XXII

THE INTI]IINAL ENVIRONMENT

DTIRING HIBERNATION
Ily I'Il,nvtN f;. lirnot:snr,
l)epartncrrt of Occupational llealth (:h'aduate School of Pu].r1ic. I{ealth Ulir.ctsi.ty of Pittsbulgh, Pittsburgh, l'errri.

i,onered boci;' tempc'lature ancl reclucecl metabolie rate fol an extendecl period of time are included in the simplest clescription of hibernation. liecentl1., ne have learnecl to expect numerons bjochernical changes chiring liibernation. Riologieal proeesses ale lecognizell as being subject to rnodi{ication by these threc factors : ternperature, time anrl (:iicrnical envirorrment. Befor:e considering the biochemical changes r'r.hich occur with hibernation, let us consider briefl.v some examples of the interclependence of these factors. The interclepenclence of time and chemical environrnent iir biologitral processes is demonstratecl b1' thtr catalytic actiorr of enzynres ancl ions. The interaction of temper:ature and chemical environnrent is iilustraterl b1- Rachtach's stuclies (I3aclirach, 19,t6). TTe observcd a tlro1t ol 17"C in the olrtinurn lemperature for contraction of the snail (Hel'i:r a,spero L\Iull) healt rviien lireb's solution \vas rcplacec'l |11r ic6f6p's ryl'o nesium chloride. The optimum temperature for contraction jn isotonic potassium aild sodiuni chlorjcie u'as intcrtnecliate. Other tlemonstrations of the interdependencl. of chernical ertvironment turtl temperrature rr.ere macle b1r Conl'a1- aiitl Geoglregan (19;15) and bl Adolph ancl Richmond (1956). Thel'reltoltecl a gain irr rr-eiglrt rihen tissues \r'ele suspendecl in cold isotonic solutions. -\tlolph and Riehinontl liale strggested a reclefinitiort of isotoiric-

itI- ltt ,.tirrr of tempc'r"ature antl time. Interclellcnrleitce of teruperattrle atrtl tirte is cletuonstrated 1t1' the effect of timc npotr the optimum terirperature 0f enzl'111gs zrnd enzyrtte systellls (Spec tor, 1956; Dixon ancl \\rebb, 1958). Thc iirpoltatrrre of tinc irr r'lefining tolerance linrits of anirtrals to heat ancl colti is arlotherr c-xample of the interdependernce of time arttl tcirtllelaturc. It appears that a stuciy of bioJogical processes dur:ing hibelnation rnust consicler the iirter:clcpericlence of tenperatnre, tjnre ancl rlttttrit'lrI ettt'ilolttrtt'ttt.

+22

Btu,rrETrN: trIrsE{IM oF ool{pARATrvE zoorroey Yol,

12.1

Serum Electrolyte Levels Duling Hibematiorr The relation of the uragnesiurn ion to temperature regulation particular interest to the elevation of serum magnesium during hibernatioir. Three types of studies other than hibernatiorr have related the ruagnesiurn ion to heat loss. Parenteral inhas given

jection of magnesiuni has been clemonstrated to facilitate hypothermia (Schutz, 1916; Heagy and Burton, 1948; Hall et al.. 1951) and elevated serllm rnagnesium has heen reported to be l)roduced with hypothermia in a nurnber of animals (Steadnlan ei al., 1943; Piatner, 1950; Platner ancl l{osko, 1953). The antipyretic ection of magnesium has been described in experirneutal animals and in human beings (Barbour antl Winter, 1 9!8 : Sollman. 1957 )
.

'l,q.er,s

I
InYestigator

Reltorts ou Senrnr Magnesiurn clurilg Hibernation

Coltnt
orr

Nattr e

Scientilic Narne
C,itcllus
.llo Iitr,eahts

Increase over'

Controls 65/o

Thirteen-linecl ground squir:rel

Woodchuch
Golclen harnster

trid,eaenr moilt.t us seroti,nus

Rietlesel and Folk (1957)

nnota

637
25% 62% 53%

'Vesocriaetus
attralus
lztciJ'ug 'Eyttesious

-\{cBirnie et al,. (1953) Riedesel and Folk (1957)

'liieclesel

Little brorvr bat tr[yotis

I3ig blown bat
I'Ieclgehog

Er'tmaccu.seuropaeus l)2%
Erirutcetts ?url9)(reus rlone

Jleclgehog

ancl Folk (1957) Il,iedesel (1957) Suomalainen (1939) {Jiiirck r:t rul. (1956)

Itrlevation of the seluln nlagnesium appears to be a character'istic of hibernatiorr. Reports of eler,ated seruln magrlesium ha\:e been made on a lal'ge sample of ttre hibernators by several indepenclent laboratories (Table I). The extent of the increase in selum maguesiuln is depenclent r.rpon the species of the hibernator'. Some of the details of the change in serum magnesium \r:ere deterlninecl in studies on the little brorvn bat. There $'as no sigtrilicant increase in the inagnesiurn $,hen esophageal teinperature had log'ered to 17"C, but an elevation of serum magnesiurn was obsel'ved s,hen the esophageal temperature hacl dropped to 13"C (Fig. I t. 'lhe elevation of serum magnesiunl appears to

960

MA}IMAITIAN HIBERNATION

,{

oD

be deperrdent upon cooling of cells. Bats raised their botly tern, perature to the semiactir,e ler.el of 18"C in fou.r to eight rninutes 'level l-ithout

2).

ture clurirrg arousal from hiberiration. Then, rvhen the bod-v temperature lras raisecl further b-y exposure in a l arm room for one hour'. thc selum mitEnesinnr l.as back to the basal le.r'el of

altcring the hiberrration of serum magnesium (Fig. The rnagnesium ler.cl appears to be inclcpenclent of tempera-

-o o)7
Q'l

E^ fo a l!

.o o

z LD.
:l

a
-c
@

(I)

<.3 =

I o L
!

ft4 U)
3Oo 25" 2Oo l5o
BODY TEMp. oC (Esophogeot)

qJ

lo"

50

}-ig. 1. Setnnr uruguesiurrr ralucs il ltats cooled to ltrogrcssir-e11- los'er botly tcrnpelaturcs. (Lightest shaded alcr rcll'csetts trro st:rntlarcl cleviatiols lubove arncl beiol' thc tueern.) active bats. The eler.ation of bocly temperature r-ithout a redu(rtion of the serurn lnagnesiuin contraindicates the role of lnagne-

sium as a causative factor in hibernation. This arguiitent is $,eakened by the fact tirat awakening from hibelnation appeals to be a very differeirt process from "going into" this state. Ileports on serulll clectroll-tes other than maEnesium clescribe plimarily homeostasis of potassiuni, socliuru and calcium during hibernation. There are some exceptions. I)epending upon thc

421

BI]LITETIN

NI]SEUN{ OF CO\,IPARATIVE ZOOI]OCIY YOl- 124

species stutlied, the serum potassium remains near control levels

or increases cluring hibernation. An 82 pel celt increase in the serttrn ler-el ofi potassiurn during lril,rcriration of the l'oorlchucli lras bcen reportecl (l{cl}irnie et a!.. 1.95:}) (Table TI). A consistent increase jn serum l)otassiilril has been observerl l.ith active hamsters. g'r'orLncl squirrels aiirl bats in a colrl environment (Ricclcscl anci lrollr. 'l 9i8). The cause antl effect relationship oI the changes in semm irotassiunr alcr not apparerrt, Jrut

)Z s.r"

z,s"

300
Active

oC. (Esophogeol) BODY TEMP,

-!'ig.

hr.

2.

Selurn ruaglesiLrru Iet-cJs tlulirrg alonsll

frorl

hil rernation.

thc

charrges

activity or utilization of glygsgsll. 956) havc reported an increase in intracelh.rlar lrotassiunr u'ith tlepositiorr of. gl1.cogen. Thus. the irrcrease of serum 1rotassiunr ruav lesult flont tire i:ecluction in gl1-cogen stores rrhich occru's cluring hibernation (Zimiry. 1956). The r-alues of serrn soclium clnring hibernatiou of the heclgehog l-ere similar to those found- in actile aniilals (Suomalaineir, 1939, 1953; BiiJlcli at al., 1956). Reports of seruni calciuni coucentration cluring hibelnatior-r are controver:sial. No change has been repoltecl u.itli hibernatioir of the grouncl sqtirrel. hamster antl heilgehog, rvheleas hrpocalcenria has been obserretl u.itir hiber'nation of the little brori'n bat ancl Eulopean marrnot. An 88
effectecl b1' aclrenal cortical

in selrm
(.1

potassium tluring hibelnation rna)- bc

Fenrr ancl Asarro

1960

}TAMMAIIIAN HIBERNATION

per cent inerease in the serllrn calciurn was lepolted rvith hibernation of the Eruopean lnannot (tr'erdrlann and Feinscirmidt, 1932). A more detailed stu.d1- of the little brol-n bat has given rise to interesting speculation. The clata in Figure 3 suggest that thc serum levels observed during hibemation mav varJr l'ith the body temperature and./or clepth of hibernation. The lot,ering of serum calcitul I'ith reclucecl body temperature cloes not appear to bc large, but jt is consistcnt. The lorvering of sertnr

'lAsln II
Iteports on Selurri Electrol;'tes clurirrg Hiliernation
AnimaI

ls Compared to Controls Potnssium Calciurn Soclium

tlecreasert

Dlec trol)"te Concentrations

Investigator

\{ooclehuck int,reasecl European marmot

tlecreaseti

I[cBirnie et al. (7953) Adler (1926)

X'ertlmann and

increased
uci cha.nge

'l'hilteen-linecl
grouncl squinel

rro change

X'einschmidt (1932) Rietlesel ancl Folk (1958) Rieriesel and Irolk (1958) Rierlesel and !'otk (1958) Riedesel ancl Folk (1958)
no change no change Suomalainen

Ilarnstcr

no change

no ohange
decleasecl"
tn

l,ittle brown bat

Big brown bat
I{eclgehog

ircr

eased'F

lo

change no change

clccreased
rro cLange

(1e3e) (1e53)

lo chauge

Bitirck cf ol. (195ti)

*'.lho itrcrease $'as collsistent but rot statisticallJ' signilicant. **'l'lro sellrrD cnlcinur trppears to rary with dcl)th of hillerntrtion.

calciurn with hibernation of the little bror,vn bat receives further support from the observation of a 54 per cent reduction in serum calcium in bats rvhich had hibernated for ten $'eeks and a 34 per cent decrease after nine weeks of hibernation (Rieclesel, 1957). The lorv and apparently fluctuating calcium levels with
extended hibernation canrot be explained on the basis of the data available. The calcium let'el may cycle during long-term hibernation, and the data cited here may have been taken at times \\'hen the calcium level happened to be at a low ebb of the cycle. Strch a cycle lila)' accoullt for the contraclictory reports on the ca.lciunl content of thc selurn during hibernation $'hich appear

.126
t,o

BULT,ETTN: MUSEUM oF coMPARATTvE

zoorJocY Yol. 124

in Tabie II. It

m&;r [. that during hibernation the circulation calcium stores and,/or hi<Lney function is not consistently aderluate to meet the tissue clemands for calcium, and at the same time maintain a cotrstant serum calcium level.

lo

+
o6

a
= ?4

o
J

o2
AcrrvE

COOLED COOLED WARMEO WARMEO

ACTIVE

DAYS

l7-20'C lt-13"c l3'c

STAGES OF HIBERNATION
measur:ements

TO

TO

TO

TO l8'c

HR.

hibernation. (shacled area represents one stanclalc'l deviation above

I.relo'n'

f ig. 3. Serun calcium

the mean.)

of Myotis lucifugtr's in stages of

a,ntl

Body X'luicls

l'elv rneasulremerlts of bocly fluicl have been uracle during hibernation. The susceptibility of the hibernating auimal to manipulation limits the success of such lneasurements. SmaII decreases in plasma r'olutne are inclicated by bloocl volllme ancl total serurn proteiu rneasurentents. The increase in blooil volume/body \\.eight d.uring'hibernation of the hamster r'vas largely cxplainecl b.v loss of bocl;' $reight (L)'man et al', 1957)' An increase in serun concentration is inclicated by the 21 per cent increase in total serum proteins cluring hibernation of the hamster (South ancl Jelfay, 1958). Actually, information regarcling blood. and plasma volture is limitecl to hematological observations. The hematological stuclies shorv inconsistent results (Table UI). The data on the golclen hanster ancl European rnarmot inclicate concentration of the bloocl, if not the plasma. Cyclic

1960

ilIAMMAIJIAN HIBERNATION

427

shifts of body rvater may account for the controversial hernatological clata. The electroll.ts data citecl earlier indicate homeostasis 'n'ith regard to body fluid compartments since magnesium, potassium and calcium concentrations change independently of each other; for instance, if the elevation of serum magnesium tluring hibernation rvere due to a decrease in plasma water, one rvoulcl expect similar increases in serum potassium, calcium ancl sodium values. The rrrine of hibernating glround. squirrels has been reportecl to be of verl!' small volume and dilution
Taer,n

III

Indiees of Hemoconcentration during Hibernation

Animll
'l'hirtecnlined ground squirrel
Woorlchuck
Change

Criteria

with IfemoHiberlation colcentration

Inrestigator

Ir)r'ythrocyte count d.ecreaserl 1h'.vthrocyte count increaseil []Iematocrit sl. increase llematocrit no change Serum sp. gr. no change

+ + 0 0 + 0 0 + + + + + + + 0 + 0 0 0 + + 0

Elythrocyte count decleased Ilernatocrit increased

T,Iermoglobin rro change

Stuckey ancl Coco (1942) Svihla ancl Borvman (1953) Svihla ancl Bowman (1953) liieclesel (1957) Rieclesel (1957) R,asmussen (1916)

McBirnie et aI. (1.953') Ra.smussen (1916)

Rasmussen (1916)

P'lood sp. gr.

no change

European

Rlootl sp. gr.

ilcrcaserl

Dubois (1896)

marnot

Erythroeyte count increasecl \Vater content of tl ec rea se rl

blood )Ir'-trthroeyte count increaseri I{ematoerit incleased I{ematocrit increased Hema.tocrit increased Serum sp. gl. uo change Total Serum iucleaserl
p

Dubois (1896) Aeby (1875)

I{a.rnster

l)ubois (1896) Lyman ef al. (1957)

Lyman af aI. (1957)
ll,ieclesel (1957)

Sorith ancl Jetray (1958) Riec'lesel (1957) South ancl Jetray (1958) .lliedesel liieclesel Riedesel Eiedesel (1957) (1957) (1957) (1957)

lotoirrs
no change no cirange no change
incr eased.

l,ittle brom Hematocrit

bat

Senul sp. gr'.

Ilenratocli

Big brown
lt:rt

St'runr sp. gr'.

Ileclgthog

Ilernatoerit 'I'otal serurrr

ploteins

increased no changc

Biiirck et oZ. (1956) Biiirck et al. (1956')

428

BUI]I]ETIN:

N,IUSDTTM OF CONIPARATI\TE

ZOOITOGY YO]. 124

(Holg, 19;8). Adclitional information on kidney fuirction l'ould facilitate an rrnderstancling of $'ater balance during hibernation. No ruajor sliifts irr body nater cluring hibemation are apparent flom existing clata.
Other Changes in the Lrternal Environment

'l'he

sub

jects of

pII, pO2 and pCO2 of the bloocl, euergy

sollrccs, bJoorl srrgai' arrd enckrcrines liar-e been rcr,iewcd. recentl.y by Lynian and Chatfield (195' ) ancl I(ayser (1957). These clata accumulatecl on harnsters, s.ooclchucks ancl ground, stluirrels indicate that hibernating animals maintain oxygenation of the

blood,

pH and pCO2 near the values of active animals. Data on the respiratorv qlrotient ancl bloocl glucose levels indicate that fat is the priircipal sortrce of energy cluring hibernation. The role of the endocrines as a causal factor in hibernation is rluestionabkr, but charrges in endocrine actirity may effect a pre-conditioning of the animal for entrancc into hiberiration. Tlie facility of some animals to hibelnate jn the laboratory the ;'ear round conttadicts the supposition that enclocrines have a causative role in hibelrration (Rieclesel, 1957).
'I'heories on thc Der,elopment of Hibernation

The eler,ation o[ serurn ruagnesiltrn antl the le]atiorr of the iou to heat loss in othcl tl.ltes of stuclies suggest magnesium as a causal factor in the <lcvelopnent of hiberrtation. \\re have presentccl seletal theories on the clerelopment of thc
ruragnesium

l.ith refercnce to magnesium (Riedesel, 1957 ) . 'lhe "Indepenclerrt-Ttfluence'Iheor.v" implics that exposurtr to a colcl cnvirornncnt inclependentll- aiters the activltl- of thtr
state of hibernation

hypotlialaums anc'l also procluces elelatecl serurn magnesiunt. The serum rnagnesirLm ler,el has no causatir,e role in the clecreasc in bocly temperature. 'l'his theory receives suppolt from tlte eviclence that elclation of rnagnesitrn irncl lowerecl bocl1' tempera turer are separable. This las obserled during arousal frot)r 'bocl1' tet.trllelattrtre to 20'C hilrernatiorr l-ltcrr bats laisec'l tlieir rvithout lou.erinq the serum magnesium. The " I)jrect-Iirfluenc:e " theorl- simplr' rueans that co1t1 e-r. l)osrue ancl the lesriiting cooliitg of cells clirectly prochice a releasc of irragrtesittlu b1- thc rclls. antl the lesttlting eler-atc'd lcrcl oll selum trragrresiunr in{lncnccs t}re h1-pothalarnns to inclcasc' heat loss. This theory receives support frorl tl-o obsen'ations.

1960

\'IAMMAI]IAN HIBERNA'IION

429

lirst is that a high level of rnagnesiurri \r,as observed before tlte teniperatures of deep hibernation u'ere reached.. Thus, the elevatcd magnesinrn observed rvith 13"C esophageal temperature may faciiitate the development of the lorver temperatures. The second line of evidence in support of this theory is that intravenous and rnicro-injection of magnesium ion have been demonstratecl to facilitate heat loss (Schutz, 1916; Heagy and Burton, 1948 ; Hall et al., I95I). The "Additive-Influence" theory assumes that exposure to the cold and elevated. serllrn magnesium both influence the activity of the heat loss center and have an additive effect. The theory implies that cooling of tissues, endocrine and cerebral cortical activitv ancl otlier factors initiate the lorvering of bocly temperature ancl that the elevatecl serr-lnl magnesium facilitates the process by affecting the heat loss center. This theory receives support from the observation that the serllm magnesium had not increased u,hen the esophageal temperature had dropped to 17"C. This evidence inclicates that a factor other than elevated magnesiurn is requirerl for initiating the clecrease in body tempera'I'ire ture.

in arorrsal frorn hibernation. No srich stimuli have been relatecl to the clevelopment of liibernation. ,\rousal from hibernation

theory is the most acceptable in vies' of the evidence cited. EIevation of the esophageal temperature to 20"C during the arousal from hibernation rvithout reduction of the serum magnesium level represents the major eviclence that contradicts this theory. This argument is Neakened by the fact that ar,r'akening from hibernation appears to be a lerr. different process from "going into" this state. Irousal from hibernation can be initiated by discrete external stimuli, such as hanilling. Internal stimuli from thirst, hunger or a full bladder are also uncloubtedll. involvecl

The author is of the opinion that the "Additive-Tnfluence"

must be the result of neural stimulation of the hypothalamus ancl this stimulation must be strong enough to overcome the influence of magnesium on the heat loss eenter. To restate the "Aclditir.e-Influence" theory, the developmerit

activitl' produce a cooling of peripheral tissues, anil a release of nlagnesium fron-r cells to plasma occurs. This may start lvhen the animal is asleep. The increase in serurir
exposnre and reclu.cecl magnesium affects the heat loss center so that bocly temperaturc and metabolism of the animals clrop to hibernation levels.

of hibernatiorr may proceecl in thc foliorving manner :

Colcl

430

BUTTTTETIN:

IITISEIII{ o!' coMPARArrvE

zoolocY Vo]. 124

Research

Questions and Suggestions

for Future

Questions arrtl suggestions to be consiclered. when planning resealch on hibernation include the follorving:

1. ]Iore information is needecl regarding the irrterdependence of temperature, tirne ancl chemical environment in biologieal
I)rocesses.

2. ll'he ch.emical euvironment and temperature of in' uil'ro sttrtlies should be similar to those clescribed in uiuo. 3. Are changes in intracellular electrolyte concentrations a universal response of cells to cooling? 4. Iilclitional information is neecled. on 'water balance during

hibernation; for instauce, "\Vhat is the extent of the kidnel' activit.y cluring hibernatiorr ? " 5. Additional information is neecled regarcling the possible clclic changes in serutn calcium concentration during hibernatiou. 6. \Ve need a bettel clefinition of hibernation in terms of spt'cies iliffereuces aird stages of hibernation.
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Aunv,
C.

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norrnaltr untl pathologisclrel

PhysioJogie, l7 : 105-133.

18?5. Tleber tlel Ejnfluss

Pharmakol.,
An()r,PH,

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E. F.

,t.ND

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1960

MAMMATJTAN

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pa.ris,

l-nnw, W. O. auo T. Asano

1956. Effects of carbon dioxicle inhalation on potassium liberatior from the liver. Am. J. l,hysiol., lB5: i67-576.
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Il.rlr,, V. ll., R,. GR,\NII,r.lrl \\r. J. \Vrrrlltx 1951. 'I'he influerrce of l{g arrcl p].rogens on teniperature r.egulation. AF Tech. Rt'por't No. 6682 (Wright Air Developrnent Center). Iir.rcv, ]'. (,'. ,rNn A. C. Bunrox 1948. Hffert of IV injectiol of MgCl2 on the borlv tenperatur.e of the unanesthctizccl ilog, rvith some oLrselvations on X{g levels ancl
hoclr'tentperattle in man. Arr. J. Ph;,si0l., 152:407-416.
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Ii.rvsrn, C. 1957. Le somuteil hirelrral

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Lvrrlx,

C. J). ,rnl P. O. Cn.r.rprnr,l 19J5. Pliysiolog;' of hibernation ir mrtrnnal-s. Physiol. Rer., 125.

OS:403-

Lr:-u.r-r. C. P.,

L. P. \Vrirss, R. C. O,BnrtN -LNo A. A. Bannn,tu l95i. The effect of hiliernation on the replacenent of bloocl in golilen hanrster.. J: Erp. Zoo1., lS6:421-486.
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the

llcBrnxrn, J. !1., F. G. Ptrnsox,

W. G. BrGELorv
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19;3. Physiological stutl.ies of the

J. \Iecl. Sci., 3l:421-430. Pl-rtNnn, W. S. 19J0. Effects of lorv ternperature
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groundho

g (.Marmota

,tnonar).

ol l1g content of btood, body fluicts of golclfish ancl turtle. AnL. J. Physiol., 161:39g-40b.

432

BUr,rrETrN: MUSEUIT oF coMpARATrvE zoorrocy Vol. 124

Pr,-a.rNnn,'W. S. ,LNo tr,I. J. HosKo

1953. I'Iobility of serurn magnesium in hypothermia. Am. J. Physiol.,

174:273-276.

R-+suussnr, A. '1. 1916. The corpuscles, hemoglobin content and specifie gravity of the blootl during hiberna,tion in the wooclchtck (Marmota monan), Am. J. Physiol., 4l:464-482.
Rrnonsnr,, trf. L.

1957. Serum nagnesiurn levels i.n mammalian hibernation. Trans.

Kansas Acacl. Sci., 60 :99-141. Rrornsnr,, XI .L. rxp G. E. For,ri, Jn. 19J7. Ser,rm nragnesiurn changes mal., 38 :123-421.
92 :307-312.

in

cold-exposetl mammals.

J.

Mant-

1958. Serum electrolyte levels in hibelnating mammals. Amer. Nat.,

Scnurz, J.
'1

91(i. Zul Kelntnis cler Wirliung tles \Iagnesium auf die Korperternperatur. Arch. e-xp. Pathol. Pharmakol., 79:285-290.

Sor,r,rrr-r.x, T.

1957. A manual ot' phalruacology. Philadelphin, 1535 pp. (Pp.

1062).
Sou'r'u, F. E. .,lxn H.
Soc.

1057-

Jnrr.rv
98 :885-887.

1958. Alterations in serum proteins of hibernating hamsters. Proc.

Exp. Bio1. Ilecl.,

Srlcron, W.

S,

1.956. Hanclbook of biological clata,. Philaclelphia ancl Lontlon, 584 pp. (Pp.28-29).

Srnlorr-lx, L. '1., I. Anrnr, ,l,xl

S.

1943.

Stuclies on the effect

L. \Y.qnrrlN of hypothermia. I\-. The lise of serum llg

in ral:rbits iluring the hypothermic states as sholvn by the spectrochemictrl methocl, Calcer Res., 3:477'174.
St'r.rcr<nt, J. ,r.No R.

II. Coco 194:. A comparisol of the blootl pictures of active ancl hibernating ground sqnirrels. Am. J. Physiol., 137:437-435.
1939. Hibelnation of tlie lietlgehog VI. Selunr Iilg antl Ca. Artilieial hibellatiou. AIso a contribution to chemical physiology of
diur'nal s1eep. Anu. Acatl. Sci. Fenn.
63 :131-144.

uolr,r.r,'lrNnN, P,

(A) 53(7):1-7f.

19riil. llibelnation of the hetlgeltog. I'roc. Finn. Acacl. Sci. Lettels,

1960

I{AMMAI]IAN I-IIBERNATION

433

Svrnl,t, A. ,tNo I{. C. Bowrraw

1

!i5 3.

Stimuli rricl theil cffects on arvakening scluirrels. Am. J. Physiol., 172:681-683.

of clormarrt

grouncl

Zrrrxr-,

lI.
l{etabolisrn of some calbohyalrate and phosphate compounals tluring hibernation in the ground squirrel. J. Oell. Comp.
I'h1 siol., 48 :371

l95ti.

-39j.

DISOI]SSION I'OI,IIIO\VING RIEDESEI,/'S PAPER

ther evidence for cyclirrg of hiirerutrtion. In visiting bat caves et'ell tu,o \\reelis (huing thlee rvinters he observecl that tlie clnsters of bats tnovetl, and bauding stuclies s]rorvecl rnovements of aninals betu'een ca\-es in the miclclle of l'inter. Even in an artificial hibernacnlrrrrr thc.re ale tiiiles \\.hen bats are active in the liiberrrating seasrirr. ltlEDESEL thought this rvas true, arrd he felt that the cJ'cle naJ' partly leflect tetlperature changes. With respect to moveurents of bats in caves. IiOI:K (G. Il. tr'olh, J. n'Iammai., 2l:306, 1940) rvas citecl as having reportecl changes in positions of bats in u'inter. cluite a bit of movement being
characteristic.

WIMSATT observecl that RIEDESELT'S serum measurements colrl:l l'eflect cliscontirlrit). in hiLrelnatiot, aucl luight also lrrovide cvidence for arousal lf so, one nlaJi be able to malripulate mechanisms in such a way as to eliminate arousal. lle also gal'e fur-

,\DOLPH therr asked if SIIOM,\LAINEN \vouicl give his prescnt vierv of tlic rolc of niagnesium in hibernation. SOIITH also nslied if SIjO,\IAL,\INEN hekl to hjs olcl f is11'point. SI.|OX{AL;\INEN rernarliec'l that it is a cliflicult question, but that he l'as srue rnagnesium is a typical irr<licator of the hibernating state, rvhether ir-r a priman- ol seconrlar1- role he coulcl not sa)'.

RIEDESEL remarlied that the data cannot be interpreted leadily to rnean tliat magnesium is a factor in initiating hibernation, antl that he clicl not intelrrl to leale the impression that rnaguesirrrn initiates hibernatioir.
I'OPOVIC stated tha1. he felt bats rvere not \yell-chosen anirnals 1ol this u-orli since the.r. cliffer considerabl.y from grouncl squirl'els ancl other liiireniators. A hibernating grouncl squirrel and au rirtificrialll' cooled ground squirrel \youlcl probabll' shola big ph1-siolosical clifference in respect to magnesium, in contrast to bats. Other striliing' contrasts are seen; for example, the

+:14

BuLLETTN: rrusEUM op cor{l'ARATrvIt

zoorrocy Vol.

124

bloo<l pressure is lorv in hibernation, n'hereas in the artificially cooled animal, it is 90 mm I{g. IJeat procluction is 5 to 15 times higher in cooled than in hibernating animals. Ife believecl that further experiments shoulcl be performed to see if the changes in rnagnesium should be attributed to hypothermia or to hiberna-

tion. rl.hether the bat is a good example of a hibernator. " I{e defendctl the bat as a hibernator, saying that he had spent 10-11 hours in a colcl rooir lvaiting for bats to go into hibernation to rnake study possible. IIc checlied each one inclividually everl' l5 minutes. 'lhey rernained relatively active ancl kept their bocly temperature tp. lle checkecl bodl' temperature until it lorvered to 20'C, therr dreu' biood ancl analyzecl it. Sometimes bodl temperatnle rose 7-8"C in 15 rninutes, but half an hour Iater it woukl ire clol'n again. Concerning changes in body temperatule and rnagrt'siurrr, hc belieles that on the cellular level hypothermia ancl hibernation are quite similar. With respect to the u,hole grouncl stluir:rel put into liypothennia, he felt that cliff

RIEDESITIT lr:plied that he hatl "heard rumbiings as to

elences

trt s.vstrrur, orgall olr tissue levels, but not at the cellular level.

onlcl exist lretrveen this corrdition anrl hibernatiotr

St-lI{ONi},\Lill saicL that ar inclcase in magnesium in the hibelnator's bloocl hatl to come from sorlex'herc ; dicl RIEDESEII haver anJ- itletr as to l'hich part of the organism gave up magrresilrn lirsl. --- l1e6l1- ficsslss generally or specific organs, such as rnuscle ? IIe also rvonderecl l'hat happens to the magnesium rr'hich iras entered tire semn. RIEDESEI- said that he had. no evitlelce on this, but his implession I'as that temperature afiects

the extracellular:intracellular rnagnesitlm ratio rvhich at 37'C is 20:l. ,\s perillheral cells (skin anil n.ruscle) are cooled. this ratio becornes smaller aircl the sertlln magnesium level increases. Ife belieles that the first release of magnesium into the serum occrlr's iu the peripheral tissues l'hele the temperature is lotl'el. In nature. bats in the temlterate zone go in and out of hibernation at least once a claf ilr the spring ancl fall, and since there is no eliclerrce cif ruagnesirtin clcficietrcl'. it is doulttful that extraordinary' amounts of trtagrresitull are excretetl in the uriue. I{e
believes magnesium does not leave the body during hibernation. but returns flon lrlasna to cells on arousal from hil-rernation.

T(AYSER then stated that he believes there is a clear relationship betrveen magnesium levels ancl liypothermia. Otte sees an

960

trT

AMMAI]IAN I]IB]trIiNATION

435

in hypothermia. ilelieves magnesiurn increase irr the serum is related to (is perhaps the corrsec3rence of) hypotherrnia. He said he rvas not convincerl that magnesium hacl a causal effect on hibernation, but rather beiieved that elevatecl serum magnesium was a con-

rncrease of serum rnagnesium in hibernation ancl

IIe

sequence
F

of cold.

OLK remarked that he felt the discussion was difficult benot time enough to go into methods. Relative to WINISATT'S and POPOVIC'S comments, he said it should lle emphasized that lneasurements u'ere rnaile after sacrifieing animals in spontaneous hibernation.
cause there was

}}ARTFIOI,/OME W, t-'xtenclin g I(AYSEIi,'S remarlis, pointed out that hibernation-h;'pothermia discussions are impecled b-v the chlonic problem of causation and correlation. FIe rvoulcl like to separate hypotherrnia and iribemation. By experience with a variety' of forms, he hacl noted tliat hypothermia, per se, is not tin cssential causal factor for hibernation. Ife felt that peri-

pheral cooling is a result rather than a cause. He asked that

release ourselves

rve

from dependencl- or1 the iclea that colcl exposlrre is a necessary prior condition to entering liibernation.

RIIIDESEIT state<l tirat it is difllcult to designate magnesiunr as a causati'r'e factor in initiating hibernation. IIowever, it appears logical that the elevated serum rnagnesium (by iis effect on the heat loss center) facilitates loss of bocl1' heat ancl the recluction of bodl- lgltt.tattrr:e to ler-els characteristic of deep hibernation.