bioenergetics of mammalian hibernation

7/29/2019 Bioenergetics of Mammalian Hibernation

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STUDIES IN ENVI RONMENTAL PHYSIOLOGY

Proceedings of a Symposium Honoring Raymond J. Hock,Dedication of a Room to His Memory, and Memorabilia

(Held at the Laboratory of Environmental Patho-Physiology,Boulder City, Nwada, June 28, 1971)

G. Edgar Folk, Jr.* and D.B. Dill, Editors

Papers by:Marvin L. Riedesel and G.L. RiglerRobert Em. SmithHerman P. Roth


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TABLE OF CONTENTS

David Bruce DillNTRODUCTORY COMMENTS:PREFACE: G. Edgar Folk, Jr.SCIENTIFIC PAPERS:"Bioenergetics of Mammal ian

Marvin L. Riedesel and

Page

H ibernation":G.L. Rigler"Ecological Considerations of the White Mountain Biota":

Robert Em. Smith"Ways of lnterpreting the

Herman P. RothDEDICATION OF A ROOM INMEMORABILIA

Natural Thermal Environment":

MEMORY OF RAYMOND J. HOCKRecollections of Ray Hock: Donald R. Grif finMemorial Statement Read Before the Board of Regents of the

University of Nevada System: Paul S. McDermottContributors to Raymond J. Hock Memorial FundCurriculum VitaComplete Bibliography of Raymond J. HockList of Photographs Deposited in the University of Nevada Library and

Donors of Photographs (the photographs of Ray Hock also representviews of f ield work in Canada, United States, Alaska, South Americaand Japan)

14

2137

38

41424344

50


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INTRODUCTORY COMMENTSDavid Bruce Dill

Director of the Laboratoryof Environmental Patho-PhysiologyDesert Research I nstitute

On June 28, 1971, friends of Raymond J. Hock gathered at the Desert Researchlnstitute's Laboratory of Environmental Patho-Physiology in Boulder City, Nevada todedicate a room as a memorial to him.Dr. Hock, world-renowed environmental physiologist" was killed in an accident inthe Grand Canyon August 27, 1970. He had joined the faculty of the University ofNevada, Las Vegas only a year earlier. His death was a tragic blow to the Universitycommunity and to the world of science. He had been my friend for many years and hadwritten two chapters for our volume, Adaptations to the Environment which waspublished by the American Physiological Society. His chapters were entitled "TerrestrialAnimals in Cold: Reptiles" and "Animals in High Altitudes: Reptiles and Amphibians."Mrs. Hock and Ray's four sons presented to the laboratory his library, his valuablecollection of scientific journals and reprints and instruments of his own design. To housethis collection a room 14' x 24' has been built on the ground floor of the laboratorywhich is located on the grounds of the Metallurgy Research Laboratory, United StatesBureau of Mines. The new room will serve as library and laboratory; it was built by JohnRichardson and fellow students who are laboratory assistants. lt is fitting that its firstofficial use will be for the purpose of having Ray's close friends present scientific papersin his honor.

I am particularly pleased to welcome as special guests Mrs. Hock and her four sons;President John M. Ward, Desert Research lnstitute. University of Nevada System;Professors Wesley E. Niles and W. Glen Bradley, University of Nevada. Las Vegas(UNLV); Dean Robert B. Smith, College of Science and Mathematics, UNLV;Vice-President Donald H. Baepler. UNLV; and Thomas S. White, M.D., Boulder City.


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PREFACEG. Edgar Folk, Jr.

Department of Physiology and BiophysicsThe University of lowa

Ray Hock made a warm and lasting impression on the many people that he met.They liked him immediately. He enjoyed discussing biological problems and challenges,and he liked to express his philosophy as an outdoor scientist. I believe he symbolized anewly developing area of study. I remember an occasion when he had listened to anumber of laboratory workers give a series of papers on environmental physiology. Heturned to me and said, "These fellows shouldn't be giving papers like this. They don'tknow anything about the environment. Why, some of us consistently experience theenvironment while we collect data. Really, you've got to be sort of miserable 'out there'to be an environmental physiologist." Ray liked to give papers and attend meetings andhave a good "talk-fest" about them afterward. lt appeared suitable for us to carry out thistradition before dedicating his Memorial Room today. lt is appropriate now to turn ourattention to some of the meaty challenges in environmental physiology as reviewed bysome of his intimate colleagues.


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BIOENERGETICS OF MAMMALIAN HIBERNATIONM.L. Riedesel and G.L. Rigler

Department of Biology, University of New Mexicoln the pre-Ray Hock era of mammalian hibernation, an author may have simply

described bioenergetics of hibernation as follows: animals metabolize fat as an energysource during winter hibernation whereas they increase body fat during spring, summerand early fall in preparation for hibernation. However, today we recognize, to a largeextent as a result of Ray's relentless activities, that the bioenergetics of hibernationinvolve many exciting facets. Biologists, particularly the authors, will be working formany years before we attain Ray Hock's understanding of this subject. ln this article wehope to express some of our views of the bioenergetics of hibernation and providereferences for additional information and research. ln depth presentations of this subjecthave been written by Kayser,(26) South and House(51) and Fisher and Manery.(9)Research reports on bioenergetics were given at the Mammalian Hibernation-HypothermiaSymposium lV held January 4-8, 1971 at Snowmass in Aspen, Colorado. Abstracts ofreports will appear in Cryobiology Volume 10, May-June 1971. Review papers given atthe plenary session will be edited by F.E. South and J.P. Hannon and published byElsevier Publishing Co., Amsterdam. The Netherlands.

ln a recent publication of Dr. Hock's,(21) he related the physiology andparticularly the temperature regulation of Peromyscus species (nonhibernators) to theirhabitat. l'd like to note a few of the points raised in this article because they are veryappropriate to any consideration of bioenergetics. (1) The 24-hour rhythm of metabolicrate needs to be considered when one estimates the energy requirements of animals. (2)The temperature regulation characteristic of animals is subject to change withacclimatization. Thus the responses of animals to a given thermal environment may bequite different in different seasons. {3} Thermal conductance and fur thickness of ananimal may change depending upon the avenue of heat exchange. Desert animals have lowconductance values due to high radiation of the environment and conversely have highconductance at upper critical temperatures to allow for convective and conductive heatloss.(32) (4) Reduction of evaporative water loss can be aided by low bodytemperatureand boreal habitat. (5) The physiological characteristics of an animal will be indicative ofthe environment in which the animal is living. lf an animal is kept in an animal-colonycondition for long periods of tirne, he may be expected to have shown a loss of thosecharacteristics which are acclimatizing responses to his native environment and to retainonly those which are genetically adaptive, and thus invariable. ln a similar vein, Dr.Hoct(21) hus expressed belief in the concept that the physiological characteristicsofananimal can reveal information regarding the nature of the environment in which thespecies evolved. (6) Captive animals tend to become overweight. The body weight andenergy expenditure of an animal in its native habitat involves complex interaction amongenergy expenditures essential for food gathering, thermal regulation and behavioralcharacteristics. (7) lf we want to learn mammalian physiology, we must take ourlaboratories out into the natural environment because that's where most mammalianphysiological systems are doing their thing.


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The bioenergetics of hibernation is a subject of great contrasts. Metabolic rate andmany other physiological processes are often expressed as a function of body weight. Thecontrasts among hibernators range from 5-g bats to 150 kg bears. During hibernationthere is a very slow breakdown of energy stores (1/100th of resting); whereas arousalfrom hibernation involves a very high rate of energy expenditure by brown fat, muscleand other tissues. Because the body temperature during hibernation variei with animalsize,(25,51) torpid animals of greatly varying size have energy expenditures that arenearly identical. At 10 C a 100-kg bear has a rectal temperature of 31 C and a 5-g bat hasa rectal temperature of 11 C. Hibernators appear to have an extreme amplitude in theannual cycle of body weight. ln addition hibernators may very well be unique in the rapidrate at which they can store energy. Kristoffersson and Suomala;nsn(29) describe weightchanges in the hedgehog as: the animals have a 50% weight gain prior to hibernation andmay lose 4oo/o of their body weight over a winter hibernation period. Similar weight gainsand losses have been described for marmots.(1,8) tne impressive aspect of this cycle isthat the animals gain 50% body weight within a 2-week period in the fall. This capacity togain large amounts of weight within a brief period of time may be associated with otherseasonal cycles. On the other hand, 150- to 275-9 ground squirrels, Cifellus lateralisandc. spilosoma, have been deprived of drinking water to 2o or 3o% body weight losses atdifferent times of the year.(48) When the animals are then given water, they regain weightlost within 3 to 4 days. An annual weight set-point concept has been presented.(38) Thisconcept notes that regardless of the amount of food available the animals gain weight tothe set-Roint weight characteristic of that particular time of year. Thus the ability to havea rapid weight gain apparently persists throughout the year but animals will only gain upto the body-weight set point. The rapid weight gains must involve augmentation ofappetite, secretion of digestive enzymes and marked increase in cardiac output asincreased blood flow must occur to gut and body tissues involved in synthesis andnutrient storage. The capacity to gain weight must be a very innate behavioral andphysiological nature of hibernators because you must control the amount of availablefood very closely if you want to control the weight of a colony of captive groundsquirrels. A recent stuOy(59) has tried to demonstrate the relationship of weight gains forfield and captive animals however their data best supports the hypothesis that both fieldand captive 13-lined ground squirrels have seasonal changes in body weight.SEASON

Hibernators display marked changes in overt activity with season and there is anever increasing amount of information accumulating regarding the fact that hibernatorsundergo seasonal physiological and biochemical changes. Dr. Hock was a person whooften used the terminology, "these animals are in the only physiological state typical ofthe hibernation season."Cold acclimatization prior to entrance into hibernation has been described inh2m51svs(44) and ground squirrels.(45) This acclimatization persists throughout thehibernation period and can be demonstrated by the thermogenic response tonorepinephrine.The circannian rhythm in body weight of ground squirrels and bats needs to beexamined with regard to the efficiency of the utilization of nutrients. Jameson(24) noted


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counting of the number of scats in feces can be an index of the amount of food intake.We need similar studies conducted on an annual basis. Kristoffersson andSuomalainen(29) described a rapid weight gain for hedgehogs on a high protein and fatdiet whereas animals on a high carbohydrate diet had only half the weight gain. Seasonalchanges in the food consumption of the bat have been demonstrated to occur underlaboratory conditions with a constant ambient temperature.(53)Dr. Hock was involved in some of the first studies which described seasonalbiochemical changes.(15) Fat has been classically described as the major metaboliteduring hibernation.(30' 51) A recent study of field and laboratory 6n;6615(59) describes a20 to 80% change with season in the amount of carbohydrate stored in various 13-linedground squirrel tissues. The major triglycerides of brown fat have also been described tochange with season.(40) tre importance of seasonal changes in cytochrome C and watercontent of brown fat may be related to seasonal changes in rates of synthesis and storageof energy in this tissue'(39) however, the significance of seasonal changes in serum lipidsand proteins is not obvious and needs to be related to the overall seasonal physiology andbiochemistry .{.12,521ln our laboratory we have noted seasonal changes in nitrogen excretion andtolerance for water deprivation.(48) The ground squirrels, Citetlus lateralis and C.spilosoma, deprived of drinking water have a larger urine volume and higher ureaconcentration during February and March than at other months (Table 1). Thesedifferences appear to be due to changes in nitrogen metabolism rather than differences inkidney function as evidenced by high serum urea values at the same time as they havehigh nitrogen concentration in urine (Table 2).

1. Twenty-Four Hour Urine Nitrogen of Control and Water-Depriued Citellus lateralis andCitellus spilosoma at Different MonthslCitellus spilosoma Citellus lateralisSeptember February - March DecemberDays ofWater mg mg/100sbody wt mg/1oogmg body wt mg/1oogmg body wt

April - Maymg/1oogmg bodv wtg2 114.0345.2(3)

32.O7.4(71

29"75.O(8)

80.430.o(3)25.6

5.717t27.7

5^3(8)

146.97"4(e)7'1.5

8.6(8)86.313.1(s)

108.37.1(e)

68.41'l .1(8)89.914.6(5)

142.O10.o(8)59.O

6.5(8)39.7

9.O(71

42.5'18.3(7127.99.9(71

21.16.4(7\

245.2 130.824.7 13.3(10) (10)112.4 75.4

4.1 6.3(10) (10)133.1 106.0'17,7 15.6(1 0) (1 0)

23

Data taken from G.L. Rigler's doctorate dissertation to be submitted in partial fulfillment of the re-quirements for the degree, Doctor of Philosophy, at the University of New Mexico"Controls were food deprived 24 hr. previous to urine collection, water adlibitum.MeanS. E.(n)


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TABLE 2. Blood Urea of Control and Water-Depraved Citellus lateralislDays ofNo Water December April - Maymgo/o mg%"

70.43.9(1 0)101.O8.8(1ol116.4

14.O(1o)

1 Dut" taken f rom G.L. Rigler's doctorate dissertation to be submittedin partial fulfillment of the requirements for the degree, Doctor ofPhilosophy, at the University of New Mexico,2 Mean

S. E.(n)A given hibernator in a given month of the year apparently represents a verydifferent physiological state from the same or another species at another time. The extentand precision of the annual weight cycle(42, 43) also emphasize the importance ofseason.TEMPERATU RE REGU LATION

ln hibernation writings there is a great deal of controversy and confusion regardingtemperature regulation. There is agreement in describing the active and alert hibernatorsas being good homeotherms; the disagreements arise when an animal is hibernating. Eventhe authors of this paper disagree as to whether hibernators have temperature regulationduring hibernation. Riedesel votes yes. Rigler votes no. To some extent this controversy,like many others, arises from differences in definition of the term "temperatureregulation." lf you accept the idea that acclimatization to environmental temperature isan expression of temperature regulation, then hibernators have temperature regulation ascold acclimatization has been reported to persist throughout hibernation.(45) lf youdefine spontaneous arousal in a cold environment as an expression of temperatureregulation, then most certainly mammalian hibernators retain temperature regulationduring hibernation. We will not review all aspects of this controversy but would like togive some indication of the problem.Henshaw,(17, 18) vcruab(33) 666 others have evidence of temperature regulationthroughout hibernation. The vital organs--heart, brain and lung--can be expected to havehigher metabolic rates than peripheral tissues during hibernation. This differential inmetabolic rate and the concomittant differential blood flow as evidenced by maintenanceof blood pressure during hibernation, imply that some temperature regulation must beoperational.(17) D.finition of the temperature regulation is very difficult because the

4A322.9(10)50.33.6

(1 0)73.47.4(e)


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metabolic rate is 1/100th that of the resting rate and this low rate of heat productionmay keep the thermal gradients in the animal very small-0.01 to 0.001 C--per cm tissuedepth.Studies of neotropical bats support the hypothesis of temperature regulation duringhi[spns1is6.(33) Behavioral temperature regulation as expressed by movement andclustering has been described for bats.(10, 7) A reduction in the cost of thermoregulation

as a result of clustering has been reported.(14, 19)Some persons presenting evidence and arguing in favor of poikilothermia duringhibernation include 11e6p,(20) Tucker,(S5, 56) Morrison,BS' 12l, Hurrngl(14) 366co-authors. The fact that metabolic rate varies directly with temperatures is mostfrequently taken by these authors to be the best evidence thai hibernators arepoikilothermic during deep hibernation. The technology and design of experimentsconducted by Hammel g-t g!.(14) are impressive but we can argue that the temperaturethey measured in the hypothalamus may not have been at the location of the temperatureregulation center which is operational during hibernation.One can expect homeotherms to have a greater metabolic response to thermalenvironments than poikilotherms. The 01g values can be expected to be 3 to 5 duringhomeothermia and 2 or less during poikilothermia. ln the literature the O10 values of 3to 5 occur over the 10 to 30 C temperature range(20,35) whereas in the 0 to 10 C rangemost OtO values are near 2 or less for both mammalian hibernators andpoikilotherms.l2o,2S, 14) Considerations of differences in 01g values do not resolve thequestion of the absence or presence of temperature regulation during hibernation. Futurestudies may describe arousal from hibernation as resulting from the breakdown or failureof temperature regulation during hibernation. To date there is no good explarration forthe periodic arousals from hibernation; thus we may find that periodic arousals occurbecause the animals approach poikilothermy during a bout of hibernation. Mrosovsky(37)has described similarities between pathological conditions and hibernation.METABOLISM

Recognizing the sensitivity of chemical reactions to temperature and noting thelarge temperature range over which hibernators operate, has raised many questionsregarding the type of biochemical changes which accompany hibernation. Thephysiological challenges become even more obvious when we note that a hibernatinganimal represents a system with no energy input and the energy expenditure is metwithout upsetting the osmotic balance. There are exceptions but most hibernators don'teat or drink; however, they may urinate during periodic arousals.(36) There is a widerange in the water content of the energy stores since glycogen- and protein-storing tissuescontain 75o/o water whereas fat tissue contains 2SYowaler. The various factors involved inwater and energy balance are presented in Table 3. The animal must catabolize the propermixture of tissue such as to meet energy requirementsand osmotic balance. Data on ROhas been cited as evidence that fat is the energy source during hibernation.(51) tt is ofinterest to note that evaporative water loss (EWL) accounts for 8 to 9% ofthe heat lossduring hibernation.(2O, 2' 14l. lt is pertinent that these measurements of EWL have beenmade in dry environments whereas natural hibernacula arei humid. Most tissues aredehydrated during hibernation.(47 , 9, 28, S8) tfre inability to make proper balances--(1)


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energy needed from body tissue available and (2) proper osmotic pressure from wateravailable from catabolism--is a likely causative factor for initiation of arousal fromhibernation.TABLE 3. Pertinent Data for Calculating Water and Energy BalanceStoragpTissue ROI

1g- Caloricl FreeSolids Value Water

O2ls TotalSolid Water of1 Water/g Water/CalDry Oxidation Wet Tissue Energy(s) {CaUs wet (mll (mll (ml/gl (mllTissue) (mllAdipose O,71(fat)Liver 1.OO(glycosen)Muscle O,81

o.75o.25o.25

o.25o.75o.75

7.O1.O1.O

2.O2 0.80o.83 0.15o.97 0.10

1 .O5 0.1 5o.90 0.90

1 Values based on data given by Consolazio et 61.(6)lsolated tissues of hibernators withstand lower temperatures than do similar tissuesof other mammals and strengthen the argument for biochemical changes occurring priorto or during hibernation. These differences have been related to the habitat andphysiological characteristics of the organism and are not merely a result of speciesdifferenees.(23) To u""ount for the differences between tissues of hibernators and

nonhibernators investigators have studied heat of enzyme activation,(51) ,n.y."concentrations(34, 5, 58, 4, 39) and substrate concentrations.(1 1, 49. 54. 12]' No one ofthese approaches has come up with all the answers needed to explain the differencesbetween the tolerance for cold by tissues of hibernators and nonhibernators.Periodic arousals account for at least 5}o/o of the energy expended during winterhibernation and certainly complicates the study of the metabolism of hibernation. Bodyfat stores may be nearly depleted during a winter but this undoubtedly involvesgluconeogenesis from fat stores during the periods of wakefulness. During arousal brownfat represents a major source of energy at low body temperature,116,22' 50) out most ofthe energy for arousal comes from protein and glycogen stores.(3, 27 ,57,12) fte sourceof energy during continuous hibernation appears to be fat tissue; however a recent articleby Galster and Morrison(12) d"-onttrates a progressive-drop in blood glucose duringbouts of hibernation. The blood glucose rises during the short active periods b.etween

cycles of hibernation. These authors suggest that glucose accounts for 1oo/o of themetabolic requirements for an average bout of hibernation. They further suggest that thedecline of blood glucose to one half the value in resting active animals may serve as asignal for arousal of the Arctic ground squirrel from hibernation. Thus imbalance ofmetabolites is another possible causative factor for periodic arousals.BEHAVIOR

Motility, an expression of animal behavior, may account for a large portion of theenergy requirements of an animal. There is no doubt but there is a great future ahead inthe study of behavior of hibernators, if for no other reason than the simple fact there hasbeen very little research conducted in this field to date. \A/e can wonder why this void of


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information exists when one considers that migration, like hibernation, is often describedas a response which permits an animal to avoid exposure to adverse environmentalconditions. There are a vast number of behavioral changes associated with migration evento the extentthat a diurnal animal becomes nocturnal. Many animals initiate migration inresponse to environmental clues prior to onset of adverse environmental conditions.Often animals seek isolation prior to hibernation {bats and some marmots are notableexceptions as they tend to change from isolation prior to hibernation to clustering duringhibernation). The authors have noted that Citellus lateralis go underground for 1 to 2weeks following a day or two of rain in the month of August. McCarley(3l) has noted"hibernation" of the 13-lined ground squirrels in August. We doubt'if these bouts ofunderground living are in response to physiological strain imposed on the animals by theirenvironments. Thus entrance into hibernation may be dependent on proper behavioralresponse to some environmental clues.The literature on the evolution of hibernation is controversial and perhaps sobecause hibernation evolved following the evolution of the behavioral response of seekingisolation following exposure to cold and other environmental clues. The isolated animalscan be expected to spend extended periods of time asleep. The physiological capacity tohibernate could evolve more readily in isolated animals. The idea that hibernation isdependent upon proper behavioral activity may explain why some hibernators exposed tocold in the laboratory do not enter hibernation.Selection of a hibernacula must be a critical phenomenon. McCarley(31) hasreported 13-lined ground squirrels do not necessarily hibernate in the same burrow eachyear. Temperature preference has been described as a factor in selection of hibernationsites by bats.(10, 7) Movement of bats within hibernacula represents a behavioral activitywhich could be essential as animals may freeze if the temperature drops too low and maystarve to death if the ambient temperature and metabolic rate rise too high. q66ssms(46)suggests that starvation is the principal cause of death of insectivorous bats and thethermal environment outside can limit the success of hibernation of the greaterhorse-shoe bat. No one has demonstrated a temperature preference for rodents prior tohibernation in nature; however, Gumma and South(13) have described hamsters as havinga preference for cool temperatures following hypothermia. Brief cold temperature in thefall may effect a preference for cool hibernating temperature for rodents. Thustemperature preference may aid rodents in selection of hibernacula.The bioenergetics of hibernation is a nebulous topic. We do not know the energycost per year for a single species of hibernator. We do know that we must measurephysical parameters including temperature, humidity and air velocity during bioenergeticstudies. We know the torpid bear may be similar to the bat in cal/g energy expenditure,but the biochemical and physiological adjustments which accompany hibernation of eachspecies are not likely to be similar and are not well defined to date. The reader shouldkeep in mind that the seasonal changes in physiological conditions, temperatureregulatory capacity, metabolic pathways and behavioral characteristics of each species ofhibernator may be different from every other hibernator. Environmental physiologists areleft with monumental tasks but, thanks to the efforts of scientists like Ray Hock, theyare asking interesting questions in their search.


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REFERENCES1. Bailey, E.D. and D.E. Davis1965 The utilization of body fat during hibernation in woodchucks. Can. J. Zoot.

43:701-7O7.2. Bartholomew, G.A. and J.W. Hudson1962 Hibernation, estivation, temperature regulation, evaporative water loss, and heart

rate of the pigmy possum, Cercaertus nanus. Physiol Zool. 35:94-1O7.3. Burlington, R.F. and G.J. Klain1967 Gluconeogenesis during hibernation and arousal frqm hibernation. Comp.

B iochem. Ph ysiot. 22 :7 O1 -7 O8.4. Burlington, R.F. and J.H. Simpson1968 Distribution and activity of lactic dehydrogenase isozyme in tissues from ahibernator and a non-hibernator. Comp. Biochem. Physiol. 25:185-192.5. Chaffee, R.R.J., F.L. Hoch and C.P. Lyman1961 Mitochondrial oxidative enzymes and phosphorylation in cold exposure andhibernation. Amer. J. Physiol. 2O1:29-32.6, Consolazio, C.F.. R.E. Johnson and L.J. Pecora1963 Physiological Measurements of Metabolic Functions in Man. 313-339, The

Blakiston Division, McGraw Hill Book Company, New York. pp. 505.7. Davis, W.H.1964 Winter awakening patterns in the bats Myotis lucifugus and Pipistrellus

subflavus. J. Mammal. 45:645-647.8. Fall, M.W.1971 Seasonal variation in the food consumption of woodchucks lMarmota monaxl.J. Mammal.52:37O-375.9. Fisher, K.C. and J.F. Manery1967 Water and electrolyte metabolism in heterotherms. ln Mammalian Hibernationlll (Fisher 9! al., eds.), pp.235-279. Oliver and Boyd, Edinburgh and London.10. Folk, G.E., Jr.1940 Shift of population among hibernating bats. J. Mammal.21:306-315.

1 1. Galster, W.A. and P. Morrison1966 Seasonal changes in serum lipids and proteins in the 13-lined ground squirrel.Comp. Biochem. Physiol. 18:489-501.

12. Galster, W.A. and P. Morrison1970 Cyclic changes in carbohydrate concentrations during hibernation in the arcticground squirrel. Amer. J. Physiol. 218:1228-1232.13. Gumma. M.R. and F.E. South1970 Hypothermia and behavioural thermoregulation by the hamster lMesocricetusauratusl. Anim. Behav. 1 8:504-51 1.14. Hammel, H.T., T.J. Dawson, R.M. Abrams and H.T. Anderson1968 Total calorimetric measurements on Citellus lateralis in hibernation. Physiol.Zool. 41:341-357.'!5. Hannon, J.P., D.A. Vaughan and R.J. Hock1961 The endogenous tissue respiration of the arctic ground squirrel as affected by

hibernation and season. J. Cell. Comp. Physiol. 57:5-'lO.10


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16. Hayward, J.S. and E.G. Ball1966 Ouantitative aspects of brown adipose tissue thermogenesis during arousal fromhibernation. ?iol. Bull. 131 :94-103.17. Henshaw, R.E.1968 Thermoregulation during hibernation: Application of Newton's Law of Cooling.J. Theoret. Biol. 2O:79-9O.18. Henshaw, R.E.1970 Thermoregulation in bats. ln About Bats (Slaughter and Walton, eds.) SouthernMethodist University Press, Dallas, Texas, pp. 188-232.19. Herreid, C.F., ll1963 Temperature regulation and metabolism of Mexican free-tailed bats. Scr'ence142:1573-'1574.20. Hock, R.J.1951 The metabolic rates and body temperatures of bats. Biot. Bull. 1o1:28g-2gg.21. Hock, R.J.1969 Temperature regulation of xeric, mesic, montane and uniquitous Peromyscusspecies. ln Psysiological Systems in Semiarid Environments (C.C. Hoff and M.L.Riedesel, eds.), pp. 53-69. The University of New Mexico Press, Albuquerque.22. Horwitz, B.A., P.A. Herd and R.E. Smith1968 Effect of norepinephrine and uncoupling agents on brown adipose tissue. Can. J.Physiol. Pharm. 46:897 -9O2.23. Hudson, J.W.1971 Thermal sensitivity of isolated-perfused hearts from the ground squirrels, Citellustereticaudus and Citellus tridecemlineatus. Z. Vergl. PhysiologieTl:342-349.24. Jameson, E.W., Jr.1965 Food consumption of hibernating and nonhibernating Citellus lateralis. J.Mammal. 46:634-640.25. Kayser, C.1960 Hibernation vs. hypothermia. Harvard Museum of Comparative Zootogy Bulletin124:9-29.26. Kayser, C.1961 The Physiology of Natural Hibernation. Pergamon Press, New york, 325 pp.27. Klain, G.J. and B.K. Whitten1968 Carbon dioxide fixation during hibernation and arousal from hibernation. Comp.

B iochem. Physiol. 25:363-366.28. Kristoffersson, R., A. Soivio and P. Suomalainen1965 Studies on the physiology of the hibernating hedgehog 3. Changes in thewatercontent of various tissues in relation to seasonal and hibernation cycles. Ann.Acad. Sci. Fenn. A. lV. 92. 17 p.29. Kristoffersson, R., and P. Suomalainen'1964 Studies on the physiology of the hibernating hedgehog 2. Changes of bodyweight of hibernating and non-hibernating animals. Ann. Acad. Sci. Fenn. A. lV.76,'11 p.30. Lyman, C.P. and P.O. Chatfield1955 Physiology of hibernation in mammals. Physiol. Rev.35:403-425.

ll


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31. McCarley, H.1966 Annual cycle, population dynamics and adaptive behavior of Citellustrideceml ineatus. J. Mammal. 47 :294-316.32. McNab, B.K. and P. Morrison1963 Body temperature and rnetabolism in subspecies of Peromyscus from arid andmesic environments. Ecol. Monogr. 33:63-82.33. McNab, B.K.1969 The economics of temperature regulation in neotropical bats. Comp. Biochem.Physiol. 31:227-268.34. Mokrasch, L.C., H.J. Grady and S. Grisolia1960 Thermogenic and adaptive mechanisms in hibernation and arousal fromhibernation. Amer. J. Physiol. 199:945-949.35. Morrison, P. and F.A. Ryser1962 Metabolism and body temperature in a small hibernator, the meadow jumpingmouse, Zapus hudsonius. J. Cell. Comp. Physiol. 60:169-180.36. Moy, R.M.1971 Renal function in the hibernating ground squirrel Spermophilus columbianus.Amer. J. Physiol. 22O:7 47 -753.37. Mrosovsky, N.1970 Regulatory extremes in hibernators and hibernation-likesymptoms in man. J.Psy ch oso matic R es. 1 4:239-246.

38. Mrosovsky, N. and K.C. Fisher1970 Sliding set points for body weight in ground squirrels during the hibernationseason. Can. J. Zool. 48:241-247.39. Paleus, S. and B.W. Johansson1968 Seasonal variations in cytochrome c content of hedgehog brown adiposetissue.Acta Chem. Scand. 22:342-344.40. Paulsrud, J.R. and R.L. Dryer1968 Circum-annual changes in triglyceride fatty acids of bat brown adipose tissue.Lipids 3:34O-345.41. Pearson, O.P.1960 The oxygen consumption and bioenergetics of harvest mice. Physiol. Zool.33:1 52-1 60.42. Pengelley, E.T. and K.C. Fisher

1961 Rhythmical arousal from hibernation in the golden-mantled ground squirrel,Cirellus lateralis tercorum. Can. J. Zool. 39:106-1.2O.43. Pengelley, E.T. and K.H. Kelly1966 A "circannian" rhythm in hibernating species of the genus Cifel/us withobservations on their physiological evolution. Comp. Biochem. Physiol.1 9: 603-61 7.44. Pohl, H.1965 Temperature regulation and cold acclimation in the golden hamster. J. AppliedPhysiol. 2O:4O5-41O.45. Pohl, H. and J.S. Hart1965 Thermoregulation and cold acclimation in a hibernator, Citellus tridecem-lineatus. J. Appl. Physiol. 2O:398-4O4.

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Ransome, R.D.1968 The distribution of the greater horse-shoe bat, Bhinolophus ferrum-equinum,during hibernation, in relation to environmental factors. J. Zool. Lond.154:77-112.Riedesel, M.L., L.R. Klinestiver and N.R. Benally1964 Tolerance of Citellus lateralis and C. spilosoma for water deprivation. 4nnAcad. Sci. Fenn. A. lV. 71/27,377-388.Riedesel, M.L?Y. Lin, J.J. Young and G.H. Bryan

1967 Cesium-137 metabolism in active and hibernating Citellus lateralis. lnMammalian Hibernation lll {Fisher, et al., eds.), pp.219-234. Oliver and Boyd,Edinburgh and London.Sarajas, H.S,S.1967 Blood glucose studies in permanently cannulated hedgehogs during a bout ofhibernation. Ann. Acad. Sci. Fenn. A. lV. 120,11 p.Smith, R.E. and B.A. Horwitz1969 Brown fat and thermogenesis. Physiol. Rev.49:33O-425.South, F.E. and W.A. House1967 Energy metabolism in hibernation. ln Mammalian Flibernation lll (Fisher. q!a|.,. eds.), pp. 305-324. Oliver and Boyd. Edinburgh and London.South, F.E. and H. Jeffay1958 Alterations in serum proteins of hibernating hamsters. Proc. Exper. Biol. Med.

98:885-887.Stones, R.C. and J.E. Wiebers1965 Seasonal changes in food consumption of little brown bats held in captivity at a"neutral" temperature of 92 F. J. Mammal. 46:18-22.Suomalainen, P. and P. Saarikoski1967 The content of non-esterified fatty acids and glycerol in the blood of the

hedgehog during the hibernation period. Experientia 23:457-458.Tucker, V.A.1965a. Oxygen consumption, thermal conductance, and torpor in the California pocket

mouse Perognathus californicus. J. Celt. and Comp. Physiol. 65:393-404.V.A.1965b The relation between the torpor cycle and heat exchange in the Californiapocket mouse Perognathus californicus"..l. Cell. and Camp. Physiol. 65:4O5-414.

Whitten, B.K. and G.J. Klain1968 Protein metabolism in hepatic tissue of hibernating and arousing groundsquirrels. Amer. J. Physiol. 214:136O-1362.Willis, J.S.1968 Cold resistance of mammalian hibernators: cation transport vs. respiration.Amer. J. Physiol. 214:923.Zimney, M., H. Packman and R. Haydel1969 Carbohydrate metabolism in ground squirrels during the summer season. Comp.B iochem. Physiol. 31 :21'l -216.

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