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. Rigler Robert Em. Smith Herman P. Roth

TABLE OF CONTENTS
Page

NTRODUCTORY COMMENTS:
Jr.

David Bruce Dill

PREFACE: G. Edgar Folk,

SCIENTIFIC PAPERS: "Bioenergetics of Mammal ian H ibernation": Marvin L. Riedesel and G.L. Rigler "Ecological Considerations of the White Mountain Biota": Robert Em. Smith
"Ways of lnterpreting the Natural Thermal Environment": Herman P. Roth

14

21

DEDICATION OF A ROOM IN MEMORY OF RAYMOND J. HOCK

37

MEMORABILIA
Recollections

of Ray Hock: Donald R. Grif fin

38

Memorial Statement Read Before the Board of Regents of the University of Nevada System: Paul S. McDermott Contributors to Raymond J. Hock Memorial Fund Curriculum Vita Complete Bibliography of Raymond J. Hock List of Photographs Deposited in the University of Nevada Library and Donors of Photographs (the photographs of Ray Hock also represent views of f ield work in Canada, United States, Alaska, South America
and Japan)

41

42 43
44

50

INTRODUCTORY COMMENTS
David Bruce Dill

Director of the Laboratory

of Environmental Patho-Physiology
Desert Research I nstitute

On June 28, 1971, friends of Raymond J. Hock gathered at the Desert Research lnstitute's Laboratory of Environmental Patho-Physiology in Boulder City, Nevada to dedicate a room as a memorial to him. Dr. Hock, world-renowed environmental physiologist" was killed in an accident in the Grand Canyon August 27, 1970. He had joined the faculty of the University of Nevada, Las Vegas only a year earlier. His death was a tragic blow to the University community and to the world of science. He had been my friend for many years and had written two chapters for our volume, Adaptations to the Environment which was
published by the American Physiological Society. His chapters were entitled "Terrestrial Animals 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 valuable collection of scientific journals and reprints and instruments of his own design. To house this collection a room 14' x 24' has been built on the ground floor of the laboratory which is located on the grounds of the Metallurgy Research Laboratory, United States Bureau of Mines. The new room will serve as library and laboratory; it was built by John Richardson and fellow students who are laboratory assistants. lt is fitting that its first official use will be for the purpose of having Ray's close friends present scientific papers in 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.

PREFACE
G. Edgar Folk, Jr. Department of Physiology and Biophysics The 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 a newly developing area of study. I remember an occasion when he had listened to a number of laboratory workers give a series of papers on environmental physiology. He turned to me and said, "These fellows shouldn't be giving papers like this. They don't know anything about the environment. Why, some of us consistently experience the environment 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 and have a good "talk-fest" about them afterward. lt appeared suitable for us to carry out this tradition before dedicating his Memorial Room today. lt is appropriate now to turn our attention to some of the meaty challenges in environmental physiology as reviewed by
some

of his intimate

colleagues.

BIOENERGETICS OF MAMMALIAN HIBERNATION

M.L. Riedesel and G.L. Rigler
Department of Biology, University of New Mexico

ln the pre-Ray Hock era of mammalian hibernation, an author may have simply described bioenergetics of hibernation as follows: animals metabolize fat as an energy source during winter hibernation whereas they increase body fat during spring, summer and early fall in preparation for hibernation. However, today we recognize, to a large extent as a result of Ray's relentless activities, that the bioenergetics of hibernation involve many exciting facets. Biologists, particularly the authors, will be working for many years before we attain Ray Hock's understanding of this subject. ln this article we hope to express some of our views of the bioenergetics of hibernation and provide references for additional information and research. ln depth presentations of this subject have been written by Kayser,(26) South and House(51) and Fisher and Manery.(9) Research reports on bioenergetics were given at the Mammalian Hibernation-Hypothermia Symposium lV held January 4-8, 1971 at Snowmass in Aspen, Colorado. Abstracts of reports will appear in Cryobiology Volume 10, May-June 1971. Review papers given at the plenary session will be edited by F.E. South and J.P. Hannon and published by Elsevier Publishing Co., Amsterdam. The Netherlands.

ln a recent

publication

of Dr. Hock's,(21) he related the physiology

and

particularly the temperature regulation of Peromyscus species (nonhibernators) to their habitat. l'd like to note a few of the points raised in this article because they are very appropriate to any consideration of bioenergetics. (1) The 24-hour rhythm of metabolic rate needs to be considered when one estimates the energy requirements of animals. (2) The temperature regulation characteristic of animals is subject to change with acclimatization. Thus the responses of animals to a given thermal environment may be quite different in different seasons. {3} Thermal conductance and fur thickness of an animal may change depending upon the avenue of heat exchange. Desert animals have low conductance values due to high radiation of the environment and conversely have high conductance at upper critical temperatures to allow for convective and conductive heat loss.(32) (4) Reduction of evaporative water loss can be aided by low bodytemperature and boreal habitat. (5) The physiological characteristics of an animal will be indicative of the environment in which the animal is living. lf an animal is kept in an animal-colony condition for long periods of tirne, he may be expected to have shown a loss of those characteristics which are acclimatizing responses to his native environment and to retain only those which are genetically adaptive, and thus invariable. ln a similar vein, Dr. Hoct(21) hus expressed belief in the concept that the physiological characteristicsofan animal can reveal information regarding the nature of the environment in which the species evolved. (6) Captive animals tend to become overweight. The body weight and energy expenditure of an animal in its native habitat involves complex interaction among energy expenditures essential for food gathering, thermal regulation and behavioral characteristics. (7) lf we want to learn mammalian physiology, we must take our laboratories out into the natural environment because that's where most mammalian physiological systems are doing their thing.

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

SEASON
Hibernators display marked changes in overt activity with season and there is an ever increasing amount of information accumulating regarding the fact that hibernators undergo seasonal physiological and biochemical changes. Dr. Hock was a person who often used the terminology, "these animals are in the only physiological state typical of the hibernation season." Cold acclimatization prior to entrance into hibernation has been described in h2m51svs(44) and ground squirrels.(45) This acclimatization persists throughout the hibernation period and can be demonstrated by the thermogenic response to norepinephrine. The circannian rhythm in body weight of ground squirrels and bats needs to be examined with regard to the efficiency of the utilization of nutrients. Jameson(24) noted

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

and

Suomalainen(29) described a rapid weight gain for hedgehogs on a high protein and fat diet whereas animals on a high carbohydrate diet had only half the weight gain. Seasonal changes in the food consumption of the bat have been demonstrated to occur under laboratory conditions with a constant ambient temperature.(53) Dr. Hock was involved in some of the first studies which described seasonal biochemical changes.(15) Fat has been classically described as the major metabolite during hibernation.(30' 51) A recent study of field and laboratory 6n;6615(59) describes a 20 to 80% change with season in the amount of carbohydrate stored in various 13-lined ground squirrel tissues. The major triglycerides of brown fat have also been described to change with season.(40) tre importance of seasonal changes in cytochrome C and water content of brown fat may be related to seasonal changes in rates of synthesis and storage of energy in this tissue'(39) however, the significance of seasonal changes in serum lipids and proteins is not obvious and needs to be related to the overall seasonal physiology and
biochemistry .{.12,521

ln our laboratory we have noted seasonal changes in nitrogen excretion and tolerance for water deprivation.(48) The ground squirrels, Citetlus lateralis and C. spilosoma, deprived of drinking water have a larger urine volume and higher urea concentration during February and March than at other months (Table 1). These differences appear to be due to changes in nitrogen metabolism rather than differences in kidney function as evidenced by high serum urea values at the same time as they have
high nitrogen concentration in urine (Table 2). TABLE

1.

Twenty-Four Hour Urine Nitrogen of Control and Water-Depriued Citellus lateralis and Citellus spilosoma at Different Monthsl
Citellus spilosoma September February - March mg/100s mg/1oog Citellus lateralis December April - May mg/1oog mg/1oog

Days of No Water mg
g2

body wt
80.4 30.o (3) 25.6 5.7
17t

mg

body wt
108.3
7.1

mg
142.O

body wt
42.5
'18.3
(71

mg

bodv wt
130.8 13.3 (10) 75.4 6.3 (10) 106.0 15.6
(1 0)

114.03 45.2 (3)

32.O

146.9 7"4 (e) 7'1.5

10.o
(8) 59.O

(e)

245.2 24.7 (10) 112.4 4.1 (10) 133.1 '17,7 (1 0)

68.4
1'l .1

7.4
(71

8.6
(8)

6.5
(8)

27.9 9.9
(71

(8)

29"7
5.O

27.7
5^3

86.3
13.1

89.9 14.6
(5)

39.7
9.O
(71

21.1

(8)

(8)

(s)

6.4 (7\

Data taken from G.L. Rigler's doctorate dissertation to be submitted in partial fulfillment of the requirements for the degree, Doctor of Philosophy, at the University of New Mexico"
2 3

Controls were food deprived 24 hr. previous to urine collection, water adlibitum.
Mean
S. E.

(n)

TABLE

2.

Blood Urea of Control and Water-Depraved Citellus lateralisl

Days of No Water

December mgo/o
4A32
2.9 (10) 50.3 3.6
(1

April - May
mg%"

70.4 3.9
(1

0)

101.O

8.8

0)

(1ol
116.4
14.O

73.4 7.4
(e)

(1o)

1 Dut" taken f rom G.L. Rigler's doctorate dissertation to

be submitted in partial fulfillment of the requirements for the degree, Doctor of Philosophy, at the University of New Mexico, Mean

S. E.

(n)

A given hibernator in a given month of the year apparently represents a very different physiological state from the same or another species at another time. The extent and precision of the annual weight cycle(42, 43) also emphasize the importance of
season.

TEMPERATU RE REGU LATION

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

metabolic rate is 1/100th that of the resting rate and this low rate of heat production may keep the thermal gradients in the animal very small-0.01 to 0.001 C--per cm tissue
depth. Studies of neotropical bats support the hypothesis of temperature regulation during hi[spns1is6.(33) Behavioral temperature regulation as expressed by movement and clustering 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 during hibernation include 11e6p,(20) Tucker,(S5, 56) Morrison,BS' 12l, Hurrngl(14) 366 co-authors. The fact that metabolic rate varies directly with temperatures is most frequently taken by these authors to be the best evidence thai hibernators are poikilothermic during deep hibernation. The technology and design of experiments conducted by Hammel g-t g!.(14) are impressive but we can argue that the temperature they measured in the hypothalamus may not have been at the location of the temperature regulation center which is operational during hibernation. One can expect homeotherms to have a greater metabolic response to thermal environments than poikilotherms. The 01g values can be expected to be 3 to 5 during homeothermia and 2 or less during poikilothermia. ln the literature the O10 values of 3 to 5 occur over the 10 to 30 C temperature range(20,35) whereas in the 0 to 10 C range

poikilotherms.l2o,2S, 14) Considerations of differences in 01g values do not resolve the question of the absence or presence of temperature regulation during hibernation. Future studies may describe arousal from hibernation as resulting from the breakdown or failure of temperature regulation during hibernation. To date there is no good explarration for the periodic arousals from hibernation; thus we may find that periodic arousals occur because the animals approach poikilothermy during a bout of hibernation. Mrosovsky(37)
has described

most OtO values are near 2 or less for both mammalian hibernators

and

similarities between pathological conditions and hibernation.

METABOLISM
Recognizing the sensitivity of chemical reactions to temperature and noting the large temperature range over which hibernators operate, has raised many questions regarding the type of biochemical changes which accompany hibernation. The physiological challenges become even more obvious when we note that a hibernating animal represents a system with no energy input and the energy expenditure is met without upsetting the osmotic balance. There are exceptions but most hibernators don't eat or drink; however, they may urinate during periodic arousals.(36) There is a wide range in the water content of the energy stores since glycogen- and protein-storing tissues contain 75o/o water whereas fat tissue contains 2SYowaler. The various factors involved in water and energy balance are presented in Table 3. The animal must catabolize the proper mixture of tissue such as to meet energy requirementsand osmotic balance. Data on RO has been cited as evidence that fat is the energy source during hibernation.(51) tt is of interest to note that evaporative water loss (EWL) accounts for 8 to 9% ofthe heat loss during hibernation.(2O, 2' 14l. lt is pertinent that these measurements of EWL have been made in dry environments whereas natural hibernacula arei humid. Most tissues are dehydrated during hibernation.(47 , 9, 28, S8) tfre inability to make proper balances--(1)

energy needed from body tissue available and (2) proper osmotic pressure from water available from catabolism--is a likely causative factor for initiation of arousal from hibernation.
TABLE
Storagp

3.

Pertinent Data for Calculating Water and Energy Balance

Tissue
1g

ROI

Caloricl Solids Value

Free

Solid

O2ls

Water

(s)
O,71
1.OO

{CaUs Tissue)
7.O 1.O 1.O

wet

(mll
o.25 o.75 o.75

of1 Water/g Water/Cal Dry Oxidation Wet Tissue Energy (mll (ml/gl (mll (mll
Water 0.80 0.15 0.10
1

Total

Adipose
(fat)

o.75 o.25 o.25

2.O2 o.83 o.97

.O5

0.1 5

Liver
(glycosen)

o.90

0.90

Muscle 1 Values

O,81

based on data given by Consolazio et 61.(6)

lsolated tissues of hibernators withstand lower temperatures than do similar tissues of other mammals and strengthen the argument for biochemical changes occurring prior to or during hibernation. These differences have been related to the habitat and physiological characteristics of the organism and are not merely a result of species differenees.(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 of these approaches has come up with all the answers needed to explain the differences between the tolerance for cold by tissues of hibernators and nonhibernators. Periodic arousals account for at least 5}o/o of the energy expended during winter hibernation and certainly complicates the study of the metabolism of hibernation. Body

stores may be nearly depleted during a winter but this undoubtedly involves gluconeogenesis from fat stores during the periods of wakefulness. During arousal brown fat represents a major source of energy at low body temperature,116,22' 50) out most of the energy for arousal comes from protein and glycogen stores.(3, 27 ,57,12) fte source of energy during continuous hibernation appears to be fat tissue; however a recent article by Galster and Morrison(12) d"-onttrates a progressive-drop in blood glucose during bouts 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 the metabolic requirements for an average bout of hibernation. They further suggest that the decline of blood glucose to one half the value in resting active animals may serve as a
signal for arousal of the Arctic ground squirrel from hibernation. Thus imbalance of metabolites is another possible causative factor for periodic arousals.

fat

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

information exists when one considers that migration, like hibernation, is often described to avoid exposure to adverse environmental conditions. There are a vast number of behavioral changes associated with migration even to the extentthat a diurnal animal becomes nocturnal. Many animals initiate migration in response to environmental clues prior to onset of adverse environmental conditions. Often animals seek isolation prior to hibernation {bats and some marmots are notable exceptions as they tend to change from isolation prior to hibernation to clustering during hibernation). The authors have noted that Citellus lateralis go underground for 1 to 2 weeks 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 of underground living are in response to physiological strain imposed on the animals by their environments. Thus entrance into hibernation may be dependent on proper behavioral response to some environmental clues. The literature on the evolution of hibernation is controversial and perhaps so because hibernation evolved following the evolution of the behavioral response of seeking isolation following exposure to cold and other environmental clues. The isolated animals

as a response which permits an animal

can be expected to spend extended periods of time asleep. The physiological capacity to hibernate could evolve more readily in isolated animals. The idea that hibernation is dependent upon proper behavioral activity may explain why some hibernators exposed to cold in the laboratory do not enter hibernation. Selection of a hibernacula must be a critical phenomenon. McCarley(31) has reported 13-lined ground squirrels do not necessarily hibernate in the same burrow each year. Temperature preference has been described as a factor in selection of hibernation sites by bats.(10, 7) Movement of bats within hibernacula represents a behavioral activity which could be essential as animals may freeze if the temperature drops too low and may starve 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 the thermal environment outside can limit the success of hibernation of the greater horse-shoe bat. No one has demonstrated a temperature preference for rodents prior to hibernation in nature; however, Gumma and South(13) have described hamsters as having a preference for cool temperatures following hypothermia. Brief cold temperature in the

fall may effect a

preference

for cool

hibernating temperature

for

rodents. Thus

temperature preference may aid rodents in selection of hibernacula. The bioenergetics of hibernation is a nebulous topic. We do not know the energy cost per year for a single species of hibernator. We do know that we must measure physical parameters including temperature, humidity and air velocity during bioenergetic studies. 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 each species are not likely to be similar and are not well defined to date. The reader should keep in mind that the seasonal changes in physiological conditions, temperature regulatory capacity, metabolic pathways and behavioral characteristics of each species of hibernator may be different from every other hibernator. Environmental physiologists are left with monumental tasks but, thanks to the efforts of scientists like Ray Hock, they are asking interesting questions in their search.

REFERENCES
1. Bailey, E.D. and D.E. Davis

1965 The utilization of body fat during hibernation in woodchucks. Can. J. Zoot.
43:701-7O7.

2. Bartholomew, G.A. and J.W. Hudson 1962 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. Klain 1967 Gluconeogenesis during hibernation and arousal frqm hibernation. Comp. B iochem. Ph ysiot. 22 :7 O1 -7 O8. 4. Burlington, R.F. and J.H. Simpson 1968 Distribution and activity of lactic dehydrogenase isozyme in tissues from a hibernator and a non-hibernator. Comp. Biochem. Physiol. 25:185-192. 5. Chaffee, R.R.J., F.L. Hoch and C.P. Lyman 1961 Mitochondrial oxidative enzymes and phosphorylation in cold exposure and hibernation. Amer. J. Physiol. 2O1:29-32. 6, Consolazio, C.F.. R.E. Johnson and L.J. Pecora 1963 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. Manery 1967 Water and electrolyte metabolism in heterotherms. ln Mammalian Hibernation lll (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. Morrison

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. Morrison 1970 Cyclic changes in carbohydrate concentrations during hibernation in the arctic ground squirrel. Amer. J. Physiol. 218:1228-1232. 13. Gumma. M.R. and F.E. South

1966

1970 Hypothermia and behavioural thermoregulation by the hamster

auratusl. Anim. Behav. 1 8:504-51 1. 14. Hammel, H.T., T.J. Dawson, R.M. Abrams and H.T. Anderson

lMesocricetus

1968 Total calorimetric measurements on Citellus lateralis in hibernation. Physiol.

Zool. 41:341-357. '!5. Hannon, J.P., D.A. Vaughan and R.J. Hock 1961 The endogenous tissue respiration of the arctic ground squirrel as affected by hibernation and season. J. Cell. Comp. Physiol. 57:5-'lO.
10

16. Hayward, J.S. and E.G. Ball 1966 Ouantitative aspects of brown adipose tissue thermogenesis during arousal from hibernation. ?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.) Southern Methodist University Press, Dallas, Texas, pp. 188-232. 19. Herreid, C.F., ll 1963 Temperature regulation and metabolism of Mexican free-tailed bats. Scr'ence 142:1573-'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 Peromyscus species. 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. Smith 1968 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, Citellus tereticaudus and Citellus tridecemlineatus. Z. Vergl. PhysiologieTl:342-349.
24. Jameson, E.W., Jr.

1965 Food consumption of hibernating and nonhibernating Citellus lateralis.

Mammal. 46:634-640.

J.

25. Kayser, C. 1960 Hibernation vs. hypothermia. Harvard Museum of Comparative Zootogy Bulletin 124:9-29. 26. Kayser, C. 1961 The Physiology of Natural Hibernation. Pergamon Press, New york, 325 pp. 27. Klain, G.J. and B.K. Whitten 1968 Carbon dioxide fixation during hibernation and arousal from hibernation. Comp. B iochem. Physiol. 25:363-366. 28. Kristoffersson, R., A. Soivio and P. Suomalainen 1965 Studies on the physiology of the hibernating hedgehog 3. Changes in thewater content 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 body weight of hibernating and non-hibernating animals. Ann. Acad. Sci. Fenn. A. lV. 76,'11 p.
30. Lyman, C.P. and P.O. Chatfield 1955 Physiology of hibernation in mammals. Physiol. Rev.35:403-425.

ll

31. McCarley, H.

1966 Annual cycle, population dynamics and adaptive behavior

trideceml ineatus. J. Mammal. 47 :294-316. 32. McNab, B.K. and P. Morrison

of

Citellus

1963 Body temperature and rnetabolism in

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