The thermogenesis of digestion in rattlesnakes
1 Department of Biological Sciences, Brock University, St Catharines, ON,
L2S 3A1, Canada
2 Department of Zoology, University of British Columbia, 6270 University
Blvd, Vancouver, British Columbia, Canada, V6T 1Z4
3 Departamento de Zoologia, c. p. 199, Universidade Estadual Paulista,
13506-900, Rio Claro, SP, Brasil
* Author for correspondence (e-mail: gtatters{at}brocku.ca)
Accepted 7 November 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: reptile, rattlesnake, Crotalus durissus, specific dynamic action, infra-red imaging, thermogenesis, thermoregulation, endothermy, digestion
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
As in other ectothermic organisms, temperature exerts a pervasive influence
on all activities in snakes. Different activities, however, are affected
differently by changes in body temperature
(Stevenson et al., 1985;
Van Damme et al., 1991
), and
thus different activities (e.g. locomotion, digestion) may be optimal at
different temperatures. As a consequence, snakes may alter their body
temperature in activity specific patterns. For example, if given a choice of
environmental temperatures during digestion, snakes
(Cowles and Bogert, 1944
;
Regal, 1966
;
Walker and Taylor, 1966
;
Greenwald and Kanter, 1979
;
Huey, 1982
; Slip and Shine,
1988a
,b
;
Jaeger and Gabor, 1993
;
Sievert and Andreadis, 1999
),
as well as other reptiles (see Huey,
1982
), behaviorally increase their preferred body temperature, the
so-called post-prandial thermophilic response. The primary consequence of such
an increase in body temperature, in almost all cases examined, is a shortening
of digestion time at the expense of increased rates of metabolism during the
period of SDA (Wang et al.,
2003
; Toledo et al.,
2003
). Toledo et al.
(2003
), however, found that
the SDA of boas fed different meal sizes was energetically less costly at
30°C than at 25°C. Thus, at least in this one particular case, it
seems that the post-prandial thermophilic response was advantageous not only
by decreasing the duration of digestion but also by improving the energetic
return on the meal.
The post-prandial thermophilic response has always been associated with
adjustments in thermoregulatory behavior that would allow animals to alter
body temperature by exploring the natural heat sources available in their
environment (e.g. Blouin-Demers and
Weatherhead, 2001). The possibility of using metabolism as a
source of heat to increase body temperature was thought to be of minor
importance, perhaps due to the widespread belief that ectothermic vertebrates
in general (Pough, 1983
), and
some snakes in particular, have a relatively low aerobic capacity
(Ruben, 1976
;
Lillywhite and Smits, 1992
),
that would preclude any considerable heat generation by metabolic means. Such
an interpretation, although generally true, ignores the fact that the
metabolism of some snakes may increase by up to 17-fold during digestion
(Secor and Diamond, 1995
,
2000
), which will generate a
considerable amount of heat (Benedict,
1932
; Van Mierop and Barnard,
1976
; Marcellini and Peters,
1982
). Therefore, in the present study, we investigated whether
snakes could use this heat source. Specifically we examined whether the body
temperature of the South American rattlesnake Crotalus durissus
terrificus is affected by the increased metabolic rate experienced during
digestion at a constant environmental temperature using infra-red (IR) imaging
technology. We took IR pictures from digesting and non-digesting snakes for a
period of 7 days, and compared their body surface temperature with the ambient
temperature. We also examined the effects of meal size on the magnitude of the
thermogenesis in these snakes, since meal size is one of the most influential
determinants of the SDA response: the larger the meal, the greater the
post-prandial metabolism and the longer the duration of the SDA
(Andrade et al., 1997
;
Toledo et al., 2003
). We
hypothesized that body temperature following feeding (i.e. thermogenesis)
would rise with a similar time course to the SDA that is well characterized in
snakes, and that the magnitude and duration of the metabolic, post-prandial
thermogenesis would be positively correlated with meal size.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Experimental protocol
Three groups of snakes were used in this study. The control group
(N=4) was fasted throughout all measurements. The remaining snakes
were fed varying numbers of mice (either 1, 2 or 3) to create a small meal
group and a large meal group. The small meal group (N=6) was fed
enough mice to produce a meal ranging from 1025% (average 19.4%) of the
snake's pre-meal Mb. The large meal group (N=8)
was fed enough mice to produce a meal ranging from 2650% (average
33.7%) of the snake's pre-meal Mb (see
Table 1 for details of snake
body masses and meal masses). These mice were consumed within 30 min of
presentation to the snakes. Prior to feeding, an IR thermal image was taken of
each snake, serving as the fasted (time 0) value. Immediately following this,
snakes were either allowed to continue to fast, or fed the appropriate number
of mice, and thermal images were taken again 3, 16, 24, 36, 48, 64, 72, 96,
120, 144 and 168 h later. These images allowed the precise determination of
both snake surface temperature and local ambient temperature within the
individual animal's cage.
|
Infrared imaging
IR thermal images were taken with a MikroScan 7515 Thermal Imager (Mikron
Infrared®, Oakland, NY, USA). This device produces a 12-bit image
(320x240 pixels) and stores the temperature information of each pixel at
a resolution of 0.1°C. All temperature readings are automatically
corrected for nonblackbody properties by assuming an emissivity of 0.95, which
is a reasonable estimate for biological tissues. We assessed the validity of
this assumption by examining the IR from black electrical tape (known
emissivity = 0.95) held at the same temperature as snake skin. Both the tape
and the skin were found to radiate the same degree of IR, suggesting that an
emissivity of 0.95 is a safe assumption. The procedure for taking IR images
involved briefly opening the glass front of the cage and taking an image at a
distance of 3045 cm from the snake. The snakes were well accustomed to
this procedure by the time the experiment started, and most individuals simply
remained coiled and passive as the image was taken. No changes in body surface
temperatures associated with agitation were observed.
Data analysis and statistics
IR images were analyzed using MikroSpec RT (Mikron Infrared®) software.
Regions of interest on the body were outlined and the average surface
temperature determined. Since there was little variability in the surface
temperature of the body (except for the head region), random regions
(comprising approximately 10% of the body surface area) were used to determine
body surface temperature (hereafter referred to as body temperature,
Tb). The background temperature of the wooden cage was
also determined, and served as a local ambient temperature comparison. The
difference between body temperature and ambient temperature
(T) was determined for every snake at every time point. To aid
in the analysis, the maximum
T during SDA, the time at which
the maximum
T occurred, and the area under the
T curve during SDA were determined for each individual snake.
A one-way ANOVA using a Bonferroni post-hoc comparison was used to
test the significance of all changes in these three variables (max.
T, time of max.
T, and area under the
T curve). The comparison between pre- and post-feeding values
of
T were made using a one-way repeated measures analysis of
variance (ANOVA), followed by the post-hoc Dunnett's test, which
tested for differences between post-feeding values against a control value
(pre-feeding value). Differences were considered significant when
P<0.05.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Thermal increment of feeding
Fasted snakes did not show any significant changes in T
throughout their fasting period (Fig.
1), although
T did fluctuate over time by
approximately 0.1°C to +0.1°C.
|
Snakes fed both small and large meals demonstrated significant and
sustained increases in Tb following feeding
(Table 2; Figs
1,
2). Within 3 h of being fed a
meal, both the small and the large meal group exhibited a significant rise in
T, which remained above the pre-feeding value for up to 6 days
(144 h; Fig. 1). The maximum
T of 0.93±0.11°C in the small meal group occurred
on average 23±4 h post-feeding, whereas the maximum
T
of 1.3±0.04°C in the large meal group occurred 42±7 h
post-feeding. Both the maximum
T and the time at which maximum
T occurred were significantly higher in the large meal than in
the small meal group. Furthermore, the total area under the
T
curve during the SDA period was significantly higher in the large meal group
than in the small meal group (Table
2). Interestingly, the rate of rise of
T was
identical in both groups. Slight regional variations in surface temperature
did exist in some snakes (Fig.
2),however, most surface temperatures over most of the snake's
body were relatively uniform (<0.2°C difference).
|
|
The effect of diet size is further demonstrated in the correlations between
maximum T and the SDA area versus meal size for
individual animals (Fig. 3).
Significant positive correlations exist between maximum
T and
meal size (%Mb) (r2=0.83) and between
SDA area and meal size (%Mb)
(r2=0.83), suggesting tight correlations between these
variables, although there was a tendency for the relationships to asymptote at
the largest meal sizes, suggesting that diet-induced thermogenesis does not
continue to increase linearly with meal size.
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Specific dynamic action and meal size effects on thermogenesis
By overlapping the thermal increment associated with feeding (present
study) with the post-prandial metabolic response of rattlesnakes
(Andrade et al., 1997), a clear
correlation emerges between both variables (See
Fig. 2). While digesting meal
sizes 1050% of their own body masses, this species experiences peaks in
metabolism between 15 h and 33 h post-feeding, at values 3.7- to 7.3-fold
higher than the values measured during fasting
(Andrade et al., 1997
).
Similarly, we have found that thermogenesis attained greater magnitude in
those snakes fed with larger meals and that the attainment of peak values in
Tb occur in accordance with the peak in metabolism. It
thus appears that the thermal effect of feeding that we recorded reflects a
total body temperature increment arising from the SDA, as previously
conjectured by Benedict
(1932
).
There are other possible explanations for the source of this heat
production. Marcellini and Peters
(1982) conjectured that
undetectable muscular contractions and chemical decomposition of food may have
contributed substantially to the post-prandial thermogenesis of snakes. Our
data, however, suggest that the latter is unlikely. Indeed, we observed that a
decaying, uneaten mouse produced no significant heat under the same
experimental conditions (G. J. Tattersall, unpublished data). Further, the
only increase in muscular activity that could be anticipated for digesting
snakes is an increase in gut motility, since activity in general is decreased
in fed snakes (Beck, 1996
).
This renders it improbable that an undetectable increase in muscular activity
might have been involved in the increase in heat production after feeding. The
maintenance of all snakes in a temperature-controlled room, with no
possibility of changing heat exchange rates by behavioral means, excludes the
possibility that the increment in body temperature exhibited by fed
rattlesnakes is the result of an adjustment in thermoregulatory behavior, i.e.
a post-prandial thermophilic response. Finally, the rattlesnakes' body
temperatures returned to fasting levels with a time course that is in good
agreement with the duration of the metabolic SDA response recorded for this
species (Andrade et al.,
1997
).
Temperature effects on digestion and significance of thermogenesis
The benefits often associated with the post-prandial thermophilic response
in reptiles include an increased rate of digestion and/or digestive efficiency
(Stevenson et al., 1985;
Lillywhite, 1987
;
Hailey and Davies, 1987
;
Reinert, 1993
;
Sievert and Andreadis, 1999
)
and an increase in gastrointestinal motility, secretion and absorption
(Dandrifosse, 1974
;
Skoczylas, 1978
;
Mackay, 1968
; Diefenbach,
1975a
,b
;
Skoczylas,
1970a
,b
).
Moreover, temperature may affect chemical digestion more directly, since some
digestive enzymes have maximal activity at higher temperatures
(Licht, 1964
). The general
consequence of such temperature effects on digestion may be characterized by
the shortening of the SDA duration at the expense of increased rates of
metabolism (see Toledo et al.,
2003
; Wang et al.,
2003
). For snakes that ingest large meals and have their locomotor
and defensive ability temporarily impaired, speeding up the digestive process
through an increase in temperature may be especially relevant since it would
reduce the risk of predation (Garland and
Arnold, 1983
; Ford and
Shuttlesworth, 1986
). Higher temperatures and faster digestion may
also be accompanied by increased rates of food intake, as documented in skinks
(Du et al., 2000
), which will
result in better body condition, growth and perhaps an increased fitness.
Finally, the energetic cost of digestion itself seems to decrease at higher
temperatures (Toledo et al.,
2003
).
For rattlesnakes, our results suggest that all beneficial consequences
associated with the post-prandial thermophilic response listed above may be
achieved not only by altering thermoregulatory behavior, but also through the
thermogenic consequences of the elevated metabolism during digestion. In
C. durissus, we have found that thermogenesis alone may account, on
average, for a 0.91.2°C increase in body temperature during the
first 23 days after feeding. The important question is whether such an
increase would be of any physiological significance to the rattlesnake's
digestion. We tried to address this issue by calculating the effect of a
1°C change in body temperature on the digestion of snakes, by regressing
SDA duration and SDA cost (expressed as a percentage of the calorific content
of the meal, i.e. SDA coefficient; see
Toledo et al., 2003) against
body temperature, using a set of data obtained for C. durissus at
25° and 30°C (S. P. Brito, A. S. Abe and D. V. Andrade, unpublished
data). This procedure revealed that a 1°C increase in body temperature,
under the conditions in which we performed the experiments, may account for a
19 h decrease in SDA duration and a 0.3% decrease in the SDA coefficient.
Thus, the thermogenic effect of feeding, per se, may, indeed, affect
the digestive performance and the duration of digestion in rattlesnakes.
Moreover, the ability to increase body temperature after feeding by
thermoregulatory behaviors is reported to be constrained in rattlesnakes by
the availability of adequate thermal microhabitats, reduced mobility and
reclusive behaviors (Beck,
1996
). Thus, it seems possible that the beneficial effects of
metabolic thermogenesis on digestion may assume a greater importance during
the night, on cloudy days, or whenever behavioral thermoregulation and the
achievement of the post-prandial thermophily are constrained. Finally, by
using the infrared imaging technique, we assessed only body surface
temperature and, therefore, differences in deep core body temperature due to
digestion associated thermogenesis may be even larger. Indeed, in experiments
performed with pythons fed with meals containing temperature data loggers,
Marcellini and Peters (1982
)
were able to detect increases in body temperature up to 4°C (see also
Benedict, 1932
;
Van Mierop and Barnard, 1976
).
Moreover, digesting pythons experience metabolic responses that are far larger
than those observed in rattlesnakes
(Andrade et al., 1997
;
Secor and Diamond, 2000
),
which could also contribute to the larger thermogenic effect of feeding
exhibited by this species (Benedict,
1932
; Van Mierop and Barnard,
1976
; Marcellini and Peters,
1982
).
The thermogenic effect of feeding has been examined in one lizard species
by Bennett et al. (2000) who
found that digesting Varanus at 32 and 35° C tripled and
quadrupled metabolic rate, respectively, but the resulting heat generated by
such increases accounted for increases in body temperature of less than
1°C. This was mainly caused by the fact that the increased heat production
was accompanied by increases in thermal conductance attributed to the greater
ventilatory rates needed to support the higher rates of metabolism
(Bennett et al., 2000
).
Although the same phenomenon may have prevented further increases in body
temperature in C. durissus, the magnitude of this process in
rattlesnakes most likely was smaller than that recorded in Varanus.
Reptiles are known to exhibit a relative hypoventilation during digestion
(Wang et al., 2001
), but while
the air convection requirement for O2 in Python was
reduced by 46% (Secor et al.,
2000
), in Varanus this reduction was only 21.4%
(Hicks et al., 2000
). Thus,
the heat loss due to the changes in conductance associated with the increased
total ventilatory rates during digestion should have been greater for
Varanus compared to C. durrisus. Finally, the larger
thermogenic effect of feeding in rattlesnakes compared to Varanus may
also be related to the larger metabolic response to feeding in C.
durissus; metabolism increases from 4- to 7-fold
(Andrade et al., 1997
),
compared to a 3- to 4-fold change seen in Varanus
(Bennett et al., 2000
).
In brooding pythons Python molurus body temperature can increase
up to 7.3°C above ambient temperature by endogenous heat production, due
to increased metabolic rates associated with the spasmodic contractions of the
body musculature (Hutchison et al.,
1966). This figure is far more impressive than the thermogenic
effect of feeding found in rattlesnakes (present study) and in varanid lizards
(Bennett et al., 2000
).
Interestingly, however, brooding pythons showing such a large increase in body
temperature experience metabolic rates that are only 9.3 times higher than
non-brooding females under the same environmental conditions
(Hutchison et al., 1966
).
Thus, the discrepancy between the increase in metabolism and body temperature
among brooding pythons and digesting rattlesnakes and lizards indicates that
other factors may affect the thermoregulatory ability of brooding pythons. One
likely factor is posture; by remaining coiled around the eggs, brooding
pythons decrease the surface area, which otherwise would serve as an avenue
for heat loss (see Vinegar et al.,
1970
). Other possibilities are changes in conductance associated
with circulatory adjustments, however, changes in heat transport via
the circulatory system remain to be investigated.
Concluding remarks
Endotherms may use SDA or exercise-generated heat for thermogenesis, saving
a substantial amount of energy that would otherwise be used for this purpose
(Costa and Kooyman, 1984). For
an ectotherm, the general notion is that the heat generated during digestion
is a wasteful byproduct generated from the metabolic increment
(Hailey and Davies, 1987
)
since they naturally do not use metabolism to generate heat for
thermoregulation. However, thermogenesis in snakes may act in concert with the
behavioral post-prandial thermophilic response to achieve the suite of
ecological and energetic benefits of increased body temperature during
digestion. Particularly poignant in the case of snakes is the long, protracted
digestion process. So, although the magnitude of the thermal increment
following feeding may seem negligible, the duration of this sustained increase
in body temperature is sufficient to suggest that digestion-derived heat in
this ectotherm is a physiologically and ecologically important phenomenon.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Andrade, D. V., Cruz-Neto, A. P. and Abe, A. S. (1997). Meal size and specific dynamic action in the rattlesnake Crotalus durissus (Serpentes: Viperidae). Herpetologica 53,485 -493.
Beck, D. D. (1996). Effects of feeding on body temperatures of rattlesnakes: a field experiment. Physiol. Zool. 69,1442 -1455.
Benedict, F. G. (1932). The Physiology of Large Reptiles with Special Reference to the Heat Production of Snakes, Tortoises, Lizards, and Alligators. Washington: Carnegie Institute Publication.
Bennett, A. F., Hicks, J. W. and Cullum, A. J. (2000). An experimental test of the thermoregulatory hypothesis for the evolution of endothermy. Evolution 54,1768 -1773.[Medline]
Blouin-Demers, G. and Weatherhead, P. J. (2001). An experimental test of the link between foraging, habitat selection and thermoregulation in black rat snakes Elaphe obsoleta obsoleta. J. Anim. Ecol. 70,1006 -1013.[CrossRef]
Costa, D. P. and Kooyman, G. L. (1984). Contribution of specific dynamic action to heat balance and thermoregulation in the sea otter, Enhydra lutris. Physiol. Zool. 57,199 -203.
Cowles, E. R. and Bogert, C. M. (1944). Thermophilic response following feeding in certain reptiles. Copeia 1944,588 -590.
Dandrifosse, G. (1974). Digestion in reptiles. In Amphibia and Reptila, vol 9 (ed. M. Florkin and B. Scheer), pp. 249-276. New York: Academic Press.
Diefenbach, C. O. (1975a). Gastric function in Caiman crocodilus (Crocodylia: Reptilia). I. Rate of gastric digestion and gastric motility as a function of temperature. Comp. Biochem. Physiol. 51A,259 -265, 1975.
Diefenbach, C. O. (1975b). Gastric function in Caiman crocodilus (Crocodylia: Reptilia). II. Effects of temperature on pH and proteolysis. Comp. Biochem. Physiol. 51A,267 -274.
Du, W.-G, Yan, S.-J. and Ji, X. (2000). Selected body temperature, thermal tolerance and thermal performance in adult blue-tailed skinks, Eumeces elegans. J. Therm. Biol. 25,197 -202.[CrossRef]
Ford, N. B. and Shuttlesworth, G. A. (1986). Effects of variation in food intake on the locomotory performance of juvenile garter snakes. Copeia 1986,999 -1001.
Garland, T. and Arnold, S. J. (1983). Effects of full stomach on locomotory performace of juvenile garter snakes (Thamnophis elegans). Copeia 1983,1092 -1096.
Greene, H. W. (1992). The ecological and behavioral context for pitvipers evolution. In Biology of the Pitvipers (ed. J. A. Campbell and E. D. Brodie), pp.107 -118. Tyler, Texas: Selva.
Greene, H. W. (1997). Snakes: The Evolution of Mystery in Nature. Berkeley: University of California Press.
Greenwald, O. E. and Kanter, M. E. (1979). The effects of temperature and behavioral thermoregulation on digestive efficiency and rate in corn snakes (Elaphe guttata guttata). Physiol. Zool. 52,398 -408.
Hailey, A. and Davies, P. M. C. (1987). Digestion, specific dynamic action, and ecological energetics of Natrix maura. Herpetol. J. 1,159 -166.
Hicks, J. W., Wang, T. and Bennett, A. F.
(2000). Patterns of cardiovascular and ventilatory response to
elevated metabolic states in the lizard Varanus exanthematicus. J.
Exp. Biol. 203,2437
-2445.
Huey, R. B. (1982). Temperature, physiology, and the ecology of reptiles. In Biology of the Reptilia, vol. 12: Physiology C Physiological Ecology (ed. C. Gans and F. H. Pough). pp.25 -74. Ithaca, NY: Academic Press.
Hutchison, V. H., Dowling, H. G. and Vinegar, A. (1966). Thermoregulation in a brooding female Indian python, Python molurus bivittatus. Science 151,694 -696.[Medline]
Jackson, K. and Perry, G. (2000). Changes in intestinal morphology following feeding in the brown treesnake, Boiga irregularis. J. Herpetol. 34,459 -462.
Jaeger, R. B. and Garbor, C. R. (1993). Postprandial thermophily in rough green snakes (Opheodrys aestivus). Copeia 4,1174 -1776.
Jayne, B. C., Voris, H. K. and Ng, P. K. L. (2002). Snake circumvents constraints on prey size. Nature 418,143 .[CrossRef][Medline]
Kleiber, M. (1961). The Fire of Life: An Introduction to Animal Energetics. New York, New York: Wiley & Sons.
Licht, P. (1964). The temperature dependence of myosin adenosine triphosphate and alkaline phosphatase in lizards. Comp. Biochem. Physiol. 12,331 -341.[CrossRef][Medline]
Lillywhite, H. B. (1987). Temperature, energetics, and physiological ecology. In Snakes: Ecology and Evolutionary Biology (ed. R. A. Siegel, J. T. Collins and S. S. Novak), pp. 422-477. New York, McGraw-Hill.
Lillywhite, H. B. and Smits, A. (1992). The cardiovascular adaptations of viperid snakes. In Biology of the Pitvipers (ed. J. A. Campbell and E. D. Brodie), pp.143 -154. Tyler, Texas: Selva.
Mackay, R. S. (1968). Observations on the peristaltic activity versus temperature and circadian rhythms in undisturbed Varanus flavescens and Ctenosaura pectininata.Copeia 1968,252 -259.
Marcellini, D. L. and Peters, A. (1982). Preliminary observations on endogenous heat production after feeding in Python molurus. J. Herpetol. 16, 92-95.
Overgaard, J., Busk, M., Hicks, J. W., Jensen, F. B. and Wang, T. (1999). Respiratory consequences of feeding in the snake Python molurus. Comp. Biochem. Physiol. 124,359 -365.
Pough, F. H. (1983). Amphibians and reptiles as low-energy systems. In Behavioral Energetics: The Cost of Survival in Vertebrates (ed. W. P. Aspey and S. I. Lustick), pp.141 -188. Columbus: Ohio State University Press.
Regal, P. J. (1966). Thermophilic response following feeding in certain reptiles. Copeia 1966,588 -590.
Reinert, H. K. (1993). Habitat selection in snakes. In Snakes: Ecology and Behavior (ed. R. A. Siegel and J. T. Collins), pp. 201-240. New York: MacGraw-Hill.
Ruben, J. A. (1976). Aerobic and anaerobic metabolism during activity in snakes. J. Comp. Physiol. 109,147 -157.
Ruben, J. A. (1995). The evolution of endothermy in mammals and birds: from physiology to fossils. Annu. Rev. Physiol. 57,69 -95.[CrossRef][Medline]
Secor, S. M. (2001). Regulation of digestive performance: a proposed adaptive response. Comp. Biochem. Physiol. 128,565 -577.
Secor, S. M. and Diamond, J. (1995). Adaptive responses to feeding in Burmese pythons: pay before pumping. J. Exp. Biol. 198,1313 -1325.[Medline]
Secor, S. M. and Diamond, J. (1997). Determinants of the postfeeding metabolic response of Burmese pythons, Python molurus. Physiol. Zool. 70,202 -212.[Medline]
Secor, S. M. and Diamond, J. (2000). Evolution of regulatory responses to feeding in snakes. Physiol. Biochem. Zool. 73,123 -141.[CrossRef][Medline]
Secor, S. M., Hicks, J. W. and Bennett, A. F.
(2000). Ventilatory and cardiovascular responses of a python
(Python molurus) to exercise and digestion. J. Exp.
Biol. 203,2447
-2454.
Sievert, L. M. and Andreadis, P. (1999). Specific dynamic action and postprandial thermophily in juvenile northern water snakes, Nerodia sipedon. J. Therm. Biol. 24, 51-55.[CrossRef]
Skoczylas, R. (1970a). Influence of temperature on gastric digestion in the grass snake, Natrix natrix L. Comp. Biochem. Physiol. 33,793 -803.[CrossRef]
Skoczylas, R. (1970b). Salivary and gastric juice secretion in the grass snake, Natrix natrix L. Comp. Biochem. Physiol. 35,885 -903.[CrossRef]
Skoczylas, R. (1978). Physiology of the digestive tract. In Biology of the Reptilia, vol.8 (ed. C. Gans and K. A. Gans), pp.589 -717. New York: Academic Press.
Slip, D. J. and Shine, R. (1988a). Feeding habits of the diamond python, Morelia s. spilota: ambush predation by a boid snake. J. Herpetol. 22,323 -330.
Slip, D. J. and Shine, R. (1988b). Thermophilic response to feeding of the diamond python, Morelia s. spilota (Serpentes: Boidae). Comp. Biochem. Physiol. 89A,645 -650.
Speakman, J. R. and Ward, S. (1998). Infrared thermography: principles and applications. Zoology 101,224 -232.
Starck, J. M. and Beese, K. (2001). Structural
flexibility of the intestine of Burmese python in response to feeding.
J. Exp. Biol. 204,325
-335.
Starck, J. M. and Beese, K. (2002). Structural
flexibility of the small intestine and liver of garter snakes in response to
feeding and fasting. J. Exp. Biol.
205,1377
-1388.
Stevenson, R. D., Peterson, C. R. and Tsuji, J. S. (1985). The thermal dependence of locomotion, tongue flicking, digestion, and oxygen consumption in the wandering garter snake. Physiol. Zool. 58,46 -57.
Taylor, C. R. (1980). Evolution of mammalian homeothermy: a two-step process? In Comparative Physiology: Primitive Mammals (ed. K. Schmidt-Nielsen, L. Bolis and C. R. Taylor), pp. 100-111. Cambridge, UK: Cambridge University Press.
Toledo, L. F., Abe, A. S. and Andrade, D. V. (2003). Temperature and meal mass effects on the post-prandial metabolism and energetics in a boid snake. Physiol. Biochem. Zool. 76,240 -246.[CrossRef][Medline]
Van Damme, R., Bauwens, D. and Verheyen, R. F. (1991). The thermal dependence of feeding behaviour, food consumption and gut-passage time in the lizard Lacerta vivipara Jacquin. Funct. Ecol. 5,507 -517.
Van Mierop, L. H. S. and Barnard, S. M. (1976). Thermoregulation in a brooding female Python molurus bivittatus.Copeia 1976,398 -401.
Vinegar, A., Hutchison, V. H. and Dowling, H. G. (1970). Metabolism, energetics and thermoregulation during brooding of snakes of the genus Python (Reptilia, Boidae). Zoologica 55,19 -48.
Walker, J. M. and Taylor, H. L. (1966). Thermophilic response following feeding in certain reptiles. Copeia 3,588 -590.
Wang, T., Busk, M. and Overgaard, J. (2001). The respiratory consequences of feeding in amphibians and reptiles. Comp. Biochem. Physiol. 128,535 -549.
Wang, T., Zaar, M., Arvedsen S., Vedel-Smith, C., and Overgaard, J. (2003). Effects of temperature on the metabolic response to feeding in Python molurus. Comp. Biochem. Physiol. 133A,519 -527.
Related articles in JEB: