Behavioural Processes 49 (2000) 61–68 www.elsevier.com/locate/behavproc Behavioural rise in body temperature and tachycardia by handling of a turtle (Clemmys insculpta) Michel Cabanac *, Ce´cile Bernieri De´partement de Physiologie, Faculte´deMe´decine, Uni6ersite´La6al, Que´., Canada G1K 7P4 Received 20 September 1999; received in revised form 13 December 1999; accepted 17 December 1999 Abstract Three turtles, Clemmys insculpta, were kept together in a terrarium in a climatic chamber at 18°C, with lights on at 07:00 h and off at 19:00 h. In one corner of the terrarium an infrared lamp produced an operative temperature of 42.5°C, thereby allowing behavioral temperature regulation during the light period. When the turtles were handled only once a day for the purpose of taking cloacal temperature, their body temperature held stable at about 22–23°C. Immediately after being handled the turtles sought the radiant heat and regulated their body temperature at about 4°C higher than before the handling. When repeatedly handled every 15 min for 2 h the turtles maintained a high body temperature by their behavior. When not repeatedly handled the turtles returned to their initial preferred body temperature ca 22–23°C within 2 h. It is hypothesized that handling causes in turtles a fever similar to that observed in stressed mammals. The turtles were equipped with an electrocardiogram radio transmitter and their heart rate was recorded at a distance. Heart rate in undisturbed turtles was 28.390.6 bt/min. During a 1-min handling, their heart rate rose to 40.290.8 bt/min. This tachycardia persisted several minutes, then their heart rate returned to the baseline value in ca. 10 min. Stress fever and tachycardia are taken as signs of emotion in turtles. © 2000 Elsevier Science B.V. All rights reserved. Keywords: Reptile; Emotion; Heart rate; Fever; Body temperature; Thermopreferendum 1. Introduction known since the beginning of this century (Krehl and Sœtbeer, 1899; Langlois, 1902). A logical The capacity of reptiles to regulate their body extension of that knowledge is the recognition temperature through behavioral means has been that reptiles can have fever: the upper resetting of the body thermostat in response to bacterial or viral infection. * Corresponding author. Tel.: +1-418-6563068; fax: +1- 418-6567898. Fever is distinguishable from hyperthermia in E-mail address: [email protected] (M. Ca- that the thermoregulatory responses promote ris- banac) ing body temperature in the former, and oppose it 0376-6357/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved. PII: S0376-6357(00)00067-X 62 M. Cabanac, C. Bernieri / Beha6ioural Processes 49 (2000) 61–68 in the latter. Since they virtually possess no auto- 2. Materials and methods nomic thermoregulatory responses, ectotherms, 2.1. Animals and maintenance when feverish should produce and maintain their fever behaviorally. This has been demonstrated Three amphibious turtles Clemmys insculpta, experimentally: the lizard Dipsosaurus dorsalis se- native to Canada, served as subjects. The animals lected a warmer environment and thus raised its were lent by the E´ comuse´e de la Socie´te´ d’histoire body temperature after being injected with pyreto- naturelle de la valle´e du Saint-Laurent, on the gens (Vaughn et al., 1974). Such a behavioral condition that they undergo no surgery or inva- fever had survival value in that lizard (Kluger et sive treatment. They weighed 1300 g (male), 1060 al., 1975). Behavioral fever has been shown to g (female 1), and 1040 g (female 2). The animals exist in other ectothermic vertebrates, in shared the same common terrarium of 1 m×1 arthropods (also with improved survival value m×0.5 m. The terrarium floor was covered with (Louis et al., 1986)), and in annelids (see reviews a 50 mm layer of sand. A container provided in Kluger (1979) and in Cabanac (1990)). water ad lib. Twice a week the turtles were fed Negative results in reptiles are puzzling in this with Iams® canned dog food, fresh apples, car- context. It has been reported recently that some rots, and Roman lettuce. No change in preferred Old World reptiles seem to not have the ability to body temperature was observed after food intake. develop a fever response. The main argument in This was not systematically recorded because food these studies is that lizards (Laburn et al., 1987), intake did not seem to influence the preferred snakes (Zurovsky et al., 1987a), and turtles body temperature of some other reptiles, the (Zurovsky et al., 1987b) injected with bacterial iguanid lizard Crotaphytus collaris (Sievert, 1989; pyretogens show the same behavior when injected Ming-Chun and Hutchinson, 1995) (interested with the vehicle in control sessions. Yet, a close readers will find this point reviewed in Ming- examination of the data provided in these articles Chun and Hutchinson (1995)). In addition, even if shows that the similarity between pyretogen-in- there were a change in prefered temperature, such jected and control animals was not due to an an influence would not have interfered with the absence of temperature rise after the injection of short-term responses to stress because each ani- pyretogens, but rather from an equal rise in con- mal was its own control over short sessions. trol sessions. The problem of no fever in Old 2.2. Thermoregulatory beha6ior World reptiles seems to lie in the control sessions. This has been confirmed in lizards Callopistes The terrarium was located in a climatic cham- maculatus, which moved toward a heat source and ber set at 18°C. In one corner of the terrarium a raised their core temperature when simply han- 250-W infrared lamp went on and off at the same dled (Cabanac and Gosselin 1993), thus confirm- time as the rooms lights. The operative tempera- ing that during control sessions the reptiles of ture, recorded from a thermocouple in the center Laburn et al. (1987), and of Zurovsky et al. of a glass bottle approximately the size of a turtle, (1987a,b) might have raised their body tempera- was about 42.5°C beneath the lamp. The animals ture by behavioral means, because of the stress of could therefore behaviorally thermoregulate by being handled. Since taxonomic differences have alternating their position from one end of the been reported, it is of interest to explore the terrarium at 18°C to the other beneath the in- emotional responses of other reptiles. In the frared lamp at 42.5°C. The animals therefore had present study, we used turtles in an attempt to access to a temperature gradient of 24.5°C over 1 replicate with very different reptiles the results m. On top of the infrared lamp, an ultraviolet obtained previously with lizards. In addition to bulb (75-W Repti™-Basking-Spot lamp, especially the thermoregulatory response occurring after devised for reptilian UV irradiation), serving to handling, we used another index of stress, the prevent vitamin deficiency, went on and off at the heart rate response. same time. All lights were on from 07:00–19:00 h. M. Cabanac, C. Bernieri / Beha6ioural Processes 49 (2000) 61–68 63 2.3. Body temperature and stress of the three animals. At the end of a 2-h session of repeated cloacal temperature recordings, the Recording of body temperature implied picking animals were left alone for 2 h. After the delay, up the animal from its terrarium, handling and their coacal temperatures were taken again once. immobilizing it in a supine position, and introduc- For the measurement of their heart rate re- ing the tip of a thermocouple into the cloaca. The sponses, one turtle at a time was equipped with thermocouple was introduced at least 30 mm from the radiotransmitter then left alone for at least 15 the anus. Body temperature was displayed digi- min and its access to the warm corner of the tally on the screen of an electronic thermometer terrarium was prevented by a physical barrier. (Exacon, model MC9200) with an accuracy of Then after a 5-min recording of its baseline heart 0.1°C. The handling of the temperature taking rate, the animal was picked up by an experimenter served as the stressful stimulus. and handled for 1 min. Then the turtle was put back in the cool corner (behind the barrier) and 2.4. Heart rate its heart rate was recorded for 15 min. A small radio transmitter (Data Science Inter- 2.6. Statistics national, model TA10CA-F40) was taped to the turtles back and the electrocardiogram was All data were averaged for each animal, then recorded between two electrodes. One electrode the overall mean was computed for the group of was located in the cloaca and the wire was taped three turtles. ANOVA or ANOVA for repeated to the animals tail. A surface electrode, covered measures, then post-hoc Fisher tests when appro- with conductive paste, was glued to the skin be- priate, were used to test the significance of the tween the forelimb and the neck. The electrocar- differences observed. diographic signal was recorded at a distance and the heart rate was counted and recorded minute by minute during the 15 min following the 3. Results handling. 3.1. Handling 2.5. Procedures Fig. 1 shows the mean cloacal temperature In order to obtain baseline measurements and during the light period of the nycthemeron. It can to check whether there was a nycthemeral cycle of be seen that when the cloacal temperature was core temperature, the body temperatures of the taken only once a day, the result was steady at undisturbed turtles were obtained by taking the 23.590.3°C, i.e.