Body temperature, heart rate and oxygen consumption of normothermic and heterothermic Western jumping mice (Zapus princeps)

0300-9629’83’030595-05903 0

BODY TEMPERATURE, OXYGEN CONSUMPTION AND HETEROTHERMIC MICE (ZAPUS

1983

Pergamon

00/o

Press Ltd

HEART RATE AND OF NORMOTHERMIC WESTERN JUMPING PRINCEPS)

JACK A. CRANFORD Biology

Department,

Virginia

Polytechnic

Institute

and State University,

Blacksburg,

VA 24061. USA

(Rrceiced 25 May 1982) Abstract-- 1. Heart rates and oxygen consumption were measured for normothermic. hibernatmg, and arousing Zapus princrps. 2. Rectal and oral body temperature were monitored and differential rates of rewarming of the body were recorded. 3. Lengths of periodic arousals differ in two stages of hibernation; days 5G30 arousal durations were I2 hr, 43 min while days 14G210 were 10 hr, 28 min. cycle based on the 4. Total energy budget of hibernation was calculated for a 295 day hibernation utilization of 18,020 cc of oxygen for that period. The calculated utilization of fat would be 8.97 g while the observed use was 9.5-l 1:1-g.

INTRODUCTION

The western jumping mouse (Zapus princeps) belongs to a small family of hibernating rodents, Zapodidae, members of which are distributed through the temperate and boreal regions of the northern hemisphere. Z. hudsorxiu.s and Napaeozapus insignis, two closely related North American forms, hibernate for varying lengths of time, partially dependent on weather conditions and geographical location (Whitaker, 1972; Whitaker & Wrigley, 1972). Z. princeps occurs in the Rocky Mountains region where it hibernates for 2355292 days in a hibernaculum located 59.9 + 11.2 cm below the soil surface where the average temperature during the hibernation season is 4.6”C (Cranford, 1978). Oxygen consumption rates of Z. lzudsonius under hibernating and non-hibernating conditions have been reported by Pearson (1947) and Morrison & Ryser (1962). Body temperature for hibernating Z. hutisonius has been reported to be 3’C above ambient temperature (Waters & Stockley, 1965) and in nonhibernating individuals to undergo a daily cycle between 35.1 and 4O.l”C (Morrison & Ryser, 1962). Brower & Cade (1966) and Pearson (1947) both reported oxygen consumption for N. insignis under ambient temperatures of 3s-3 I C to be between 1.8 and 2.4 cc/hr per g. The total hibernation period for Z. princeps of 295 days at 4.5’C can be divided into two phases: the first 90 days during which weight loss per day decreases from 0.21 g/day to 0.08 g/day and periodic arousals occur every 8.5 days on the average, and the remainder of the hibernation period during which the rate of weight loss is 0.04 g/day and periodic arousals occur every 21.3 days on average (Cranford, 1978). These values are very similar to those reported for Z. lrudsonius by Muchlinski (1980). This paper reports on physiological aspects of the hibernation cycle for Zapus prinreps, including heart

rate, O2 consumption, and body temperature data from the active and hibernation phases. Data on O2 consumption and arousal frequency in hibernation are used to calculate the energetic costs of the entire hibernation cycle. METHODS

A’VD .MATERIALS

Twenty-five Z. princeps were trapped between 6 and 15 July. 1977, in Lambs Canyon, 50 km east of Salt Lake City. Utah. The animals were housed individually in rectangular cages (30 x 20 x 15 cm) with attached nest boxes (12 x 14 x 14cm) containing cotton batting for nest material in an environmental chamber at 18C and a photoperiod of LD 12:12. During the prehibernation fat deposition phase. food and water were supplied ad lib. with only water available after hibernation was initiated. The laboratory diet was composed of one part by weight each of millet and corn. one part ground Purina Mouse Chow. ground and sieved to a particle size of 3.3 mm, and two parts sunflower seed (Cranford, 1977). After 10 September. when all animals were in hibernation. the chamber was held m constant darkness at 4.5 C to simulate the environment of a field hibernaculum (Cranford. 1978). Animals were weighed to the nearest 0.1 g every 15 days and also before and after each electrocardiogram (ECG) or metabolic rate determination, A twenty-channel Esterline Angus Event Recorder was utilized to continuously record activaity from treadle-operated microswitches in each cage. A 30 channel Leads & Northrup thermocouple recorder was used to continuously record nest box temperatures and skin surface temperatures during hibernation. Electrocardiograms were recorded with a Physio-five physiograph with leads attached across the chest of the animal with a Velcro harness. During all ECGs anal and oral temperatures and respiration Yates were recorded every minute manually and electronically. The rate of 0, consumption was continuously measured at 4.5-C over periods from 3 to 120 hr during full hibernation. through periodic arousals and hibernation reentry. Measurements of oxygen consumption on animals fasted for 12 hr were made during the pre-hibernation period at 4.5. 18 and 30 C. Oxygen consumption. core body temperature and

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JACK A.CRANFORD

respirometer chamber temperature were continuously recorded with an automatic recording respirometer (2-l. volume) modified after one described by Clayton (1970). The apparatus was housed in a constant temperafor ammonia and CO2 utilture cabinet with absorbents ized to maintain constant environmental quality.

RESULTS

The average anal body temperature of active summer Z. princeps with a mean body weight of 26.2 + 1.8 g was 37.2”C, with a range of 35%38.2”C at an ambient temperature (TA) of 18°C. Ninety-eight percent of all Z. princeps activity was confined to the dark period and was nearly continuous from 2000 to 0800 hr each day. Mean body temperature (7”) during the nocturnal active period was 37.8”C which was significantly higher than the mean Ts of 36.6”C during the inactive period (t = 8.6, P < 0.001). Heart rates of resting summer animals varied frm 395 to 460 beats/ min as measured at the midpoint of the inactive period. Respiratory exchanges varied from 185 to 260/min through both the active and resting periods. Oxygen consumption rates were 1.95 cc/hr per g at 30°C 2.65 cc/hr per g at 18°C and 6.20 cc/hr per g at 4”C, which are comparable to those reported by Morrison & Ryser (1962) for Z. hudsonius. The 22 animals which later entered hibernation gained weight at the rate of 0.71 k 0.15 g/day, reaching 37.5 & 4.6 g at entrance into hibernation. During periodic arousals from hibernation body temperatures increased from 5.5”C at an average rate of O.S”C/min orally and 0.31”C/min anally (Fig. 1). The difference between oral and anal rates of rewarming from seven adults measured through 18 arousals was statistically significant (t = 14.7, P < 0.01). Oral body temperature reached 33°C within 4&80 min, after which it stabilized at 35.8 f 1.2”C for the remainder of the normothermic period. The duration of the periodic arousals and a breakdown of their three components (arousal, normothermy and hibernation re-entrance) are shown in Table 1. Coordinated locomotion utilizing both fore and

rear limbs occurred 53-65 min after arousal hat begun, when both anal and oral temperatures were ir excess of 20°C. Prior to that, only the anterior portior of the body exhibited well-coordinated movement First urination occurred at oral temperatures ovel 28°C with 60% of first urination events 75-120 mir after initiation of arousal. In 90% of all arousals observed (N = 42) two urination events were recorded with the second just prior to hibernation re-entrance 2-5 hr after the arousal had begun. Body temperature decrease during re-entry into hi. bernation took four times as long as the return tc normothermy body temperature increase phase (Table 1). Both heart rate and oxygen consumptior dropped rapidly to low levels during re-entrance while body temperature dropped slowly demon. strating the passive nature of heat loss. No statistically significant differences (N = 36, t = 0.82. P < 0.2) between anal and oral temperatures were recorded during the re-entrance phase which is ir contrast to the differences observed during arousal. Heart rates of 20 animals were recorded during both phases of hibernation. During the first 90 days 01 a hibernation season the lowest heart rates recorded from animals with oral temperatures of 5.5 + 0.5”C were 18 beats/min with a mean of 24.23 + 4.6 beats, min as determined from 15-min recordings. These values are significantly higher (t = 8.3, P < 0.001~ than during the 16&210 day period when the lowest heart rates recorded were 6 beats/min but the mean was 14.6 f 2.4 beats/min from 15-min recordings. During the first 45 min of arousal from hibernation heart rate increased rapidly from 14 to 560 beats/min. Over the next 25 min it returned to a mean rate ol 420. which is characteristic of the normothermic period (Fig. 2). Re-entrance into hibernation required 160 min to reach heart rates of 50-70 beats/min. Hibernation levels of 14 beats/min took up to 15 hr to be reached (Fig. 2). The increase in heart rate seen in the first 22 min of spontaneous arousals (Fig. 2: required 3-O min during temperature induced forced arousals (with ECGs recorded from animals subjected to a change from a TA of 4.5”C to a T, 01

CL 0

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Fig. 1. Body temperatures during arousal from five arousals of six animals. T,, = oral body ture, THA= anal body temperature, TA = ambient temperature.

tempera-

Hibernation Table

I. Periodic

arousals periods

physiology

of Zaps.\ prir1cep.s

and their component segments in the hibernation cycle

Time required to return to normothermy from hibernation (TB = 6’C to T” = 33’C) Length of normothermic period (TB > 33’C) Time required for hibernation re-entrance (TB = 33’C to TB = 5.5’C) Mean duration of arousals

at two time

Days 5@-80 (N = 21)

Days 14@210 (IV = 39)

1:15 * 0:15

1:02 * 0:13

5:20 + 2:Y.I

5:06 + 2146

6:08 + I:20

4:20 f 1:08

12:43

10:28

The time required to return to heterothermy is significantly shorter in the 14&210 dav time Deriod (t = 5.25, P < 0.001). All figures are times in hr and min. and are given as means i SD.

18‘ C). Following that the two heart-rate curves would be identical, except that the terminal heart rate observed in hibernation at 18°C was 45 k 12 beats/min, as opposed to 14.6 f 2.4 beats/min at 4.5’C. Oxygen consumption of 20 animals (mean body weight 33.6 + 1.2 g) recorded for a minimum of 24 hr in hibernation at 4.5”C with a TH of 5.5 k OYC during the first 90 days in hibernation was 0.042 cc/hr per g which decreased to 0.024 cc/hr per g at a mean body weight of 27.7 k 1.1 g in the later phase of hibernation. Oxygen consumption during periodic arousals and for a representative portion of the normothermic phase and during re-entrance into hibernation are shown in Fig. 3. DISCUSSlON

The body temperatures of normothermic summer active Z. princeps fluctuated from 35.9 to 38.2% which is a smaller range of variation than has been reported for Z. hudsonitrs (3.5.1L40.1-C) by Morrison & Ryser (1962). Morrison & Ryser (1962) demonstrated a significant cyclic variation in body temperature with high nocturnal and low diurnal body temperatures. A similar pattern was observed in Z. prinwith the nocturnal active ceps and was correlated phase and the diurnal sleep phase. No body temperature cycles were noted in animals in deep hibernation

OO

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40

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~-:i-

TIME (MINUTES)

-70

and they typically had a body temperature of 5.5 _t 0.5-C at an environmental temperature of 4.5”C. Waters & Stockley (1965) reported that rectal temperatures of hibernating Z. hudsonius were 3’C above environmental temperatures (7”) but during this study on Z. princeps the oral temperature was lL1.5’C above TA while the anal temperature was 0.5-l.O’C above TA. The active heat generation phase of an arousal from hibernation took 45-50 min at a mean increase in TB of 0,5’C,imin. Arousals were broken into three distinct phases: Phase 1. when the T, increased from 5.5 to 8°C at a rate of 0.25’Cimin; Phase II. when the TH increased from 8 to 18 C at 0.50’C/min, and Phase III, when TB increased from 18 to 35’C at l.O’C/min. Body temperature stabilized within the following 3645 min with oral and a& temperatures equal. Full arousal and body temperature stability took a total of 7clOOmin in Z. princrps, whereas Waters & Stockley (1965) reported that it took 130min in Z. hudsonius. Z. princeps forced to arouse by a sudden temperature change from a TA of 4.5’C to 18’C required 2@-25 min in Phase I. after which the rate of temperature increase was essentially the same as for spontaneous arousals. The observations by Waters & Stockley (1965) and those of Clough (1955) on arousal in Z. hudsonius were probably on animals which were disturbed, and may not be representative of spontaneous arousals. Differences

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Fig. 2. Heart rates of five individuals recorded during periodic arousals (left panel) and during re-entry into hibernation (right panel) between days 18&200 of the hibernation cycle at a T,, of 4.5 C.

800

85C

598

JACK

A. CRANFORD

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(MINUTES)

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(MINUTES)

Fig. 3. Mean oxygen consumption rates for 15 arousals of 10 2. princrps from hibernation (left panel). The oxygen consumption data were synchronized setting 1 cc/hr per g as a minimum rate which had to be attained by the animals, which weighed 27.5 + 1.6g. Mean oxygen consumption rates for 15 reentries into hibernation by 10 Z. princeps (right panel). The oxygen consumption data were synchronized by using the last 20 min of the normothermic phase as a starting point. Dots represent means, thin vertical bar one standard deviation on either side of the mean. The inset in the upper right of the figure shows the 140-560 min segment with the vertical axis expanded.

between temperature-induced arousals and spontaneous arousals showed that in spontaneous arousals Phase I involved active heat generation, while induced arousals were characterized by passive heat accumulation which must subsequently trigger the arousal and transition to Phase II. Significant differences between anal and oral temperature increase rates have been reported in the birch mouse, Sicista hetulina (Zapodidae) by Johansen & Krog (1959) who attributed it to vasoconstriction in the abdominal region. Bullard & Funkhouser (1962) estimated regional blood flow using rubidium 86 in Citellus tridecemalineatus. and correlated the oral-anal rewarming rate difference with abdominal vasoconstriction during arousal from hibernation. Two observations support the hypothesis of abdominal vasoconstriction in Z. princeps. First, during hibernation their feet were generally reddish in color and remained red during arousals. However, when the oral body temperature reached 8810°C the rear feet became blue to black in color. Secondly, a shivering response was seen in the forelimbs and shoulders throughout the arousal, but the rear limbs and rump only began to shiver when the oral temperature exceeded 20-24°C. During arousal, heart rates increased from 14 beats/ min to 560 beats/min within 40-45 min and remained above the normothermic level for 7-10 min. Ambid & Agid (1967) observed that the European garden dormouse, Eliomys quercinus (Gliridae) became hyperglycemic during the early part of arousal. which they attributed to increased adrenalin secretion. Pajunen (1970) recorded higher than normal heart rates in E.

quercinus early in arousal, with a subsequent return to normothermic levels. Similar observations in both E. quercinus and Z. princeps could be attributed to adrenalin secretion causing both increased heart rates and hyperglycemic conditions. Oxygen consumption for Z. princeps at a TA of 30°C was 1.95 cc/hr per g, which is between the values reported by Morrison & Ryser (1962) of 1.5 cc/hr per g for fat Z. hudsonius and 2,4cc/hr per g for starved individuals. Pearson (1947) and Brower & Cade (1966) reported minimum oxygen consumption of 1.8 cc/hr per g and 2.4 cc/hr per g, respectively, for the woodland jumping mouse, N. insignis under similar conditions. Oxygen consumption for Z. princeps during hibernation at 4.5”C was 0.042 cc/hr per g during the first 90 days of hibernation which was similar to Z. hudsonius (Muchlinski & Rybak, 1978) and 0.024 cc/hr per g during the later phase. During arousal, oxygen consumption increased from 0.024 cc/hr per g to a peak of 9910.5 cc/hr per g then dropped to 5 cc/hr per g during the normothermic phase prior to reentrance into hibernation. Morrison & Ryser (1962) determined average oxygen consumption of hibernating Z. hudsonius at a TA of 10°C to be 0.04 cc/hr per g, which increased to 5 cc/hr per g when the animals terminated a hibernation bout. They showed peak levels slightly above 8 cc/hr per g, while Z. princeps had a mean maximum of 9.7 cc/hr per g. Differences were probably due to the difference in ambient temperatures (10.0 vs 4.5”C in this study). Short-term high rates of oxygen consumption during emergence of Z. princeps were coincident with peak heart rates, and were observed in the phase when body temperature

Hibernation physiolclgy of was increasing at l”C/min. Body temperature increase during arousal lagged behind the increases in heart rate and 0, consumption. During reentrance into hibernation both heart rate and O2 consumption decreased quite rapidly while body temperature decreased very slowly. Animals which are fully prepared for hibernation entered with 68% of their dry body weight as fat, which is equivalent to 12-14 g of fat (Cranford, 1978). The metabolism of these fats would yield approx 9.5 kcal/g and would require approx 2020~~ of 0,/g, resulting in the production of slightly more than 1 g of water per gram of fat. Z. princeps hibernating in the laboratory at 4S”C for 295 days emerged from hibernation with slightly more than 1 g of fat remaining (Cranford. 1977). During the first phase of hibernation (O-90 days) animals utilized an average of 746 cc of O2 during each arousal. In the second phase (9&295 days) animals consumed an average of 619 cc of O2 during each arousal. This resulted in a total consumption of 12,304~~ of O2 for all arousals. The average total consumption by an animal during deep hibernation was 2599 cc of O2 for the CL90 day period, and 3032 cc of O2 for the subsequent period (90-295 days). The total average consumption (for both arousals and hibernation) over the complete 295-day hibernation cycle was 18.020~~ of oxygen. This would result in the metabolic conversion of 8.97 g of fat during a hibernation season. The observed fat loss for animals in hibernation for 295 days ranged from 9.5 to 11.1 g (Cranford. 1978). The calculated values very closely approximate the observed fat losses by animals in hibernation in the laboratory. The cost of the 8.1 days spent in periodic arousals represented 69;:, of the total energy utilized during the hibernation season, The remaining 31’:” was utilized during the 286 days spent in deep hibernation. If the animal remained normothermic at a TA of 30°C consuming 2.0ccjhr per g of Oz. the same 8.97g of fat would be utilized in 14 days, which points out the extremely conservative nature of hibernation.

Acknowledgrmrnts~

Biology at Virginia

1 want to thank the Departments of Polytechnic Institute and State Univer-

Zapus

princeps

599

sity and the University of Utah various phases of this research.

for their

support

during

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59, 435-437.

MORRISON P. & RYSER F. A. (1962) Metabolism and body temperature in a small hibernator. the meadow jumping mouse. Zapus hudsonius. J. Cell. Physiol. 60, 169-180. PAJUNEN I. (1970) Body temperature, heart rate, breathing pattern. weight loss and periodicity of hibernation in the Finnish garden dormouse (Eliornyc quercirms L.) At~nls Zool. Fewz. 7, 251-266. PEARSON 0. P. (1947) The rate of metabolism of some small mammals. Ecology 28, 127-145. WATERS J. H. & S~OCKLEY B. H. (1965) Hibernatmg meadow jumping mouse on Nantucket Island. Massachusetts. J. Mumm. 46, 67-76. WHITAKER J. 0. (1972) Zapus hudsonius. Mammalian species note No. 11, pp. I-7. American Society of Mammalogists. WHITAKER J. 0. & WK~GLEY R. E. (1972) jVapeo;ap~ts Mammalian species note No. 14. pp. I-6. insignis. American Society of Mammalogists.