WATER, BATH STUDIES OF MAMMALS FROM SEVERAL ECOLOGICAL AREAS

7/29/2019 WATER, BATH STUDIES OF MAMMALS FROM SEVERAL ECOLOGICAL AREAS

1/11

WATER, BATII STUDIES OX' MAMMALS FROM SEVERALECOI,OGIOAL AIi,EASII. L. RIEDESEL and J. T YELVIRTOI\

Biology Depart'ment, The {Jniversity of New Mexico, Albuquerque, New Mexico, U.S.A.

Reprinted lromBIOI{ETEOROLOGY II.Proceedirt gs o| the T hird. Internati,onal B'iometeorological C ongressheld at Pau, S. Irance, 7-7 Beptember 7963

PETI,CA-\ION PRESSOXFOIiD LONDON EDINBUR,GTI NEW YORKTORONTO PAR,IS FR,ANI(FLTR,T

1966


2/11

WATER, BATII STUDIES OF MAMMALS FROM SEVERALECOLOGICAL AREAS*M. L. RIEDEStsL anrl J. T. YELYERTON

Biology Deparfment, The University of Nerv Mexico, Albuquerque, New Mexico, U.S.A.Alrsl,raet - Waterbath (25" C) experiments onC. Iateralis C. spilosoma M. auratus .aneJ.D. ord,i' demonstrate differences in the capacities of these animals to tolerate a severe coldstress. The laleralis and spilosomo, Lrad a, greater capacitv for shivering. Tbe ktte.ralis hada greal,er al-.ility to limit heat loss by peripheral vasoconstriction. The principal methodof combating cold available to ordi ancl auratus rvas preferential cooling of peripheraltissues.Zusammentassung - C.lateralis C. spilosorna M. auratus und D. ordi zeigten unt,er-schiedliclie Kiilteempfindlichkeiten im Wasserbadexperiment, (25' C). Laterolis rnd spilo-soma habten grbssere Kapazitiit fiir Muskelzittern. Lateralis verhinderte den \4'5rmever1ust,am besten durch periphere Gefd,ssverengung. Die I(dlteabwehr in ordi und auratus beruhtehauptseichlich auf der schnelleren Abkiihlung der d,usseren Gervebe.R6sum6 - C.l'ateral'is C. sptilosoma M. auratus el D. ordi d6montrent diff6rentes sensi-bilit6s au froid dans I'exp6rience i, l'eau (25' C). Laleralis el spilosoma d6montrent uneplus grande capacit6 de frisson. Lateral,is limitait la perte de chaleur par striction desvaisseaux sanguins peripheriques. La principale m6thode de combattre le froid reposeavant tout sur une possibilit6 plus rapide de rafraichissement des tissus extdrieurs.

Bnnevron patterns and insulative values of fur are recognized as being primarvfactors in determining tolerance of anima,ls to thermal stress (Burton a,nd Edholm,1955; frving and Krog, I954; Prosser and Brown, l96l). Few studies have exploredphysiological differences which may be important in determining the transfer orconseryation of body heat. Physiological capacity may be of great importance indetermining the survival of a given species at extremes in the thermal environment,for instance: Irhen the limits of protection by insulation and behavior ha,ve beensurpassed, physiological capacity would determine survival. Regarding physiolog-ical capacity there is evidence of species differences in temperature regulation,zone of thermal neutrality, tolerance for hypothermia and cooling of peripheraltissues (Hannon and Viereck, 1955; Kayser, 196l; Prosser and Brown, 1g6f).Additional information is needed in these areas, particularly with respect tophysio-logical capacity of animals from various ecological groups. The v'ater bath is a

* This study was supported in part by NSF Grant GB216 and a NSF fellowship.s90


3/11

Water Bath Studies of Mammalsuseful tool for describing transfer and conservation of body heat in response tothermal stress because environmental factors, such as radiant heat, air velocity,fluctuating air t'emperature and humidity are not involved. (Wilber, 1957).

MATERIALS AND MNTHODSThe animals studied include three hibernators from different ecological areasand a non-hibernator. Ci,tellus spilosoma rnclrg,inatus inhabit warm regions (meanair t'emperature - summer, 24' C; winter, 3" C) at elevations of 1500 to 2000 m.Ci,tellus lateral'is lateralis inhabit cool regions (mean air temperature - summer,13" C; winter, -7" C) atelevations of 2600 to 4300 m. Mesocreci,tus auratus, Asianancestory, were purchased from a pet shop. The fourth species, Dipotlomys ord,'i,are nocturnal non-hibernators and inhabit the same areas as spilosoma in NewMexico.A1l animals had been in the laboratory for I to 12 months prior to the studies.Periodic body weight measurements to the nearest 0.5 g indicated they were ingood health: mean body weight 231 g (7.0f s.n.) lateralis; 132 g (4.58 s.n.;

spilosoma; 1f8 g (2.99 s.n.) auratus; 68 g (3.68 s.n.) ordi. The swim chamber(33X33X25.5 cm) was constructed from 1.2 cm lucite. A rubber gasket fitted toa groove on the top edge of the chamber insured an airtight seal when the lidwas fastened to the chamber with adjustable vise grip clamps. One side of the cham-ber was fitted with a drain outlet, while the lid was fitted with four outlets fortemperature probes and an oxygen source. A wire-meshbag athached to the under-side of the lid filled with soda lime provided absorption of carbon dioxide. A heatingelement of 110 v, 300 w resistance wire in a coiled aluminum tube was insertedthrough the drain outlet. Cooling was effected by immersion of the swim chamberin a I00 I water tank which provided constant temperatures t0.4o C. Metabolicrate determinat'ions were made by measuring oxygen consumption with a spiro-meter sensitiye to 0.6 cm3. All rectal and water temperature me&surements weremade with thermistor probes.Three series of water immersion experiments were conducted : (1 ) free swimming,(2) confined, and (3) dead animals for a total of 96 water bath experiments on 14lateralis, 10 spilosoma, 8 ordi and 4 auratus. Repetitive exposure to cold waterdid not effect acclimatization as reported by Adolph and Richmond (1956). Theprotocol for the free swimming experiments of 30 min duration was as follor'vs:weigh animals, measure rectal tempera,ture, place in water at time zeto, and. ail0 min intervals the a,nimals were removed from the water for I - 2 rnin for rectaltemperature measurements. Metabolic rate me&surements were made during thesecond 10 min swim period. The series on confined and dead animals involved plac-ing the animals in a cone of one centimeter mesh wire and immersing to the headin water. Rectal temperature determinations of dead animals were made at twominute intervals for the first l0 min and at 5 min intervals for the last 20 min.

891


4/11

892 M. L. Rrnnnsrl aND J. T. Ynr-vnnroNShort term experiments of 2, 4, 6, 8, and l0 min duration were conducted onswimming animals. fn this series the animal was removed from the bath at thespecified times: 2, 4, 6,8, ancl l0 min, and rectal temperature w&s recorded. Threeanimals of each species were tested for each time interval and a given a,nimal rvassubjected to no more than one swim per day.Several assumptions have been made to facilitate interpretation of the data:

(f ) Heat loss from the head which was above the water in all experiments was neg-Iigible. (2) Heat loss from the respiratory tract was negligible. (3) The skin tem-perature wa,s constant, and equal to the ba,th temperature; therefore, the insulationvalue of the fur was lost. (a) The specific hea,t of the tissues was 0.83. (5) A re-spiratory quotient of 0.90 was assumed. (6) Surfa,ce area, (SA) calculations weremade with the formula: SA : Weight,0'73. (?) Mean body temperature (MBT) wascalculatedas follows: MBT:0.8 Tr*0.1 Ts (Burton, 1955). (8) Theinitial (IRH)and final body heat (X'BH) values were determined by multiplying the MBT by thespecific heat of tissues and body weight. (9) Body hea,t loss (8H1,) was determinedby the difference between IBII and X'RII. (10) Total heat loss (TI{L) was equalto BHL plus metabolic heat (M).RXSULTS

The cha,nges in rectal temperature while swimming describe 25o C water as asevere cold stress for all animals studied, 30' C as a moderate cold stress for C.lateral'is and C. sp'ilosoma,33'C bath as a neutral temperature for C.lateralis andC.spt'ilosoma bul a moderate cold stress for M.a,uratus and D" orcli. The 36'Cwater bath represents a moderate heat stress for C. lateral,is and C. siti,losoma.(Figs. 1, 2,3, 4).The responses of the animals to severe cold, 25o C water, are of major interest.The greatest heat loss was during the first' few minutes of the cold water exposure

Animal species Free swimming animals25"C 330c00c animals25" CO. lateralisC. spil,osomaM. auratusD. ordi

13.6*(2.65)10.1( 1.7e)12.2(0.89)

8. ?3(1.26)

r 1.8(2.28)r0.7(2.67)r0.9(1.23)6.52(1.24)

12.9(0.74)10.8(2.63)TI.2(0.73)

9.9(0.52)

14.6(3.38)TL.2( 1.40)4.03(0.67)5. r0(r.6e)

Tabl,e 7. Mean Metabolic Rate ol Animals in Waterbath (ltcallhr lmz )

* (One standard deviation)


5/11

Water Bath Studies of Mamrnals(Figs. 1, 2, 3). The lateralis had least change in rectal temperature because of highermetabolic rates (Table l). The experiments cond,ucted for 2,4,6, 8 and. l0 minintervals demonstrate that maximum ra,te of heat loss for all animals occurs during

x-x loterolis i=12,n=6H spilosomo l=ll,n=6H ourolus t = 3,n= 3;-; ;;;; "" ;= 3:;= 3 IIro 20 J0Min33"C Swim

893

oFEro

)e-x loterolisH sPilosomo(H ourotus+-a ord izoMin

X're. I Mean rectal l,emperal,ure of animals swimming in water bat'hs(f : number of swim t'rials; rz - number of animals)

Frc. 2. Mean rectal temperature of confined living and dead animals after10, 20 and 30 min immersion in water(l : number of trials; zz : number of animals)

t=6,n=6t=6, n =6t=3,n=3t=3,n=3

25"C Swim:ninqx--x loterolisH spilosomo(H ouroius&-{ ordi

=8, n=5=3, n=3=2, n =2

x-x loierolis t =3' n =3H spilosomo I =3, n =3

25oC Confined

OoEoFEaoE.coo

a

25"C DeodF-{ loterolis I =2, n =2H sPilosomo I =2,n=2o---o ourotus 1"2,n=2


6/11

894 M. L. RrnossEL.AND J. T. ynlvnnroNTable 2. Mean Total Heat Loss ol Animals in 2so c water B0 Min (hcallhr/m2)

Species

Swimming

Confined

Swimming minus deadConfined minus dead

20.9*(1.5)18.8(r.80)I1.3(0.87)9.67.5

r9.2( 1.68)t 6.7(2.7t)9.32(0.00)9.9i.4

19.5(1.21)Il.4(r.56)9.41(0.r0)

10. I2.0

15. r(0.e4)12.r(1.11)9.1(0.e1)6.03.0

* (Standard deviation)the first 2 min of the exposure. The difference betlreen the dead and swimminga,nimals demonstrates the facilitation of heat loss by the blood circulation at leastduring the first 4 to 5 min (X'ig. B, Table 2).

| = loleroliss = spilosomoo = ou/otu9o = ordiFre. 3. Mean change in rectal temperature of swimming and dead animalsafter short term irnmersion in water (3 animals of each species at each timeint'erval)

EFEE.E

Swimming Animo ls


7/11

Water Bath Studies of Mammals 895There was no visual evidence of shivering when the animals were swimming butshivering began within I min after the animals were removed, from the water asevidenced bv visual observation and handling of the animals. The capacity forshivering was &n important factor in det'ermining the extent of heat loss of theanimals confined during immersion (Figs. 5, 6). When confined, the lateralis and

Second & ThirdPeriods

First, Second IThird Periodsirst Period

Fre. 4. Mean change in rectal temperatur:e of animals during three swirnperiods of l0 minutes duration in 25' C water(l : number of swim lria"ls; m : number of animals)

ooEoFEotooccc)co

l= loteroliss = spilosomoo = ourotus

Second I Third First, Second IFirst Period Periods Third Periods

t=4'n=31 ll I I r=roteroriss= spilosomoo= ourotuso= ordit=3, n=3' t=2'n=2

Confined Animols

Second I Third First, Second &First Period Periods Third Periods

| = loleroliss= spilosomoo= ourotuso= ordit=2.n=2 s.D.=o.o' Deod Animols


8/11

NNNNNN

ONrt otNE

EY-m

l

E96 M. L. RrnorsEr, AND J. T. YnlvontoN

Swimming Animols Confined Animols Deod Animols

Confined Animols Deod Animolsmeta,bolic rate during 30 min immersion in25'C water(, : number of swim t'rials; m : number of animals)

spilosoma were a,ble to maintain core temperature by a high metabolic rate butthe a,uratus and ord.i were unable to preyent lowering of rectal temperature, partic-

Swimming Animols Confined Animols Deod AnimolsTre. 6. Total heat loss of animals during 30 min immersion in 25o C water(kcal/brim'z)

E

o

r.9o

Swimming AnimolsFre. 5. llody heat loss and

NEEooYo.Joq-EoF

I otero I isspilosomoou roiu sordi


9/11

Water Bath Studies of Mammalsularly during the first ten-minute-swim period (X'ig. ). The metabolic rates of theconfined animals confirm the visual evidence of shivering by lateralis and spilo-soma (Table 1). Shivering, an important mechanism for rewarming during arousalfrom hibernation, is apparently weli developed in lateralis and spilosoma.Two additional points to be noted are: (1) Differences in body weight did noteffect differences in the heat loss of the dead animals over a 30-min period (Fig. 6,Table 2) (2) The live animals were in or near thermal balance during the last twoswim periods (Fig. a).

DISCUSSIONThese water bath studies permit comparison of the capacity of animals to re-spond to thermal stress by shivering, increased gross activity and vasomotor activ-ity. The curlres in Figs. I and 2 are similar and asymptotic. The bath temperature,body mass and form, and initial body temperature appear to be major factors indetermining the extent of the drop in body temperature which occurs within thefirst 2 min. The capacity of a,nimals to increase metabolic rate under hypothermicconditions was important in determining the shape of the curve a,fter the first few

minutes. All animals had the highest activity during the first few minutes ofsubmersion and became docile and easy to handle after 10 min in the water.There are several points of interest regarding the heat loss of animals during30-min immersion in 25" C water. The srvimming lateralis, spilosoma, and auratus(Fig. 6) had verv similar lotalheat' loss (THL) (tt:0.2-0.7). When confined, thelateralis and spilosoma had much greater THL than auratus and ordi (Fig. 5)(p : O.Ot-0.05) primarily because of a greater metabolic rate (Ta,ble 1, Fig. 5).The auratus and ordi have limited capacity for shivering when compared to late-ralis and spilosoma. Hvpothermia was undoubtedly an important faclor in limit-ing the metabolic rate of free swimming and confined ordi. The THL of spilosomaand lateralis were similar when confined and when swimming (Fig. 6, Table 2);however, as a result of shivering, the confined animals had less lowering of rectaltemperature during the first swim period (Fig. 4). Shivering was more effectivethan swimming in maintaining core temper&ture, presumably beeause the meta-bolic rate was higher when shivering (Horvath et al., f 956). The capacity of auratusand ordi to resist lowering of body temperature when in 25" C water is limited, asevidenced by the similarity of the THL of confined and dead animals (Table 2).The second and third. periods of swimming and confined animals represent steadystate conditions (X'ig. 4). During this thermal balance, total heat loss (THL) isequal to M plus BHL and is the sum of heat conducta,nce through tissues and heattransferred. by the circulation of blood from the warmer cote to the cooler periphery.The data collected on dead animals provides information regarding the rate ofheat loss by tissue conductance. The thermal gradients within dead and live con-fined animals are undoubtedly different; however, by assuming that the conduct-ance of heat through live and dead tissues is similar at a given rectal to water

897


10/11

898 M. L. RrsnnsEr, AND J. T. Yar,vsnroNbath temperature gradient, it is possible to estimate the amount of heat transferredby tissue conductance, and to estimate the amount of heat transferred by circula-tion of blood.In Table 3 we have compared the rate of heat transfer of the swimming, confined,and dead animals. The rate of heat transfer per unit surface area for dead, animalsof each species, given in Table 3, was the rate which occurred over the mean tem-Table 3. Mean Heat Loss of Amimals ,in 25" C Water during Seiond, amd, Third, Per,iod.s (kcal,lhr/rn2)

ITotalheatLossswim. aSwim. bConfined

r4.9

17.8

2Totalheatlossconfined

3 Heat, loss deadanimals 2 less3b1 less3aSpecies and Range oCC. IateralisSwimming 33.0-28.0Confined 37.5-32.3C, spilosomaSwimming 28.5-26.0Confined 33.8-29.3M. auratus

I4.5 19. ?

10.8 I 1.4

t 3.8

pera,ture gradient (mean rectal less water bath temperature) existing during thesteady state condition ofthe second and third swim periods. X'or instance, the rectaltempera,ture of slrimming lateralis during the second and third swim periods rang-ed from 28.0 to 33.0' C; therefore, the heat loss of the dead animals, 8.b kcalfhrf mz,in this temperature range is given in Table 3 and compared with the rate of THLof the swimming animals. The heat loss for all animals while swimming was greaterthan the heat loss of dead animals: lateralis, 40 per cent greater; spilosoma, 65per cent; auratus, 60 per cent; and ordi,46 per cent. These differences are relatedto the volume of blood flow to the skin. Blood flow accounted for 6.0 and 4.2kcallhrlm2 heat loss in lateralis and ordi while blood flow was effective in losing7.0 and 8.2kcallfu lm2 in spilosoma and auratus.When considering the THL of confined and dead animals over the same tem-perature gradient, it is ofinterest to note that blood flow accounted for 20 per cent

Swimming 29.4-27.2Confined 29.7-28.0

Swimming 28.7*26.6Confined 30.2-27.9


11/11

Water Bath Studies of Mammals 899of the hea,t loss of the confined lateralis. The greater heat loss of dead anim&ls ascompared- to confined, animals of the spilosoma', auratus, and ordi species must beexplained by differences in the thermal gradients of the dead and confined animals.fn a dead animal the thermal gradient is nearly equal throughout the body, whereasin a live animal peripheral tissues cool to a lower temperature than in the deadanimal. With a given RI{L greater peripheral cooling means less heat is lost fromthe core, or in other words, there is heat loss from the periphery in preference toheat loss from the core. Estimation of the extent to which preferential cooling occursin lateralis is not possible from the data available. That preferential peripheralcooling is verSr important, is evidenced. by heat loss of confined animals being 80per cent, auratus, 34 per cent, spilosoma, and 33 per cent, ordi, Iess than heat lossof dead animals of the same species.trn summary, the major contribution of these wa,ter bath st'udies has beerr topoint out physiological mechanisms which are operative in determining the toleranceof a given species to a given environmental stress. The C. lateral'is and C. spilosomaresponded to cold water primarily by increasing metabolic rate. The spilosoma wereeffective in limiting cooling of the core .by cooling peripheral tissues. The M. auratusand D. ord,,ihave limited capacity for shivering but confined auratus demonst'ratedconservation of body heat by peripheral cooling. It is da,ngerous at t'his time tosay that a,ny given physiological response is responsible for survival of a givenspecies in a given environment. Ilowever, capacity for shivering and peripheraicooling are important physiological mechanisms in determining the capacity ofa,nimals to tolerate short term cold stress.

REFERDNCESAlolrn, E. F. antl R,rcrnroNo, J. (f 956) Adaptation to cold in golden hamster and groundsquirrel measured chiefly by rates of body cooling. J. appl. Phgsi,ol.9' 53 - 58'Bunrow, A. C. and Eouor,rr, O. G. (1955) Man in a Cold, Enu'ironment. Monographs of thePhysiological Society, No. 2. Edward Arnold, London, p. 23.IIeNNox, J. P. and VrrnECr, E. (ed.) (1955) Proceedings, S;znposia on Arctic Biology andMedicine, II. Comparative Physiology of Temperature R,egulation, Arctic Aerornedical Labo-rai,ory, Fort Wainwright', Alaska.Ifonvaru, s. M., srunn, G. 8., T{urr, B. K. and I{lurr,ron, L. H. (1956) Metabolic cost ofshivering. J. appl. Physi,ol.8, 595 - 602.Invrwe, L. and Kaoe, J. ( 1954) Temperature of skin in the arctic as a regulator of .heat. J . appl.Physi,ol. 7, 355 - 364.I(evsnn, C. (1961) The Physi,otogy of Natura,l Hi,bernat'ion fnternational series of monographson pure and applied biology. Pergamon Press, London, p' 109.Pnossrn, E. L. and BnowN, F. A. (ed.) (196I\ comparati,ue Animal Phgsi.ology. w. B. Saunders,Philadelphia, London.W$,rrn, C. G. (195?) Influence of temperature on performance in guinea ptgs. Amer. J. Physi,ol,,100,457-458.

Documents

WATER, BATH STUDIES OF MAMMALS FROM SEVERAL ECOLOGICAL AREAS