Cold acclimation in arctic lemmings

/.'otrIp. tlloch~'wl. PJI~ <l~,t.. Iq*?6. I ol. 5-1A. pp 175 to 178. Per,I,I.p,J. l~r~.ss. P*'itil4"d i~l (Jretll Jlrltoill C O L D A C C L I M A T I O N IN A R C T I C L E M M I N G S J. J. BERB.ERtCH A N D G. E. FOLK, JR. Department of Physiology and Biophysic~ University of Iowa, Iowa City, IA 52242, U.S.A. (Receired 19 Au~lust 1975) Abstraet-~l. The lemmings, Arctic rodents, show cold acclimation as measured by a number of variables: food and water consumption, liver temperature, and organ weights. 2. Cold acclimation of lemmings is apparently more rapid than that of temperate mammals. 3. The rapid cold acclimation in lemmings supports the hypothesis that compens.'ltion of a number of physiological variables is essentially complete within the tirst week of cold exposure as opposed to requiring months. INTRODUCT|ON Initial physiological responses to cold and cold acclimation have been studied extensively in temperate mammals, notably the white rat and hamster (H6roux, 1961). Arctic mammals, however, m a y serve as better models of cold acclimation since they naturally experience lower temperatures. T h e opportunity was afforded to investigate at the N a v a l Arctic Research Laboratory, Barrow, Alaska, the cold acclimation of two' species of Arctic rodents: the brown lemming, Lentmzt.s trimztc'ronatzts, and the varying lemming, Dicrostotu'_x .qroettlatzdicux. These two species are the most northerly distributed N o r t h American small m a m m a l s and are unique in being endemic to the Arctic as genera (Schwartz, 1962). This report presents data of some basic physiological indices o f cold acclimation in the lemmings which may be c o m pared readily to those of temperate mammals. MATERIALS AND 51ETHODS Lemmings, wild-caught or laboratory-bred, were maintained in an animal colony for at least 2 months prior to investigation at thermoneutral temperature (18°C) on a summer photoperiod (22L:2D) and fed carrot and rat chow (Purina). Carrot was used as the primary food source and the water source since lemmings ingest wet food in the wild and prefer it over liquid water. Subsequently, animals were exposed either progressively to cold (3+_2':C) for l. 3, 6, 9, 15 or 30 days prior to sacrifice or to thermoneutral temperature (18 _.+ 2°C) as controls. All experimental animals were housed in open, wire-mesh metabolism cages under summer photoperiod at 1.0 Ix and fed carrot and rat chow. Animals were sacrificed by decapitation and the following physiological indices were measured: liver temperature and wet and dry organ weights of ventricles, lung, liver, spleen, left kidney, adrenal glands, gonads, right gastrocnemius and abdominal skin sample. Body weight and carrot consumption were measured. Carrot consumption was calculated as water consumption and dry food consumption; little or no rat chow was eaten. Data were analyzed by analysis Of variance for species, sex, temperature, and day of temperature effects. RESULTS T w o simple questions were asked: D o Arctic lemmings show cold acclimation as measured by a number of variables? If so, h o w does lemming cold acclima175 lion c o m p a r e to that of temperate m a m m a l s as to extent and time course? When exposed to cold, the brown lemming finds itself in a negative energy balance and loses weight (Table 1). Although the loss of weight had suggestively stabilized by day 10 of cold exposure, the drop in weight of day 30 animals makes the acclimation of the brown lemming as measured by body weight problematic. In contrast, the varying lemming was able to maintain weight with prolonged cold exposure, at least through day 14 (Table 1). Thus, any changes observed in other parameters for the varying lemming can be directly attributed to the effects of cold. Indirect effects due to negative energy balance would be minimal and difficulty in normalizing data to body weight is also reduced. Increased food and water consumption o f both lemming species correspond to the typical response of other m a m m a l s upon cold exposure (Table 2). In the case of the lemmings, however, one thing was different: the lemmings were consuming wet food. even though dry food was always present. U p o n initial exposure to cold, body temperature of both lemming species dropped slightly, but significantly (P < 0.01) (Fig. I). Presumably this drop resulted because temporarily increased metabolism could not overcome increased heat loss in the cold. Table l. Body weight BI~OWN ~ I N G DAyS o f qol.dl ~ x p o s u ~ e 3 4 3 6 7 8 9 10 11 12 13 14 30 N VAK¥1~G X ~ 3? 29 28 -0.7 -1.6 -2.7 + 0.8 4- 1 . 0 4- 1.,6 32 29 31 31 2,5 J.5 24 18 12 12 9 -3.7 -7.1 -4.9 -4,2 -2.7 -5.9 -9.4 -5.0 -5.5 -5.1 + "+ ~ '~ ~ ~ ~ + ~ ~ 17 16 17 16 16 23 16 12 12 7 7 7 7 7 1.2 1.4 1.5 1...~ 2.2 3.1 2.0 2.9 2.3 2.4 -15.7 ~ 3.2 ~ G :t -2.0 ~ 1.2 0.0 + 1.8 - 1 . 3 -,t,. 1 . 1 +0.7 + 1.6 -0.5 ÷ 1.8 +1.6 ~ I.B +Z.O ~ 1 . 9 +2,1 + 2.5 4 0 . 7 "~ 2 , 2 "tO.2 ~ 3 ° 6 +1.0 + 3.7 -1.1 ~ 4.5 + 0 . 4 ~ ,~.2 - 0 . 7 4- 4 . 9 Body weight changes for prolonged cold-exposed (3°C) brown and varying lemmings are listed. Values listed represent data from male animals; however; females showed the same results. Values are per cent change from control body weight and are mean _+ S.E.M. 176 J. J. Table D4yl cold VBYIW~ 12FIHING Natal Intake (~,1 I O O A ' I ) Food ..........Water t~tekm Intake (1~ 100~-1) ( m l 1001~'1} ~'.3 ~ ),2 10.9 ~ 1.0 1 111.1 + 10,0 lJ,? 2 1 4 101,9 ~_ 7,7 t 1 5 . 9 '~ ~,4 l ] 3 . b ~ 6,1 l ~ l , O 4- 8,1 126.1 i" 6 , 2 1~7,3 i 5,g 137,7 7~ 5 . ; 142.7 ~ $ . 9 115,0 "#" 4 , l 153,5 ~ 3 . 2 151.1 '~ 6,] I / ~ * , } ~ 5,~1 162.~ ~ 6 . 7 ÷ 1,2 111,2 t11,9 ll],& 118,? * ~ T ~ 8.2 11.~" 11.1 9,0 * I.O ~ 0.7 ;/: 0,7 ~ 0.7 121.2 ~ 7,1~ 121.I lOl,Z 107,8 IO~,2 111,1 llg0] t ~ ¥ $ ~ ~ 9.A 6,Z 8.6 S.3 8.0 8,¢Q 6 I IO 11 t2 1J 14 |'. l-()i.t.:,, JI,t. Organ Wet Weights 11,0 11,5 16.$ 16,1 I$,6 18,1 17,0 17.6 l&,l 18,g 19.1 20.0 20.0 ,,7 0.9 ~ O,II ~0,8 + g ~ + ~ ~ O.; 0.6 O,,; O*} 0.7 O,B 85.5 ~ 6.6 l ] & , 2 ~" 8.b 120,0 ~" ?,0 111.g ~ 8 . 2 Brown Lemmings N=11-26 IgI'~|NG Control $ G. 2, F()()d alld water Clm~,ttmplion I1~ of I],l U i l i i R l t ' t l . ~ N I ) Food Intake (R tOOK° l ) 11,6 Varying Lemmings N • 8-14 HEART 6' 4" 0 , 9 1'~,1 + l , O 1~.8 ~" l , k IA,O +--"! , 6 14,6 ~ 1,1 1 1 . 1 ÷ 1,0 1 5 . 0 *" 1,2 lZ,8 ~ 0,8 13.6 ~ 1.o 11.; ~ 0.7 11,~ ~ 1,0 It,.9 ~ 1-0 16,4 + 1,1 14.6 ~ 1,0 14.~ { 0.9 ~'5 KIDNEY ] C a r r o t consumption is calculated as daily water con- sumplinn and dry food consumptinn for control 118 C) and prolonged eold-expo~d (3'C} brown anti varying lemmings. Values from one expcrimcn| are used to illusIrate dat~, ([]rOwll, n = 9: varying, n = 10f Values are 7 t~conr,,ol 6t b, 5 E mean ± S.E.M. However, the brown lemming regulated body temperature at a new level, lower than control, by day 6. Varying lemming body temperature had retunlcd to control at day 9; the decrease on day 15 can be altribuled to experimental artifact since day 15 animals were sacrificed at a different time from other varying lemmings. In resptmsc to the challenge of cold and the conseqtlenl incrensed metabolic tlenl;Hlds, heart and kidney of both lemming species hyl~crtrophicd a t ' < OAK)I) (Fig, 2), Liver laypertrophy ,vas also found lot the brown lemming (P < 0.001) {Fig. 3); Ihilurc of lhe vurying lemming liver to hypertrophy was atypical for cold-exposed nmmmuls. T h e weights o f other organs measured showed either no systematic change with cold exposure or more usually no change fl'om control. T h e differences in organ wet weights were not due to increased water content of these organs, as water content did not change with cold exposure, Lack of change of water content may be illustrated Brown Lemmings N- tl-26 Varying Lemmings N " 8-14 LIVER TEMPERATURE 39.0- ::~'~'Confrot 5 o to ]5 30 6 -g to ~5 ~o O~ysof Cold Exposure Fig. 2. Hearl and kidney wet weights. Wet weights of heart (ventricle) and left kidney arc illustrated for control ( l g U ) alnd prhmged cold-expo,~ed 13 CI hrnwn (@) and varying 10) lenunmgs. Organ ~vcl weights lexpresscd in rag) are normalized to g body wt ig). Values are mean ± S.E.M. by c o m p a r i s o n of control and 9-day cold-exposed lemmings I Fig. 4). Difl~,'ences in organ wet weights were f a t e d between the sexes, the female usually having heavier organ weights. Sex differences (P < O,(R)I ) were found for liver, heart, kidney, adrenal glands, spleen and gastrocncmius, These ditlkrcnces are illustrated for spleen, gastrooaemius, and kidney (Fig. 5). Organ Wet Weights Brown Lemmings N ~il-zs LIVER Varying Lemmings N = e- 14 SE 58,5' P 50~ / - I ~ ; P I 38 o, 0 0 5 I0 15 30 0 5 Days of Cold Exposure 10 15 30 Fig. 1. Liver temperature. Liver body temperature is illustrated for control (i 8 "C) and prolonged cold-exposed (3°C) brown (e) and varying (O) lemmings. Values are m e a n ± S.E.M. 5 I0 15 30 0 5 Daysof ColdExF~sure EO 15 30 Fig. 3. Liver wet weight. Wet weighl of liver is illustrated for control (18~C) and prolonged cold-exposed 13°C) brown (e) and varying (O) lemmings. Organ wet weight (expressed in rag) is normalized to g body wt (g). Values are mean ± S.E.M. Cold ;icclinmliori in Arctic Icnlmings Organ Water Content Voz¥ing Lemmings Brown Lemmings "resles Spleen Lung Kidney Heorl Gasiro¢. Uterus LNer Skin %H20 Fig, 4. Orgart water cotltellt. |:}el"cent water ill niu¢ orgallS is illustrated for control (18 C} and day 9 cold-exposed (3 C} brown and varying lemmings. Values are meatl ± S.iZ,.M. I)IS('US,SlON This study was designed to ascertain whether o r not Arctic rodent.,;, when exposcd to the environmental challenge of cold, d e m o n s t r a t e cold acclimation and, if so, whether acchmation occurs at the same rate ;rod extent as literature values for temperate mammals. Body weight has been a valuable indicator of cold acclimation [HOroux, 1961:. Barnett & Mount, 1967). Essentially adult small manlmals that are acclimated to cold lose weight initially and after some period OrcJan Wet Weights Brown Lemmings GASTROCNEMIUS 1,01 ~ 0 5 Vorying Lemmings ? IO 15 30 Dey.~of Cold EXlDOSUre I~, ,; % Fig. 5. Sex effect on organ wet weights. Wet weights are illustrated for right gastrocnemius muscle, spleen, and left kidney for control (18°C) and prolonged cold-exposed 13"C) male ( - - t - - ) and female ( - - I t - - ) brown, and male 1---O--) and female ( - - O - - ) varying lemmings. Organ wet weights (expressed in rag) are normalized to g body wt (g). Values are mean _ S.E.M. 177 of t o l d c×posurc, loss of wcight ceases and body weight cither remains at this stabilized level o r returns to control level. Evidence of cold acclimation by day 7 of cold exposure as measured by body weight has been rcportcd for the hamster (Farrand, 1959; I:'eist, 1972: Minor, 1973). Similar results have been reporled for the rabbit (H6roux, 1967) and while rat (Baker & Sellers, 1957; Schonbaum, 1960; Fregly & Tyler, 1972). However, other resulls d e m o n s t r a t e a much longer acclimation period when body weight is the measure (Ht3rotlx, 1961; Chaffer et at., 1963; .Chaffer et M.. 1969; Lynch, 1972). The results of this study cannot be clarilied for the brown lemming since the body weight of the day 30 animals had not certainly stabilized. The maintenance of body weight o f the varying lcmming with prolonged exposure to temperatures just a b o v e freezing is u!lique a m o n g small mammals. Stabilization of food c o n s u m p t i o n has also been reported by day 7 for the rabbit (}ltTroux, 1967), hamster (Farrand, 1959: Minor, 1973), rat (Fregly, 1968: Frcgly & Tyler, 1972) and mice (H6roux, 1961). However, only after 10 weeks was there evidence o f c o m plete levelling off of food constimption in the rat (Mefl~rd et al., 1958) and Perom)'scus (Lynch, 1972). F o o d c o n s u m p t i o n apparently had levelled off for the brown and wtrying lemming by days 10 and 4, respectively, supporting significant physiological adjustc e n t to cold in the initial few days. W h e t h e r or not body temperature change can be used as an indicator of cold acclimation is uncertain (Hart, 1971). In the hamster, for example, no change in body temperature was reported, although cold acclimation was indicated by changes in other variables (Farrand, 1959}. However, rabbit (H&oux, 1967) and rat (Leduc, 1961) b o d y temperatures had stabilized by days 14 and 18, respectively. In contrast, brown lemming body temperature in this sludy acclimated by d a y 6. C o m p e n s a t o r y tissue change measured as change in gross organ weight often has been used as an index of cold acclimation. Admittedly, such measurement :,uffers from the assumption that the observed hypertrophy is due to increase in the mass of functional as o p p o s e d to non-functional tissue. H y p e r t r o p h y of liver, kidney and heart has been reported for temperate rodents with prolonged cold exposure. Reports of acclimation range from 8 days (Farrand, 1959: Minor, 1973) up to 60 days (Chaffee et al., 1969) in the hamster and from 15 days (Emery et aL, 1940) up to 3 - 6 m o n t h s (Chaffee et at., 1969) in the rat. In contrast, changes in relative organ weights were stabilized after only 3 d a y s in the lemmings. Thus, this study would support the hypothesis that a n u m b e r of significant physiological variables for Arctic rodents indicate cold acclimation after only a short period of cold exposure as has been indicated for the h a m s t e r {Minor, 1973). The extent of change {per cent) of cold-exposed lemmings in this study has not been dissimilar to the changes found in temperate mammals. In this respect, the study has brought forth m o r e similarities than differences between cold acclim a t i o n of Arctic r o d e n t s and temperate rodents. Differences in the rate o f cold acclimation o f the Arctic rodents, however, seem to be supported by the shortened time course o f organ h y p e r t r o p h y a n d liver 178 J. J. BERBERICHAND G. E. Fc)~ :, JR. FARRANt) R. L. (1959) Cold acclimatization in the golden hamster. StutL nat. Hist. Iowa Univ. 22, 3-29. FEIST D. D. (1972) Effects of cold exposure on urinary and adrenal catecholamines ill a hibernator, the golden hamster. Comp. Biochem. PhysioL 42A, 833-840. FREC;LV M. J. (1968) Water and electrolyte exchange in Acknowledgements--This work was sul~ported by The rats exposed to cold. Can. d. PhysioL Pharmac. 46, Arctic Institute of North America with approval and finan873-881. cial support of the Office of Naval Research under contract FREGLY M. J. & TYLER P. E. (1972) Renal responses of number N00014-72-A-0375-0002 (subcontract ONR-453), cold-exposed rats to Pitressin and dehydration. Am. j. and the National Science Foundation. 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Biol. 28, 1029-1034. SCHOSaAUM E. (1960) Adrenocortical function in rats EMERY F. E.. EMERY L. M. & SCtlWAaE E. L. lt940) The exposed to low environmental temperatures. Fethl Proc. effect of prolonged exposure to low temperature on the Fetha Am. Sots exp. Biol. 19, 85--88. hod.~ growth and on the weight of organs in the albino SC-71WARI~ZS. S. (1962) Problems of the North, translated titl. Growth 4, 17-32. by National Research Council, Ottawa 4, 75. temperature acclimation of the lemmings. At any rate, that cold acclimation occurs for Arctic rodents as well as for temperate rodents is clearly indicated by the data presented here,