Iturbaum, B. A.

and 14. L. Riedesel. 1974. Temperature re gu1 at i on responses of ornate box turtles, Terrapene

ornata, to heat.
Vol.

Comp. Biochem.
Press.

Physiol.

+eA-:

-577:53e.

Comp. Biochem. Physiol., 7974,

48A.,

pp. 527 to 538. Pergamon

Printed in Great Britain

TEMPERATURE REGULATION RESPONSES OF ORNATE BOX TURTLES, TERRAPENE ORNATA, TO HEAT*

B. A. STURBAUMT and M. L. RIEDESEL
Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131, U.S.A.
(Recehsed 25 June 7973)

Abstract-l.

Eleven ornate box turtles after being preheated to 30oC core temperaturewere exposed to 38,47,43.3,48 and 51"C experimental environments to assess their ability to thermoregulate. 2. Exposure to 38 and 41'C was not a heat stress for these turtles as evidenced by absence of restless activity, very little evaporative weight loss, no frothing and no change in heart rate. 3. Frothing was adopted as an indicator of maximum physiological thermoregulation because after frothing commenced, core to air temperature gradients were established, Core to air gradients were larger in the hotter environments

and onset of frothing began earlier during the heat exposure. At 48'C an 8'5oC core to air gradient was maintained for 3 hr and at 51oC a 10'5"C core to

air gradient was maintained for 1'5 hr.

4. Increased heart rate and evaporation of saliva and urine were effective responses which accompanied thermal balance. Weight loss appears to be a much better index of thermal stress than is heart rate.
INTRODUCTION UNorn favorable conditions many reptiles are able to maintain body temperatures relatively independent of environmental temperatures. Studies of temperature regulation in lizards have clearly demonstrated both behavioral and physiological thermoregulatory responses (Schmidt-Nielsen & Dawson, 1964; Dawson, 1967). However, there is a paucity of information in the literature concerning the extent to which turtles can thermoregulate under heat stress. In several turtle species
physiological responses have been observed when the body temperature is elevated (Boyer, 1965; Weathers & White,l97l). Copious salivation in response to high ambient temperatures has been reported for Terrapene ornata (Riedesel et al., 197I), Gopherus agassizii (McGinnis & Voigt, L971), Testudo silcata Miller (Cloudsley-Thompson, 1971) and Chrysemys marginatabelli zndChelydra serpentina (Baldwin, 1925a, b). The present study was undertaken to determine the extent * Taken

in part from a dissertation

submitted

in partial fulfilment of the Ph.D.,

December 1972. f Present address: Department of Science, St. John College, Cleveland, Otrio44114.
527

528

B. A. SrunaauM AND

M. L.

Rrporsor.

to which one turtle species, T. ornata, can thermoregulate when exposed to various warm and hot environments.

MATERIALS AND METHODS

Eleven ornate box turtles (Terrapene ornata) collected in the Portales, New Mexico area, were the experimental animals. Prior to and between experiments the animals were housed individually with 23-28'C temperature and a 12-hr L and 12-hr D photoperiod. The animals had water ad lib. and were fed carrots, lettuce, squash, cantaloupe and dog
food.

Thoracic and abdominal thermocoupies were inserted 1'5 cm through 1'5 mm diameter holes which had been drilled into the second and third neural elements of the carapace. The surgery under ether anesthesia was conducted at least 1 week prior to experimentation. These thermocouples were secured

in

place

by applying dental cement. The surface

temperatures were measured by applying thermocouples to the surface of the carapace with masking tape such that the tip of each thermocouple was covered. Temperatures were measured to the nearest 0'1'C with a Leeds and Northrup Speedomax W Recorder. The animals were weighed to the nearest 0'1 g as a criterion for water loss. The onset of frothing was designated when saliva accumulated in or on the beak or in the oral cavity. Urine and excess saliva were collected by placing each turtle on a 0'5 cm mesh wire screen

over mineral

mesh and into the mineral oil, The saiiva was more viscous than the urine and most of the saliva evaporated from the surface of the animal or wire screen. Therefore, fluid collected under mineral oil is referred to as urine. The urine was weighed and the amount of water evaporated was computed by calculating the difference between change in body weight and weight of urine. Before an animal was used in any given experiment, weight lost during a previous experiment had been regained, Recording of heart rates on a physiograph required placing three silver-foil electrodes on areas of the carapace which had been scraped to expose bone during ether anesthesia, Electrode paste and stripping tape aided electrical contact, The two exposure chambers provided control of air temperature to the nearest 1'0oC and the animals could be observed throughout the experiments. The water vapor pressure was less than 3 mm Hg as determined by wet and dry bulb temperature measurements to the nearest 0'1"C. Air velocity was iess than 8 m min-1 as measured with a hot-wire anemometef. During experiments, animals were confined individually in a plastic cylinder, 25 cm diameter and26 cm depth. Turtles were preheated at an ambient temperature of 55"C in chamber A before being placed in the experimental environment in chamber B, thus each turtle had a 30'C core temperature when it entered the experimental environment. Experimental groups and temperatures were: group 1 (38'C), group 2 (41'C), group 3 (43'3'C), group 4 (48'C) and group 5 (51'C). The experimental protocol involved each of the five experimental groups being (i) preheated 20 min in a 55'C chamber to 30'C core temperatures, (ii) transferred to an experimental temperature of 38,47,43'3,48 or 51"C, and (iii) allowed to cool in 24'C for 30 min. Heart rates were recorded for. a minimum of 1 min at four different times: prior to preheating, after preheating to core temperature of 30oC, upon removal from the experimental environment and after cooling for 30 min in an ambient temperature of. 24'C. Student's ,-tests have been applied to the data and the 95 per cent confidence level has been accepted to represent significant differences.

oil.

Very small amounts of saliva dripped from the animal onto the wire

RESULTS

The ornate box turtles detect and respond to adverse environmental temperatures. During preheating to core temperatures of 30'C in 55'C ambient,

or,n",,,o,,l,l] the animar s .,n, oT"; t." gasping, panting, buccopharyngeal movements, climbing and pacing. When transferred to the experimental environments, there were variations in behavioral and physiological responses. In 38'C, the turtles were quiet and appeared to have no discomfort. Some moisture accumulated about the eyes, but there was no frothing, and both core and surface temperatures approach the ambient (Fig. 1).

*""*;ffiffi ;;;

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IVINUTES

MINUTES zfo

Frc. 1. Mean temperature and time to frothing of animals preheated to 30oC core

in 55'C ambient and exposed to 38, 41, 43'3, 48 and 51'C ambient. There was very little weight loss (Table 1). Evidently 38'C is not a stressful environment for the ornate box turtle. In 41 and +3'3"C environments escape activity was constant and there were continuous mouth movements. Moisture accumulated about the eyes and in the folds of the neck skin and frothing occurred (Fig. 1). Weight losses were greater at 43'3'C (Table 1). In the hottest experimental temperatures (48 and 51"C), copious amounts of saliva flowed from the mouth and mouth movements were continuous. Much moisture appeared about the eyes and in the folds of the neck skin. Weight losses were considerable (Table 1). Urine was excreted in large amounts, some of which flowed onto the legs and skin between the carapace and plastron. Short periods, 0'5-1'0 min, of activity were followed by longer periods, 10-15 min, of inactivity. Immediately upon

530
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TEMPERATURE REGULATION OF ORNATE BOX

TURTLE

531

removal from experimental environments to the 24'C ambient, all the animals became quiet; frothing, urinating and mouth movements ceased. Frothing had been adopted as the onset of physiological thermoregulation (Riedesel et al., 1.97I); but as a result of examining more experiments involving frothing, we have adopted frothing as a good indicator of maximum thermoregulation. Prior to and continuing after the onset of frothing, there was gasping, gaping of the mouth, panting and buccopharyngeal movements. After frothing commenced, the gradient between the core and ambient was nearly constant (Fig. 1). No frothing was observed in group 1 (38"C) even though the mean final core temperature was 37'6'C which was at least 0'5"C higher (P<0'001) than at the onset of frothing for the other groups (Table 2). In group 2 (41'C) the onset of

frothing occurred late in the experiment (203 min). The delay in onset of frothing was very evident because the mean time for the other groups was 67'9 min.
TanlB 2-DerA coLLEcrED
AT oNSET oF FRoTHING

Gradients

Group,

?" (N-value)
't, 38'C
(6)

Time to frothing*
(min)

T@te ("c)
37'6t
(0.2)x 37.0 (0.6)
35.6

?.o"ru""

('c)

T"-"

("c)
0.7t

('c)

T^-"

38.4t
(0.2) 38.7

0.st
(0.2) 4.2

(0.6)
1.8

t
J, +,
5

41"C 203.6 (3s.6) (7) 43.3"C 69.8 (6) (s.4) 48'C 66.t (3.s) (6) 51'C 67.8

(0'3)
39.0

(0.3) 3'5 (0.1)

4.1

(0.6) (0.3)
12.2

(0'3)
3

(0'3)
39.9

5'8

(0'6)
35.9

(0'3)

(0'3) 4'5
(0.2)

(0'6)
15.1

(4)

40'4
(0'4)

(s.s)

(0'6)

(0'7)

* Includes time of preheating.

t Values at 300 min. f Standard errors'

determine the mechanism or mechanisms which initiate frothing, it is perhaps pertinent to consider a statistical analysis of the various body temperatures and temperature gradients within the animal at the onset of frothing. There were no differences in core temperatures among groups 2,3, + and 5 at the onset of frothing which occurred at a mean core temperature of 36'1"C (P>0'05). The mean surface temperatufe was 39'5'C. The only differences in surface temperature existed between groups 2 (+t"C) and 5 (51"C) (P< 0'02) and between groups 3 (43.3"C) and 5 (51"C) (P<0'05). The animals at the higher experimental temperatures had higher surface temperatures.

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TEMPERATURE REGULATION OF ORNATE BOX

TURTLE

533

After the onset of frothing, core-surface and core-air gradients were established. The mean core to air gradients were 2'6"C (group 2),4'5'C (group 3), 8'5"C (group 4) and 10'5'C (group 5). There were differences in core to surface gradients at the end of heat exposures among all groups except between groups 3 and 4 where the gradients were the same (P>0.4). As the ambient temperature increased, there were increases in the final core tempefatures (Table 1). However, statistically, the final core temperatures were the same between groups 1 (38"C) and2 (41'C),2 and 3 (43'3"C) and 4 (48'C) and 5 (51"C). Whenever urine was collected and weighed, the amount of evaporation was calculated by subtracting urine weight from body weight loss. As the ambient temperature increased, weight loss per hour increased except between groups 3 (43'3'C) and 4 (48"C) (P> 0'1) and between 4 (48"C) and 5 (51"C) (P> 0'05) where weight losses were similar. IJrine was not collected for groups 1 (38'C) andZ (4L"C). There v-ere no differences in the amount of urine collected per hour or in the amount of evaporation occurring per hour among groups 3, 4 and 5. The mean heart rate values for all groups were similar when heated to 30"C core temperature (Table 3). Increasing the mean core tempefature another 7'6'C to 8.5"C by exposure to a warm environment,3S, +I or 43.3oC, did not result in a significant increase in the mean heart rate values. However, increasing the mean core temperature to 39.9 or 41'0'C in 48 and 51"C environments respectively did result in significant increases in heart rate (P<0'05 to 0'001). When heart rates of all turtles at 30'C after preheating and after cooling at 24"C were considered together and compared, there were no differences in the heart rates after preheating and after cooling (P > 0.2). There were wide ranges in heart rates after preheating and at all experimental temperatures except at 51"C. Heart rates of most of the turtles examined increased at the higher core temperatures and the responses of the four animals to the 51"C environment were very similar (Table 3). However, all turtles examined did not respond the same to the same set of conditions (Table 4 and Fig. 2). Mter exposure to 41 and 48"C, turtle 36, for example, had a lower heart rate at core temperature of 38'1 and 40.1'C than at a core temperature of 30"C after exposure to 55"C. Heart rates of this turtle were not consistent at a temperature of 30'C, the rate being 58, 31 or 49 beat/min; but the heart rate was consistent after exposure to the 41,43'3 and 4BoC environments (40, +2,42beatfmin) and after cooling for 30 min (33, 32 and 34 beat/min). This turtle was continuously active in 41 and 43'3"C environments and was quiet with only spurts of activity at 4B'C. Turtle 29, as another extreme example, did not have a consistent heart rate, for instance: 37 and 56 beat/min were recorded at difierent times when the core temperature was 30oC in preheating periods. Heart rates of 78 and 107 beat/min occurred with only a0'2"C difierence in core temperatures in the 43'3 and 48"C experimental environments. These large differences in heart rate with small differences in core temperature clearly indicate gross activity as well as severity of thermal environment are impoitant determinants of heart rate. In the 43'3'C environments, the animal wai active during the first 15 min and then was relatively quiet; whereas, in the

534
TESLN

B. A. SrunsauM AND M. L. RrroBsu. 4-HBART

RATES AND coRE TEMPERATURES

oF INDIVIDUAL TURTLEs

Turtle No.

Initial in24"C
ambient (beat/min)

After After exposure After 30-min to to experimental recovery in 55'C for 20 min conditions 24oC ambient (beatimin) (beat/min'C) (beat/min)
exposure
65

Experimental condition: environmental chamber of 38'C for 280 min

1+
22 18

33
15 2S

36

62

(37.7) 36 (36.9)
s6
(39.6)

(38.3)*

48 36 33
JJ

Experimental condition: environmental chamber of 41'C for 280 min

21 317 22 36 34 34
t4

24
18 14 23

42 40
58 s5

s8
60

(36.6)

se

(38.6)

44
3s
JJ

40 (38.1)

2l
21

46
60

s7 (38.2) s7 (38.s) s4 (37.s) s0 6s 42

(37.e) (3e.0)

42
41

47 34 52 53

Experimental condition: environmental chamber of 43.3"C for 280 min

21 29 22 30 36 34

28 18 18 18 10

76 37
31

78 (39.2) 71 (39'1)
(3e'O) 7e (39.2)

56 45

J2
50 47 35

22
22 22 18
13

40 47 46

Experimental condition: environmental chamber of 48oC for 280 min

10 30 189 14 36 29
t4

2t

30 44 4e s6 s0 60
+4
45

78 (40.4) e0 (3e.e) 88 (3e.7)

s4
52

s1 42
107

(39.7)

(40.1) (3e.4) (41.s)

34
66 60

Experimental condition: environmental chamber of 51'C for 160 min

314

8s

30 34

23

23 18

e4 (40.3) 90 (42.0) 90 (40.1)

48
51

58

* Temperature of the core upon removal from the experimental environment.

48oC environment, the animal was quiet most of the time. Perhaps an integration of core temperature and activity or core temperature and stressful environmental temperatures determines heart rate.

DISCUSSION When the ornate box turtle, T. ornata, is sutijected to stressful environmental temperatures and has no way of escaping, it employs physiological mechanisms to keep the body temperature within tolerable limits as evidenced by the core to air

TEMPERATURE REGULATION OF ORNATE BOX TURTLE

535

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TEMPERATURE OF
ENVIRONMENT

TEMPERATURE

oF coRE c"

Flc. 2. Heart rates at various core and ambient temperatures.

gradients established after frothing commenced (Table 1 and Fig. 1). At a 38'C ambient temperature the turtles appeared comfortable and there were no observable indications of physiological thermoregulation. In higher ambient temperatures the core to air gradients became greater which indicates that the animals were actively engaged in keeping their body tempratures below ambient temperature. In a 47oC environment, the lizard, Sauromalus obesus, can maintain body temperature

4oC below ambient for periods of at least 3 hr and such thermoregulation is accomplished by evaporative cooling (Case, 1972). The ornate box turtles at 48'C kept body temperatures 8'C below the ambient for at least 3 hr and at 51'C ambient, 10'C below ambient for at least 1'5 hr (Fig. 1). The heart rute data describe the thermal environment as being the primary

factor determining heart rate in very hot environments,48 and 51'C; but at moderate temperatures, heart rate is not a good index of core or ambient temperature. Apparently moderate thermal stress results in complex cardiovascular responses which may or may not involve increased heart rate as indicated by the wide range in heart rates at all the experimental temperatures except 51oC. Because these animals rarely have body temperatures above 35'C in nature (Legler, 1971), heart rate would not be a good index of heat stress in natural conditions. Only in extreme heat is heart rate a reliable index of heat stress. Frothing has been adopted as an observable indicator of maximum physiological thermoregulation because gradients were established between core and air and the core temperatures were kept below intolerable limits after frothing commenced. Prior to frothing, there were some noticeable physiological responses such as buccopharyngeal movements, gasping, panting, gaping of the mouth;

536

B. A. SruneauM AND M. L. RrpoBsrl

however, these responses alone were not adequate to keep core temperatures from rising. For maximum physiological heat-stress responses to commence, the

temperature regulation center must integrate information regarding core and ambient temperatures. The importance of hot environmental and surface temperatures is evidenced bV (i) absence of frothing in 3B'C ambient although core temperature exceeded the core temperature,36'1,oC, at which frothing began in warmer environments; and (ii) cessation of frothing immediately upon removal from hot environments to 24oC ambient when core temperature was as high as 41"C. The importance of core temperature in determining onset of frothing is emphasized by frothing occurring as body temperature approached 36'C in all experiments except group 1, 38'C. Boyer (1965) reported that turtles can sense stressful environmental temperatures and make behavioral responses; these box turtles, too, can sense stressful temperatures as manifested by differences in physiological activities in the various experimental environments. During physiological thermoregulation there is a loss of body water as determined by weight lost by the animals during heat exposure. Some of the water is lost as urine and some through the skin, carapace and as saliva. The weight losses increased as the ambient temperatures increased. Turtles have large bladders and a function of the large bladder may be to store water for emergencies, and heat stress is one type of emergency. Once the bladder water is depleted, the turtle can no longer call upon this source for cooling. Most of the urine voided during these experiments was not available for cooling because it was collected under mineral oil. Some urine was observed between the carapace and plastron and the urine spread onto the legs. A few measurements of leg skin temperature clearly indicated cooling upon evaporation of urine from the leg. Under heat stress in natural environments the large amounts of urine voided would wet the soil and provide a cooler environment for the animal for at least a short period of time. Both cutaneous and respiratory evaporative water losses occur in turtles with cutaneous water loss being more than two-thirds the total (Bentley & SchmidtNielsen, 1966; Schmidt-Nielsen & Bentley, 1966). The moisture that accumulated around the eyes and in the folds of the neck skin when the turtles were exposed to warm and hot environments, is evidence of cutaneous water loss. Evaporation of cutaneous and carapace water would be effective in keeping temperatures of the shell surface, skin, and subdermal tissues below that of the ambient as evidenced by the surface to air gradients in these experiments (Fig. 1). Evaporation from the oral cavity is more effective in dissipation of body heat than evaporation from exterior body surfaces. Evaporation from the shell cools the microenvironment of both the shell surface and air. In the oral cavity more of the microenvironment involves body tissues. Panting, gasping, gaping of the mouth and buccopharyngeal movements facilitate respiratory evaporation. The physiological responses of turtles are effective in regulating the body temperatures during heat stress. The overall efficiency of evaporation (Table 5) can be estimated if you consider the metabolic heat dissipated and the extent to which the core temperature was kept below ambient by evaporation.

TEMPERATURE REGULATION OF ORNATE BOX TURTLE

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538

B. A. SrunsauM AND M. L. Rrsonsrl

CONCLUSIONS When exposed to high environmental temperatures, the ornate box turtle has physiological body-temperature regulation although by classical definition turtles are poikilothermic because their body termperatures do rise and fall as environmental temperature rises and falls. However, they are homeothermic to the extent that if behavioral responses to heat exposure are inadequate, physiological responses are employed. These animals pant, gasp, their mouth gapes open and buccopharyngeal movements occur. When core temperatures continue to rise during exposure to stressful temperatures, frothing occurs and is a good observable indicator of physiological thermoregulation. Following the onset of frothing, core temperatures are kept below ambient and core to air gradients are established. The ornate box turtle employs both behavioral and physiological means to combat heat stress; and doing so, can keep core temperatures well below stressful ambient temperatures (48-51"C) for as long as 1.5-3 hr. Evaporative water loss plays a major role in thermoregulation.
Acknowledgements-We thank Dr. A. L. Gennaro, Department of Biological Sciences, Eastern New Mexico LJniversity, for collecting animals in the field.

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