Hibernation patterns and energy expenditure in ... - Springer Link

J o u m a l of

Comparative

J Comp Physiol B (1984) 155:117 123

Systemic, Biochemical, and Environ-

Physiology B me.,., Physiology 9 Springer-Verlag 1984

Hibernation patterns and energy expenditure in hedgehogs from semi-arid and temperate habitats Razi Dmi'el and Miriam Schwarz Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel Accepted April 3, 1984

Summary. Hibernation patterns, body temperature (Tb) and oxygen consumption 0?o2) were measured during hibernation in two hedgehog species, a desert species Hemiechinus auritus (body mass 367 g) and a temperate habitat species Erinaceus europaeus (body mass 598 g). A continuous ambient temperature of 11 ~ was the only necessary condition for both species to enter hibernation outdoors and in the laboratory. At this temperature, hibernation could be induced at any time of the year. Hibernation bouts of Hemiechinus were regular and short (average 4.8 days), whereas those of Erinaceus lasted 5 to 27 days (average 9.3 days). The frequency of spontaneous arousals was 5.3 and 2.9 per month for Hemiechinus and Erinaceus, respectively. None of the hedgehogs took any food during arousal periods. Both species had the same Tb during hibernation (12.5 ~ and during arousal (33 ~ Vo2 of the hibernating Hemiechinus was twice the rate of Erinaceus (0.050 vs. 0.025 ml g- 1 h-1), but during arousal it was the same for both. The monthly average energy expenditure for both species was 1,477 kJ per animal, which is 15% of the energy used by non-hibernating hedgehogs. The corresponding amount of fat catabolized was 37 g per month. This mass loss would limit the hibernation in Hemiechinus to 3.9 months and in Erinaceus to 6.5 months. Although hibernation in Hemiechinus does not constitute a special adaptation to hot environments, it significantly improves the hedgehog's energy economy during the desert winter.

Introduction Hibernation is considered to be an adaptive mechanism which enables homeothermic animals to

overcome unfavorable environmental conditions especially like those prevailing in the cold winter, when energy demands for thermoregulation are high but food availability is at a minimum. In mammals, hibernation occurs primarily in various species of rodents, bats, and insectivors (Kayser 1961 ; Lyman et al. 1982). Three species of hedgehogs (Insectivora, Erinaceidea), each inhabiting a different climatic region, are common in Israel (Bodenheimer 1935; Harrison 1964). Erinaceus europaeus Linnaeus 1758, the European hedgehog, is abundant in the mesic northern part of the country. Hemiechinus auritus Gmelin 1770, the long-eared hedgehog, inhabits arid and semi-arid areas on the verge of the desert, and penetrates to the coastal plain, a region in which Erinaceus is also very common. Paraechinus aethiopicus Ehrenberg 1833, the Ethiopian hedgehog, inhabits the extreme arid terrain of the Negev Desert. In Israel all three species are nocturnal and their activity season lasts from early April to the end of November. During the rather short winter (December-March) they disappear. This phenomenon is well known among local naturalists. Yet, it has not been established whether the hedgehogs enter a state of hibernatiop or merely reduce markedly their activity level during the winter months. A1-Bardy and Taha (1982, 1983) have studied the biochemical changes occurring in artificially hibernating Hemiechinus from Egypt. However, systematic data on the hibernation pattern and energy expenditure of this species have not been published. Erinaceus from Northern Europe is a typical deep hibernator (Kristoffersson and Soivio 1964b; Soivio et al. 1968; T/ihti 1978). Yet, no information has been published on the ability of this hedgehog to hibernate in the most southern region of the species' geographic distribution, where the winter is much milder and warmer.

118

R. Dmi'el and M. Schwarz: Hibernation patterns in hedgehogs

The comparative studies on the physiology of the hedgehogs of Israel (Yaakobi and Shkolnik 1974; Shkolnik and Schmidt-Nielsen 1976) have dealt only with euthermic, non-hibernating specimens. The aims of the present study were: (1)to find out whether and under which conditions the local hedgehogs enter the state of hibernation, and (2) to compare the hibernation patterns of two species in relation to their different habitats.

tures of known proportions of either air/N z or air/CO r The experimental error was +_2.5% of the measured value.

Materials and methods Animals. A total of 30 Hemiechinus (mean body mass 367 g + 73 g S.D., range 230-510 g) and 29 Erinaceus (mean body mass 598 g _ 110, range 400-800 g) were used in this study. 17 Hemiechinus and 18 Erinaceus were captured in their natural environments during the nights of June 1981. The others were captured previously and had been kept in captivity for 3-5 years. The animals were housed in individual cages and the floor of each cage was covered with a layer of sand and sawdust. Drinking water and a mixed diet of fly larvae, chopped meat, eggs, baby milk powder, fruits and vegetables was available ad libitum.

Experimental design. Two sets of experiments were designed. In the first one the animals of both species were divided into three groups (Table 1). Hedgehogs of the first group were maintained outdoors for two years (two summers and two winters). Their cages were protected from strong wind, rain and direct sun, but otherwise they were exposed to the natural climatic variations typical of that area. Two groups were kept indoors for up to 5 months at constant ambient temperatures: 27 +_ 1 ~ and 11+_1 ~ Light regimes, 8L: 16D, and relative humidity, 70-80%, were the same for both groups (" winter conditions"). The floors of the cages of the cold environment group was made of wire net through which the urine was collected continuously. In mid-November half the number of each of the three groups were deprived of food (but not water) for 3M weeks. The cages were inspected daily and the date of hibernation commencement, the number of spontaneous arousals (as was indicated by urination, Pengelley and Fisher 1961) and the length of the hibernation period were obtained for each specimen. The second set of experiments was aimed at measuring body temperatures and metabolic rates of hedgehogs during the various phases of their hibernation. These experiments were performed on animals which were kept for at least 1 month in the cold environment (12 specimens for each species).

Measurements. Body temperature was measured and recorded by copper-constantan thermocouples made from 40 gauge wire which were connected to a Leeds and Northrup recording potentiometer (Speedomax W). The thermocouples were implanted subcutaneously into the back of the dormant animal. The implantation site was locally anesthetized by ethyl chloride. Metabolic rates were determined by measuring O z consumption and CO z production. The animal's metabolic chamber, a 20 x 20 x 20 cm glass container, was placed inside a temperature controlled (+0.5 ~ cabinet. Air was pumped through the chamber at rates of 200-4,000 ml rain- 1 (sTpn). Oxygen and CO 2 concentrations in the air leaving the chamber were measured with a Beckman paramagnetic O2 analyzer (model G-2, range 20-21% 02) and with a Beckman infrared CO2 analyzer (model IR 215). During each experiment the system was checked regularly by bleeding into the metabolic chamber mix-

Procedure. After the individual rhythm of the hibernating hedgehogs had been ascertained, each specimen was taken from the cold room and weighed to the nearest gram. The spines of a small area on the animal's back were cut, the naked area was sprayed with ethyl chloride, and a syringe needle was inserted to a depth of about 2 cm through the subcutaneous layer of fat and muscles. The thermocouples were implanted through the needle, and, after removing the needle, they were stitched to the skin. During this treatment none of the hedgehogs awoke from its torpor state. The animal was then placed onto a metal mesh above a layer of paraffin oil inside the metabolic chamber. The hedgehogs stayed in the metabolic chambers from 1 to 4 months at an ambient temperature of 11 +_ 1 ~ All measurements were made simultaneously and continuously throughout periods that varied from 36 h to more than 10 days. Calculations. Values of 1)'o2 were corrected to STPD conditions after corrections were made for the difference in volumes of 02 consumed and CO2 produced. The expected metabolic rate of hedgehogs hibernating at a T b of 10 ~ was calculated from Kayser's (1964) empirical equation: H P = 2.09 mb 0"69

(J)

where HP is heat production (kcal 24 h -1) and M b is body mass (kg). The thermal conductance of hedgehogs in a steady state (hibernation and euthermia) was calculated from the equation: C-

HP (Tb-- T,) A

(2)

where C is thermal conductance (W cm -z ~ HP is heat production (Watts) ; T b and T, are body and ambient temperatures (~ respectively; A is the hedgehog's body surface (era2). The latter was calculated from the body mass of the animal (Mb, g), using the relationship: A = 10 Mb ~ (Shkolnik and Schmidt-Nielsen 1976). For the non steady-state phases (arousal and hibernation re-entrance) the conductance was calculated from the slope of the curves describing the changes in Tb and 1?o2 during these phases. For energy equivalents we used 4.1868 Joules per calorie and, unless specified otherwise, 19.845 J (=4.74 cal) per ml O z. The significance of differences between mean values was checked by Student's t-test.

Terminology. In the present work the terms hibernation and euthermia describe the two distinct physiological phases of the hibernating hedgehogs (Lyman et al. 1982). However, for the purpose of energy budget calculations we refer to the period in between hibernation bouts as the awakening period. This period includes the phases of arousal (in its strict sense), euthermia and hibernation re-entrance. For the same reason we use the term hibernation cycle to denote the period consisting of a single hibernation bout plus awakening.

Results Onset of hibernation The results of the different experimental groups a r e s u m m a r i z e d i n T a b l e 1. F r o m m i d - O c t o b e r u p to mid-December, when the minimum air temperature was 14-t-3 ~ (10-18 ~ none of the outdoor

R. Dmi'el and M. Schwarz: H i b e r n a t i o n patterns in hedgehogs

119 ,

Table 1. Onset o f hibernation in hedgehogs kept at various envir o n m e n t a l conditions ( n u m b e r o f animals in parentheses). H, Hemiechinus ; E, Erinaceus ; +, hedgehogs entered hibernation; - , no hibernation. Values for the o u t d o o r T~'s are the m e a n minima and range Month

Ta

(oc)

Feeding

,

,

,

,

22

,

,

r

I

,

I

,

,

,

r

,

|

,

,

,

,

I

E # 10

20 18 16 14

F o o d deprived

~, 12 H

E

H

E

@ lO 8

Outdoor e~

mid-Octmid-Nov

15.8 11 18

-

(10)

-

(10)

mid-Novmid-Dec

13.1 10-16

-

(5)

-

(5)

-- (5)

-- (5)

mid-Decmid-Jan

10.8 7-13

+ (5)

+ (5)

+ (5)

+ (5)

mid-Octmid-Nov

27

-

(8)

-

(7)

mid-Novmid-Dec

27

-

(3)

-

(3)

-

(4)

-

(4)

mid-Decmid-Jan

27

-

(4)

-

(3)

-

(4)

-

(4)

11

+ (6)

52

Indoor

All the year r o u n d

1

+ (6)

+ (6)

5

10

15

20

Sequence of arousals Fig. 1. H i b e r n a t i o n p a t t e r n o f Hemiechinus (H # 13) and Erinaceus (E # 10). Both specimens were allowed to hibernate continuously for four m o n t h s at a constant 11 ~

+ (6)

hedgehogs became torpid. In the second week of December the minimum temperature fell to 12___2 ~ (9-14 ~ and all of the hedgehogs, both fasting and normally fed, became torpid for short periods of 2-5 days. They lay inactive in a small depression of sawdust in the rolled posture typical for hedgehogs. During this period they did not respond to noise or touch, nor did they eat or drink in times of spontaneous arousal. This behavior went on up to mid-March when they returned to normal activity. Although each specimen had its own rhythm, it seemed that in Erinaceus the hibernation bouts became progressively longer in January (minimum air temperature 9 + 2 ~ and then shortened again towards the end of February. On the other hand, hibernation bouts in Hemiechinus remained rather short and regular throughout the entire winter (see also Fig. 1). The hedgehogs which were kept indoors at 27 ~ did not show any sign of torpidity as long as they remained at that temperature. In this respect, neither food restriction nor altering the light regime to 16L:8D had any noticeable effect on the hedgehog's activity. When placed in an ambient temperature of 11 ~ all the hedgehogs of both species entered hibernation at any time of the year within 20-48 h. Here again, no difference was found between fasting and normally-fed speci-

mens, nor between the recently caught hedgehogs and those of the previous years. Periodicity of hibernation

Hibernation is a cyclic process in which periods of dormancy and spontaneous arousals occur alternately (Kayser 1961; Lyman et al. 1982). Hibernation of Erinaceus and Hemiechinus at a constant 11 ~ is also periodical. However, although the duration of the awakening period was similar (20-25 h) in both species, the frequency and regularity of arousals recurrence differed markedly. The number of spontaneous arousals per hibernation month was 5.3_+0.8 (SD) in the desert species Hemiechinus and only 2.9+0.8 in Erinaceus. The hibernation bouts in Hemiechinus w~re quite short and regular whereas in Erinaceus they were short at the beginning, very long (up to:27 days) in the middle, and became shorter again towards the end of the hibernation period. The latter pattern was found also in hibernating Erina

~

3.0

H#13

\

E

m

20 16

\

12

7

\l

,

-2 0 2 4 ; 8 1;

~J

32 28

24

2.0

-1/,

36

,".~--..._.

;2 1'4- 1'6 18 20 22 24 26

Hours

Fig. 2. A typical hibernation cycle of Hemiechinus (H # 13) and Erinaeeus (E # 10) hibernating at a constant 11 ~ The data of oxygen consumption ([2o~) and body temperature (Tb) were synchronized by using the last 3 h of the hibernation phase as a starting point

rate of increase during arousal. The rate of oxygen consumption of the hibernating Hemiechinus is twice the rate of Erinaceus (Table 2), despite the fact that both species have the same body temperature. This difference is statistically significant. To find out whether this is not a mere reflection of the different body masses, we compared the ob-


121

served 12o2with the expected values (equation (1)). By assuming a Qlo effect of 2.3 we have corrected the values presented in Table 2 to T b of 10 ~ The corrected l?o~ of a 367 g Hemiechinus is 60% higher than the expected value (0.040 vs 0.025 ml 02 g-1 h - l ) , whereas that of a 598 g Erinaceus is about the same as the expected (0.021 vs. 0.022 ml O 2 g-~ h - l ) . The rate of oxygen consumption during each phase of the awakening period was much the same for both species. It increased rapidly during the arousal phase and reached an average peak of 3 ml g-1 h-1. Then it dropped and stabilized at about 2 ml g - t h-1 during euthermia (Table 2, Fig. 2). No statistically significant difference was found between the euthermic values in this work and the oxygen consumption obtained for resting, non-hibernating hedgehogs at 11 ~ by Shkolnik and Schmidt-Nielsen (1976). Towards the end of the hibernation re-entrance phase the drop in oxygen consumption became slower and it took an additional 5-8 h before the hibernation level was reached. The pattern of CO 2 production and the ratio of CO2/O2 (R.Q. values) during each of the various phases of the hibernation cycle were similar for both species (Table 2). These values are similar to the R.Q. obtained for Erinaceus from Northern Europe (Tfihti 1978), and to the R.Q's found in many other hibernators (Kayser 1961). The thermal conductance of the hibernating hedgehogs is given in Table 3. The figures presented in this table tend to over-estimate the thermal conductance, since we did not measure and, consequently, did not subtract the heat lost by evaporation from the metabolic heat production (equation (2); Dawson and Schmidt-Nielsen 1966). However, the evaporative heat lost by non-hibernating hedgehogs kept at 11 ~ (Shkolnik and Schmidt-Nielsen 1976) is only a small fraction of the total heat loss. No statistically significant difference was found between the conductance of the two species during each of the different phases of the hibernation cycle. It should be noted that during a period of about one third of the hibernation re-entrance phase, the thermal conductance was the same as that obtained during the phase of euthermia (Table 3). This may indicate that at a Ta of 11 ~ it would be sufficient for the euthermic hedgehog to 'shut off' its high metabolism, and to decrease it to a level which is adequate for the non-hibernating hedgehog at temperatures of thermoneutrality. While the rates of heat loss during the first part of hibernation re-entrance are still maintained at the high level as during euthermia (no change in

Table 3. Thermal conductance of hedgehogs hibernating at 11 ~ Values are means __+SE calculated for a single hibernation cycle. " a " , " b " and " c " during the phase of re-entrance into hibernation refer to durations of 35%, 70% and to the end of this phase Phase

Thermal conductance (W cm -2 ~ -1) x 10 ~

Hemiechinus (N = 8)

Erinaceus (N = 7)

1.140 _+0.174 5,652 + 0.872 3.954 +_0.616

0.872 _+0.198 5.792_+ 0.8/4 3.838 +_0.570

Hibernation re-entrance a 4.059 • 0.593 b 2.559_+ 0.349 c 2.500 • 0.349

3.815_+ 0.535 2.768_+ 0.442 3.349 +_0.407

Hibernation Arousal Euthermia

thermal conductance), this metabolic decrease would lead to a concomitant decrease in Tb . Discussion

Patterns and onset of hibernation

The short and regular hibernation bouts of Hemieehinus resemble the hibernation pattern found in Hemiechinus from Egypt (AI-Bardy and Taha /982, 1983). However, because of the different experimental conditions the results are not comparable. Hibernation of Erinaceus is very similar to the pattern observed in hedgehogs from Northern Europe. At T, of 4.2 ~ the hibernation bouts in the Finnish Erinaceus averaged about 9 days, the longest bouts occurred in the middle of the hibernation season. At T, of 12 ~ but not above it, this hedgehog still maintained all the characteristics of deep hibernation (Kristoffersson and Soivio 1964a, b). The similarity between the two populations is further emphasized by extrapolating the t7o2 obtained at Tb of 5 ~ to Tb of 12.3 ~ At Tb of 5 ~ the Finnish Erinaceus consumed about 0.011 ml O 2 g-1 h-1 (Soivio et al. 1968; T/ihti and Soivio 1977; T/ihti 1978). Assuming a Q~0=2.3, then at 12.3 ~ it would consume 0.020 ml O z g-~ h - I, a value which is not significantly;different from the actual l?o~ of our Erinaceus (Table 2). Thus, Erinaceus in Israel maintains a typical deep hibernation at a Ta which is very close to the upper limit for hibernation of this species. In our experiments both Erinaceus and Hemieehinus readily entered hibernation in any season of the year regardless of their feeding regime, whenever they were kept continuously at ambient

122


Table 4. Energy expenditure of Hemiechinus and Erinaceus hibernating at 11 ~ E Erinaceus (N= 7)

Values are means + S E , H Hemiechinus ( N = 8 ) ;

Energy Expenditure (kJ per animal) Hibernation cycle b

Hibernation month

Percent of total

H

E

H

H

45.43 _+ 3.39

•

Awakening period

242.00 • 28.26

Whole hibernation ~

287.43 • 31.02

Hibernation bout

66.24 7.24

E

E

240.74 33.91

192.17 __ 24.70

15.8

13.4

426.76 -t-43.63

1,282,42 • 123,09

1,237.62 • 134.40

84.2

86.6

493.00 + 49.03

1,523,16 • 164.54

1,429.79 _+155.75

•

100

100

The duration of hibernation cycle and the arousals frequency are 5.65 days and 5.3 per month in Hemiechinus, 10.36 days and 2.9 per month in Erinaceus b The differences between the two species are significant (P < 0.01)

temperatures of 11 ~ or below. It should be remembered, however, that the food available for these insect• in their natural habitats does decrease conspicuously along with the fall of the ambient temperature (Dubinsky et al. 1979). Therefore, the natural hibernation of the two species may be brought about by a combined effect of the two factors : a continuous, low temperature (ca. 11 ~ during December and a decrease in the food availability. The temperature factor is most probably the dominant. Energy expenditure

The amounts of energy used by the hedgehogs during a single hibernation cycle and during a month of hibernation are given in Table 4. During a hibernation bout, which is the longest hibernation phase, both species used only 15% of the total amount of energy consumed during the entire hibernation cycle. Most of the energy, 85% of the total, was consumed during the short periods of awakening. The total amount of energy consumed by Hemieehinus in a single hibernation cycle was 287 kJ, which is about half the amount consumed by Erinaceus. However, the duration of a hibernation cycle in Hemiechinus is 45% shorter (5.65 vs 10.36days) and its recurrence frequency is 1.8 times higher than that of Erinaceus. Thus, for the same number of hibernation days, the smaller species Hemiechinus would consume the same amount of energy as the larger species (Table 4). The cost of spending one month in "euthermia" can be calculated from the empirical equations which relate oxygen consumption of non-hibernating hedgehogs to the ambient temperature (Shkolnik and Schmidt-Nielsen 1976, Fig. 2).

Thus, at an ambient temperature of 11 ~ Hemiechinus and Erinaceus would consume 10,446 and 11,007 kJ per month, respectively. Therefore, by entering into hibernation the hedgehogs save about 86% of the energy required to maintain their body temperature 22 ~ above the ambient temperature, and for both species the cost for spending one day in euthermia approximates seven days of hibernation. Since none of the experimental animals ate during periods of awakening, all of the energy used must have come from catabolism of substances which had been accumulated and stored in the hedgehog's body before it entered into hibernation. If we assume lipids as the main energy source and an equivalent of 39.356 kJ per gram fat, then both species are expected to lose about 37 g of their body mass over a month of hibernation. In our experiments four Hemiechinus and three Erinaceus were allowed to hibernate continuously throughout four months. During this period they lost an average of 156 g and 150 g, which is 39 and 37.5 g per month, respectively. Apparently, the corresponding amount of metabolic water (1.07 g water per g fat) was cleared from the body by 1-2 urinations during each period of awakening. Animals which are fully prepared for hibernation enter this state with 40% of their body mass as fat (Suomalainen and Saarikoski 1971; Cranford 1983). This means that the absolute amount of fat available as an energy source depends on the hibernator's body mass. For Hemiechinus and Erinaceus it would amount to 146.8 and 239.2 g fat, respectively. Consequently, at the loss rate of 37 g fat per month, Hemieehinus would be able to hibernate for 3.9 months only, whereas Erinaeeus can continue to hibernate for up to


123

6.5 months. Thus, the duration of the entire hibernation season will be determined by the metabolic rate, the frequency of spontaneous arousals, and the body mass of the hibernator. All of these factors act unfavorably for the desert inhabitant Hemiechinus. The physiological responses of the hedgehogs to low ambient temperatures show that basically the two species cope with the cold environment, both seminatural or artificial, in a similar manner. The differences between them are more of quantitative than qualitative nature, which fully corresponds to the climatic differences in their respective habitats. The differences found in the hibernating Hemiechinus (higher metabolism and higher arousal frequency) suggest that, unlike its non-arid counterpart, Hemiechinus probably does not enter a deep hibernation in its natural environment, but rather spends the winter in a torpor-like state. It should be realized, however, that even in the desert the critical season of the year for the hedgehog, as well as for some other mammals, is the relatively short, cold winter and not the hot, dry summer (Dmi'el et al. 1980). Presumably, water is not the crucial factor affecting the hedgehog's survival in the summer: the activity of Hemiechinus during the summer is restricted to night-time (Bodenheimer 1935; and personal observations), its food contains sufficient amount of water, and its kidneys are capable of producing urine of high concentrations (Yaakobi and Shkolnik 1974). On the other hand, because of its small body size and relatively inefficient insulation (lower critical temperature of about 31 ~ Shkolnik and Schmidt-Nielsen 1976), Hemiechinus should rely mostly on metabolic energy in order to keep its body temperature constant during cold weather. However, the availability of food decreases distinctly during the winter, and the hedgehog has to face a situation analogous to that of a species inhabiting temperate regions, i.e., increasing need for metabolic energy together with a concomitant decrease of food availability. Therefore, the ability of Hemiechinus to enter hibernation improves significantly the hedgehog's energy economy during the desert winter.

A1-Bardy KS, Taha HM (1983) Hibernation-hypothermia and metabolism in hedgehogs. Changes in some organic components. Comp Biochem Physiol 74A: 143-148 Bodenheimer FS (1935) Animal life in Palestine. Mayer L, Jerusalem Cranford JA (1983) Body temperature, heart rate and oxygen consumption of normothen~aic and heterothermic western jumping mice (Zapus princeps). Comp Biochem Physiol 74A: 595-599 Dawson T, Schmidt-Nielsen K (1966) Effect of thermal conductance on water economy in the antelope jack rabbit, Lepus alleni. J Cell Physiol 67 :463472 Dmi'el R, Perevolotzky A, Shkolnik A (1980) Is a black coat in the desert a means of saving metabolic energy? Nature 283:761 762 Dubinsky Z, Steinberger Y, Shachak M (1979) The survival of the desert isopod Hemilepistus reaumurii (Audouin) in relation to temperature (Isopoda, Oniscoidea). Crustaceana 36 : 147-154 Harrison DL (1964) The mammals of Arabia, vol 1. Ernest Benn, London, 192 pp Kayser C (1961) The physiology of natural hibernation. Pergamon Press, Oxford Kayser C (1964) La depense d'energie des mammif~res en hibernation. Arch Sci Physiol (Paris) t 8 : 137-I 50 Kristoffersson R, Soivio A (1964a) The periodicity of hibernation of undisturbed animals during winter ir~ a constant ambient temperature. Ann Acad Sci Fenn Ser A4 80 : 1-22 Kristoffersson R, Soivio A (1964b) Hibernation in the hedgehog (Erinaceus europaeus k). Changes of respiratory pattern, heart rate and body temperature in response to gradually decreasing or increasing ambient temperature. Ann Acad Sci Fenn Set A4 82:1-17 Lyman CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and torpor in mammals and birds. Academic Press, New York Pengelley ET, Fisher KC (1961) Rhythmical arousal from hibernation in the golden-mantled ground squirrel (Citellus lateralis tescorum). Can J Zool 39:105-120 Proctor F (1949) Temperature changes in hibernating hedgehogs. Nature 163 : 108-109 Shkolnik A, Schmidt-Nielsen K (1976) Temperature regulation in hedgehogs from temperate and desert enkzironments. Physiol Zool 49 : 56-64 Soivio A, Tfihti H, Kristoffersson R (1968) Studies on the periodicity of hibernation in the hedgehog (Erinaceus europaeus L.). III. Hibernation in a constant ambient temPerature of - 5 ~ Ann Zool Fenn 5:224-226 Suomalainen P, Saarikoski PL (1971) Studies on the physiology of the hibernating hedgehog. 14. Serum free fatty acid, glycerol and total lipid concentrations at different times of the year and of the hibernating cycle. Ann Acad Sci Fenn A4 184: 1-6 T/ihti H (1978) Seasonal differences in 0 2 consumption and respiratory quotient in a hibernator (Erinaceus europaeus L.). Ann Zool Fenn 15:6%75 T/ihti H, Soivio A (1977) Respiratory and circulatory differences between induced and spontaneous arousal in hibernating hedgehogs (Erinaceus europaeus L.). Ann Zool Fenn 14:198-203 Yaakobi D, Shkolnik A (1974) Structure and co,ncentrating capacity in kidneys of three species of hedgeliogs. Am J Physiol 226 : 948-952

References A1-Bardy KS, Taha HM (1982) Hibernation-hypothermia and metabolism in hedgehogs. Changes in free amino acids and related compounds. Comp Biochem Physiol 72A:541-547