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Reprinted for prirale circularion Irom PHyslorocrcAl Zodrocy, Vol. 44, \o. l, January L971, oo. 2g-32Copyright @ i971 by rhe Lniversity of Chicago. Ali rights reseived. prihred in 0. S. i. ' '-'

EVAPORATIVE THERMOREGULATION IN TURTLES1M. L. RIEDESEL, J. L. CLOUDSLEY-THOMPSON,zAND J. ANNE CLOUDSLEY-THOMPSON

Department of Bioiogy, University of New Mexico, Albuquerque, New Mexico 87106It has been found experimentallythat when the body temperature ofyoung African tortoises, Testudo sul'-cata Miller, rises to 40 or 41 C, copioussalivation takes place, wetting thehead, neck, and front legs. This pro-duces evaporative cooling which pre-vents any further rise (Cloudsley-Thompson 1968, 1970). In the workdescribed below, the physiology of asimilar phenomenon was investigatedin the box turtle, Terrapene ornata.

MATERIAL AND METHODSBox turtles, Terrapene ornata ornata(Agassiz), were collected from variouslocalities in New Mexico and Okla-homa. A total of nine specimens wasstudied. Between experiments, the ani-mals were housed in a constant tem-perature room at 27 C, illuminatedbetween 05oo and 20oo hr and pro-vided with water and vegetable food.

Body weight was regained within 24hr after each experiment.Temperatures were measured withthermistor probes connected to a tele-thermometer (Yellow Springs Instru-ment Co.) and heart rates were re-corded by means of a physiograph(B & M Instrument Co.). The air ve-l This study was supported by NSF grantGB 5339.2 Present address: Department oI Zoology,Birkbeck College, Malet Street, Londor W.C.1E?HX. This work was carried out during tenure

of a National Science Foundation Senior VisitingScientist Fellowship, for rvhich appreciative ac-knowledgment is hereb5' given.

iocity ranged from 25 to 35 m/minuteand the water vapor pressure rangedfrom 10 to 16 mm Hg.Special methods were needed in ex-periments involving the heating orcooling of the head. A day or two be-fore each experiment, a collar com-prised of a cork ring was fitted roundthe neck of each turtle while the ani-mal was anesthetized with ether. Thiswas necessary to prevent withdrawal

of the head into the shell during theperiod of the experiment. Immediatelybefore experimentation, oral and clo-acal thermistor probes were insertedand a third probe was attached to thetop of the head. Electrocardiographprobes were inserted at the bases ofthe limbs and the turtle strapped to ametal clamp. In preliminary experi-ments the head was exposed to therays of an infrared radiant heat lampwhile the body was shielded, but theheat produced in this way tended to beeither minimal or so excessive as tocause blistering. In the reported ex-periments, therefore, the lamp was re-placed with an electric heating coilembedded in plastic. This was partiallyinsulated from the head of the turtleby means of a pad of cotton. In anycase, the presence of a probe in themouth made it difficult to see the exactmoment at which salivation started.In other experiments, turtles wereplaced in an ambient temperature of45 C and their heads cooled by drip-ping ice water onto a pad of cotton

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EVAPORATIVE T}IERMOREGULATION IN TURTLES 29bound around them. Heart rate andtemperature measurements were madeat S-min intervals.

RESULTSBODY TLMPERATURT AND SEART RATE

The relationship between heart rateand body temperature was establishedin turtles no. I (223.2 g) and no. 2(196.5 S) by placing them in an am-bient temperature of 50-55 C andrecording both parameters simultane-ously while their cloacal temperaturesrose from 24.5 to 42 C and again asthey cooled. The relationship was simi-lar in all turtles, but some individualsshowed consistently lower heart ratesat all temperatures than did others.For any given body temperature theheart rates in a particular individualwere similar whether the animal wasbeing cooled or heated. Some typicaldata plotted in figure 1 show a directrelationship between heart rate andcloacal temperature. A Qro value ofnear 2.0 describes the heart-rate data.In contrast to heart rate, the thermo-regulatory response of the turtles wasnot predictable.

TURTLE Ib,I

CLOACAL TEMP 'CFrc. 1.-A typical plot of heart rate versuscloacal temperature.

AND URINATIONEvaporative cooling in Terrapeneornata is engendered either by saliva-tion or by urination. In the former, aconsiderable amount of frothy salivawas produced from the mouth and nos-trils. This was smeared onto the frontlegs, which were used to wipe themouth, and it also ran over the headand neck. Urine was rubbed onto theback legs, which frequently becamecoated with a pad of cool damp mud.Urination usually occurred before sali-vation (frothing), but sometimes after-ward, in an erratic fashion. Salivationwas therefore adopted as the indicatorof thermoregulation.In order to determine the tempera-

ture at which salivation began, turtleswere placed in various high ambienttemperatures and their cloacal temper-atures recorded at intervals of 2-5min until 10 min after salivation(frothing) was first noted. The results(table 1) do not describe a specificenvironmental or body temperature forsalivation. Weight loss prior to saliva-tion was presumably due to urinationplus respiratory water loss, as therewas no evidence of defecation duringthe experiments. Ambient tempera-tures of 65 and 75 C represent acutethermal stress, and at both tempera-tures the turtles with the highestweight loss (nos. 8 and 9) startedfrothing at the lowest cloacal tempera-ture.

RELATIONSEIP BETWEEN BODY TEMPERATI'REAND EVAPORATIIIE COOLING

Experiments were carried out,mainly on turtles no. 1 and 2, to ascer-tain the relationship between body tem-perature and evaporative cooling. Theanimals were weighed and then ex-posed to various high ambient temper-

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30 u. L. RTEDESEL, J. L. cLoUDsLEy-TrroMpsoN, AND J. A. clorrDslDy-TrroMpsoNTABLE 1DlrA conrcruo oN TURTLIs rN vARrous Eor ENvTRoNMENTs

TURTLENo.INITIAL AMBIENT TIME ToWEToET TEMPERATURT SerrverroN(e) (c) (min)

CLoAcAlTnup. nrOusrr orSerwerro*(c)BoDYWETGI{T Loss-6- cF..:

228.O231.O2t7.5209.OL27.S210.5232.O215.5196.0222.Or17.5261.O2t7.5t22.O278.5139.0387.5

/J11590363439ZJ23z3402646t?t7?)t418

s7.840.438.4s6.4J/.O37.O36.939.3JO-O37.938.037.839.837.236.836.052 -.t

10.75.1ll.121.s21.917.821.77.946.O4.79.2.5-l72.9t2.s26.164.38S.O

4545455555556565656565657S/J/J/J75

6.64.38.16.29.8+.J3.61.48.9t.43.41.1o(ao5.010.86.9

atures for periods of 6 hr. After a 2-hrperiod to allow for equilibration, theywere reweighed and their cloacal tem-peratures measured. This was repeatedat hourly intervals for 4 hr. It wasnoticeable that once the body tempera-ture had approached the ambienttemperature during the first hour ofexposure, it tended subsequently tocontinue to rise only slowly and, indeed,between some hourly readings at the

lower ambient temperatures it evendropped. The results, summarized intable 2, show a clear relationshipbetween ambient temperature and rateof water loss. The mean depression ofthe cloacal temperature increased withambient temperature, as did the rateof water loss. Some saliva and urinewere lost without producing evapora-tive cooling. In the natural environ-ment, however, soil and mud may

TABLE 2Tgr lrnex TLMIERATURE, wErcET Losr By ruRTr,Es, AND RELATED cALcutATroNs oF.DATA cot-LEcrEDDuRrNc FwE 4-rrn srrlnv srATE EXpERTMENTS

Ossrnvro Dlu CALCULATDD VALUESTunrrrNo.

Ambient LessCloacal Temp,(c) WeightLoss(e/hr)AmbientTemp.(c)Calorica Equiv, Caloricb Equiv. Estimatedof Temp. of Weight EfficiencycDifferential Loss of Cooliug(cal) (callhr) (%')

1089580706t

4509?0

495931

lr2lr2l'2lr23-9

40.541.044.O45.345.5

2.6(0.14)t-o(0.25)5.8

( l.os)6.5(0.88)6.4(0.1s)

0.8(0.1s)r.7(0.44)2.4(0.40)3.1(0.44)J.J(0.2s)

1 100t23s12l9

137011701998

Norr.-Figures in parentheses are sE.a Based on specific heat of tissue (0.85) and mean body weight of animals (224 g).b Based on heat of vaoorization of water at 45 C (571 cal/eram),c Bced on caloric eqdivalent of temperature differei:tial; weight loss represents evaporation; and the assumption meta-bolic rate ard heat gain from tlc envimnment are equivaleat in 8ll experiments.

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EVAPORATIVE TIIERMOREGULATION IN TURTLES 3laccumulate on the legs to a greaterextent than it did under experimentalconditions, and thus change the effi-ciency of cooling.

CONTROI, OI' THERMOREGUI,ATIONA few experiments were conductedin an attempt to describe the role ofhead and body temperatures in deter-mining onset of frothing. In three ofthe experiments we were able to inducefrothing by applying heat to the head,whereas on two occasions raising oraltemperature to 33.2 and 35.2 C failed toresult in frothing (table 3). Coolingthe head of a preheated turtle did notstop frothing on one of two occasions.DISCUSSION

The work described above indicatesthat, in addition to behavioral thermo-regulation and panting, box turtlesshow physiological control of body

temperature achieved by salivating(frothing) and by urinating on thelegs. A function of the very large blad-der in these animals may well be tostore urine for use in emergency ther-moregulation. In some species thisbladder is known to retain a consider-able quantity of watel for long periods(Mayhew 1968). Under natural condi-tions evaporative thermoregulation bysalivating (frothing) or urinatingprobably occurs only rarely and in ex-ceptional circumstances. High temper-atures are normally avoided, and acertain amount of cooling is achievedby panting. Panting and the evapora-tion of urine and saliva probably ac-count for the fact that we observedoral and cloacal temperatures fluctuat-ing over long periods in many of ourexperiments.The calculated efficiency of coolingpresented in table 2 represents roughestimates. However, the magnitude of

TABLE 3Bonv lwo EEAD TEMpERATURES AND HEART RATE rN EEAD-EEATTNG oR HEAD-coorrNG EXpERrtr4ENTsCONDUCTED UNTII- ONSET OR CESSATION OF T'ROTIIING

TEMPERATURE (C)

TURTLENo, AmbientHead Hlenreonrs/Surface MrN

IFIF DURATION oFExPERIMENTCouurNrs (min)Head-heating Experiments2t.o

24.02t.s

I ..,, ZZ.5I .... Z,t-s

23.7 26.124.4 26.223.7 29.223.9 29.925.5 s2 .O

23.O 29.126.1 29.422.6 33.224.2 33.827.3 35.3

31.0 42.ONA

40.0 45.539.O 45.235.6 40.s

45 5652 7054 66

105 min tofrothing75 min tofrothing80 min andno frothing95 min tofrothing125 min andno frothing

1108080

100t2s

NANA

[Iead-cooling Experiments? .... 45.01 .... 45.0

37.4 37 .638.0 38.4

3s.6 28.137,6 28.4

20.o 19.5t7.o 20-o

85 8214 78

90 min ofcontinuousfrothingfrothingstoppedafter 35min

90

45

Norn,-I = initial; F = final; NA = not available,

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32 v. L. RTEDESEL, J, L. cLouDsLEy-THoMpsoN, AND J. A. cLouDSLEy-THoMpsoNthe differential between cloaca andambient temperatures is impressive.Panting can represent more efficientcooling than frothing and urinating,but evaporation from the body sur-faces must be important in minimizingthe rate of heat transfer from environ-ment to body surface to core.The existence of physiological ther-moregulation implies thermosensitiv-ity, and a temperature-sensitive centermanifested by thermally induced bloodpressure changes has been demon-strated in the brain of the turtlePseud.emys elegans by Rodbard, Sam-son, and Ferguson (1950). Warmingthe brain promotes a rise in blood pres-sure, cooling it results in a fall. Thedegree of response is proportional bothto the intensity and the site of thestimulus, the most sensitive regionbeing on the level of the third ventricle.The data in table 3 may be affectedby the temperature of both the headand the body. The circulation of bloodto and from the head is extremelyefficient, as evidenced not only by thelength of time necessary to raise oraltemperature when the head was beingheated, but by the fact that the cloacaltemperature rose nearly as quickly. Itis possible therefore that blood fromthe body may influence the brain tem-perature before coming into equilib-

rium with the temperature at thesurface of the head.Future studies involving the record-ing of temperatures in the brain maydisclose a thermoregulatory center inTerrapene ornata. The data presentedhere suggest the existence of a primi-tive thermolegulation system whichmay, or may not, involve a single spe-cific neuroregulatory center.SUMMARY1. A direct correlation has beenestablished between heart rate andcloacal temperature in Terrapene or-nata.2. Bvaporative cooling is engen-dered by salivation (frothing) andurinating.

3. Salivation begins when the bodytemperature reaches 32.3-40.4 C.4. Evaporative water loss dependsupon the thermal stress.5. Heart rate is correlated with thetemperature of the body rather thanof the head, but salivation (frothing)may depend upon both. Blood fromthe body may influence brain tempera-ture before coming into equilibriumwith the temperature at the surface ofthe head.6. It is suggested that a function ofthe enlarged bladder of turtles may beto store urine for emergency thermo-regulation.

LITERATURE CITEDCr,oupsr,on-Tso rpsoN, J, L. 1968. Thermoregu-lation in tortoises. Nature (London) 217:575.1970. On the biology of the desert tor-toise Testudo sulcata Miller in Sudan. l, Zool,(London) 160:17-33.Merunw, W. W. 1968. Biology of desert amphib-ians and reptiles. Pp. 195-356 in G. W.

Bnowrv (ed.), Desert biology. Vol, 1. Academic,New York.Rooneno, S., F. Seaasor, and D. Frncuson.

1950. Thermosensitivity of the turtle brainas .manifested by blood pressure changes.Amer. J. Physiol. 100:402-408.