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Duration of hibernation bouts in Zapus hudsonius
Comp. Biochem. Ph~~iol. Vol. 6lA. pp. 287 to 289 0 Pergamon Press Ltd 1980 Prmted in Great Bnmn
DURATION
OF HIBERNATION ZAPUS HUDSONIUS
BOUTS
IN
ALAN E. MUCHLINSKI* Department
of Zoology,
Michigan
State University,
(Rrcrired
25 January
East Lansing,
MI 48824, U.S.A.
1980)
Abstract--l. Meadow jumping mice demonstrate an exponential increase in duration of hibernation bouts. 2. This exponential increase differs from the pattern of hibernation bouts previously described for Sprrrnophilus lateralis. 3. An exponential increase in hibernation bout length complicates the hypotheses that attempt to explain the mechanism of periodic arousals.
INTRODU(XION
MATERIALS AND METHODS A continuous record of hibernation and activity was maintained for I2 animals held in a walk-in environmental chamber under LD 12:12. 5°C with a light intensity of approximately 85 lx. Each animal was housed in a plastic cage measuring 26.7 x 20.3 x 15.9 cm with access to a nest box painted black to reduce light penetration. A tracking plate, sprayed with a mixture of alcohol and talc was placed in front of the next box opening. Evaporation of the alcohol left a smooth surface of talc which was disturbed if the animal left the next box. The tracking plates were checked once per day giving an accuracy of + 1 day in the duration of a hibernation bout. Body weight was also monitored in this experiment, being taken during or shortly after a periodic arousal. Since hibernating mammals are more irritable near the end of a hibernation bout (Twente & Twente, 1968). this minimized the possibility that an animal would be aroused before the natural termination of a hibernation bout.
An animal in hibernation does not remain in a continuous state of torpor over the winter. Instead, short bouts of activity break up the hibernation season into a number of shorter hibernation bouts (Pengelley & Fisher, 1961). The duration and pattern of bouts has been
described
for the golden-mantled
ground
squir-
rel, Spermophilus later&, (Torke & Twente, 1977). In the described pattern, there is an autumn phase in which bout length increases, a winter (Plateu) phase in which bout length is maximum and fairly constant and a spring phase during which bout length decreases. In this paper, data are presented on hibernation bout length in meadow jumping mice held under LD 12: 12. S’C. This species demonstrates a pattern of hibernation bouts different from the previously described species under the same experimental conditions. * Present address: State University U.S.A.
Department
at Los Angeles,
of Biology, Los Angeles,
RESULTS
California CA 90032,
The pattern of hibernation bout length is shown for six animals in Fig. 1. All 12 of the animals monitored
LIL 7s
Fig. 1. Pattern of hibernation bout length for six animals under LD 12:12, 5’C. Each vertical line represents the length of one hibernation bout. Animals 104, 106 and I08 show data for 2 consecutive years. C.B.P.67;2~-~
287
ALAN E. MUCHLINSKI
288
40.
106 -
35.
1el 0
-
lo5
10
15
20
o
25
5
10
I5
20
25
15
20
25
,lONTH
“ONTH
40 -
35 30.
104 -
-
25 20 15,1ci”i 101 0
5
10 tlONTH
Fig. 2. Body weight and hibernation
graphs
underwent an exponential increase in duration of hibernation bout length up to a maximum length of 30.5 k 4.0 SD days. In several instances there were hibernation bouts that deviated from the exponential increase (No. 104 and No. 108). However, the deviation was usually double the expected value. This indicated that the animal may have aroused from and entered back into hibernation without coming out of the box to disturb the tracking plate. Following the attainment of maximum bout length. there was a rapid decrease in bout length leading to a terminal arousal and entrance into the active (summer) state. Figure 2 shows body weight and hibernation graphs for three of the animals from Fig. 1. After an animal enters into hibernation there is a phase of rapid weight loss and this correlates with the shorter hibernation bout lengths. After about one-third of the hibernation interval has passed, hibernation bout length increases substantially and this correlates with a decrease in the rate of body weight loss. When an animal does not hibernate at all after undergoing a weight increase (animal 89 from Fig. 2, third and fourth weight increase). the weight loss is very drastic. Therefore. the rate of weight loss depends upon the duration of the hibernation bout. Longer bout lengths reduce the rate of weight loss because the periodic arousals. which consume approximately 52’; or more of the total energy used in a hibernation bout (Muchlinski & Rybak. 1978). are less frequent. DISC’CSSION
Two hypotheses have been put forward to explain the occurrence of periodic arousals during hibernation. The first of these (Pengelley & Fisher. 1961) suggests that an accumulation of metabolic waste products during the hibernation bout triggers arousal upon reaching some threshold level. Since the kidney is essentially nonfunctional at the low body temperatures achieved during hibernation (Clausen & Storesund, 1971; Zatman & South. 1972). waste products should accumulate in the blood. However, data on this aspect of hibernation are contradictory. Pengelley et al. (1971) found that the concentrations of sodium,
for three individuals
from Fig. I.
potassium, calcium, magnesium and urea in the blood remained constant between periodic arousals while Kristoffersson (1963) determined that hedgehogs (Erinaceus europaeus) show a marked increase in blood and tissue urea concentrations while in the hibernating state. The constancy of the winter phase hibernation bouts in Sperrnophilus lateralis lends support to the metabolic waste product hypothesis. If a buildup of metabolic end products is causing the periodic arousals, bout length should be fairly constant. However. the shorter hibernation bouts in the autumn and spring are not as easily explained by this hypothesis. The pattern of hibernation bouts in Zapus hudsouius is likewise hard to interpret in light of the metabolic waste product hypothesis since there is no phase of constant hibernation bout length. In order for metabolic waste products to trigger arousal, one would have to postulate some form of cellular acclimation so that the threshold for arousal is continuously increased up to the last one or two hibernation bouts. This would then give an exponential increase in hibernation bout length. The second hypothesis (Lyman & O’Brien, 1969) postulates that there is a progressive loss of potassium (K) from nerve and muscle tissue leading towards a state of nerve disfunction. A decrease in K in nerve and muscle tissue would lead to a depolarization of the membrane and increased excitability. Therefore, increased irritability would result and this correlates with the results of Twente & Twente (1968). Periodic arousals would be necessary to restore the normal balance of K in the tissues. This hypothesis has been supported by Willis et al. (1971). These authors demonstrated a loss of K from excitable tissue during hibernation and restoration of K to original levels during the periodic arousal. This hypothesis, however, has the same drawback as the metabolic waste product hypothesis. Since Zupus hudsonius shows a continual increase in hibernation bout length, one would have to postulate either a progressive lowering of the rate of K loss by changes in the cell membrane or a change in the nerve or muscle cell so that it can function with lower and
Hibernation
in jumping
lower K reserves as hibernation proceeds. A progressive lowering of K loss is a realistic possibility since it has been demonstrated that nerves do function better at lower body temperatures in a hibernating mammal than in a nonhibernating one (Chatfield er nl., 1948) and that mitochondrial lipid changes do occur in hibernating mammals during late summer and early autumn (Cremel et al., 1979). Although the data on Zapus hudsonius do not reject either of these hypotheses, they do show that the phenomena of periodic arousal and duration oi hibernation bouts are more comDlicated than originally perceived and that more research needs to be conducted on both of these hypotheses.
REFERENCES CHATFIELD P. O., BATTISTA A. F., LYMAN C. P. & GARCIA J. P. (1948) Effects of cooling on nerve conduction in a hibernator (golden hamster) and non-hibernator (albino rat). A~I. J. Ph_vsiol. 155, 179-185. C‘LAUSENG. & STORESUND A. (1971) Electrolvte distribution and renal function in the hibernating hedgehog. Acta physiol. stand. 83, 4-l 2. CREMEL G.. REBEL G., CANGUILHEM B., RENWN A. & WAKSMAF; A. (1979) Seasonal variation of the composition of membrane lipids in liver mitochondria of the hibernator. Cricefus cricetus. Relation to intramitochon-
mice
289
drial intermembranal protein movement. Cornp. Biothem. Physiol. 63A, 159-l 67. KRISTOFFERSSONR. (1963) Urea-level in blood and tissues of hibernating and non-hibernating hedgehogs. Nature 197. 402403. LYMAN C. P. & O’BRIEN R. C. (1969) Hyperresponsiveness
in hibernation. Symp. Sm. exp. Biol. 23, 489-509. MUCHLINSKI A. E. & RYBAK E. N. (I 978) Energy consumption of resting and hibernating meadow jumping mice. J. Mammal. 59, 435437. PENGELLEY E. T. & FISHER K. C. (1961) Rhythmical arousal from hibernation in the golden-mantled ground squirrel, Citellus lateralis fescorum. Can. J. Zool. 39,
105-120. PENGELLEY E. T., ASMUNDSON S. J. & UHLMAN C. (1971) Homeostasis during hibernation in the nolden-mantled ground squirrel, Cl7ellu.s lateralis. Camp.-Biochem. PhyGo/. 38A, 645-653. TORKE K. & TWENTE J. W. (1977) Behavior of Spermophilus lateralis between periods of hibernation. J. Mammal. 58, 385-390. TWENTE J. W. & TWENTE J. A. (1968) Progressive irritability of hibernating Cirellus lateralis. Camp. Biochrm. Phy siol.
25, 467474.
WILLIS J. S.. GOLDMAN S. S. & FOSTER R. F. (1971) Tissue K concentration in relation to the role of the kidney in hibernation and the cause of periodic arousal. Camp. Biochem. Physiol. 39A, 437445.. ZATMAN M. L. & SOUTH F. E. (1972) Renal function of the awake and hibernating marmot. Marmota jfuti~entris. Am. J. Phq‘siol. 222, 1035~1039.
DURATION
OF HIBERNATION ZAPUS HUDSONIUS
BOUTS
IN
ALAN E. MUCHLINSKI* Department
of Zoology,
Michigan
State University,
(Rrcrired
25 January
East Lansing,
MI 48824, U.S.A.
1980)
Abstract--l. Meadow jumping mice demonstrate an exponential increase in duration of hibernation bouts. 2. This exponential increase differs from the pattern of hibernation bouts previously described for Sprrrnophilus lateralis. 3. An exponential increase in hibernation bout length complicates the hypotheses that attempt to explain the mechanism of periodic arousals.
INTRODU(XION
MATERIALS AND METHODS A continuous record of hibernation and activity was maintained for I2 animals held in a walk-in environmental chamber under LD 12:12. 5°C with a light intensity of approximately 85 lx. Each animal was housed in a plastic cage measuring 26.7 x 20.3 x 15.9 cm with access to a nest box painted black to reduce light penetration. A tracking plate, sprayed with a mixture of alcohol and talc was placed in front of the next box opening. Evaporation of the alcohol left a smooth surface of talc which was disturbed if the animal left the next box. The tracking plates were checked once per day giving an accuracy of + 1 day in the duration of a hibernation bout. Body weight was also monitored in this experiment, being taken during or shortly after a periodic arousal. Since hibernating mammals are more irritable near the end of a hibernation bout (Twente & Twente, 1968). this minimized the possibility that an animal would be aroused before the natural termination of a hibernation bout.
An animal in hibernation does not remain in a continuous state of torpor over the winter. Instead, short bouts of activity break up the hibernation season into a number of shorter hibernation bouts (Pengelley & Fisher, 1961). The duration and pattern of bouts has been
described
for the golden-mantled
ground
squir-
rel, Spermophilus later&, (Torke & Twente, 1977). In the described pattern, there is an autumn phase in which bout length increases, a winter (Plateu) phase in which bout length is maximum and fairly constant and a spring phase during which bout length decreases. In this paper, data are presented on hibernation bout length in meadow jumping mice held under LD 12: 12. S’C. This species demonstrates a pattern of hibernation bouts different from the previously described species under the same experimental conditions. * Present address: State University U.S.A.
Department
at Los Angeles,
of Biology, Los Angeles,
RESULTS
California CA 90032,
The pattern of hibernation bout length is shown for six animals in Fig. 1. All 12 of the animals monitored
LIL 7s
Fig. 1. Pattern of hibernation bout length for six animals under LD 12:12, 5’C. Each vertical line represents the length of one hibernation bout. Animals 104, 106 and I08 show data for 2 consecutive years. C.B.P.67;2~-~
287
ALAN E. MUCHLINSKI
288
40.
106 -
35.
1el 0
-
lo5
10
15
20
o
25
5
10
I5
20
25
15
20
25
,lONTH
“ONTH
40 -
35 30.
104 -
-
25 20 15,1ci”i 101 0
5
10 tlONTH
Fig. 2. Body weight and hibernation
graphs
underwent an exponential increase in duration of hibernation bout length up to a maximum length of 30.5 k 4.0 SD days. In several instances there were hibernation bouts that deviated from the exponential increase (No. 104 and No. 108). However, the deviation was usually double the expected value. This indicated that the animal may have aroused from and entered back into hibernation without coming out of the box to disturb the tracking plate. Following the attainment of maximum bout length. there was a rapid decrease in bout length leading to a terminal arousal and entrance into the active (summer) state. Figure 2 shows body weight and hibernation graphs for three of the animals from Fig. 1. After an animal enters into hibernation there is a phase of rapid weight loss and this correlates with the shorter hibernation bout lengths. After about one-third of the hibernation interval has passed, hibernation bout length increases substantially and this correlates with a decrease in the rate of body weight loss. When an animal does not hibernate at all after undergoing a weight increase (animal 89 from Fig. 2, third and fourth weight increase). the weight loss is very drastic. Therefore. the rate of weight loss depends upon the duration of the hibernation bout. Longer bout lengths reduce the rate of weight loss because the periodic arousals. which consume approximately 52’; or more of the total energy used in a hibernation bout (Muchlinski & Rybak. 1978). are less frequent. DISC’CSSION
Two hypotheses have been put forward to explain the occurrence of periodic arousals during hibernation. The first of these (Pengelley & Fisher. 1961) suggests that an accumulation of metabolic waste products during the hibernation bout triggers arousal upon reaching some threshold level. Since the kidney is essentially nonfunctional at the low body temperatures achieved during hibernation (Clausen & Storesund, 1971; Zatman & South. 1972). waste products should accumulate in the blood. However, data on this aspect of hibernation are contradictory. Pengelley et al. (1971) found that the concentrations of sodium,
for three individuals
from Fig. I.
potassium, calcium, magnesium and urea in the blood remained constant between periodic arousals while Kristoffersson (1963) determined that hedgehogs (Erinaceus europaeus) show a marked increase in blood and tissue urea concentrations while in the hibernating state. The constancy of the winter phase hibernation bouts in Sperrnophilus lateralis lends support to the metabolic waste product hypothesis. If a buildup of metabolic end products is causing the periodic arousals, bout length should be fairly constant. However. the shorter hibernation bouts in the autumn and spring are not as easily explained by this hypothesis. The pattern of hibernation bouts in Zapus hudsouius is likewise hard to interpret in light of the metabolic waste product hypothesis since there is no phase of constant hibernation bout length. In order for metabolic waste products to trigger arousal, one would have to postulate some form of cellular acclimation so that the threshold for arousal is continuously increased up to the last one or two hibernation bouts. This would then give an exponential increase in hibernation bout length. The second hypothesis (Lyman & O’Brien, 1969) postulates that there is a progressive loss of potassium (K) from nerve and muscle tissue leading towards a state of nerve disfunction. A decrease in K in nerve and muscle tissue would lead to a depolarization of the membrane and increased excitability. Therefore, increased irritability would result and this correlates with the results of Twente & Twente (1968). Periodic arousals would be necessary to restore the normal balance of K in the tissues. This hypothesis has been supported by Willis et al. (1971). These authors demonstrated a loss of K from excitable tissue during hibernation and restoration of K to original levels during the periodic arousal. This hypothesis, however, has the same drawback as the metabolic waste product hypothesis. Since Zupus hudsonius shows a continual increase in hibernation bout length, one would have to postulate either a progressive lowering of the rate of K loss by changes in the cell membrane or a change in the nerve or muscle cell so that it can function with lower and
Hibernation
in jumping
lower K reserves as hibernation proceeds. A progressive lowering of K loss is a realistic possibility since it has been demonstrated that nerves do function better at lower body temperatures in a hibernating mammal than in a nonhibernating one (Chatfield er nl., 1948) and that mitochondrial lipid changes do occur in hibernating mammals during late summer and early autumn (Cremel et al., 1979). Although the data on Zapus hudsonius do not reject either of these hypotheses, they do show that the phenomena of periodic arousal and duration oi hibernation bouts are more comDlicated than originally perceived and that more research needs to be conducted on both of these hypotheses.
REFERENCES CHATFIELD P. O., BATTISTA A. F., LYMAN C. P. & GARCIA J. P. (1948) Effects of cooling on nerve conduction in a hibernator (golden hamster) and non-hibernator (albino rat). A~I. J. Ph_vsiol. 155, 179-185. C‘LAUSENG. & STORESUND A. (1971) Electrolvte distribution and renal function in the hibernating hedgehog. Acta physiol. stand. 83, 4-l 2. CREMEL G.. REBEL G., CANGUILHEM B., RENWN A. & WAKSMAF; A. (1979) Seasonal variation of the composition of membrane lipids in liver mitochondria of the hibernator. Cricefus cricetus. Relation to intramitochon-
mice
289
drial intermembranal protein movement. Cornp. Biothem. Physiol. 63A, 159-l 67. KRISTOFFERSSONR. (1963) Urea-level in blood and tissues of hibernating and non-hibernating hedgehogs. Nature 197. 402403. LYMAN C. P. & O’BRIEN R. C. (1969) Hyperresponsiveness
in hibernation. Symp. Sm. exp. Biol. 23, 489-509. MUCHLINSKI A. E. & RYBAK E. N. (I 978) Energy consumption of resting and hibernating meadow jumping mice. J. Mammal. 59, 435437. PENGELLEY E. T. & FISHER K. C. (1961) Rhythmical arousal from hibernation in the golden-mantled ground squirrel, Citellus lateralis fescorum. Can. J. Zool. 39,
105-120. PENGELLEY E. T., ASMUNDSON S. J. & UHLMAN C. (1971) Homeostasis during hibernation in the nolden-mantled ground squirrel, Cl7ellu.s lateralis. Camp.-Biochem. PhyGo/. 38A, 645-653. TORKE K. & TWENTE J. W. (1977) Behavior of Spermophilus lateralis between periods of hibernation. J. Mammal. 58, 385-390. TWENTE J. W. & TWENTE J. A. (1968) Progressive irritability of hibernating Cirellus lateralis. Camp. Biochrm. Phy siol.
25, 467474.
WILLIS J. S.. GOLDMAN S. S. & FOSTER R. F. (1971) Tissue K concentration in relation to the role of the kidney in hibernation and the cause of periodic arousal. Camp. Biochem. Physiol. 39A, 437445.. ZATMAN M. L. & SOUTH F. E. (1972) Renal function of the awake and hibernating marmot. Marmota jfuti~entris. Am. J. Phq‘siol. 222, 1035~1039.