.
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Results |
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Increasing Ta led to a significant increase in both cutaneous and cloacal, but not ventilatory, evaporative fluxes (cutaneous: F4,5=10.27, P=0.0001; cloacal: F4,5=21.34, P<0.0001; ventilatory: F4,5=2.38, P=0.086, Fig. 1, Table 1A). Cutaneous flux showed a relatively constant increase throughout all trial temperatures (Q10=1.61), while cloacal flux was low and relatively constant between 20.5°C and 35°C, but rose dramatically above 35°C (Q10=8.3x107).
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Trial temperature affected the difference between chamber temperature and Tb, with increasing chamber temperatures leading to a greater suppression of Tb below chamber temperature (F4,5=27.90, P<0.0001; Fig. 2). While applying the diaper consistently reduced the degree of temperature suppression at all higher temperatures, the lack of an effect at lower temperatures led to no overall effect of diaper application on temperature suppression (F1,5=2.57, P=0.14). However, the interaction between chamber temperature and diaper application approached, but failed to reach, statistical significance (F1,5=2.39, P=0.067).
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Experiment 2
Restricting food and water to six experimental animals for 610 weeks
led to a significantly greater loss in body mass compared to animals provided
with no food but free access to water (water-deprived: 78±1% of initial
body mass, range 7581%; ad libitum water: 95±2%, range
87101%; P<0.0001). Furthermore, serum osmolality of the
water-deprived Gila monsters was significantly higher than that of the animals
provided water ad libitum (water-deprived: 603±7 mOsm
kg1 H2O; ad libitum water:
487±37 mOsm kg1 H2O; P=0.013).
Combined, these results demonstrate that the majority of mass lost in the
experimental group was water, and, although the degree of dehydration is not
quantifiable, the water-deprived animals were considerably dehydrated.
As in experiment 1, Ta had a significant effect on EWL in both the head and body compartments for the dehydrated Gila monsters (head: F1,5=51.50, P<0.0001; body: F1,5=14.30, P=0.0036). Also, similar to the results of experiment 1, applying the diaper had a significant effect on EWL in the body compartment (cloacal patency main effect: F1,5=8.44, P=0.016; cloacal patency x Ta: F1,5=10.03, P=0.010), but not the head compartment (cloacal patency main effect: F1,5=0.13, P=0.72; cloacal patency x Ta: F1,5=0.37, P=0.56). Post-hoc tests indicate that significant results from the body compartment were due to a diaper-induced reduction in EWL at 40°C (P=0.021).
Increasing Ta had a positive effect on all fluxes (cutaneous: F1,5=7.56, P=0.040; cloacal: F1,5=10.67, P=0.022; ventilatory: F1,5=15.54, P=0.011; Table 1B). Comparing results from experiments 1 and 2 reveals that dehydration had a significant effect on cloacal and ventilatory fluxes, but not on cutaneous flux (cutaneous: F1,5=0.75, P=0.41; cloacal: F1,5=19.74, P=0.0012; ventilatory: F1,5=8.08; P=0.018; Fig. 3). Dehydration suppressed cloacal flux relative to that of hydrated animals at both temperatures tested (P=0.0038 and P=0.0082 at 37.5 and 40°C, respectively). While the effect of dehydration was negative for cloacal flux, it was positive for ventilatory flux (i.e. ventilatory flux in dehydrated animals was higher than that of hydrated animals).
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Discussion |
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The current trend is to evaluate EWL simply for its negative impact on
water balance (e.g. Eynan and Dmi'el,
1993; Dmi'el,
1998
,
2001
;
Winne et al., 2001
), but high
EWL has the potential to be a major contributor to thermostasis, assuming
sufficient water availability. This is especially true at higher temperatures,
where EWL can help maintain Tb below the thermal maximum
temperature (i.e. below those temperatures where locomotory activity is
substantially impaired). Several lizard species have been shown to
dramatically increase EWL at higher temperatures
(Table 2). In each of the
previously studied species, the increase in EWL is a result of increases in
ventilatory flux (predominantly a reflection of panting). Gila monsters are
apparently unique among studied species in that EWL rates at high temperatures
are considerably higher than even those of panting lizards, and in that the
source of this dramatic increase in EWL is the cloaca. Previous studies either
ignored (e.g. Dawson and Templeton,
1963
) or prevented (e.g.
Templeton, 1960
;
Warburg, 1965
;
Crawford and Kampe, 1971
) any
EWL occurring from the cloaca. Cloacal EWL might be a unique physiological
adaptation of Gila monsters, or it might be more widely spread among lizard
taxa. It is worth noting that none of the Gila monsters in the current study
panted during the trials, even at the highest Ta. This
observation is reinforced by the small change in ventilatory EWL as
temperature increased. While panting is common among lizards, other species
also fail to pant at thermally challenging temperatures
(Dawson, 1960
). Cloacal
evaporation might simply be an alternative mechanism by which lizards can
decrease Tb. Lastly, the temperature at which Gila
monsters exhibit extreme elevations in EWL is somewhat lower (37.5°C) than
that of other species studied (typically
40°C). For some species this
difference could be a result of a lack of data for temperatures between 37 and
40°C, but this difference might also be attributable to the relatively low
selected body temperature of Gila monsters. While it might have been
advantageous to examine the response of Gila monsters at temperatures higher
than 40°C, such temperatures are extremely risky to the health of this
species, especially when cloacal EWL is prevented.
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Data regarding the ability of EWL to reduce Tb of
lizards to below Ta are mixed. Evaporation seems to be of
marginal importance in decreasing Tb in some species
(Templeton, 1960;
Crawford and Kampe, 1971
), but
it can significantly reduce Tb in others
(Dawson and Templeton, 1963
;
Warburg, 1965
;
DeWitt, 1967
; this study).
Regardless of its effectiveness, EWL is probably not used to extend activity
bouts for long durations at high Ta, because of the
relative scarcity of water in habitats with such high temperatures.
Nevertheless, it might allow the lizard to slightly extend the duration of
activity (Dawson and Templeton,
1963
), and even a slight extension could be important in an
extreme environment.
The Sonoran Desert is characterized by an extended period of high
temperature. Maximum daily temperature often exceeds 40°C from mid spring
until early fall (i.e. AprilOctober). Despite living in a hot
environment, Gila monsters have a relatively low selected body temperature of
approximately 29°C (Bogert and del
Campo, 1956; D. F. DeNardo, unpublished data). Furthermore, Gila
monsters are active foragers, preying on the contents of bird, mammal and
reptile nests. Relying on such widely dispersed resources requires Gila
monsters to forage over long distances
(Beck, 1990
). To regulate
Tb during the summer, Gila monsters restrict activity to
the cooler periods of the day. However, EWL might allow extension of the
activity period to complete critical activities (e.g. locating shelter,
consuming prey or engaging in combat) without reaching temperatures that
approach their critical thermal maximum.
While water is a limited resource in all deserts, much of the Sonoran
Desert has a reliable summer monsoon season (mid-July to mid-September) that
provides relatively frequent access to water for at least the latter half of
the hot summer. Therefore, the length of time during which Sonoran Desert
residents cope with arid conditions (typically mid-April through mid-July) is
reduced compared to many desert environments. The periodic availability of
water and the concomitant increase in food availability associated with the
summer monsoon season might underlie the predominant restriction of Gila
monsters to these areas of the Sonoran Desert. Additionally, Gila monsters
possess extremely large urinary bladders that potentially act as reservoirs
for water during the dry periods. Previous studies support such a role for the
bladder in other desert lizards (Beauchat et al., 1986;
Cooper and Robinson, 1990),
but water storage in the bladder remains unexplored in Gila monsters.
Despite experiencing a summer rainy season and perhaps possessing a water
reservoir, Gila monsters are vulnerable to dehydration during the dry summer
months (Bogert and Del Campo,
1956; Beck and Jennings,
2003
), and high EWL rates at this time would be costly and
possibly fatal. Therefore, it is not surprising that Gila monsters reduce
cloacal EWL rates when dehydrated by increasing the minimum temperature at
which significant cloacal EWL occurs and by reducing evaporative flux at
higher temperatures. We recognize that the decrease in evaporative flux during
dehydration is almost certainly due in part to the physical effect that the
increased osmotic pressure of the blood has on the vapor-pressure gradient
driving the evaporation. However, the direct effect of increased osmolality is
unlikely to account for the full magnitude of the reduction in EWL. Instead,
it is likely that much of the reduction in EWL is due to physiological
adjustments made to minimize loss of body water. For example, alteration in
cloacal perfusion and or vent gape could substantially affect the rate of
cloacal EWL. While vent gape has been anecdotally observed in Gila monsters at
high environmental temperatures, possible regulatory mechanisms remain to be
tested. Similarly unknown yet interesting and deserving of future study are
the regulatory parameters for cloacal EWL. In dehydrated desert iguanas
Dipsosaurus dorsalis, an increase in plasma osmolality delays the
onset and extent of panting, which induces a `right shift' and blunting of the
EWLtemperature response curve
(Dupré and Crawford,
1985
). While serum osmolality increased significantly in the
dehydrated Gila monsters, it is unknown whether cloacal EWL in Gila monsters
is similarly regulated by osmolality. However, since the presence of water in
the urinary bladder might allow for water expenditure without changing plasma
osmolality, regulation of cloacal EWL in Gila monsters might also be
influenced by urinary bladder volume. While the results presented here do not
provide insight into the underlying mechanisms or regulatory parameters
involved in cloacal EWL, this study presents a previously undescribed means
for controllable evaporative water loss and points out the possible importance
of EWL for thermoregulation in ectotherms. The degree to which EWL can serve
as a thermoregulatory mechanism depends on the availability of water (within
both the organism and the environment) and on the ability of the organism to
regulate water loss. Further studies of this and other species are warranted
to better understand how desert organisms trade off between thermostasis and
hydrostasis.
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Acknowledgments |
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References |
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Beck, D. D. (1990). Ecology and behavior of the Gila monster in southwestern Utah. J. Herpetol. 24, 54-68.
Beck, D. D. and Jennings, R. D. (2003). Shelter-site selection and habitat use by Gila monsters. Herpetol. Monogr. 17,111 -129.
Beuchat, C. A., Vleck, D. and Braun, E. J. (1986). Role of the urinary bladder in osmotic regulation of neonatal lizards. Physiol. Zool. 59,539 -551.
Bogert, C. M. and Del Campo, R. M. (1956). The Gila monster and its allies. Bull. Amer. Mus. Natur. Hist. 109,1 -238.
Braysher, M. and Green, B. (1970). Absorption of water and electrolytes from the cloaca of an Australian lizard, Varanus gouldii (Gray). Comp. Biochem. Physiol. 35,607 -614.[CrossRef]
Brown, D. E. and Carmony, N. B. (1991). Gila monster: Facts and Folklore of America's Aztec Lizard, 2nd Edition. Silver City, NM: High-Lonesome Books.
Calder, W. A. and King, J. R. (1974). Thermal and caloric relations of birds. In Avian Biology, vol.IV (ed. D. S Farner and J. R. King), pp.260 -413, New York: Academic Press.
Campbell, G. S. and Norman, J. M. (1998). An Introduction to Environmental Biophysics, 2nd Edition. New York: Springer.
Cheung, W. W. K. and Marshall, A. T. (1973). Water and ion regulation in cicadas in relation to xylem feeding. J. Insect Physiol. 19,1801 -1816.[CrossRef]
Cohen, A. C. (1975). Some factors affecting water economy in snakes. Comp. Biochem. Physiol. 51A,361 -368.[CrossRef]
Cooper, P. D. and Robinson, M. D. (1990). Water balance and bladder function in the Namib Desert sand dune lizard, Aporosaura anchietae (Lacertidae). Copeia 1990,34 -40.
Crawford, E. C., Jr and Kampe, G. (1971).
Physiological responses of the lizard Sauromalus obesus to changes in
ambient temperature. Am. J. Physiol.
220,1256
-1260.
Crompton, A. W., Taylor, C. R. and Jagger, J. A. (1978). Evolution of homeothermy in mammals. Nature 272,333 -336.[Medline]
Dantzler, W. H. and Schmidt-Nielsen, B. (1966). Excretion in fresh-water turtle (Pseudemys scripta) and desert tortoise (Gopherus agassizii). Am. J. Physiol. 210,198 -210
Dawson, W. R. (1960). Physiological responses to temperature in the lizard Eumeces obsuletus. Physiol. Zool. 33,87 -103.
Dawson, W. R. and Bartholomew, G. A. (1968). Temperature regulation and water economy of desert birds. In Desert Biology, vol. 1 (ed. G. W. Brown, Jr), pp.357 -394. New York: Academic Press.
Dawson, W. R. and Templeton, J. R. (1963). Physiological response to temperature in the lizard Crotaphytus collaris.Physiol. Zool. 36,219 -236.
DeWitt, C. B. (1967). Precision of thermoregulation and its relation to environmental factors on the desert iguana, Dipsosaurus dorsalis. Physiol. Zool. 40, 49-66.
Dmi'el, R. (1998). Skin resistance to evaporative water loss in viperid snakes: habitat aridity versus taxonomic status. Comp. Biochem. Physiol. 121A, 1-5.
Dmi'el, R. (2001). Skin resistance to evaporative water loss in reptiles: a physiological adaptive mechanism to environmental stress or a phyletically dictated trait? Israel J. Zool. 47,55 -67.
Dupré, R. K. and Crawford, E. C., Jr (1985). Control of panting in the desert iguana: roles of peripheral temperatures and the effect of dehydration. J. Exp. Zool. 235,341 -347.[Medline]
Eynan, M. and Dmi'el, R. (1993). Skin resistance to water loss in agamid lizards. Oecologia 95,290 -294.
Flatau, P. J., Walko, R. L. and Cotton, W. R. (1992). Polynomial fits to saturation vapor pressure. J. Appl. Meteorol. 31,1507 1513.[CrossRef]
Hayes, J. P. and Garland, T., Jr (1995). The evolution of endothermy: testing the aerobic capacity model. Evolution 49,836 -847.
Hensel, H., Brück, K. and Raths, P. (1973). Homeothermic organisms. In Temperature and Life (ed. H. Prect, J. Christophersen, H. Hensel and W. Larcher), pp. 503-761. New York: Springer-Verlag.
Lasiewski, R. C., Acosta, A. L. and Bernstein, M. L. (1966). Evaporative water loss in birds. I. Characteristics of the open flow method of determination and their relation to estimates of thermoregulatory ability. Comp. Biochem. Physiol. 19,445 457.[CrossRef]
Lowe, C. H., Schwalbe, C. R. and Johnson, T. B. (1986). The Venomous Reptiles of Arizona. Phoenix: Arizona Game and Fish Dept.
Mautz, W. J. (1982a). Patterns of evaporative water loss. In Biology of the Reptilia, Vol.12 (ed. C. Gans), pp. 443-481. New York: Academic Press.
Mautz, W. J. (1982b). Correlation of both respiratory and cutaneous water losses of lizards with habitat aridity. J. Comp. Physiol. 149,25 -30.
McNab, B. K. (1978). The evolution of homeothermy in the phylogeny of mammals. Am. Nat. 112, 1-21.[CrossRef]
Minnich, J. E. (1976). Water procurement and conservation by desert reptiles in their natural environment. Isr. J. Med. Sci. 12,854 -861.[Medline]
Schmidt-Nielsen, K. (1964). Desert Animals: Physiological Problems of Heat and Water. London: Oxford University Press.
Templeton, J. R. (1960). Respiration and water loss at the higher temperatures in the desert iguana, Dipsosaurus dorsalis. Physiol. Zool. 33,136 -145.
Toolson, E. C. (1987). Water profligacy as an adaptation to hot deserts: water loss rates and evaporative cooling in the Sonoran Desert cicada, Diceroprocta apache (Homoptera: Cicadidae). Physiol. Zool. 60,379 -385.
Warburg, M. R. (1965). The influence of ambient temperature and humidity on the body temperature and water loss from two Australian lizards, Tiliqua rugosa (Gray) (Scincidae) and Amphibolurus barbatus Cuvier (Agamidae). Aust. J. Zool. 13,331 -350.
Winne, C. T., Ryan, T. J., Leiden, Y. and Dorcas, M. E. (2001). Evaporative water loss in two natricine snakes, Nerodia fasciata and Seminatrix pygaea. J. Herpetol. 35,129 -133.