energy requirements of freely diving muskrats ( ondatra zibethicus )

Energy requirements of freely diving muskrats (Ondatra zibethicus)

ROBERT A. MACARTHUR AND ROBERT E. KRAUSE Department of Zoology, University of Manitoba, Winnipeg, Man., Canada R3T 2N2

Received September 19, 1988

MACARTHUR, R. A., and KRAUSE, R. E. 1989. Energy requirements of freely diving muskrats (Ondatra zibethicus). Can. J. Zool. 67: 2194-2200.

The metabolic costs of spontaneous diving in the muskrat were estimated from measurements of oxygen consumption (vo,), using a purpose-built open-circuit respirometer. Total Vo, value was measured over a 15-min immersion period in 30°C water and related to the frequency and duration of voluntary dives during that period. The correspondence between Vo, and diving behavior varied with the level of motor activity during interdive periods at the surface. There was no relationship between these variables in runs characterized by appreciable surface swimming in the respirometer. When surface activity was negligible, Vo, was positively correlated (P < 0.001) with both the frequency of dives and the proportion of time spent underwater. For trials in which muskrats spent > 50% of available time diving, the estimated cost of voluntary submergence was 2.22 mL 0, . ggl . hgl, or 2.8 times the mean thermoneutral rate in air (0.78 mL . g-I . h-I). Our results suggest that underwater exercise is accompanied by an increase in energy expenditure which approaches that of surface swimming in this species.

MACARTHUR, R. A., et KRAUSE, R. E. 1989. Energy requirements of freely diving muskrats (Ondatra zibethicus). Can. J. Zool. 67 : 2194-2200.

La mesure de la consommation d'oxygkne (vo,) au moyen d'un respiromktre spCcial h circuit ouvert a permis d'estimer les coats mCtaboliques reliCs h la plongCe volontaire chez le Rat musquC. La consommation d70xygkne a CtC mesurCe au cours d'une pCriode d'immersion de 15 min dans de l'eau B 30°C et confrontCe hala frCquence et h la durCe des plongCes volontaires au cours de cette pCriode. La correspondance entre la consommation Vo, et le comportement de plongCe variait selon 1'intensitC de 1'activitC motrice en surface entre les plongCes. Ces variables n'Ctaient pas relikes au cours des essais caractC- risks par une activitC de surface trks intense dans le respiromktre. Lorsque 1'activitC en surface Ctait negligeable, la valeur de Vo, Ctait en correlation positive (P < 0,001) avec deux facteurs, la frCquence des plongCes et la proportion du temps passe sous l'eau. Au cours des expCriences ou les animaux ont pass6 plus de 50% de leur temps disponible en plongCe, le coat estimC de la submersion volontaire a CtC Ctabli B 2,22 mL 0: . g-I - h-I, ou 2,8 fois le taux thermoneutre moyen dans l'air (0,78 mL . gg ' . h-I). Nos rCsultats indiquent que l'exercice sous l'eau s'accompagne d'une augmentation de la dCpense CnergCtique voisine de celle qui est reliCe B la nage en surface chez cette espkce.

[Traduit par la revue]

Introduction Physiologists have long been aware that forcible sub-

mergence of aquatic vertebrates evokes a marked increase in peripheral resistance and a concomitant decline in cardiac output. Perfusion of hypoxia-sensitive tissues such as brain and heart is maintained at the expense of circulation to muscle, gut, liver, kidneys, and skin (Butler and Jones 1982). A logical corollary of these vascular changes is a fall in metabolic rate, and several lines of evidence suggest that a state of hypo- metabolism prevails in forced dives. These include a fall in core temperature that occurs despite increased tissue insula- tion, and an exceptionally low postdive oxygen debt. Past studies have shown that the postdive oxygen debt usually fails to account for the oxygen deficit incurred during forced dives, assuming that the predive resting metabolic rate (RMR) is sus- tained during submergence (see Scholander 1964; Butler and Jones 1982).

Recent evidence suggests that the freely diving animal presents a more complicated picture, in which cardiovascular and metabolic adjustments reflect a compromise between the conflicting demands of aerobic exercise and the need to ration oxygen for underwater endurance (Millard et al. 1973; Butler 1982; Castellini et al. 1985; Guppy et al. 1986). Conse- quently, the profound cardiovascular changes typical of classical laboratory dives may be attenuated or even absent in voluntary dives (Butler 1982; Jones 1987), and much con- troversy currently surrounds the metabolic status of freely diving endotherms (Castellini et al. 1985). The cost of spontaneous diving has been estimated at 1-3.5 times RMR in several endothermic divers, including the tufted duck, Aythya

fuligula (Woakes and Butler 1983), the Humboldt penguin, Spheniscus humboldti (Butler and Woakes 1984), the little penguin, Eudyptula minor (Baudinette and Gill 1985), and the harbour seal, Phoca vitulina (Craig and Pische 1980). By con- trast, respiratory studies of the Weddell seal, Leptonychotes weddelli (Kooyman et al. 1973), suggest that metabolic rate is slightly reduced during underwater activity. A depressed metabolic state in freely diving Weddell seals has also been inferred from clearance kinetics of labelled metabolites and from rates of depletion of body oxygen stores (Guppy et al. 1986).

We are thus confronted with a spectrum of physiological responses to voluntary diving in birds and mammals. Meta- bolic profile studies of freely diving grey seals, Halichoerus grypus (Castellini et al. 1985), and Weddell seals (Guppy et al. 1986) tend to support the conventional view of a reduced cardiac output and redistributed vascular bed during submergence. Other divers, including the tufted duck, display modest changes in cardiac function and diving metabolic rates which are typical of strenuous surface swimming. Especially intriguing are those species that routinely engage in vigorous underwater activities, yet appear to exhibit qualitatively similar cardiovascular adjustments in free and restrained dives (Castellini et al. 1985; MacArthur and Karpan 1989). Is the reduced cardiac output and peripheral blood flow in these divers matched by a commensurate reduction in metabolic heat production, or do they achieve diving metabolic rates compa- rable with those developed during surface swimming? In other words, to what extent do the metabolic demands of working skeletal muscles compensate for the reduced metabolism of the

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MACARTHUR AND KRAUSE 2195

heart and hypoperfused tissues such as the skin and abdominal organs?

An ideal model for investigating such questions is the semi- aquatic muskrat, Ondatra zibethicus. Muskrats display the classical cardiovascular responses to forced submersion, with a pronounced, rapidly deployed bradycardia accompanying both forced and voluntary dives (Drummond and Jones 1979; Jones et al . 1982; MacArthur and Karpan 1989). However, little is known of the metabolic demands of diving in this species, and the existing data appear contradictory. The dra- matic fall in heart rate coupled with a high rate of body cooling in unrestrained dives (MacArthur 1984) implies a depressed metabolic state. Yet the postdive oxygen debt of unrestrained muskrats is considerably greater than the predicted value, based on the assumption that the predive RMR is maintained during submergence (Fairbanks and Kilgore 1978; MacArthur 1984). Though this observation suggests that diving is meta- bolically taxing to 0. zibethicus, it was not possible in these earlier investigations to separate the cost of diving from those of postimmersion grooming and rewarming.

Our objective in this study was first to resolve the direction of change in metabolic rate of freely diving muskrats. A second, more challenging goal was to estimate the cost of underwater activity in this species. Most previous estimates of diving costs have been based on respiratory studies of spon- taneously diving birds and mammals, in which it is operation- ally difficult to partition the energy demands of surface and diving activities (Craig and Pische 1980; Baudinette and Gill 1985; Stephenson et al . 1988). Thus, with few exceptions (i.e., Woakes and Butler 1983), measured metabolic rates usually reflect a composite of both surface and diving activities. In the present study, experiments were designed in which thermoregulatory stress and postdive grooming activity were avoided, and in which it was possible to correlate aquatic energy expenditure with the proportion of time spent diving.

Materials and methods Animals

A total of 10 adult muskrats (8 males, 2 females) were used in this study, ranging in weight from 704 to 1295 g (mean + SE = 1001 + 9.60 g). Muskrats were livetrapped during late June in Oak Hammock marsh near Winnipeg, Manitoba, and transported to the University of Manitoba. There, animals were held in a walk-in envi- ronmental chamber kept at 14 f 1°C, with a photoperiod of 12 h light : 12 h dark, as described by MacArthur (1979).

Respirometry Diving trials were performed in a fibreglass-lined rectangular ply-

wood tank (2 10.5 x 12 1.5 x 60 cm) housed in a controlled-environ- ment room. The tank was filled to a depth of 32 cm with 29-30°C water. At this water temperature, muskrats are under minimal thermal stress and exhibit strongest diving activity (MacArthur 1984). A screen-covered aluminum frame mounted just beneath the water surface prevented diving muskrats from surfacing at any point in the tank other than the respiratory chamber. The latter consisted of a 20.5-L Plexiglas box fastened to the submerged frame (Fig. 1). Room air was drawn into the chamber via a series of small holes bored in an 18-cm length of copper tubing mounted on an inside wall near water level, and exited via an exhaust port in the chamber ceiling. To stan- dardize measurements and permit comparisons of metabolic rates during different levels of diving activity, it was desirable to measure the total oxygen consumed over a constant period of immersion. This was achieved by incorporating a plunger assembly into the respiratory chamber, which enabled the investigator to remove the animal from the respirometer after precisely 15 min of immersion, without

interrupting gas analysis. The plunger assembly consisted of a handle and two steel push-rods (0.7 cm diameter) which entered the top of the chamber and attached to a perforated, 1.2 cm thick Plexiglas plate. This plate remained secured near the ceiling of the chamber except upon completion of a run, when it was gently lowered to evict the animal. To prevent air from being drawn into the top of the respirometer, the greased push-rods passed through tight-fitting rubber O-rings mounted in thick Plexiglas supports (Fig. 1). Rapid mixing of gas was facilitated by an electric fan installed in the chamber ceiling. The fan shaft (0.6 cm diameter) entered the respirometer via an airtight Teflon bearing mounted in a rubber stopper.

Exhaust gas from the chamber was drawn by vacuum through water and CO, absorbents (drierite and soda lime, respectively), and then through a calibrated Fisher Lab-Crest rotameter at a rate of 8.5 L . min-I. Fractional 0, content of the dried, C0,-free exhaust gas was continuously monitored by routing a sample of the gas through an Applied Electrochemistry S-3A oxygen analyzer equipped with a model N-22M sensor and connected to a strip-chart recorder (Fisher Recordall 5000). A representative 0, tracing for a 15-min run is presented in Fig. 1. Following removal of the animal from the chamber, the fractional 0, content of exhaust gas was monitored until it had returned to the pretrial baseline. It was thus possible to calculate total oxygen consumed during a given period in the chamber, without any need to correct for the inherent lag in open-circuit respirometry (see Bartholomew et al. 1981). Mean fractional 0, content of exhaust gas during the 15-min immersion period was derived by using a Hipad digitizer (Houston Instruments) and micro- processor to integrate area beneath the 0, tracing. The rate of 0, consumption was calculated according to eq. 4a of Withers (1977), and corrected to standard temperature and pressure.

The decision to limit run time to 15 min was based on the previous finding (MacArthur 1984) that diving activity in 30°C water declines significantly with longer periods of immersion. Animals were released into the tank via a hinged gate that was built into the submerged retaining screen and located adjacent to the respirometer. Animals entered the water voluntarily and usually dove immediately to the chamber. During each recording session, detailed observations were made of the animal's behavior in the respirometer, including the frequency and duration of spontaneous dives. The plunger on the respirometer was lowered after precisely 15 min of immersion, and the muskrat was allowed to leave the water via the entry gate. If a muskrat was diving at the 15-min termination point, the animal was denied reentry into the chamber and the final dive was disregarded. To ensure that muskrats were familiar with the tank and respirometer at time of testing, each animal was subjected to several mock trials before the experiments started. All runs were performed between 08:00 and 17:00, and each muskrat was tested only once on any given day. Muskrats were not fasted before metabolic testing.

To obtain comparative base-line measurements in air, the RMR of each animal was measured at thermoneutrality (1 8 + 0.5 "C). For this purpose, the above chamber was replaced by a 14-L glass respirometer fitted with a heavy Plexiglas lid and a removable Plexiglas floor. A positive-pressure, open-circuit system similar to that described by MacArthur (1984) was used, in which inlet flow rate was maintained at 7.0 L . min-' with a calibrated Matheson rotameter (model 605). Exhaust gas from this chamber was split into two streams. One stream was routed through drierite and soda lime and then through a Beckman F-3 paramagnetic oxygen analyzer connected to a two- channel chart recorder (Fisher Recordall 5000). The second exhaust stream was routed through drierite and then through an Applied Electrochemistry CD-3A carbon dioxide analyzer connected to the second channel of the strip-chart recorder. In each trial in air, a muskrat was allowed 1 h to adjust to the chamber, following which metabolic rate was monitored for an additional 2-3 h. Preliminary tests indicated that this was ample time for animals to settle down in the chamber and achieve stable metabolic rates. RMR was calculated from three estimates of the minimum. rate of oxygen consumption (Vo,) and carbon dioxide production (Vco,), each of at least 10 min duration and correct to STP. The VO, and VCO, calculations fol-

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CAN. J. ZOOL. VOL. 67, 1989

PLUNGER

PERFORATED PLATE

METABOLISM CHAMBER

I 1 I I I 1 1

0 5 10 15 20 2 5 30 TIME (min)

FIG. 1. Schematic diagram of the respirometer used to monitor oxygen consumption of freely diving muskrats. A sample recording of changes in the fractional concentration of oxygen in the exhaust gas ( a o 2 ) during a typical immersion run is also presented. Arrows on the graph indicate the start and end of the 15-min period during which the animal had free access to the metabolism chamber.

lowed Wang and Peter (1975). A mean respiratory quotient of 0.83 f 0.11 (n = 10) was derived from these measurements and used to convert VO, values to units of heat production (W - kg-', Stanier et al. 1984). In aquatic trials, VCO, was not monitored, owing to the high solubility of CO, in water and the variable nature of the respiratory quotient in freely diving animals (Butler and Jones 1982).

Statistical treatment of data Mean differences were compared using Student's t-test, and regres-

sions were derived by the method of least squares. Significance was set at the 5 % level, and means are presented with * 1 SE.

Results Most animals adapted readily to the testing procedure and

there was no indication that either diving behavior or response to the apparatus was altered by repeated testing of individuals. Yet we did observe considerable variability amongst runs in the proportion of time spent diving, as well as in the level and nature of surface activity within the respirometer. In 69 of the 152 aquatic trials (45 %), muskrats remained quietly floating during surface intervals, with most locomotor activity con- fined to periods of diving. In the remaining 83 trials, surface intervals were characterized by brief periods of inactivity punctuated by longer, variable episodes of swimming or, in

some instances, gnawing and scratching on the chamber walls. In several cases, animals were almost continuously active throughout the 15-min immersion run, with few rest periods at the surface.

It became apparent that surface activity in the respirometer was an uncontrolled variable that could potentially obscure the relationship between diving behavior and measured Vo2. We therefore separated runs characterized by appreciable surface movement (group A, n = 83 trials) from those in which non- diving locomotor activity was minimal (group B, n = 69 trials). It should be noted that all 10 animals were represented in each of the two data sets; no individual was assigned exclu- sively to either group A or group B. The mean number of dives per 15-min run was 20.0 f 0.72 for group A trials, compared with only 13.7 f 0.82 for the group B trials (t = 5.80, df = 150, P < 0.001). Mean duration of dives was similar for the two data sets, averaging 20.2 + 0.51 s for group A versus 21.6 f 0.66 s for group B (t = 1.76, df = 150, P > 0.05). Combining all data, dive duration averaged 20.83 f 0.41 s and ranged from 1.7 to 68.9 s (n = 2658 dives). It should be noted that all dives were spontaneous; none were intentionally provoked by the investigators. During most of these exploratory dives the animals were continuously swimming, with only occasional pauses beneath the surface.

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MACARTHUR AND KRAUSE

The relationship between Vo2 in water and proportion of time spent diving clearly varied with the level of surface activity (Fig. 2). When motor activity at the surface was minimal (Fig. 2B), Vo2 was positively correlated with the proportion of time spent diving (F1,68 = 53.25, P < 0.001). These data yielded the regression equation Vo2 = 1.07 + 0.009 (% time diving) (SE intercept = 0.047; SE slope = 0.001). Despite the higher frequency of dives, there was no significant relationship between Vo2 and proportion of time spent diving in the group A trials (Fig. 2A, F1,82 = 1.31, P > 0.05).

It occurred to us that there might not be a strict proportion- ality between cumulative dive time and metabolic rate in muskrats. That is, each dive might incur some minimal fixed cost, irrespective of dive duration, and this unit cost could be obscured by relating Vo2 only to the proportion of available time spent underwater. Therefore, we also examined the relationship between Vo2 and frequency of dives during each immersion trial. The results (Fig. 3) were consistent with those in Fig. 2, though in the group B trials, Vo2 correlated more strongly with proportion of time diving than with dive frequency. Multiple regression analysis indicated that these variables together accounted for 47 % of the variance in Vo2.

For all runs in which muskrats spent >50% of available time diving, mean metabolic rate was 1.48 + 0.02 mL 0 2 . g-l . h-l, or 8.33 W . kg-l (n = 39). This is 1.9 times the mean thermoneutral RMR of these same animals in air (0.78 f 0.07 mL O2 g-l h-l). The latter value is nearly identical with the mean Vo2 , 0.77 mL . g-I h-l, previously reported for nonfasted muskrats resting quietly in 30°C water (Fish 1983). If it is assumed that the Vo2 of muskrats resting at the surface approximated thermoneutral RMR, then the cost of diving can be estimated from the relationship

[I] diving Vo2 (mL . g- . min-l)

cumulative dive time (min)

Including only data for group B trials, in which muskrats spent > 50 % of available time diving, the mean cost of diving thus derived was 0.037 + 0.001 mL O2 g-l min-l, or 2.22 mL O2 g-l h-l. This represents a metabolic rate of 12.49 W kg-', which is 2.8 times the thermoneutral rate in air. By comparison, the regression presented in Fig. 2B predicts that if a muskrat were to spend 100% of its available time diving, Vo2 would be close to 2 .OO mL g- . h- l, or 11.26 W kg-'.

Discussion Cost of diving is ostensibly one of the most difficult param-

eters to estimate in calculations of breath-hold capacity and aerobic endurance in vertebrate divers (Castellini et al. 1985). This difficulty arises from the fact that it is not possible to directly measure Vo2 during submergence, using conventional respirometry techniques. In the past, diving metabolic rate has usually been estimated from postdive measurements of Vo2, which often failed to account for the metabolic demands of surface activity and aquatic thermoregulation. As pointed out by Kooyman et al. (1981), variation in measured RMR can introduce significant error into calculations of

0 . 6 d " 1 ' 1 " 1 " 1 " 1 0 10 20 30 40 50 60 70

PROPORTION OF TIME DIVING ( '10)

FIG. 2. Relationship between mean VO, and the proportion of time spent diving during 15-min immersion trials in 30°C water. Regressions are presented for runs involving muskrats that were predominantly (A) active (Y = 1.58 - 0.002X), and (B) inactive (Y = 1.07 + 0.009X) during interdive periods at the surface. Open triangles identify runs in which animals were continuously active throughout the 15-min trial (see text). The broken line indicates resting Vo, at thermoneutrality in air.

diving cost based on total postimmersion Vo2 in excess of the predive base line. The present study was intended to minimize ,these potential sources of error and provide a meaningful estimate of the energetic cost of voluntary diving in 0. zibethicus. The respirometer permitted accurate calculation of Vo2 over a brief (1 5 -min) immersion period, when ,the proportion of time spent diving often exceeded 50% and thermal stress was minimal. Because muskrats were continuously immersed during these trials, the metabolic costs of postimmersion grooming (MacArthur 1984) were also avoided. We assumed that oxygen was rapidly replenished during the interdive period, with no appreciable carry-over of oxygen debt from one dive to the next, or beyond the end of the 15-min run.

A major limitation of this study was the variability in the

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2198 CAN. J . ZOOL. VOL. 67, 1989

~ . ~ L I I I I I I I I I I I I I I 0 0.4 0.8 1.2 1.6 2.0 2.4 2.8

DIVING FREQUENCY ( dives . min -I 1

FIG. 3. Relationship between mean VO, and the frequency of dives during 15-min immersion trials in 30°C water. Regressions are presented for runs in which muskrats were predominantly (A) active (Y = 1.49 + 0.003X) and (B) inactive (Y = 1.12 + 0.280X) during interdive periods at the surface. See Fig. 2 for explanation of symbols.

amount of surface swimming that occurred between dives, and this factor likely contributed to much of the observed variance in Vo2 (Figs. 2 and 3). Fortunately, surface activity was minimal in 45 % of the runs, and these data revealed a positive correspondence between Vo2 and both the proportion of time spent diving (Fig. 2B) and the frequency of dives (Fig. 3B). As activity was virtually absent during the interdive period, these data clearly demonstrate that underwater exercise is accompanied by increased energy expenditure in 0. zibethicus. They also provide a first approximation of the cost of voluntary diving in muskrats, which appears to be nearly 3 times the thermoneutral rate in air. In a previous study (MacArthur 1984) in which muskrats were forced to dive for extended periods (0.5 -4 min) in 30°C water, metabolic cost increased by 43 mL O2 kg-] for each additional minute that

the animals remained submerged. This corresponds to a diving Vo2 of 2.58 mL g-I . h-l, which is only 16% higher than the current estimate (2.22 mL g-I . h-l) for freely diving muskrats.

Although swimming speed was not quantified in this inves- tigation, animals usually swam steadily during periods of submergence. Earlier studies by Fish (1982, 1983) demonstrated that Vo2 increases linearly with speed in surface-swimming muskrats. At the mean natural speed selected by muskrats (0.58 n~ s-I), cost of surface swimming in 30°C water is 1.94 mL O2 . g-l h-l (Fish 1983), or 87 % of our estimated cost of diving. That the costs of diving and surface swimming may be of similar magnitude in 0. zibethicus is also implied by the absence of correlation between Vo2 and the proportion of time spent diving in the group A trials (Fig. 2A). Here, appreciable swimming occurred during both dive and interdive periods, and there was no suggestion of change in metabolic rate with increased underwater exercise.

The metabolic performance of diving muskrats is qualitatively similar to that of the tufted duck (Woakes and Butler 1983; Butler 1988) and the harbor seal (Craig and Pfsche 1980), in which diving metabolic rate is estimated to be 3.5 and 1.7 times RMR, respectively. It is noteworthy that the metabolic cost of underwater swimming also approaches that of surface swimming in the tufted duck (Butler 1988). Like the tufted duck, the muskrat is positively buoyant, owing to the large air volume entrapped in the pelage, and the cost of remaining submerged could contribute to the elevated metabolic rate during active exploratory dives. Penguins, which are almost neutrally buoyant, have been reported to exhibit little change in Vo2 during voluntary diving (Butler and Woakes 1984).

It is also informative to examine the metabolic costs of diving in the context of available oxygen stores. Drawing upon data from several sources, Snyder and Binkley (1985) predicted that the combined lung, blood, and myoglobin oxygen stores of muskrats may be as high as 29.7 mL O2 kg-l body weight. Assuming a Vo2 of 2.22 mL g- l . h- (this study), these stores should theoretically permit aerobic diving for 48.2 s. This is 2.3 times the mean duration of spontaneous dives in this study (20.8 s) and approaches the maximum recorded dive time of 68.9 s. It would thus appear that these animals were usually diving well within their aerobic limits. Interestingly, voluntary submergence times of both free- ranging and captive muskrats may exceed 3 min when diving is intentionally provoked by the investigator (MacArthur and Karpan 1989). These "escape" dives are characterized by reduced motor activity, which we interpret as an adaptation for lowering metabolic rate and extending the aerobic dive limit. Suppression of motor activity would permit full expression of the classical diving response, with a more intense peripheral vasconstriction and a correspondingly lower Vo2. Studies of seals have revealed a higher cost of diving (Craig and ~Psche 1980) and a reduced underwater endurance (Kanwisher and Gabrielsen 1985) with increased levels of exercise.

Still unresolved is the question of how diving muskrats are able to elevate metabolic rate more than 2-fold, in the face of a 60-80% reduction in heart rate (Jones et al. 1982; MacArthur and Karpan 1989). This finding is all the more remarkable when it is considered that the peak metabolic response of this species to extreme cold or maximum sustain- able exercise is only 3.3 -3.8 times RMR (Fish 1982;

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MACARTHUR AND KRAUSE 2199

MacArthur 1984). Our findings imply that the aerobic requirements of working muscles must exceed by a substantial margin the oxygen saving in hypoperfused peripheral tissues during active diving (see also Butler 1982). As reported for the tufted duck (Woakes and Butler 1983), muskrats undoubtedly achieve a higher b'02 at a given heart rate underwater than when exercising at the surface. It is also evident that the pronounced body cooling of diving muskrats does not reflect a depressed metabolic state, as was proposed earlier (MacArthur 1984). The 3- to 5-fold increase in the rate of abdominal cooling may be due instead to more intense abdominal vasocon- striction, coupled perhaps with increased convective heat loss accompanying underwater movement.

To this point, discussion has focused on the energy expended during active diving. From an ecological perspec- tive, the "true" cost of natural diving may also include the additional metabolic demands of grooming and restoring body temperature following withdrawal of the animal to shore. For example, the postimmersion b'02 of muskrats remains elevated for an average of 10 min following 30-s dives in 20-30°C water, yielding a postdive excess b'02 of 90.4 mL . kg- (MacArthur 1984). If this excess b'02 were used only to repay the oxygen deficit incurred during the 30-s dive, it would correspond to an improbable diving metabolic rate of 11.28 m L O2 g-I h-l, which is 5.1 times the current estimate. Alternatively, if it is assumed that a muskrat diving in 20 - 30°C water consumes 2.22 m L O2 g-I h-l, then the cost incurred during 30 s submergence is 18.5 m L 02. kg-l. This is only 20.5% of the measured postdive excess b'02, suggesting that grooming and rewarming costs following withdrawal from water contribute significantly to the total energy requirements of diving. It should also be noted that while muskrats are susceptible to aquatic cooling in water <30°C, there is no convincing evidence of active thermo- genesis during cold-water dives by these animals (MacArthur 1986). Therefore, metabolic rate during diving is probably independent of water temperature, though the higher cooling rate in cold water would increase energy expended at the surface and following emergence of the animals onto land.

Acknowledgements The cooperation provided by the Manitoba Department of

Natural Resources is gratefully acknowledged. This research was supported by an operating grant to R.A.M. and an Undergraduate Research Award to R. E . K. from the Natural Sciences and Engineering Research Council of Canada.

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energy requirements of freely diving muskrats ( ondatra zibethicus )

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