Behavioural Rise in Body Temperature and Tachycardia by Handling of a Turtle (Clemmys Insculpta)

Home , Callopistes maculatus, Sudan plated lizard

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´ comuseé de la Socie´te´ d’histoire body temperature after being injected with pyreto- naturelle de la valleé 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. 5.5°C above the ambient temper- cloacal temperature only once a day, at various ature of the climatic chamber. Such a difference times of day on different days. For each hour of between body and ambient temperatures was the day, each animal was measured up to three achieved by periodic basking of the turtles be- times, but these measurements took place on dif- neath the infrared lamp. It can be seen also that ferent days. as soon as the infrared lamp was on, the turtles The influence of behavioral stress on the turtles sought heat and warmed themselves, but that no body temperature was studied following the same nycthemeral cycling was visible during the lighting procedure: at 12:30 h an initial body temperature period. was obtained as described above. Then the turtle Fig. 2 shows the influence of handling, and was returned to the place in the terrarium where it repeatedly taking body temperatures. It can be had been picked up. This measurement was re- seen that handling was followed by a rise in mean peated every 15 min for 2 h, i.e. until 14:30 h. body temperature produced by the animals heat- The duration of the influence of stress on tem- seeking behavior. Body temperature then stabi- perature preference was investigated once in each lized at a mean of 25.990.2°C. It should be 64 M. Cabanac, C. Bernieri / Beha6ioural Processes 49 (2000) 61–68 remembered that in a turtle there is no metabolic means to raise body temperature; the only way to raise body temperature is through behavior. This result may be described, therefore, as a regulation of body temperature at a higher level, i.e. at a set-point higher during and after handling than in the baseline state. The animals became feverish after being handled.

3.2. Duration of stress

Body temperature 2 h after it was last taken did not differ from normal data. Mean (9S.E.) cloacal temperature was: 21.690.9°C before handling, 26.490.8°C* during handling, and

Fig. 2. Time course of the mean (9S.E.) cloacal temperature

(Tcl) of three C. insculpta when handled every 15 min, for 2 h. The ambient temperature in the climatic chamber was set at

18°C. The rise of (Tcl) was due to the animals behavioral seeking of infrared heat, as they have no autonomic means to raise their body temperature. Beneath the infrared bulb, the operative temperature was 42.5°C. The columns marked *, are signiﬁcantly different from each other and from all other columns (ANOVA for repeated measures, PB0.02, post hoc Fisher test).

22.890.7°C 2 h after handling (* ANOVA, f= 26.42, df=2, P=0.005) shows that after a 2-h delay the mean body temperature had returned to its baseline value. This conﬁrms the transient origin of the elevated temperature obtained when the animals were handled.

Fig. 1. Time course of the cloacal temperature (Tcl) of three C. insculpta when taken only once a day, on separate days. Each 9 dot is the mean ( S.E.) of the mean measurements from each 3.3. Heart rate of the three animals. The black bars on top of the figure indicate the end and the beginning of the dark period when neither the light nor the infrared bulb were on. At 07:00 h the Fig. 3 shows the mean heart rate recorded three animals body temperatures were the same as that of the before, during, and 15 min after handling. It can climatic chamber, i.e. 18.3°C. * This recording being signifi- be seen that the mean heart rate immediately rose B cantly different from all other recordings (ANOVA, P 0.02, significantly upon handling. The tachycardia post hoc Fisher test). When the infrared bulb was turned on, the three animals immediately moved to the warm area of the faded in a few minutes after the turtles were left terrarium. Beneath the infrared bulb, the operative tempera- alone and their heart rate returned to baseline ture was 42.5°C. levels in ca. 10–12 min. M. Cabanac, C. Bernieri / Beha6ioural Processes 49 (2000) 61–68 65

4. Discussion further evidence of emotional fever in turtles. Hallman et al. (1990) and Cabanac and Gosselin 4.1. Emotional fe6er (1993) have also shown 6 and 8–10°C increases in body temperature in several species of lizards at Handling of rats (Briese and deQuijada, 1970), the outset of their experimental sessions. The ele- and mice (Cabanac and Briese, 1991) is followed vation of our turtles body temperature was a fever by rapid elevation in body temperature. This ele- because their higher body temperature after han- vation may be considered to be a fever because dling could not be a passive outcome of increased the animals own thermoregulatory responses pro- metabolism but was produced actively, and de- duced the elevated level of body temperature fended, by the animals behavior. Another reason (Briese and Cabanac, 1991), and because the an- why the elevated body temperature is a fever is tiprostaglandin drugs salicylate (Briese and Ca- the negative influence of salicylate an antagonist banac, 1980; Singer et al., 1986; Kluger et al., of prostaglandins, which are considered to be 1987; Cabanac and Briese, 1991; Cabanac and hypothalamic mediators of fever. The fever had Gosselin, 1993) and indomethacin (Kluger et al., an emotional origin because the handling and 1987; Morimoto et al., 1991) blocked or limited temperature-taking were the only cause of the the elevation. This fever is emotional in origin higher body temperature sought by the animals, because repeated measurements yielded ever and because their body temperature returned to slower rises in body temperature as the animals baseline level in less than 2 h when the animals habituated (Briese and deQuijada, 1970; Cabanac ceased to be handled. and Briese, 1991). 6 6 Because the time course of core temperature 4.2. Beha ioral fe er in reptiles after mere handling was similar to the results obtained in rats and mice they may be seen as Because they obtained similar results after using pyretogen and vehicle in lizards, snakes, and turtles, Laburn et al. (1987) and Zurovsky et al. (1987a,b) have concluded that Old World reptiles are not as susceptible to fever as New World reptiles. An alternative hypothesis may be offered, now, to explain these apparently negative results. We feel it is likely that fever did occur in their animals after control injections but that it was emotional fever. Our results are similar to those of Fig. 1 in Zurovsky et al. (1987a). In their other experiments, fever would therefore have been caused by the animal being handled, by its stress from trailing a cloacal thermocouple wire, by its receiving an intraperitoneal injection of saline, and perhaps also simply by its being transferred to a novel environment. The emotional fever oc- curred in baseline sessions with a magnitude similar to that of infectious fever and provided thus, apparently, a negative result. Fig. 3. Mean heart rates (+S.E.) of the turtles plotted against Actually, other authors have obtained evidence time. At time zero the animal was gently handled for 1 min by of infectious fevers in many different genera of the experimenter. The two columns with * are significantly different from each other and from all other columns before both Old World and New World reptiles. Injec- and after handling (ANOVA for repeated measures, P= tion of bacterial pyrogens is followed by a behav- 0.0001, post hoc Fisher test). ioral fever in lizards (Firth et al., 1980; Monagas 66 M. Cabanac, C. Bernieri / Beha6ioural Processes 49 (2000) 61–68 and Gatten, 1983; Muchlinski et al., 1989; Hall- sence of the heating lamp, the core temperatures man et al., 1990), turtles (Monagas and Gatten, of the turtles must have remained low and their 1983) and juvenile crocodiles (Lang, 1986). Ad- heart rates rose transitorily. Tachycardia is re- ministration of live cultures of Aeromonas hy- ported to occur also in snakes (Heatwole et al., drophila results in the death of lizards (Kluger et 1979) and in lizards (Cabanac and Cabanac, sub- al., 1975) and alligators (Glassman and Bennett, mited) when handled. Such a response is similar 1978) when the animals are prevented from qualitatively to that found in mammals (e.g. see achieving the elevated preferred temperatures. Gautier and Cook, 1997), which is consistent with Parasitic infection in snakes has been treated suc- the view that reptiles are fully equipped with the cessfully by increasing ambient temperature to same extrinsic heart nerves and reflexes as mam- 35–37°C (Deakins, 1980). When, however, the mals (Rodbard et al., 1950; Khalil and Malek, body temperature of alligators remains constant 1952; Fredericq, 1955; Comeau and Hicks, 1994; at 35°C, the parasitic infection results in death Altimiras et al., 1998). (Glassman and Bennett, 1978; Lang, 1986). Alli- gators (Glassman and Bennett, 1978) and lizards 4.4. Emotion in reptiles (Bernheim et al., 1978), which responded with fever to infection by live Aeromonas also dis- The tachycardia results is congruent with the played an increase in leukocyte counts, which was results we obtained with emotional fever. Emo- greatest in those animals whose elevation in core tional stress, such as during university examina- temperature was greatest. Furthermore, these spe- tions or sport competitions, results in fever in cies produced antibodies to diphtheria toxin only humans (Renbourn, 1960; Gotsev and Ivanov, when their body temperatures exceeded 28°C 1962; Briese, 1995). Gentle handling produces (Metchnikoff, 1901). Leukocytes from peritoneal fever in other mammals (Briese and deQuijada, exudates of lizards produce an endogenous sub- 1970; Briese and Cabanac, 1980, 1991; Cabanac stance that, when transferred to other lizards, and Briese, 1991; Marcilhac and Siaud, 1996; caused fever (Bernheim and Kluger, 1977). When Oppermann-Moe and Bakken, 1997; Saiki et al., injection of pathogenic bacteria into lizards is 1997) and also in lizards (Cabanac and Gosselin, preceded by an injection of sodium salicylate, the 1993). Thus the same response pattern, including selected ambient temperature remains at that of fever and tachycardia, was present in both the few an afebrile lizard (Bernheim and Kluger, 1976), reptilian species studied and mammals. Therefore, which is an a-contrario evidence of fever. Much- it is not unlikely that the tachycardia observed linski et al. (1998) have recently reported that the here in turtles was a sign of emotion. Further- lizard Gerrhosaurus major, considered previously more, lizards display other signs of mental capac- to be an afebrile species, is in fact chronically ity: when placed in situations where they could infected and regulates its body temperature at a use behavior to express their preference between lower value when treated with antibiotics. sensory stimuli (Balasko´ and Cabanac, 1998), Finally, modern Fish, the ancestors of which lizards display a behavior that may be described are common to Reptiles are susceptible to bacte- as indicating sensory pleasure, a phenomenon rial fever (Reynolds et al., 1976; Cabanac and closely related to emotion. Laberge, 1998), rendering more likely that Rep- Placed in an evolutionary context, the present tiles also can become feverish. Hence, we may results would suggest that emotion, and thus ele- propose, with (Kluger, 1979), that reptiles are as mentary consciousness, exists in reptiles. 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