We measured the breathing pattern and oxygen consumption of hibernating little brown bats (Myotis lucifugus) in open-and closed-circuit metabolic chambers. At 5 °C, hibernating M. lucifugus showed bouts of ventilation lasting on average 1.24 min and separated by periods of apnea lasting on average 47.59 min. The bats consumed 0.014 ml O2g−1 during ventilation bouts and 0.002 ml g−1 during apnea. The total O2 uptake was 0.016 ml g−1 for a complete ventilationapnea cycle, giving a of 0.020 ml g−1 h−1. This value is considerably lower than most values previously published for Myotis spp. and we suggest that studies using open-circuit systems that did not account for the intermittent nature of gas exchange during hibernation may be in error. Based on the dimensions of the respiratory tract, we estimate that 0.026 ml O2 g−1 h−1 and 0.009ml CO2g−1 h−1 could diffuse down the tract if the glottis was open. The low O2 uptake during apnea indicates that the glottis was closed. If CO2 retention acts to depress metabolism in hibernators, a closed glottis and arrhythmic breathing may be adaptive strategies in hibernation.

Hibernation and torpor in mammals are characterized by a depression of body temperature accompanied by a sizeable reduction in metabolic rate. For example, reported oxygen consumption rates for hibernating Tamias striatus, Zapus princeps and Myotis lucifugus are only 5.8 %, 1.2 % and 1.5 % of their respective normothermic resting rates at or near thermoneutrality (Hock, 1951; Wang and Hudson, 1971; Cranford, 1983). The reduction in metabolic rate proportionally reduces the requirements for respiratory gas exchange in torpid or hibernating animals and also appears to cause an alteration in their breathing pattern. Many species exhibit bouts of pulmonary ventilation separated by periods of apnea which may either be short (about 5 min) or extend to over 130min (see Lyman, 1982; Malan, 1982).

Whether intermittent ventilation is characterized by a single breath followed by a short bout of apnea or a series of breaths followed by a protracted period of apnea, respiratory gas exchange is clearly not constant. Uptake and clearing of O2 and CO2, respectively, could be expected to be rapid during bouts of active ventilation and greatly reduced during apnea. It is possible, however, that gas exchange continues at a low rate during apnea if the respiratory passages remain open. Observations of pressure fluctuations associated with heartbeats on plethys-mograph recordings of hibernating marmots (Malan, 1973) suggest that the glottis may be open, thus providing a free path for gas diffusion into and from the lungs. Based on estimates of the dimensions of the trachea in the European hedgehog (Erinaceus europaeus) and on the diffusion rates of gases, Malan (1982) estimated that diffusion of O2 and bulk movements of air into the lungs during a 1 h apnea could theoretically account for 40.4% of the total measured O2 uptake in hibernation. This suggests that active ventilation and passive diffusion may both be important components of gas exchange in hibernators. However, we are aware of no studies that have partitioned O2 uptake between these two processes.

The purposes of this study were to measure the pattern of ventilation and apnea shown by hibernating little brown bats (M. lucifugus) and to partition the O2 uptake between bouts of ventilation and apnea.

Hibernating M. lucifugus were collected from a disused mine in Windsor County, Quebec, in February and November, 1988, and November and January, 1989. They were stored in a refrigerator at 4°C and above 95 % relative humidity prior to the experiments.

O2 uptake during ventilation bouts

We used an open-circuit system to follow the ventilation-apnea breathing pattern and to measure the total O2 uptake during ventilation bouts. For each test, we removed a single bat from the hibernation refrigerator, weighed it (±0.01 g) and placed it in a 240 ml acrylic metabolic chamber. We positioned a copper-constantan thermocouple near to or touching the bat and placed a magnetic stirring rod fitted with 1 cm long paper wings in the bottom of the chamber. We closed the chamber and placed it on a thin foam insulating pad on a magnetic stirring plate in a constant-temperature cabinet (5±1°C). Humid air was passed through the chamber (100 ml min−1) for at least 12 h prior to initiating any measurements. During this period, the decline in chamber temperature (Ta) to about 5 °C indicated that all individuals re-entered hibernation. Although we were unable to maintain rectal temperature probes in our study bats, we verified that body temperatures (Tb) approximately equalled Ta by taking continuous rectal temperatures on a separate group of restrained bats. In all cases (N=13), Tb fell to within 0.5°C of Ta within 12 h. After 12 h, the stirring plate was turned on to rotate the magnetic rod at about 150 revs min−1 to mix the chamber gases despite the low flow rates. We then passed dry, CO2-free air through the chamber at a rate of 62 ml min−1, controlled by a Matheson high-precision flow meter. We had previously calibrated the flow meter to ± 1 % accuracy using a computerized system similar to that described in Bartholomew and Lighton (1986) based on Levy (1964). We passed the outflow gases from the metabolic chamber through a 10 ml syringe barrel filled with Ascarite and Drierite to remove CO2 and H2O, respectively, and drew a subsample (30 ml min−1) through the O2 cell of an Applied Electrochemistry S-3A O2 analyzer. Output from the S-3A and the thermocouple were read and stored at 3 s intervals by a microcomputer driven by a data-gathering software package (DATACAN; Sable Systems Inc., 1015 Gayley Ave, Los Angeles, CA). We calibrated the O2 analyzer at the start and end of each experiment by passing dry, CO2-free air through the O2 cell. We also determined the effective volume (sensuBartholomew et al. 1981) of the metabolic chamber by injecting a bolus of nitrogen into the chamber and calculating the time constant. The calculated effective volume was 303±8 ml.

Because of the relatively long time constant of our open-circuit system (about 13 min to 95 % of baseline at a flow of 62 ml min−1), the curves of O2 depletion do not accurately show the duration of ventilation bouts (Fig. 1A, B). We thus transformed the O2 depletion curves into instantaneous . curves following equation 3 of Bartholomew et al. (1981). This corrected for the washout distortions and showed ventilation bouts as short, high-amplitude peaks lasting no more than 2.5 min (Fig. 1C). We measured the duration of ventilation bouts from these peaks. The duration of ventilation bouts measured in this fashion corresponded closely with the periods of high-amplitude breathing that we observed in a head–body plethysmograph (Cloutier, 1989). The plethysmograph studies provided an independent verification that the instantaneous corrections accurately portrayed ventilation bouts. We did not use the instantaneous curves to estimate the O2 uptake because we suspected imperfect mixing of the chamber gases. We thus calculated the O2 uptake during the ventilation bout by integrating the area under the conventional curve, calculated using equation 8 of Depocas and Hart (1957).

Fig. 1.

(A) The pattern of O2 depletion in the outflow of the open-circuit metabolic chamber containing a hibernating Myotis lucifugus at 5 °C. Depletion is measured in O2% below 20.95 %. Note the exponential return to about 0% depletion typical of a washout curve. (B) V˙O2 calculated for the same bat using the conventional method of Depocas and Hart (1957) and O2 depletion data in A. The horizontal bar shows the section of the curve integrated to calculate total O2 uptake during a ventilation bout. (C) Instantaneous I’d, calculated from O2 depletion data in A. The horizontal bar indicates the duration of a ventilation bout. Note that the duration of a ventilation bout is not distorted by the washout period as it is in B. Calculations of instantaneous V˙O2 are sensitive to signal noise, giving rise to the minor peaks smaller than 0.1 mlg−1 h−1. (D) The step change in O2 depletion of a closed-circuit metabolic chamber typical of a single ventilation bout.

Fig. 1.

(A) The pattern of O2 depletion in the outflow of the open-circuit metabolic chamber containing a hibernating Myotis lucifugus at 5 °C. Depletion is measured in O2% below 20.95 %. Note the exponential return to about 0% depletion typical of a washout curve. (B) V˙O2 calculated for the same bat using the conventional method of Depocas and Hart (1957) and O2 depletion data in A. The horizontal bar shows the section of the curve integrated to calculate total O2 uptake during a ventilation bout. (C) Instantaneous I’d, calculated from O2 depletion data in A. The horizontal bar indicates the duration of a ventilation bout. Note that the duration of a ventilation bout is not distorted by the washout period as it is in B. Calculations of instantaneous V˙O2 are sensitive to signal noise, giving rise to the minor peaks smaller than 0.1 mlg−1 h−1. (D) The step change in O2 depletion of a closed-circuit metabolic chamber typical of a single ventilation bout.

O2 uptake during apnea

We used a closed-circuit system to measure the low rate of O2 uptake during periods of apnea. For each test, we weighed a bat (±0.01 g), placed it in a 240 ml acrylic chamber with a 2 g screen bag of Ascarite in the bottom and positioned a thermocouple close to the bat. We placed the chamber in a constant-temperature cabinet and passed humid air (100 ml min−1) through the system for at least 12 h to allow the bat to enter hibernation. We then re-arranged the tubing such that a peristaltic pump circulated the chamber air through a small, in-line container of Drierite, through the O2 cell, and back into the chamber. All tubes were 3.2mm i.d. Tygon tubing to minimize the volume of gas outside the chamber. Gas flow through the circuit was 10 ml min−1. This created a closed-circuit system which included the O2 cell and permitted continuous measurements of the fractional O2 concentration and Ta by the microcomputer. We measured the volume of the chamber and attached tubes by filling them with water and we calculated the functional volume by subtracting the displacement of the absorbents and bat. Functional volumes were 256–261 ml at STP.

O2 uptake during apnea resulted in a slow but steady depletion of the fractional O2 concentration in the chamber over measurement periods of about 45 min. The low rate of change made the O2 curves particularly sensitive to slight signal drifts. We measured the drift in the system without a bat in place (10 measures of 45 min) and corrected the O2 depletion curves by the mean drift. We calculated O2 uptake from the rate of O2 depletion and the functional volumes.

Bats were left in the closed-circuit system for 1–2 h only. During this period, the fractional O2 concentration never declined below 0.209, so animals did not experience hypoxia.

Respiratory tract measurements

To allow us to calculate the potential for diffusion of O2 and CO2 down the trachea and primary bronchi, assuming that the glottis was open during apnea, we dissected the respiratory tracts from three bats preserved in 10 % formalin for 1 week. We removed the glottis, trachea, primary bronchi and lungs intact. Under a dissecting microscope, we measured: (1) the total distance from the glottis to the point of entry of the primary bronchi into the lungs, (2) the internal diameter of the trachea at three points between the glottis and the origin of the two primary bronchi, and (3) the internal diameter of the two primary bronchi at their origin and at the lung hilus.

Data analysis

All gas volumes were corrected to STP. Data are presented as mean±s.E. Statistics were performed using Systat (Systat Inc., 2902 Central St, Evanston, IL).

Respiratory tract dimensions

Table 1 shows the mean dimensions of the trachea and primary bronchi for the three bats. The mean diameters of the trachea and primary bronchi were 0.83 mm and 0.56 mm, respectively. The latter tubes tended to collapse, so their measurements are less reliable. The mean cross-sectional area of the trachea was 0.54 mm2 and that of the two primary bronchi together was 0.49 mm2, indicating a somewhat uniform cross-sectional area through the tract. We took 0.54 mm2 as the crosssectional area for diffusion calculations.

Table 1.

Measurements of internal diameters and lengths of respiratory tracts from three Myotis lucifugus

Measurements of internal diameters and lengths of respiratory tracts from three Myotis lucifugus
Measurements of internal diameters and lengths of respiratory tracts from three Myotis lucifugus

Breathing pattern and O2 uptake during ventilation bouts

In the flow-through system, we observed and measured 87 ventilation bouts for 11 different M. lucifugus (mass 5.9–6.7g; Table 2). Computer failures prevented us from measuring the duration of pre-or post-ventilation apneas in 16 cases, leaving us with full data on 71 bouts of ventilation and apnea.

Table 2.

Measurements of respiratory parameters for hibernating Myotis lucifugus

Measurements of respiratory parameters for hibernating Myotis lucifugus
Measurements of respiratory parameters for hibernating Myotis lucifugus

The mean duration of ventilation bouts was 1.24±0.05 min (range 0.10–2.50 min). During this period, each bat absorbed 0.087±0.004 mlO2 or 0.014±0.001 ml O2g−1. The amount of O2 absorbed during a ventilation bout was correlated with the duration of the bout (r=0.689; df = 1, 96; P<0.001). The slope of the regression of O2 uptake per gram against bout duration gives the rate of O2 absorption as 0.009±0.0009 mlg−1min−1 (Fig. 2), which is only marginally less than the mean rate of uptake per ventilation bout (0.014/1.24=0.011 ml g−1 min−1).

Fig. 2.

The relationship between oxygen uptake and the duration of ventilation bouts for hibernating Myotis lucifugus.

Fig. 2.

The relationship between oxygen uptake and the duration of ventilation bouts for hibernating Myotis lucifugus.

In the closed system, we observed a total of seven ventilation bouts for three bats (mass 6.1–7.2 g). Each ventilation bout appeared as a step in the O2 depletion curve (Fig. ID). The O2 uptake during the ventilation bouts, calculated from the fractional O2 concentrations at the start and end of each step and the chamber volume, was 0.081 ±0.007 ml bat−1. This O2 uptake did not differ significantly from that observed in the open-circuit system (t=0.75; df=l; P=0.46) and provided an independent verification of the accuracy of our O2 uptake measurements in the open-circuit system.

The period of apnea following ventilation bouts lasted 47.59±2.64 min (range 13–128 min). Thus, a complete ventilation-apnea cycle lasted 48.83 min.

There was a weak yet significant correlation between the duration of two successive apneas (r=0.29; df=l, 78, P=0.02), but the length of the preceding apnea explained only 8.6 % of the variance in the succeeding apnea. There was not significant correlation between the duration of a ventilation bout and the length of the preceding apnea (r=0.046; df=l, 78, P=0.69). The duration of apnea was significantly related to the amount of O2 stored during the preceding ventilation bout (r=0.240; df=l, 78; P=0.032); however, O2 stores explained only 5.8% of the variance in the duration of apnea.

O2 uptake during apnea

We measured O2 uptake during apnea for 10 M. lucifugus (mass 6.08–6.67 g). The mean rate of O2 uptake during bouts of apnea was 0.023 ±0.002 ml bat−1h−1 (range 0.015–0.029 ml bat−1 h−1) or 0.003 ±0.0003 mlg−1 h−1 (range 0.002–0.004 ml bat−1 h−1). Thus, during average bouts of apnea lasting 47.59 min, bats consumed a total of 0.002 ml O2g−1.

Respiratory pattern and O2 uptake

With bouts of ventilation and apnea lasting 1.24 min and 47.59 min, respectively, M. lucifugus hibernating at 5 °C shows a clear pattern of intermittent or arrhythmic breathing and a respiratory duty cycle of only 2.5 %. Similar respiratory patterns and duty cycles have been indicated for at least eight species of rodents (Geiser and Kenagy, 1988; Goodrich, 1973; Kristoffersson and Soivio, 1966; Lyman, 1951, 1982; Pajunen, 1970; Pembrey and Pitts, 1899; Twente et al. 1970; Withers, 1977) and two species of insectivores (Chao and Yeh, 1950; Kristoffersson and Soivio, 1964), but have not previously been documented in bats. Arrhythmic breathing thus appears to occur in the three major taxa of hibernating mammals.

The factors that generate and control the pattern of arrhythmic breathing in hibernating mammals are poorly understood. Chemoreceptors measuring lung or arterial and are implicated along with lung mechanoreceptors in the control of the duration of apnea, but interactions between them cause high variability in the respiratory pattern (see Milsom, 1988; Shelton and Croghan, 1988, for reviews of arrhythmic breathing). Tahti (1978; in Malan, 1982) suggested that arterial or lung was the major chemical parameter controlling the respiratory pattern. The weak correlations between O2 uptake and the durations of preceding or succeeding apneas in hibernating M. lucifugus support the view that rather than controls the breathing rhythm. However, the weak correlation between the durations of successive apneas is difficult to reconcile with a breathing pattern generated by a steady accumulation of CO2 in the blood finally triggering breathing at some threshold value. This suggests either that CO2 production is not constant (see Malan, 1982) or that other factors interact with to determine the length of apnea (Milsom, 1988).

During ventilation bouts lasting 1.24min, bats consumed 0.087 ml of O2. A parallel study of the respiratory parameters of M. lucifugus in a head-body plethysmograph indicated that hibernating bats breathe at a rate of 0.73 breaths s−1 (Cloutier, 1989). An average ventilation bout thus contained 54.3 breaths and with each breath a bat absorbed 1.6 μl of O2. If bats have an assimilation efficiency of 16% (Thomas, 1981), they would move 10 μl of O2 and 48 μl of air into the lungs with each breath. This tidal volume of 48 μl is 46 % higher than that predicted by allometric equations for a mammal of 6.5 g (Stahl, 1967), but agrees well with the resting tidal volume of the bat Pteropus gouldii (66 % greater than predicted; Thomas, 1981).

Our data show that there is measurable O2 uptake both during bouts of active ventilation and during the intervening periods of apnea. With O2 uptakes of 0.014 ml g− 1 and 0.002 ml g− 1 for typical bouts of ventilation and apnea, respectively, the total O2 uptake over a complete ventilation-apnea cycle is 0.016 ml g− 1. Ventilation and apnea account for 87.5% and 12.5%, respectively, of this total. This uptake of 0.016 ml O2g− 1 during the 48.83 min ventilation-apnea cycle equates to a of 0.020 ml g− 1 h− 1 at 5 °C. This is similar to that measured by Hock (1951; 0.03 ml g− 1 h− 1) for M. lucifugus in a Scholander-type (closed-circuit) gas apparatus, but is substantially lower than other measurements using opencircuit systems. Henshaw (1968; his Fig. 27) showed CO2 production values for M. lucifugus of 0.07 ml g −1 h−1 at 5°C. Assuming a respiratory quotient (RQ) of 0.7, this represents 0.1 mlO2g−1h−1, a value 500% higher than this study. Similarly, Riedesel and Williams (1976) measured the minimum for M-velifer as 0.07mlg-1h-1 or 350% higher than our value for M. lucifugus. The extreme variation in at any one temperature (e.g. about 1000%; Table 1 in Riedesel and Williams, 1976) is consistent with the high-amplitude variations that would be produced by measuring for only brief periods (12 min in their study) during the long ventilation–apnea cycle and suggests that the sampling period was too short to measure adequately of bats in hibernation.

Measuring the °f hibernating animals that exhibit arrhythmic breathing is problematical in open-circuit systems. When respiratory gas exchange is episodic (as in M. lucifugus where 87.5 % of the exchange occurs in 2.5 % of the time) the mixing of gases in open-circuit metabolic chambers is too slow to permit them to achieve the steady-state or equilibrium conditions required for the calculation of by conventional methods (equation 8 of Depocas and Hart, 1957). Under conditions of intermittent ventilation or where metabolic rates change rapidly, the difference between the fractional concentrations of a respiratory gas such as O2 in the influx and efflux of a metabolic chamber is not directly proportional to at any instant. Since this proportionality is a fundamental assumption, conventional methods for calculating then become invalid (Depocas and Hart, 1957; Bartholomew et al. 1981). Under these conditions, three alternative methods are appropriate for measuring in open-circuit systems. The confounding effects of the washout distortion caused by a long metabolic chamber time constant can be removed by calculating the instantaneous (Bartholomew et al. 1981). The average can be calculated by integrating under the conventional curve over periods greatly exceeding the ventilation–apnea cycle (e.g. Geiser and Kenagy, 1988). Or the ventilation-apnea cycle can be split up and O2 uptakes measured for each of the components (this study). Any of these procedures, however, requires prior knowledge that steady-state conditions have been violated by arrhythmic breathing. Both Henshaw (1968; p. 81) and Riedesel and Williams (1976) assumed that steady-state conditions prevailed in their metabolic chambers and this apparently resulted in their high estimates. Because arrhythmic breathing appears to be common in hibernating animals, this problem may be widespread.

Respiratory gas exchange during apnea

Our data show that there is a measureable but low O2 uptake during periods of apnea. The mean uptake of 0.002 ml O2 g−1 during the apnea phase of a complete ventilation-apnea cycle represents only 12.5% of the total. This is considerably less than the value of 40.4% of the total O2 uptake that Malan estimated might diffuse down the respiratory tract during the periods of apnea exhibited by hibernating E. europaeus if the glottis was open (Malan, 1982). This places in question whether M. lucifugus kept the glottis open during periods of apnea.

Two lines of evidence argue that the glottis was closed or nearly so. First, based on the dimensions of the respiratory tract, a diffusion coefficient of 0.0178 cm2 s−1 (Weast, 1979) and a differential of 13.3 kPa between the lungs and atmosphere (Malan, 1982), the maximum theoretical diffusion of O2 into the lungs is 0.051 ml g−1 h−1 for a 6.5g bat. This is certainly an overestimate of the potential for diffusion, because no allowance was made for the resistance offered by the mouth or nasal passages. However, even assuming that the real diffusion rate is only 50% of our estimate (e.g. 0.026 mlg−1h−1), measurements of O2 uptake during apnea (0.003 ml g−1h−1) are clearly only a fraction (11.5%) of that expected were the glottis to remain open. Second, if the glottis remained open during periods of apnea, the diffusion rate (even by the conservative estimate of 0.026 ml g−1 h−1) would be sufficient to cover the O2 requirements of a bat (0.020 mlg−1 h−1). In this case, the blood would remain continuously saturated and we would observe no marked increase in O2 uptake during a ventilation bout. With 87.5 % of the O2 uptake occurring during ventilation bouts, this was clearly not the case. These data argue that the glottis was closed during apnea. The observed low O2 uptake may possibly be due to cutaneous absorption.

Why do bats not keep the glottis open and exploit gas diffusion? Assuming a differential of 5.3kPa between the lungs and the atmosphere (alveolar ; atmospheric ; Weibel, 1984) and a diffusion coefficient of 0.139 cm2s−1 (Weast, 1979), an open glottis would permit the diffusion of 0.009–0.017 ml CO2g−1 h−1 out of the lungs. With an RQ of 0.7 and a of 0.020 mlg−1h−1 (this study), bats produce only 0.014ml CO2g−1h−1. Diffusion could thus cover 64–100 % of requirements for voiding CO2 to the atmosphere and so would reduce the breathing frequency by at least 50%. If breathing is energetically costly and arrhythmic breathing is, in part, an adaptive strategy to minimize ventilation costs (Milsom, 1988), permitting diffusion through an open glottis would seem adaptive. However, a closed glottis necessarily leads to CO2 retention and respiratory acidosis which have been suggested to act as metabolic depressants in both diving and hibernating animals (see Hochachka and Guppy, 1987; Malan, 1982). By keeping the glottis closed during apnea, bats may be actively depressing metabolism and thus their energy requirements for hibernation.

This study was funded by NSERC and FCAR operating grants to DWT and an FCAR scholarship to DC. We thank Marc Gauthier and several anonymous reviewers for valuable suggestions during the development of this paper. This is publication no. 65 of the Groupe de Recherche en Energie, Nutrition, et Ecologie.

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