Comparative Biochemistry and Physiology Part A 133 (2003) 519–527
Effects of temperature on the metabolic response to feeding in Python molurus夞 Tobias Wanga,*, Morten Zaarb, Sine Arvedsenb, Christina Vedel-Smithb, Johannes Overgaardb a
Center of Old-Fashioned Physiology, Stationsgade 26, 8240 Risskov, Denmark b Department of Zoophysiology, University of Aarhus, Aarhus, Denmark
Received 1 February 2002; received in revised form 22 August 2002; accepted 23 August 2002
Abstract As ectothermic vertebrates, reptiles undergo diurnal and seasonal changes in body temperature, which affect many biological functions. In conjunction with a general review regarding the effects of temperature on digestion in reptiles, we describe the effects of various temperatures (20–35 8C) on the metabolic response to digestion in the Burmese python (Python molurus). The snakes were fed mice amounting to 20% of their body weight and gas exchange (oxygen uptake and CO2 production) were measured until digestion had ended and gas exchange returned to fasting levels. Elevated temperature was associated with a faster and larger metabolic increase after ingestion, and the time required to return to fasting levels was markedly longer at low temperature. The factorial increase between fasting oxygen ˙ 2) and maximal VO ˙ 2 during digestion was, however, similar at all temperatures studied. Furthermore, consumption (VO the integrated SDA response was not affected by temperature suggesting the costs associated with digestion are temperature-independent. Other studies on reptiles show that digestive efficiency is only marginally affected by temperature and we conclude that selection of higher body temperatures during digestion (postprandial thermophilic response) primarily reduces the time required for digestion. 䊚 2002 Elsevier Science Inc. All rights reserved. Keywords: Reptile; Snake; Python molurus; Specific dynamic action; Oxygen uptake; Feeding; Costs of digestion; Digestive efficiency; Digestion; Temperature
1. Introduction Reptiles are ectothermic and depend on external heat sources and appropriate behaviours to regulate 夞 This paper was originally presented at ‘Chobe 2001’; The Second International Conference of Comparative Physiology and Biochemistry in Africa, Chobe National Park, Botswana – August 18–24, 2001. Hosted by the Chobe Safari Lodge and the Mowana Safari Lodge, Kasane; and organised by Natural Events Congress Organizing (
[email protected]). *Corresponding author. Department of Zoophysiology, Institute of Biology, Building 131, Aarhus University, 8000 Aarhus C, Denmark. Tel.: q45-89-422694; fax: q45-86-194186. E-mail address:
[email protected] (T. Wang).
body temperature in the face of environmental changes (Cowles and Bogert, 1944). Many physiological functions and behaviours such as resting and maximal metabolic rates, locomotion and digestion are temperature dependent and reptiles are constantly faced with the need to prioritise the selected body temperature to satisfy these different needs (Dawson, 1975; Stevenson et al., 1985; Dorcas et al., 1997). Most animals must perform many tasks simultaneously, but since temperature sensitivity of different biological functions may vary, thermoregulation can impose potential conflicts between functions (e.g. Huey et al., 1989; Peterson et al., 1993). Thus, it is important to
1095-6433/03/$ - see front matter 䊚 2002 Elsevier Science Inc. All rights reserved. PII: S 1 0 9 5 - 6 4 3 3 Ž 0 2 . 0 0 2 5 0 - 7
520
T. Wang et al. / Comparative Biochemistry and Physiology Part A 133 (2003) 519–527
understand how temperature influences specific physiological functions in relation to the preferred temperature of a species performing specific biological tasks. Many reptiles, particularly snakes, can ingest very large meals. Subsequent digestion can last for several days and involve a number of physiological changes associated with gastric acid secretion and elevated metabolic rate (see Wang et al., 2001 for a review). In many species, digestion is also associated with selection of a higher body temperature (e.g. Regal, 1966; Peterson et al., 1993; Dorcas et al., 1997) and it is possible that the postprandial thermophilic response enables a more efficient andyor faster digestion. Teleologically, the existence of a postprandial thermophilic response, suggests that the optimal temperature for digestion is higher than optimal temperatures for other behaviours and functions. In the present study we report on the metabolic response to digestion at different temperatures in Burmese pythons. Pythons habitually ingest very large meals (Wall, 1912; Shine et al., 2001) and while the effects of prey size and fasting duration are well-characterised for this species, nothing is known about the temperature effects. Using these new data on Python, we discuss previous studies on reptiles and conclude that increased body temperature primarily reduces the rate of digestion, whereas costs of digestion and assimilation efficiencies are only marginally affected by temperature. 2. Materials and methods
chamber. The plastic containers were airtight, but were equipped with two small holes for continuous ventilation by mechanical pumps. The snakes always had access to water. 2.2. Measurements of oxygen uptake and carbon dioxide excretion ˙ 2) and carbon dioxide Oxygen consumption (VO ˙ production (VCO2) were measured using closedsystem respirometry. At the onset of measurements, a 30–50 ml gas sample was withdrawn from the container using a syringe and analysed immediately for fractional content of CO2 and O2 (FCO2 and FO2, respectively) with Applied Electrochemistry (Sunnyvale, CA, USA) oxygen and carbon dioxide analysers that were connected in series (S-3AyI and CD-3A, respectively). The containers were then sealed for 15–120 min, depending on the temperature and digestive state of the snake, before a second gas sample was withdrawn for analysis. The gas samples taken from the containers were fully saturated with water by adding small water droplets to the syringe, and the gas analysers were calibrated using saturated gas mixtures. In most cases, CO2 did not exceed 2.5% and O2 did not decline below 18%, and previous studies show that gas exchange of Python is unaffected by CO2 and O2 fractions within these limits (Secor and Diamond, 1997). The respiratory gas exchange ratio (RE) was calculated as: REsŽFendCO2yFstartCO2. y ŽFstartO2yFendO2.
2.1. Experimental animals Ten juvenile Burmese pythons (Python molurus) of undetermined sex and a body mass between 300 and 500 g were purchased from a commercial supplier. They were housed at The University of Aarhus in a 1.5=0.8=1.0 m container with access to shade and a heating lamp that was maintained at a 12 h:12 h lightydark cycle. All snakes fed voluntarily on mice and rat pups; they had gained weight and appeared healthy when experiments started. The snakes were fasted for at least 2 weeks before each feed and had been allowed to habituate to the experimental chambers for more than 1 week before experiments began. During the entire experimental period, snakes were kept in individual plastic containers (2.6 l) situated in a climatic
where Fstart and Fend denote the fractions of CO2 or O2 determined at the start and at the end of the ˙ 2 and VCO ˙ respirometry period. VO 2 were calculated as described by Vleck (1987): ˙ 2sVchamber=ŽFstartO2 VO yFendO2. y w1yŽ1yRE.=FstartO2x yt and ˙ ˙ VCO 2sRE=VO2 Vchamber is the volume of the respirometer (the volume of the experimental animal was subtracted assuming a density of 1 ml gy1), and t is the period during which the chamber was sealed. ˙ 2 and VCO ˙ VO 2 were corrected to STPD.
T. Wang et al. / Comparative Biochemistry and Physiology Part A 133 (2003) 519–527
521
and 14 days and we have tried to alter growth efficiency between 10 and 100%. These drastically altered assumptions led to changes in the calculated SDA coefficient of less than 2% and would not, therefore, affect the conclusions that are drawn in the present context. 2.4. Experimental protocol Fig. 1. Schematic representation of the metabolic response to feeding and the calculation of the SDA response (SDA, specific dynamic action). Standard metabolic rate is illustrated in dark grey, while the increase in oxygen consumption caused by digestion (SDA) is shown by light grey (modified from Overgaard et al., in press).
The mass specific metabolic rate had to be calculated using assumptions regarding the rate and magnitude of prey assimilation during the digestive period. We assumed that the snakes converted 50% of the ingested mass to growth at all experimental temperatures and that growth occurred at a constant rate following ingestion. Based on the temporal profile of the metabolic response, we assumed a temperature-dependent rate of assimilation, occurring over 20, 14, 10 and 6 days at 20, 25, 30 and 35 8C, respectively. The SDA coefficient, sensu Jobling and Davies (1980), was calculated as the amount of energy used for digestion (i.e. the integrated SDA response) relative to ingested energy. The calculation of the integrated SDA response is shown schematically in Fig. 1 as the oxygen consumption ˙ 2 of fasting and resting that is in excess of the VO snakes. When calculating the SDA coefficient, we assumed energy content of the mice to be 8 kJ ˙ 2 can be converted to energy by gy1 and that VO using a conversion factor of 19.7 J mly1 O2 (Gessaman and Nagy, 1988). 2.3. Critique of assumptions It is difficult to estimate body mass of snakes during digestion because they progressively assimilate the prey as digestion progresses and because a large proportion of the prey is allocated to growth. The assumed growth efficiency of 50% is close the value of 66% that we have estimated over a 6-month period of 12 snakes kept at 30 8C (Overgaard et al., in press). Furthermore, for the data obtained at all experimental temperatures, we have tried to alter the assimilation rate between 2
We measured the SDA response at 20, 25, 30 and 35 8C"1 8C. However, not all snakes were measured at all temperatures. The snakes were allowed to acclimate to each temperature for a minimum of 48 h before metabolic rate was measured in fasting animals. At each temperature, we measured the resting metabolic rate of fasting animals several times over 2–3 days and discarded measurements where the animals were visibly active. Snakes were then presented with mice amounting to 20"1% of body weight and allowed to ingest voluntarily. The snakes normally fed within an hour of being presented with food, but none of them would eat voluntarily at 20 8C. We, therefore, increased the temperature to 30 8C for 12 h, allowed the snakes to eat and decreased the temperature immediately thereafter. Oxygen con˙ 2) and carbon dioxide production sumption (VO ˙ (VCO 2) were measured up to three times daily depending on the temperature and digestive state. We allowed for metabolism to decline to fasting levels at each of the experimental temperatures (with the exception of 20 8C where the experiment was terminated early because all but one individual regurgitated the meal). Then temperature was altered and the protocol was repeated at another temperature. 2.5. Statistical analysis The SDA response at the different temperatures was compared using a one-way ANOVA and a posthoc Bonferroni test was applied to distinguish mean values that differed significantly. A P-value lower than 0.05 was considered statistically significant and all data are presented as means"1 S.E.M. 3. Results and discussion ˙ 2 of fasting snakes is presented in Table 1 at VO the different temperatures, while the temporal
T. Wang et al. / Comparative Biochemistry and Physiology Part A 133 (2003) 519–527
522
Table 1 ˙ 2) of fasting Burmese pythons (Python molurus) and the metabolic response to digestion of a meal amounting to Oxygen uptake (VO 20% of the snakes body mass at different temperatures Temperature 20 25 30 35
8C 8C 8C 8C
(Ns1) (Ns5) (Ns8) (Ns6)
˙ 2 Fasting VO (ml O2 miny1 kgy1)
˙ 2 Maximal VO (ml O2 miny1 kgy1)
Factorial increase
˙ 2 Time to max VO (days)
SDA (extra ml O2)
SDA coefficient %
0.23 0.65""0.04 0.83"0.04* 1.35"0.08*
1.43 4.36"0.33 5.23"0.28 7.68"0.49*
6.2 6.7 6.3 5.7
8.9 3.0"0.4 1.6"0.2* 0.9"0.1*
19.7 24.1"2.4 24.4"1.8 22.3"1.8
25 31"3 31"2 28"2
˙ 2, resting values before feeding; maximal VO ˙ 2 , maximal rate of oxygen consumption during digestion; factorial increase, Fasting VO ˙ 2 ; time to max VO ˙ 2, time of maximal response after ingestion; SDA, costs of the relative increment between fasting and maximal VO ˙ 2 in excess of fasting VO ˙ 2); SDA coefficient, energetic expenditure of the entire SDA digestion per gram snake (calculated as VO response relative to ingested energy (Jobling and Davies, 1980). Values are presented as mean"1 S.E.M and values that are significantly different from the mean at 25 8C are marked with an asterisk.
˙ 2 following feeding are presented changes in VO in Fig. 2. Table 1 and Fig. 3 also include the ˙ 2 that occurred during digestion, the maximal VO factorial increase and, finally, the SDA coefficient calculated from the integrated SDA response relative to ingested energy (Jobling and Davies, 1980). Because all snakes but one that were maintained
at 20 8C regurgitated 2–5 days after ingestion, the values presented for 20 8C are based on that single animal. However, in Fig. 2 we present the mean response until the time of regurgitation (note that the error bars disappears after the fifth day). ˙ 2 of fasting snakes at 30 8C is lower than VO previously published from our laboratory using
Fig. 2. The changes in oxygen uptake (a) and the respiratory gas exchange ratio (RER) following feeding in Burmese python (Python molurus) maintained at different temperatures. The resting metabolic rate of fasting snakes is depicted at 0 h. Values are presented as mean"1 S.E.M. At 20 8C, all animals but one regurgitated early in the digestive process and all data after day 5 represent that single individual which completed digestion.
T. Wang et al. / Comparative Biochemistry and Physiology Part A 133 (2003) 519–527
523
˙ 2 ) of fasting Python molurus and the metabolic response to digestion of Fig. 3. Effects of temperature on oxygen consumption (VO meals amounting to 20% of the snake’s body mass. (a). Oxygen uptake of fasting snakes. (b). Time elapsed since ingestion to maximal rate of oxygen consumption. (c) Factorial increase in oxygen uptake as the relative increment from fasting maximal values. (d) Maximal rates of oxygen consumption during digestion. (e) SDA coefficient (calculated as energetic expenditure of the entire SDA response relative to ingested energy). Values are presented as mean"1 S.E.M. and values that are significantly different from the mean at 25 8C are marked with an asterisk.
similar techniques on cannulated snakes (Overgaard et al., 1999) but similar to measures on noncannulated snakes (e.g. Secor and Diamond, 1995; Overgaard et al., in press). In a comprehensive ˙ 2 of Python molurus and other boid study on VO snakes spanning the same temperature interval, Chappell and Ellis (1987) measured even lower ˙ 2, while their temperature effects are similar to VO ˙ 2 was those reported here (our Q10 for fasting VO 2.2 between 25 and 35 8C). Our technique for measurements of gas exchange involves active manipulation of the chamber when samples are taken, and it is likely that disturbance caused by the presence of the investigator explain the higher ˙ 2 of fasting snakes compared to Chappell and VO Ellis (1987). It is our experience that postprandial snakes are less sensitive to disturbance and the values obtained during the SDA response are, therefore, less likely to be influenced. In this case, ˙ 2 following feeding the factorial increases in VO (i.e. the proportional increase from fasting conditions to maximal oxygen uptake) would be under˙ 2 for fasting snakes was estimated. Similarly, if VO high because of stress, the integrated SDA response would be underestimated (see Fig. 1). The large increase in metabolism following feeding is consistent with previous reports on Python (e.g. Secor and Diamond, 1995, 1997;
Overgaard et al., 1999, Overgaard et al., in press). As previously shown at 30 8C (Overgaard et al., in press), there were no noticeable changes in the gas exchange ratio during digestion at any of the experimental temperatures (Fig. 2b). The metabolic response to digestion of Python and other snakes was established already by Benedict (1932) and has been correlated with rapid and extensive growth of the small intestine and other gastrointestinal organs (e.g. Secor and Diamond, 1995, 2000). Recently, it has been shown that the intestine grow primarily by swelling of the individual enterocytes (Jackson and Perry, 2000; Starck and Beese, 2001, 2002), which appears to be energetically inexpensive (Starck and Beese, 2001; Overgaard et al., in press). Thus, the actual energy expenditure during digestion remains to be understood in Python (Overgaard et al., in press). 3.1. Effects of temperature on the SDA response The SDA response of Python molurus was markedly influenced by temperature and elevated body temperature was associated with a faster ˙ 2 after ingestion. Thus, animals at increase on VO ˙ 2 in less than 1 day, 35 8C reached maximal VO ˙ 2 was not reached until 3 whereas maximal VO days after ingestion at 25 8C; In the single individual that was able to digest the meal at 20 8C, we
524
T. Wang et al. / Comparative Biochemistry and Physiology Part A 133 (2003) 519–527
did not record the maximal response until 9 days after ingestion (see Table 1, Figs. 2 and 3). Increased temperature was also associated with a ˙ 2, but the significant elevation of the maximal VO factorial increase between fasting and maximal values did not change (Table 1, Fig. 3). Similar effects were observed in the frog Ceratophrys cranwelli (Powell et al., 1999). In contrast, maxi˙ 2 of plaice (Pleuronectes platessa) does mal VO not change with temperature although the duration of the SDA response was greatly reduced with increased temperature (Jobling and Davies, 1980). 3.2. Effects of temperature on digestive processes As originally noted by Cowles and Bogert (1944), reptiles require high body temperatures for digestion, and the faster metabolic response to feeding at elevated temperature is likely a reflect an augmented rate of digestion. Indeed, early studies show that the rate of digestion has a Q10 of approximately 2 in turtles (Riddle, 1909). While a comprehensive description regarding the effects of temperature on the various gastrointestinal processes involved in digestion remains to be performed, it has been demonstrated that gastrointestinal motility, secretion and absorption increases with elevated temperature (Dandrifosse, 1974; Skoczylas, 1978). Thus, in the lizards Varanus flavescenss and Ctenosaura pectininata (Mackay, 1968) as well as in Caiman crocodylus (Diefenbach, 1975a), motility increases with temperature in vivo. Secretion rate of gastric acid increases with temperature in C. crocodylus (Diefenbach, 1975a,b) and similar effects on secretion of acid and digestive enzymes also occur in the snake Natrix natrix (Skoczylas, 1970a,b). Finally, several digestive enzymes of lizards have their maximal activities at rather high temperatures (temp interval) (Licht, 1964). Elevated rate of digestive processes at increased temperature enable digestion to proceed at a faster rate. Thus, it is not surprising that all studies evaluating the effects of temperature on gastric evacuation rate and total passage time show that elevated temperature markedly reduces the time required for digestion. This effect has been observed in a number of snakes (Skoczylas, 1970a,b; Henderson, 1970; Greenwald and Kanter, 1979; Naulleau, 1983; Stevenson et al., 1985; Dorcas et al., 1997), lizards (Windell and Sarokon,
1976; Harlow et al., 1976; Waldschmidt et al., 1986) and crocodilians (Cowles and Bogert, 1944; Diefenbach, 1975a,b). Some of these studies merely measured the time elapsed between ingestion and defecation, and the analysis of such an approach may be confounded by the ability of some reptiles to retain faeces for prolonged periods (Lillywhite et al., in press). However, in an elegant study using X-ray analysis of stomach contents and labelling of the food items with fluorescent spheres in the boid snake Charina bottae, Dorcas et al. (1997) confirmed this relationship. In our study on Python, we noted that the snakes defecated soon after an increase in body temperature. The impaired ability to digest at low temperature may explain the great reduction in appetite at low temperature. In our experiments, none of the animals would eat voluntarily at 20 8C. This observation tallies with an apparent inability of Python to digest at 20 8C; only one of the five individuals was able to complete digestion, whereas the other four individuals regurgitated the prey within the first few days. The lizard Uta staniburiana exhibited a similar pattern, where voluntary feeding was greatly suppressed at 20 8C (Waldschmidt et al., 1986) and other studies show similar patterns although the exact temperature regimes may differ among species. Thus, the herbivorous lizard Dipsosaurus dorsalis is unable to pass food beyond the stomach and dies if denied the possibility of increasing body temperature above 28 8C (Harlow et al., 1976) and the rubber boa Charina bottae regurgitates at 10 8C (Dorcas et al. 1997). This latter study also defined a very sharp upper temperature limit for digestion, showing that all boas regurgitated at 35 8C (Dorcas et al., 1997). The marked inhibition of low temperature on appetite and rate of digestion may be an important factor that determines the ability of reptiles to occupy cold environments. Indeed, digestive processes appear more sensitive to low temperature than other physiological and behavioural processes such as locomotion (e.g. Stevenson et al., 1985). 3.3. Effects of temperature on digestive efficiency and the costs of digestion Digestive efficiency (Deff) represents the proportion of the ingested energy (Eing) that is assim-
T. Wang et al. / Comparative Biochemistry and Physiology Part A 133 (2003) 519–527
ilated. The assimilated energy (Eass) is typically assessed on the basis of measuring the energetic content of the faeces (Eexc), so that Deff can be expressed as: DeffsŽEingyEexc. yEing Because Eexc includes the nitrogenous waste that is excreted following assimilation, this manner of calculating Deff estimates an apparent efficiency (e.g. Mitchell, 1964). The apparent Deff of snakes is very high and most studies show more than 90% of the ingested energy is assimilated (e.g. Vinegar et al., 1970; Bedford and Christian, 2000). A number of studies on both carnivorous and herbivorous reptiles have used this approach to investigate the effects of temperature on Deff. Most of these studies show reduction in Deff with decreased temperatures (e.g. Harlow et al., 1976). The effects are, however, modest (typically less than 10% change), and several studies show no effect of temperature on Deff (e.g. Greenwald and Kanter, 1979). Thus, the impact of temperature on Deff is much lower than the effects of temperature on the rate of digestion. We did not measure Eexc, so our study does not allow for a direct evaluation of Deff in Python. Nevertheless, by integrating the SDA response at the different temperatures we can evaluate whether metabolic costs associated with digestion (i.e. the SDA coefficient, Table 1 and Fig. 3) of a meal is affected by temperature. The estimated SDA coefficient ranged between 28 and 31% in the temperature span of 25–35 8C and the means at these temperatures were not significantly different. The SDA coefficients determined in the present study are in good agreement with previous studies on Python (Vinegar et al., 1970; Secor and Diamond, 2000). Because the SDA coefficient remains remarkably constant over the entire temperature range investigated here, it seems that the energetic costs associated with digestion is temperature independent. As in Python (Table 1, Fig. 3), the SDA coefficient does not vary with temperature in the toad Ceratophrys cranwelli and in the plaice Pleuronectes platessa (Powell et al., 1999; Jobling and Davies, 1980). 4. Conclusion Python exhibit a large metabolic response to digestion and the temporal changes in oxygen consumption following feeding are influenced by
525
temperature. In spite of temporal differences at the different temperatures the overall costs of digestion (i.e. the SDA coefficient) appears temperature insensitive. The data on the Python are consistent with previous descriptions on the effects of temperature on digestion in other species of reptiles, and it appears that the digestive efficiency is only minimally affected by temperature in most species. Therefore, the primary effect of increasing body temperature during digestion (postprandial thermophily) seems to be a marked reduction of the time required for digestion rather than an energetic saving or increased efficiency of digestion. During environmental conditions where suitable prey items are readily available, the faster rate of digestion with increased body temperature may enable higher consumption and growth rates. In addition, the locomotor performance of reptiles is reduced substantially during the postprandial period (e.g. Garland and Arnold, 1983; Huey et al., 1984; cf. Ford, 1986) and it may be advantageous to reduce the duration of digestive period because of increased risk of predation. Acknowledgments This study was supported by The Danish Research Council. We thank Dr Stephen Jay Warburton for discussion of the data and comments on the manuscript. References Bedford, G.S., Christian, K.A., 2000. Digestive efficiency in some Australian pythons. Copeia 2000, 829–834. Benedict, F.G., 1932. The Physiology of Large Reptiles with Special Reference to the Heat Production of Snakes, Tortoises, Lizards and Alligators. Carnegie Inst. Publ, Washington. Chappell, M.A., Ellis, T.M., 1987. Resting metabolic rates in boid snakes: allometric relationships and temperature effects. J. Comp. Physiol. B 157, 227–235. Cowles, R.B., Bogert, B.C.M., 1944. A preliminary study on the thermal requirements of desert reptiles. Bull. Am. Mus. Nat. Hist. 83, 261–267. Dandrifosse, G., 1974. Digestion in reptiles. In: Florkin, M., Scheer, B. (Eds.), Amphibia and Reptila, Vol. 9. Academic Press, New York, pp. 249–276. Dawson, W.R., 1975. On the physiological significance of the preferred body temperatures of reptiles. In: Gates, D.M., Schmerl, R.B. (Eds.), Perspectives in Ecological Ecology. Springer, New York, pp. 443–473.
526
T. Wang et al. / Comparative Biochemistry and Physiology Part A 133 (2003) 519–527
Dorcas, M.E., Peterson, C.R., Flint, M.E., 1997. The thermal biology of digestion in rubber Boas (Charina bottae): physiology, behavior, and environmental constraints. Physiol. Zool. 70, 292–300. 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. A 51, 259–265. Diefenbach, C.O., 1975b. Gastric function in Caiman crocodilus (Crocodylia: Reptilia). II. Effects of temperature on pH and proteolysis. Comp. Biochem. Physiol. A 51, 267–274. Ford, N.B., 1986. Effects of variation in food intake on locomotor performance of juvenile snakes. Copeia 1986, 999–1001. Garland, T., Arnold, S.J., 1983. Effects of a full stomach on locomotory performance of juvenile garter snakes (Thamnophis elegans). Copeia 1983, 1092–1096. Gessaman, J.A., Nagy, K.A., 1988. Energy metabolism: errors in gas-exchange conversion factors. Physiol. Zool. 61, 507–513. Greenwald, O.E., 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. Harlow, H.J., Hillman, S.S., Hoffman, M., 1976. The effect of temperature on digestive efficiency in the herbivorous lizard, Dipsosaurus dorsalis. J. Comp. Physiol. 111, 1–6. Henderson, R.W., 1970. Feeding behaviour, digestion and water requirements of Diadophis punctatus arnyi Kennicott. Herpetologica 26, 520–526. Huey, R.B., Bennett, A.F., John-Alder, H., Nagy, K.A., 1984. Locomotor capacity and foraging behaviour of Kalahari lacerid lizards. Anim. Behav. 32, 41–50. Huey, R.B., Niewiarowski, P.H., Kaufmann, J., Herron, J.C., 1989. Thermal biology of nocturnal ectotherms: is sprint performance of geckos maximal at low body temperatures? Physiol. Zool. 62, 488–504. Jackson, K., Perry, G., 2000. Changes in intestinal morphology following feeding in the brown treesnake, Boiga irregularis. J. Herpetol. 34, 459–462. Jobling, M., Davies, P.S., 1980. Effects of feeding on metabolic rate, and the specific dynamic action in plaice, Pleuronectes platessa L. J. Fish Biol. 16, 629–638. Licht, P., 1964. The temperature dependence of myosin adenosine triphosphate and alkaline phosphatase in lizards. Comp. Biochem. Physiol. 12, 331–341. Lillywhite H.B., de Delva, P., Noonan, B.P. Patterns of gut passage time and the chronic retention of fecal mass in viperid snakes (in press). 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. Mitchell, H.H., 1964. Comparative Nutrition of Man and Animals, Academic Press, New York 840 pp. Naulleau, G., 1983. The effects of temperature on digestion in Vipera aspis. J. Herpetol. 17, 166–170.
Overgaard, J., Busk, M., Hicks, J.W., Jensen, F.B., Wang, T., 1999. Respiratory consequences of feeding in the snake Python molurus. Comp. Biochem. Physiol. A 124, 359–365. Overgaard, J., Andersen, J.A., Wang, T. The effects of fasting duration on the metabolic response to feeding in Python: An evaluation of the energetic costs associated with intestinal growth. Physiol. Biochem. Zool. (in press). Peterson, C.R., Gibson, A.R., Dorcas, M.E., 1993. Snake thermal ecology: the causes and consequences of body temperature variation. In: Seigel, R.A., Collins, J.T. (Eds.), Snakes: Ecology and Behavior. McGraw-Hill, New York, pp. 241–314. Powell, M.K., Mansfeld-Jones, J., Gatten, R.E., 1999. Specific dynamic effect in the horned frog Ceratophrys cranwelli. Copeia 1999, 710–717. Regal, P.J., 1966. Thermophilic responses following feeding in certain reptiles. Copeia 1966, 588–590. Riddle, O., 1909. The rate of digestion in cold blooded vertebrates. The influence of season and temperature. Am. J. Physiol. 24, 447–458. Secor, S.M., Diamond, J., 1995. Adaptive responses to feeding in Burmese pythons: pay before pumping. J. Exp. Biol. 198, 1313–1325. Secor, S.M., Diamond, J., 1997. Effects of meal size on postprandial responses in juvenile Burmese pythons (Python molurus). Am. J. Physiol. 272, R902–R912. Secor, S.M., Diamond, J., 2000. Evolution of the digestive responses to feeding in snakes. Physiol. Biochem. Zool. 73, 123–141. Shine, R., Harlow, P.S., Keogh, J., Boeadi, S., 2001. The influence of sex and body size on food habits of a giant tropical snake, Python reticulatus. Func. Ecol. 12, 248–258. Skoczylas, R., 1970. Influence of temperature on gastric digestion in the grass snake, Natrix natrix L. Comp. Biochem. Physiol. 33, 793–803. Skoczylas, R., 1970. Salivary and gastric juice secretion in the grass snake, Natrix natrix L. Comp. Biochem. Physiol. 35, 885–903. Skoczylas, R., 1978. Physiology of the digestive tract. In: Gans, C., Gans, K.A. (Eds.), Biology of the Reptilia, Vol. 8. Academic Press, New York, pp. 589–717. Starck, J.M., Beese, K., 2001. Structural flexibility of the intestine of Burmese python in response to feeding. J. Exp. Biol. 204, 325–335. Starck, J.M., 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., 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. Vinegar, A., Hutchison, V.H., Dowling, H.G., 1970. Metabolism, energetics and thermoregulation during brooding of snakes of the genus Python (Reptilia, Boidae). Zoologica 55, 9–48. Vleck, D., 1987. Measurement of O2 consumption, CO2 production, and water vapor production in a closed system. J. Appl. Physiol. 62, 2103–2106.
T. Wang et al. / Comparative Biochemistry and Physiology Part A 133 (2003) 519–527 Waldschmidt, S.R., Jones, S.M., Porter, W.P., 1986. The effect of body temperature and feeding regime on activity, passagetime, and digestive coefficient in the lizard Uta stansburiana. Physiol. Zool. 59, 376–383. Wall, M.F., 1912. A popular treatise on the common Indian snakes. J. Bombay Nat. Hist. Soc. 21, 447–475.
527
Wang, T., Busk, M., Overgaard, J., 2001. The respiratory consequences of feeding in amphibians and reptiles. Comp. Biochem. Physiol. A 128, 535–549. Windell, J.T., Sarokon, J.A., 1976. Rate of gastric evacuation in the lizard, Anolis caroliensis (Sauria: Iguanidae). Herpetologica 32, 18–23.
