TRANSACTIONS OF THE KANSAS ACADEMY OF SCIENCE Vol. 109, no. 3/4 p. 184-190 (2006) Influence of meal size on postprandial thermophily in cornsnakes (Elaphe guttata) LYNETT R. BONTRAGER, DAPHNE M. JONES, AND LYNNETTE M. SIEVERT 1 Department of Biological Sciences, Emporia State University, 1200 Commercial Street, Emporia, Kansas 66801 1. Corresponding author (lsievert@emporia.edu) Postprandial thermophily occurs because snakes presumably select body temperatures to maximize digestive functions. However, there seems to be little to no literature available on meal size affecting the degree of postprandial thermophily in snakes. We were interested in determining if meal size influenced post-feeding thermoregulation. To test this, we placed individual snakes into linear thermal gradients with floor temperatures ranging from 10 ± 0.5º C to 40 ± 1.0º C. After a 24 h habituation period, substrate temperatures were measured underneath the snake s body, 1/3 of the way down its length, at 3-hour intervals from 0900 to 1800 h. Each snake was monitored under three different conditions: during a fast, after ingesting a 5% body mass meal, and after ingesting a 10% body mass meal. The size of the meal had a significant effect (P=0.0365) on selected substrate temperatures. Keywords: body temperatures, meal size, post-feeding thermoregulation, snakes INTRODUCTION Postprandial thermophily is an increase in selected body temperature following a meal. Snakes accomplish this by selecting appropriate habitat that allows the individual to heat. By selecting higher body temperatures the snake incurs a higher metabolic cost, but shortens digestion time (Tattersall et al., 2004) allowing the snake to decrease the interval between meals. Over time, a snake that selects higher post-feeding body temperatures can potentially consume more food than a snake that does not display postprandial thermophily, if prey are readily available. The physiological performance and individual fitness of snakes may depend on opportunities to thermoregulate because not only is digestion temperature dependent, but so are a number of other physiological functions (Dorcas, Hopkins, and Roe, 2004; Wang et al., 2003). There is no single optimal temperature for a snake, therefore alterations in selected body temperature are expected in response to changes in physiological conditions such as whether the snake has just fed or not (Tu and Hutchison, 1995; Blouin-Demers and Weatherhead, 2001; Sievert and Andreadis, 1999; Sievert, Jones, and Puckett, 2005). Previous experiments with cornsnakes (Greenwald and Kanter, 1979; Roark and Dorcas, 2000; Sievert, Jones, and Puckett, 2005) as well as rough greensnakes, Oepheodrys aestivus, northern water snakes, Nerodia sipedon, and black ratsnakes, Elaphe obsoleta, showed higher temperature selection after feeding (Touzeau and Sievert, 1993; Sievert and Andreadis, 1999; Lutterschmidt and Reinert, 1990; Blouin-Demers and Weatherhead, 2001). Despite reports to support it, postprandial thermophily is not characteristic of all snake species (Blouin- Demers and Weatherhead, 2001). The striped racer, Masticophis lateralis, which maintains high body temperatures, did not increase body temperature after eating (Hammerson, 1979) nor did the semiaquatic diamond-backed watersnake, Nerodia rhombifer (Tu and Hutchison, 1995).
Transactions of the Kansas Academy of Science 109(3/4), 2006 185 Elevating body temperature increases rates of digestion and absorption (Sievert and Andreadis, 1999; Tu and Hutchison, 1995) thereby closely linking behavioral thermoregulation to digestion. The adaptive value of postprandial thermophily to juvenile snakes is that it speeds digestive rate allowing youngsters to eat more frequently and grow more rapidly (Sievert and Andreadis, 1999). For adults the advantage is that it allows them to eat more frequently and thereby allocate more energy to reproduction, growth, and maintenance. Previous studies on postprandial thermophily in snakes have not controlled for meal size and focused only on whether the animal had eaten or not. Therefore, the purpose of our experiment was to determine if meal size affected thermoregulatory behavior in cornsnakes. We hypothesized that as meal size increased, so would postprandial thermophily. We chose cornsnakes as subjects for a number of reasons. Cornsnakes eat readily in a laboratory and can easily consume a wide range of meal sizes; they adjust well to captivity and interacting with humans; and they readily thermoregulate in a laboratory setting (Roark and Dorcas, 2000; Sievert, Jones, and Puckett, 2005). MATERIALS AND METHODS Twelve captive bred amelanistic cornsnakes, Elaphe guttata, ranging in mass from 66.1 to 136.6 g were housed in a 27 ± 0.5º C environmental chamber on a 12L:12D photoperiod with photophase beginning at 0800 h. Each snake was housed in a ventilated plastic container lined with newspaper, provided a PVC pipe shelter, given water ad libitum, and fed weekly prior to experimentation. We weighed each snake and then placed it individually into one of three 153 cm wide x 29 cm deep x 26 cm high linear thermal gradients with aluminum flooring and a clear acrylic lid, located inside a walk-in environmental chamber set at 10 ± 0.5º C. The snakes were habituated for 24 h within the thermal gradients before data collection and water was provided ad libitum during habituation and testing. Each thermal gradient was fitted with a 12 cm wide strip of foam board extending from the base of the wall at a 45º angle down the length of one side of the gradient which provided a retreat within the full range of temperatures along the entire length of the thermal gradient. The thermal gradient was maintained with two subsurface heating pads (15 x 20 cm, 2.5 W/ in 2, Omega Engineering, Inc. Stamford, CT USA) placed beneath the aluminum flooring; one 10 cm from the end maintained the floor at 40 ± 1º C and the second 34 cm from the same end maintained the floor at 28 ± 2º C. Heating pad temperatures were controlled by a Dyna-Sense electronic temperature controller (Scientific Instruments, Inc. Model 2201 Skokie, IL USA). Substrate temperatures beneath the snake approximately one-third of the way down the length of the snake, between the heart and stomach, were measured with a thermocouple attached to a Datalogger (Kane May KM1242). The snakes typically remained stationary and/or coiled up under the retreat while in the thermal gradient. Substrate temperature under the snake was measured at 0900, 1200, 1500 and 1800 hours. We chose to use substrate temperature as a measurement of selected body temperature because thermocouples inserted into the snake s cloaca interfere with temperature selection in small snakes (Tsai and Tu, 2005). Also, a long, thin animal may have distinctly different cloacal and stomach temperatures (Sievert, Jones and Puckett, 2005) and using a transmitter fed to a snake would induce thermophily even if the snake had not eaten food (Lutterschmidt and Reinert, 1990). Each snake was monitored during three conditions: fasted for five days, fed a 5% body mass mouse meal after the
186 Bontrager, Jones and Sievert Table 1. Two-way Analysis of Variance table for the effect of meal size and time of day on temperature selection of cornsnakes. Key: DF = Degrees of Freedom SS = Sum of Squares MSS = Mean Squares F = F-value P = Probability 0900 h temperature reading, and fed a 10% body mass mouse meal after the 0900 h temperature reading. Prior to feeding, snakes were fasted for five days. We fasted one-third of the snakes the first time they were in a thermal gradient; one-third were fed a 5% meal, and one-third were fed a 10% meal. The snakes were rotated through each treatment as well as through each of the three thermal gradients. The same 12L:12D photoperiod to which the snakes were acclimated was maintained during the experiment. Each gradient was cleaned after every use. A two-way repeated measures Analysis of Variance (ANOVA) was performed to determine if there was an effect of treatment group or time since feeding on temperature selection for the 1200, 1500, or 1800 h readings. A Student Neuman Keuls (SNK) test determined if differences existed among treatment groups at any of the three times. A one-way ANOVA determined if temperature selection within a treatment group varied over time. Values were considered significant at P < 0.05 and temperature values are reported as mean ± SE. RESULTS The 0900 h values were excluded from the two-way ANOVA because all snakes were still fasted at that time. As expected, all three groups selected similar temperatures at this time (P=0.329, df=2, F=1.151). We found that from 1200 to 1800 h there was an effect of treatment and time since feeding on substrate temperature selection, but the group by time interaction was not significant (Table 1). A significant effect of group existed at 1200 h (P=0.032, df=2, F=3.814) with the 10% group selecting significantly higher (P=0.030) substrate temperatures than the fasted group (Fig. 1). The SNK test demonstrated that at 1500 h and 1800 h no significant differences existed among substrate temperature selected by the treatment groups (1500: P=0.084, df =2, F = 2.68; 1800: P=0.612, df=2, F=0.4980). The mean substrate temperatures selected by the snakes between 1200 and 1800 h were 24.2 ± 0.6 C for the fasted group, 25.7 ± 0.5 C for the 5% meal group, and 26.7 ± 0.5 C for the 10% meal group (Fig. 1). The one-way ANOVA showed a significant difference in temperature selection over time for fasted snakes, but it neared nonsignificance (P = 0.048, df = 3, F = 2.93) and the SNK test did not find significant differences among any of the four times. The 5% treatment group did not select significantly different substrate temperatures over time (P = 0.867, df = 3, F = 0.24) but the
Transactions of the Kansas Academy of Science 109(3/4), 2006 187 Figure 1. Substrate temperatures selected by 12 juvenile cornsnakes after being fasted or fed a meal equal to 5 or 10% of their body mass. The vertical bars represent 1 SEM. 10% treatment group did (P = 0.003, df = 3, F = 5.646). This group had significantly higher selected temperatures at all times after feeding than at 0900 h when the snakes were still fasted (fasted vs. 1200 h, P = 0.021; fasted vs. 1500 h, P = 0.002; fasted vs. 1800 h, P = 0.015). DISCUSSION Body temperature influences a variety of functions in ectotherms such as growth and development, reproductive physiology, cardiovascular physiology, metabolism, digestion, and locomotion (Lillywhite, 1987; Dorcas, Hopkins, and Roe, 2004). Although it may appear that not having the ability to maintain a constant temperature by physiological means would be detrimental, in reality it allows animals to select body temperatures that are appropriate at a given point in time. If physiological conditions change, the animal can inexpensively change its body temperature by behavioral thermoregulation. Postprandial thermophily in snakes has been known for some time (Regal, 1966), but despite this, many aspects of postprandial thermophily remain unknown. Not all snakes display postprandial thermophily and, for most species where postprandial thermophily has been documented in the lab, it is unknown as to whether it occurs in the field (Blouin- Demers and Weatherhead, 2001). Although thermoregulation can increase body temperature and thereby speed digestion or at least prevent the prey from putrifying in the snake s digestive system causing regurgitation or death, a large snake that has eaten a large
188 Bontrager, Jones and Sievert meal may be less able to flee a predator and therefore may avoid exposed thermoregulation sites (Blouin-Demers and Weatherhead, 2001). As a group, snakes exhibit extremes in meal size and frequency from very small, frequent meals, as seen in greensnakes, ringneck snakes and others, to large, infrequent meals which may exceed the mass of a snake (Greene, 1997). Despite this and the general acceptance of postprandial thermophily, there is no literature concerning the effect of meal size on temperature selection and we lack sufficient data to make generalizations about postprandial thermophily in snakes (Blouin-Demers and Weatherhead, 2001). Our results showed that meal size influenced the temperature selection of juvenile cornsnakes yet the 5% body mass meal caused no significant increase in temperature selection in those snakes relative to the fasted snakes, which indicates a possible meal size threshold for postprandial thermophily. Also, the snakes fed the 5% body mass meal selected similar substrate temperatures both before and after feeding. In contrast, after ingesting a meal of 10% body mass, snakes selected higher temperatures than before feeding. This suggests that the amount of food in the gut must be of sufficient size if it is to influence thermoregulatory behavior in cornsnakes. Although our data imply that meal size is important in postprandial thermophily, it would be helpful to examine the effect of a larger meal on temperature selection since cornsnakes can readily eat meals much greater than 10% of their body mass. Given the range in meal sizes eaten by many snakes, the lack of data on the effect of meal size on postprandial thermophily is surprising. Two possible alternatives exist for snake species demonstrating postprandial thermophily in the lab: 1) postprandial thermophily is not influenced by meal size, or 2) the degree of postprandial thermophily is a function of meal size. Optimal temperatures for digestion have been demonstrated in reptiles (Toledo, Abe, and Andrade, 2003; Dorcas, Peterson, and Flint, 1997; Du, Yan, and Ji, 2000). Selecting an optimal body temperature for digestion decreases the time spent on digestion per meal and thereby decreases the interval between meals and allows greater prey consumption over time. Therefore any meal, regardless of size, may elicit the same degree of postprandial thermophily. Alternative two might occur if small meals do not greatly impact locomotion and can be digested relatively quickly even without increasing body temperature to the optimum for digestion. In this case the postprandial response may be dependent on meal size because as meal size increases digestion time increases and the impact on locomotion increases. Although a snake can decrease the time it takes to digest and regain full locomotor capability by increasing body temperature, this comes at the cost of increased metabolism. After ingesting a small meal it might be advantageous to maintain pre-feeding body temperature or only increase it slightly to avoid elevating metabolism due to thermophily whereas after a large meal it may be important to speed digestion to decrease both the time until the snake can feed again and the time spent with impaired locomotor ability (Blouin-Demers and Weatherhead, 2001). Our data suggest the latter for cornsnakes, but more data are needed to confirm this. It is possible that some snake species exhibit the first alternative and others the second. Factors such as the risk of predation during thermoregulation, whether the species is nocturnal or diurnal, and ease of finding suitable thermoregulation sites may influence postprandial thermophily. Lastly, because we only measured body temperature during daytime hours our results must be considered tentative until data for the entire 24 h period exists. Cornsnakes are diurnal during the cooler portions of their activity season but become increasingly nocturnal when it is hot (Bartlett and Bartlett, 2003).
Transactions of the Kansas Academy of Science 109(3/4), 2006 189 Our snakes ranged from 66 to 137 g during this study. We did not determine if body mass influenced temperature selection because our snakes were growing throughout the experiment and therefore there were confounding effects of age, time of year, and experience in the gradient associated with mass. There is evidence that age and/or body size may influence postprandial thermophily in cornsnakes. Adult cornsnakes (Greenwald and Kanter, 1979) and those in the current study selected postprandial temperatures of about 26 C whereas youngsters selected postprandial temperatures of about 29 C in a thermal gradient after feeding (Roark and Dorcas, 2000; Sievert, Jones, and Puckett, 2005). Given that the procedures used by Sievert, Jones, and Puckett are identical to those used in the current study it is unlikely that methodology contributed to these differences. Younger snakes may have a greater need to eat as often as possible to rapidly attain a larger size and postprandial thermophily would aid in speeding digestion. Young snakes, due to their small size, can more easily attain higher temperatures and, if they become too warm, can quickly cool down. ACKNOWLEDGEMENTS This work was supported by the NIH Grant # P20 RR16475 from then BRIN program of the National Center for Research Resources and the Department of Biological Sciences at Emporia State University. We thank R. Ferguson for building the thermal gradients and G. Sievert for providing the snakes. This work was approved by Emporia State University s Institutional Animal Care and Use Committee (ESU-ACUC-02-014 and ESU-ACUC-02-013). LITERATURE CITED Bartlett, R.D. and Bartlett, P. 2003. Florida s Snakes: a guide to their identification and habits. University Press of Florida. Gainesville, 182 p. 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. Journal of Animal Ecology 70, p. 1006-1013. Dorcas, M.E., Hopkins, W.A. and Roe, J.H. 2004. Effects of body mass and temperature on standard metabolic rate in the eastern diamondback rattlesnake (Crotalus adamanteus). Copeia 2004, p. 145-151. Dorcas, M.E., Peterson, C.R. and Flint, M.E.T. 1997. The thermal biology of digestion in rubber boas (Charina bottae): physiology, behavior, and environmental constraints. Physiological Zoology 70, p. 292-300. Du, W-G., Yan, S-J. and Ji, X. 2000. Selected body temperature, thermal tolerance and thermal dependence of food assimilation and locomotor performance in adult bluetailed skinks, Eumeces elegans. Journal of Thermal Biology 25, p. 97-202. Greene, H.W. 1997. Snakes: the evolution of mystery in nature. University of California Press, Berkeley, California, 366 p. Greenwald, O.E. and Kanter, M.E. 1979. The effect of temperature and behavioral thermoregulation on digestive efficiency and rate in corn snakes (Elaphe guttata guttata). Physiological Zoology 52, p. 398-408. Hammerson, G.A. 1979. Thermal ecology of the striped racer, Masticophis lateralis. Herpetologica 35:267-273.
190 Bontrager, Jones and Sievert Lillywhite, H.B. 1987. Temperature, energetics, and physiological ecology. p. 422-477 In Seigel, R.A., Collins, J.T. and Novak, S.S. (eds.), Snakes. Ecology and Evolutionary Biology, MacMillan Press, New York. Lutterschmidt, W.I. and Reinert, H.K. 1990. The effect of ingested transmitters upon the temperature preference of the northern water snake, Nerodia s. sipedon. Herpetologica 46, p. 39-42. Regal, P.J. 1966. Thermophilic response following feeding in certain reptiles. Copeia 1966, p. 588-590. Roark, A.W. and Dorcas, M.E. 2000. Regional body temperature variation in corn snakes measured using temperaturesensitive passive integrated transponders. Journal of Herpetology 34, p. 481-485. Sievert, L.M. and Andreadis, P. 1999. Specific dynamic action and postprandial thermophily in juvenile northern water snakes, Nerodia sipedon. Journal of Thermal Biology 24, p. 51-55. Sievert, L.M., Jones, D.M. and Puckett, M.W. 2005. Postprandial thermophily, transit rate, and digestive efficiency of juvenile cornsnakes, Pantherophis guttatus. Journal of Thermal Biology 30, p. 354-359. Tattersall, G.J., Milson, W.K., Abe, A.S., Brito, S.P. and Andrade, D.V. 2004. The thermogenesis of digestion in rattlesnakes. Journal of Experimental Biology 207, p. 579-585. Toledo, L.F., Abe, A.S. and Andrade, D.V. 2003. Temperature and meal size effects on the postprandial metabolism and energetics in a boid snake. Physiological and Biochemical Zoology 76, p. 240-246. Touzeau, T. and Sievert, L.M. 1993. Postprandial thermophily in rough green snakes. Copeia 1993, p. 1174-1176. Tsai, T-S. and Tu, M-C. 2005. Postprandial thermophily of Chinese green tree vipers, Trimeresurus s. stejnegeri: interfering factors on snake temperature selection in a thigmothermal gradient. Journal of Thermal Biology 30, p. 423-430. Tu, M-C. and Hutchison, V.H. 1995. Thermoregulatory behavior is not influenced by sex or ecdysis in diamondback water snakes, Nerodia rhombifera. Journal of Herpetology 29, p. 146-148. 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. Comparative Biochemistry and Physiology 133A, p. 519-527.