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Heart rates in the captive, free-ranging beaver
Camp. E;ochem.P/?,sio/. Vol. 9lA. No. 3. pp. 431435, 1988
0300-9629/88$3.00+ 0.00 sc 1988Pergamon Press plc
Printed IIIGreat Britain
HEART RATES IN THE CAPTIVE, FREE-RANGING BEAVER UNA G. SWAIN,* F. F. GILeERTt and JACK D. ROBINETTE Wildlife Biology Program, Washington State University, Pullman, WA 99164-6410, USA. Telephone:
(509) 335-6166;
and Veterinary
Clinic,
Washington
State University,
Pullman,
WA 99164-6610,
USA
(Received 4 February 1988) Abstract-l. Heart rates of beaver (Casfor canadensis) under free-ranging captive conditions for active behaviors and resting in water (- 121 beats/min) were significantly (P < 0.01) higher than for resting on land (100 beats/min). 2. Although no transient recovery tachycardia was evident in swimming heart rates following diving, average swimming heart rates were higher (127beats/min) after diving than after other precursor behaviors (123 beatsimin). 3. Beaver exhibited bradycardia when sleeping (75 beats/min), diving (61 beats/min), and when threatened on land (57 beatsimin). 4. The respiratory sinus arrythmia indicated a respiratory rate of 15 breaths/min. 5. Cold temperatures (%O’C) elicited higher heart rates than did warmer temperatures (~20°C) in active, non-diving behaviors (P < 0.05).
INTRODUCTION
(1.5 x 0.7 m) for drinking and swimming. The huts were surrounded by an outdoor enclosure with a 9.1 x 3.6 m swimming pool of variable depth, maximum depth being 2.1 m. Water temperature was dictated by ambient temperatures, and rocks of varying size were placed on the bottom of the pool to serve as a natural substrate. A colony of 24 animals was housed in each hut. One colony at a time was allowed access to the outdoor enclosure in order to avoid territorial aggression. During a data collection period, the test beaver and its colony were free to roam within the enclosure. All beavers were given at least one month to acclimate to the study situation before testing began. The beaver were maintained on pelleted alfalfa cubes, rat chow and aspen (Populus tremuloides). Biotelemetry transmitters (Wyoming Biotelemetry Inc., Longmont Co., USA) were surgically implanted either subcutaneously caudal to the xyphoid process or in the abdominal cavity. ECG electrodes were sutured subdermally to the lateral chest wall, one on either side of the heart. Anaesthesia was induced by intramuscular injection of Ketamine hydrochloride (10 mg/kg) (Vetalar, Parke-Davis) and maintained with halothane and oxygen delivered either by a non-cuffed endotracheal tube or a face mask on a Bain circuit. Atropine sulphate (0.40.6 mg) was given intramuscularly to control bradycardia. The surgical procedure has been described in detail elsewhere (Swain, 1985). The transmitters (~40 g) operated in the 150-151 or 163-164 mHz range and emitted signals in response to the QRS complex. The transmitter signals were received by a 3-element Yagi antenna, converted to digital form, and fed into a microcomputer (North Star Horizon) for storage and analysis. The computer recorded the time when each heart beat occurred in hundredths of seconds. Simultaneously, the animal’s behavior was observed by use of a video system and recorded on the computer. The video system consisted of three Panasonic WV-1450 TV cameras and two Sony Black and White TV monitors, and it precluded any observer influence on behavioral responses. Heart rate was recorded for seven beavers during 175 hr of testing, which comprised 4461 individual behavioral episodes. The beavers were monitored during different seasons of the year, both at night and during the day. For night observations, red light provided the illumination for
Interest in heart rate studies has increased in recent years partially due to the use of heart rate as a physiological indicator in certain behavioral responses. For example, heart rate may be correlated with metabolic rate and physiological stress, whether it is the increased cardiovascular activity of the “flight or fight” reaction (e.g. MacArthur et al., 1979) or the decreased heart rate of the alternate response to threat, commonly referred to as fear, or alarm, bradycardia (Jacobsen, 1979; Gabrielsen et al., 1985). Beavers are semi-aquatic mammals well known for their diving habits (Irving and Orr, 1935). Understanding the biological significance of diving bradycardia depends on heart rate investigations of freely diving animals, because the bradycardic response differs when animals are forcibly submerged (e.g. Butler and Woakes, 1979; Jones et al., 1982; Kanwisher et al., 1981; Gilbert and Gofton, 1982). Beavers dive as a means of escaping potential danger; however their reaction and accompanying heart rate response to threat when water is not accessible are not known. The objectives of the current research were to determine heart rates for various behaviors of beaver in free-ranging conditions. MATERIALS AND METHODS Beavers (Castor canadensis) were live-trapped
in Idaho and Washington and housed in the Furbearer Research Facility at Washington State Universitv. The facility provided bpen-air huts (2.1 x 2.4 x 3 m), each of which contained a nest box for a lodge, and a circular water tank
*Present address: Alaska Fish and Wildlife Research Center, 1101 E. Tudor Road, Anchorage, AK 99503, USA. tAuthor to whom all correspondence should be sent. 431
432
UNA G. SWAIN et al.
the light-sensitive video cameras. Air and water temperatures were recorded for each monitoring session and averaged for individual beavers. Heart rates were determined for as wide a range of behaviors as possible. These included swimming, diving, feeding, grooming, investigating, resting (both in and out of the water) and sleeping. Another category of resting behavior was defined as “alert resting”, which differed from “true resting” in the degree of activity displayed by the beaver while remaining stationary. Resting beavers were characterized by a total inactivity, whereas alert resting beavers were attentive to their surroundings, would commonly move both their heads and upper torsos, and would frequently rest solely on their hind legs as opposed to all four limbs. Feeding behavior included the handling of twigs and branches, which frequently accompanied this activity. The effect of temperature on heart rate was analysed by grouping together the heart rates of beavers exposed to similar temperatures. Two beavers were tested during the winter, while the other five beavers provided heart rate values at warmer temperatures. The heart rate response to threat was investigated when escape to water was prevented. The sight or sound of an approaching human provided the threatening stimulus. Heart rates for different types of dives were also investigated, but these results are presented in a separate paper (Swain et al., in review).* The dives reported in this paper occurred spontaneously. The data were analysed by measuring the time interval between each QRS complex, and instantaneous heart rates (IHR) were associated with each beat recorded. Each IHR represented the delay between individual heart beats expressed in beats/min. Artifacts caused by violent muscular movement were excluded from the data analysis. The IHRs were averaged for each behavioral episode, and the episode means were then averaged by behavioral category and by individual beavers. Only behavioral episodes lasting at least 15 set were analysed for heart rate. Furthermore, the first and last 5 set of an episode were excluded from average heart rate determinations to avoid any possible transitional phases in heart rate between different behaviors. Analysis of the first I5 set of a behavioral episode showed precursor behavior had no effect on the heart rate of subsequent behavior. Statistical significance was tested by t-tests and analyses of variance (completely random design and randomized complete block) (Steel and Torrie, 1980). Pairwise comparisons of means were effected with Fisher’s protected LSD test (P < 0.05). In the text and figures, data are reported as means f SE of seven beavers (N = 7) determined from n observations (n = number of behavioral episodes) unless otherwise stated. RESULTS
The more active behaviors of grooming (121 k 3 beats/min) (n = 848), investigating (118 + 3 beats/ min) (n = 376) and swimming (126 + 3 beats/min) (n = 747), as well as the behavior of resting in water (120 & 4 beats/min) (n = 328) showed no significant differences (P > 0.05, ANOVA) in heart rates when the results from all seven beavers were analysed. These behaviors resulted in significantly (P < 0.01) higher heart rates than resting on land (100 f 5 beats/min) (n = 143), whilst diving resulted in the lowest heart rate (61 + 6 beats/min) (n = 367). The heart rate for diving represented 48% of the swimming heart rate. Only behaviors in which all the *Swain U. G., Gilbert F. F. and Robinette Diving bradycardia in captive, free-ranging mitted to Physiol. Zoo/.)
J. D. (1988) beaver (sub-
beavers were represented were included in this analysis (P < 0.01, ANOVA). Beavers not only showed a bradycardic response during diving, but also when sleeping. The average sleeping heart rate was 75 f 5 beats/min (n = 41, Iv = 5), which was 75% of the resting heart rate (P < 0.01 paired r-test). Heart rates of both feeding (123 + 5 beats/min) (n = 40, N = 6) and alert resting (115 + 4 beats/min) (n = 421, N = 5) were comparable to heart rates of other active behaviors and that of resting in water (P > 0.05, ANOVA). Following diving, no transient recovery tachycardia was observed during the first 15 set of swimming, however the average swimming heart rate, as recorded for the entire episode, was higher after diving (127 f 3 beats/min) (n = 467) than after other precursor behaviors (123 + 3 beats/min) (n = 280) (P < 0.001 paired t-test). There was also an indication that swimming heart rates following diving were reflective of dive durations, with heart rates ranging from 124 k 3 beats/min after dives of less than 10 set (n = 191) to 134 ? 5 beatsjmin following dives exceeding 2 min (n = 40) (N = 4). Heart rates were determined at different ambient temperatures (Table 1). Active and resting in-water behaviors recorded at colder average air (- 1“C) and water (1’C) temperatures had a higher mean heart rate than behaviors at warmer average temperatures (21°C for air, 17°C for water) (P < 0.05 t-test). Although not significant, this trend of higher heart rates at colder temperatures was also observed for alert resting and sleeping. Resting proved the exception with heart rates being comparable at the different temperatures (P > 0.05). However, only 11 resting behavioral episodes were recorded for the two beavers monitored during the winter. Diving heart rates were excluded from the analysis because of their dependency on dive duration (Swain, 1985). Dives recorded for beavers at colder temperatures had a mean dive duration of 10 f 15 set (n = 119), whereas dives at warmer temperatures were considerably longer (P < 0.001) with a mean duration of 32 k 38 set (n = 675). Beavers exhibited a marked fear bradycardia (57 + 16 beats/min) (n = 22) (N = 5) when threatened on land. Heart rate dropped suddenly in response to threat and remained at low levels after removal of the stimulus (Fig. 1). The lowest heart rate recorded for an episode of fear bradycardia was 9 beats/min. The heart rate of fear bradycardia averaged 57% of the rate for resting behavior and was comparable to the bradycardia observed upon diving (I’ < 0.05, ANOVA). Analysis of individual behavioral episodes on an instantaneous heart rate basis indicated a sinus arrythmia (cf. Fig. 1). Respiration appeared as a wave form of successive IHRs and gave a mean resting respiration rate of 15 f 1 breaths/min. DISCUSSION determinations restrictive captive conditions unable to carry out natural The current research allowed ral activities in the beaver, Heart
rate
are often hampered by in which the animals are behavioral repertoires. the occurrence of natualthough it is suggested
Heart rate in the beaver
433
Table 1. Mean heart rate values (f SE) for free-ranging captive beaver monitored water (T,,,) temperatures Mean ambient Behavior* Diving Sleepingt Resting Alert restingt Resting in water Investigaling Grooming Feedingt Swimming
T, = - I ‘, T,,,, = I (N = 2) 57.2 f 8.41 (69) 81.5 + 6.9 (17) 97.1 i2.1g (II) 122.1 27.3 (157) 130.4 f 7.611 (51) 125.7 k 5.711 (109) 131.4+2.21l (200) 138.3 & 0.2 (7) 132.4* 5.911 (129)
temperatures
T,=21’,
at different air (T,) and
(‘C)
THlo=17
(N=5)
P’I
62.9 + 7.51 (298) 71.1 k7.6 (24, N=3) 101.0 k 2.e (132) 110.8 i 2.6 (264, N = 3) 115.9? I.311 (187) 115.8 + I.211 (267) 116.8 f 2.211 (648) 115.2* I.1 (33, N =4) 123.4 + 1.9 (618)
Number of behavioural episodes given in brackets. Number of animals (N) given in brackets when all beaver are not represented *Significant behavioral effects, F,,, = 59.51, Fo,20= 34.34. tBehavior not included in ANOVA. $$I1 within columns, heart rates with dlfferent letter subscripts are significantly l’significance levels of t-test for heart rates at different ambient temperatures.
that probably more time was spent in investigating and less in building than in the wild. Beaver heart rates varied with respect to the activity level of the behavior. Active behaviors may be distinguished from inactive behaviors on the basis of heart rate, but the wide ranges in heart rates of the more active behaviors preclude determination of individual active behaviors. Heart rate values for grooming, swimming and diving were similar to those reported for beavers by Gilbert and Gofton (1982). However, the resting heart rate they reported was comparable to the alert resting value in this study and probably reflects the more natural conditions of this study. The higher heart rate of resting in water, as compared to resting on land, was possibly due to the increased thermoregulatory cost in water. An increase in heart rate following diving can be interpreted as part of the physiological mechanisms
0.5 0.5 0.2 0.05 0.05 0.02 0.001 0.05
in behavior
different
mean.
at the 0.01 level.
initiated upon surfacing in response to the oxygen debt incurred during the dive (Irving and Orr, 1935; Scholander, 1940) or, in the case of cold water temperatures, hypothermia induced by diving. Beaver display no transient increase in heart rate during the first 5, 10 or 15 set following a dive; however the heart rate of the entire post- or inter-dive behavior is higher, indicating that beaver-like swamp rabbits (Syfvilugus aquaricus) (Smith and Tobey, 1983) and diving ducks (e.g. Aythya ferina, Aythya fiIigulu) (Butler and Woakes, 1979) have a recovery tachycardia following diving. In diving ducks, the tachycardia lasted l&15 set following a dive, whereas the time required for the heart rate to return to pre-dive levels in the beaver was longer. However, exact determination of the time course for recovery tachycardia was not undertaken. Diving ducks also portray a relationship between the magnitude of post-dive tachycardia
TIME IN SECONDS
Fig. I. Instantaneous threatening stimulus
heart rates for beaver Ai during an episode of fear bradycardia. Bar indicates of the approach of the investigator. Note the respiratory sinus arrythmia during the pre-stimulus behaviors.
434
UNA G. SWAIN et al.
and the duration of the dive (Butler and Woakes, 1979). A similar situation was evident in beaver, where the longer dives elicited higher heart rates upon surfacing. Temperature is one of the many factors that may affect heart rate; however very few studies have investigated its influence on heart rate and, in particular, its influence on the diving heart rate. Hammel et al. (1977) have shown for the harbor seal (Phoca ritulina) that the usual vasoconstriction reflex observed during diving can be abolished if the preoptic area of the hypothalamus is artificially heated during submergence. Gilbert and Gofton (1982) found higher heart rates to be associated with all behaviors including diving in muskrat (Ondatra zibethicus) monitored at lower temperatures, while Thornton et al. (1978) recorded lower dive heart rates for muskrats in colder water temperatures. Gilbert (198 1) proposed that colder water temperatures may elevate base line heart rate values for diving in male beavers. Beavers at lower ambient temperatures displayed higher heart rates for most non-dive behaviors, probably reflecting the increased thermoregulatory costs. The lower critical temperature for beavers is given as -3°C (Coles, 1967, in Lancia et al., 1982). Behavioral observations have indicated a correlation between above-ice activity and ambient temperature (Wilsson, 1971; Lancia et al., 1982). The onset of above-ice activity occurred at air temperatures above -4°C to - lO”C, and activity increased with increasing temperatures. In the wild, the microenvironment of the lodge and frozen pond significantly moderate winter temperature extremes to near 0°C (Stephenson, 1969). Certain behavioral adaptations to cold temperatures were not feasible for the test beaver, as the study situation did not provide underwater access to the pool and hence, activity could not be restricted to below the ice during periods of subfreezing weather. Temperatures below - 3°C were common. Thus, it is likely that the beavers moving between the huts and the pool were exposed to colder ambient temperatures than they normally would have encountered in the wild, unless forced to forage on land for food when the food pile is inadequate (Gilbert, persona1 observation). The lack of emphasis placed on the influence of water temperature on diving physiology seems surprising, as any factor which may affect peripheral vasoconstriction during submergence might also be expected to alter the diving bradycardia. Definite conclusions about the effect of temperature on dive heart rates cannot be represented here, because of the effect of dive duration and because differences in heart rates may be masked when the same beavers are not represented at both temperature extremes. Both beavers monitored during the cold temperatures were females. Although the differences were not significant, dive heart rates were lower at lower temperatures. This, coupled with the observation that dives were shorter at lower ambient temperatures and should thus reflect higher heart rates (Swain, 1985), suggests that diving in colder water does elicit a deeper bradycardia in female beavers. Beavers have been shown to maintain a constant arterial blood pressure during submergence (Clausen and Ersland,
1970/71). McKean (1982) has shown that regional blood flow in beavers decreased to all organs except the adrenals, heart and lungs, and increased to the brain. It is likely that peripheral blood flow is altered to a greater degree in colder water (Thornton et al., 1978), hence the concomitant bradycardia might be expected to be of greater intensity in order to maintain a constant blood pressure (Andersen, 1966). Although our conclusions are speculative, they do point out that temperature should not be neglected in heart rate investigations. Emotional stimuli may act as strong modifying agents on heart rate. Many cases of bradycardia have been observed in non-diving situations, most of which involve an element of stress to the animal. Studies on terrestrial mammals and birds (e.g. Gabrielsen et al., 1977; Causby and Smith, 1981) suggest that the bradycardia observed in some situations has a fear component. The classic response to fear is increased heart rate and a general readiness for “flight or fight”. In those situations, however, in which the danger can be avoided more successfully by remaining motionless or hiding, bradycardia is elicited (Gabrielsen et al., 1977; Jacobsen, 1979; Smith and Woodruff, 1980). Many animals show what has been termed a “passive defence response” (Gabrielsen et al., 1985) to a threat source. Beavers display prone behavioral responses on land. They “freeze” when threatened both in the wild (personal observation) and in captivity, although if water were immediately accessible the response would be likely to be a dive. Beavers resemble incubating willow ptarmigan (Lagopus fagopus) threatened by intruders (Gabrielsen et al., 1977) white-tailed deer fawns (Odocoileus virginianus) (Jacobsen, 1979) and eastern grey squirrels (Sciurus carolinensis) (Smith and Johnson, 1984) approached by humans, and American opossums (Didelphis marsupialis) feigning death in response to a dog (Canis domesticus) (Gabrielsen and Smith, 1985). In all cases, the behavioral response was accompanied by a marked bradycardia. Studies on other diving species, such as seals, have shown that pain, abrupt noise or threatening gestures also can elicit bradycardia (Scholander, 1940). The onset of fear bradycardia was sudden in beaver and occurred immediately upon the animal’s awareness of threatening stimuli (Fig. I). The increase in heart rate observed for one of the beavers during 2 of the 4 episodes of threat is likely to be due to increased activity and movements which the investigator was unable to observe because the beaver was inside its nest box. In situations where there is no possibility of active escape, although probably rare for the beaver, fear bradycardia may enhance the prone behavioral responses which help conceal the animal and decrease the likelihood of being detected by a predator. Acknowledgements-The authors thank Dr L. Gallagher for his help with the surgical procedures and D. Douglas and J. Thomas for their technical assistance. Una Swain was the recipient of a Washington State University graduate research assistantship during part of the project. The study was supported by a grant to F. Gilbert from the International Fur Trade Federation.
Heart rate in the beaver REFERENCES
submergence on the diving response in muskrats (Ondatra zibethica).
Anderson H. T. (1966) Physiological adaptation in diving vertebrates. Physiol. Rev. 46, 212-243. Butler P. J. and Woakes A. J. (1979) Changes in heart rate and respiratory frequency during natural behaviour of ducks, with particular reference to diving. J. exp. Biol. 79,
Comp. Biochem. Physiol. 6!K,
367-370.
Clausen G. and Ersland A. (1970/71) Blood 0, and acid-base changes in the beaver during submersion. Resp. Physiol. 11, 104112. Coles R. W. (1967) Thermoregulation of the beaver. PhD dissertation, Harvard Univ., Cambridge. 82 pp. Gabrielsen G. W. and Smith E. N. (1985) Physiological responses associated with feigned death in the American oppossum. Acra Physiol. &and. 123, 393-398. Gabrielsen G. W., Kanwisher J. and Steen J. B. (1977) “Emotional bradycardia”: a telemetry study on incubating willow grouse (Lagopus lagopus). Acta Physiol. &and. 100,255-257. Gabrielsen G. W., Blix A. S. and Ursin H. (1985) The orienting and freezing responses in ptarmigan. Physiol. Behav. 34, 925-934.
Gilbert F. F. (1981) Aquatic study. Phase I-Beaver in leg hold traps (“drowning sets”). Report submitted to the Federal Provincial Committee for Humane Trapping, February I98 1. 18 pp + appendices. Gilbert F. F. and Gofton N. (1982) Heart rate values for beaver, mink and muskrat. Comp. Biochem. Physiol. 73A, 249925 1. Hammel H. T., Elsner R. W., Heller H. C., Maggert J. A. and Bainton C. R. (I 977) Thermoregulatory responses to altering hypothalamic temperature in the harbor seal. Am. .I. Physiol. 232, R18-R26. Irving L. and Orr M. D. (1935) The diving habits of the beaver. Science 82, 569. Jacobsen N. K. (1979) Alarm bradycardia in white-tailed deer fawns (Odocoileus virginianus). J. Mammal. 60, 343-349.
Jones D. R., West N. H., Bamford 0. S., Drummond P. C. and Lord R. A. (1982) The effect of the stress of forcible
Can. J. 2001. 60, 187-193.
Kanwisher J. W., Gabrielsen G. and Kanwisher N. (1981) Free and forced diving in birds. Science 211, 717-719. Lancia R. A., Dodge W. E. and Larson J. S. (1982) Winter activity patterns of two radio-marked beaver colonies. J. Mammal.
283-300.
Causby L. A. and Smith E. N. (1981) Control of fear bradycardia in the swamp rabbit Sylvilagus aquaticus.
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MacArthur R. A., Johnston R. H. and Geist V. (1979) Factors influencing heart rate in free-ranging bighorn sheep: a physiological approach to the study of wildlife harassment. Can. J. Zool. 57, 2010-2021. McKean T. (1982) Cardiovascular adjustments to laboratory diving in beavers and nutria. Am. J. Physiol. 242, R434R440. Scholander P. F. (1940) Experimental investigations on the respiratory function in diving mammals and birds. Hvalradets I-131.
Skrifter
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Smith E. N. and Woodruff R. A. (1980) Fear bradycardia in free-ranging woodchucks, Marmota monax. J. Mammal. 61, 750-753.
Smith E. N. and Tobey E. W. (1983) Heart rate response to forced and voluntary diving in swamp rabbits, Sylvilagus aquaticus. Physiol. Zoo/. 56, 632-638.
Smith E. N. and Johnson C. (1984) Fear bradycardia in the eastern fox squirrel, Sciurus niger and eastern grey squirrel, Sciurus carolinensis. Comp. Biochem. Physiol. 70A, 529-532.
Stephenson A. B. (1969) Temperatures within a beaver lodge in winter. J: Mammal. -W, 134-136. Steel R. G. D. and Torrie J. H. (1980) Principles and Procedures of Statistics. A Biome&al Approach, 2nd edn. McGraw-Hill, Inc., New York. 633 pp. Swain U. G. (1985) Heart rates and diving bradycardia in beaver (Castor canadensis). MS Thesis, Washington State University, Pullman. 53 pp. Thornton R., Gordon C. and Ferguson J. H. (1978) Role of dermal stimuli in the diving response of the muskrat (Ondafra zibethica). Comp. Biochem. Physiol. 61A, 369-370.
Wilsson L. (1971) Observations and experiments on the ethology of the European beaver (Cusror fiber L.). Viltrevy 8, 115-266.
0300-9629/88$3.00+ 0.00 sc 1988Pergamon Press plc
Printed IIIGreat Britain
HEART RATES IN THE CAPTIVE, FREE-RANGING BEAVER UNA G. SWAIN,* F. F. GILeERTt and JACK D. ROBINETTE Wildlife Biology Program, Washington State University, Pullman, WA 99164-6410, USA. Telephone:
(509) 335-6166;
and Veterinary
Clinic,
Washington
State University,
Pullman,
WA 99164-6610,
USA
(Received 4 February 1988) Abstract-l. Heart rates of beaver (Casfor canadensis) under free-ranging captive conditions for active behaviors and resting in water (- 121 beats/min) were significantly (P < 0.01) higher than for resting on land (100 beats/min). 2. Although no transient recovery tachycardia was evident in swimming heart rates following diving, average swimming heart rates were higher (127beats/min) after diving than after other precursor behaviors (123 beatsimin). 3. Beaver exhibited bradycardia when sleeping (75 beats/min), diving (61 beats/min), and when threatened on land (57 beatsimin). 4. The respiratory sinus arrythmia indicated a respiratory rate of 15 breaths/min. 5. Cold temperatures (%O’C) elicited higher heart rates than did warmer temperatures (~20°C) in active, non-diving behaviors (P < 0.05).
INTRODUCTION
(1.5 x 0.7 m) for drinking and swimming. The huts were surrounded by an outdoor enclosure with a 9.1 x 3.6 m swimming pool of variable depth, maximum depth being 2.1 m. Water temperature was dictated by ambient temperatures, and rocks of varying size were placed on the bottom of the pool to serve as a natural substrate. A colony of 24 animals was housed in each hut. One colony at a time was allowed access to the outdoor enclosure in order to avoid territorial aggression. During a data collection period, the test beaver and its colony were free to roam within the enclosure. All beavers were given at least one month to acclimate to the study situation before testing began. The beaver were maintained on pelleted alfalfa cubes, rat chow and aspen (Populus tremuloides). Biotelemetry transmitters (Wyoming Biotelemetry Inc., Longmont Co., USA) were surgically implanted either subcutaneously caudal to the xyphoid process or in the abdominal cavity. ECG electrodes were sutured subdermally to the lateral chest wall, one on either side of the heart. Anaesthesia was induced by intramuscular injection of Ketamine hydrochloride (10 mg/kg) (Vetalar, Parke-Davis) and maintained with halothane and oxygen delivered either by a non-cuffed endotracheal tube or a face mask on a Bain circuit. Atropine sulphate (0.40.6 mg) was given intramuscularly to control bradycardia. The surgical procedure has been described in detail elsewhere (Swain, 1985). The transmitters (~40 g) operated in the 150-151 or 163-164 mHz range and emitted signals in response to the QRS complex. The transmitter signals were received by a 3-element Yagi antenna, converted to digital form, and fed into a microcomputer (North Star Horizon) for storage and analysis. The computer recorded the time when each heart beat occurred in hundredths of seconds. Simultaneously, the animal’s behavior was observed by use of a video system and recorded on the computer. The video system consisted of three Panasonic WV-1450 TV cameras and two Sony Black and White TV monitors, and it precluded any observer influence on behavioral responses. Heart rate was recorded for seven beavers during 175 hr of testing, which comprised 4461 individual behavioral episodes. The beavers were monitored during different seasons of the year, both at night and during the day. For night observations, red light provided the illumination for
Interest in heart rate studies has increased in recent years partially due to the use of heart rate as a physiological indicator in certain behavioral responses. For example, heart rate may be correlated with metabolic rate and physiological stress, whether it is the increased cardiovascular activity of the “flight or fight” reaction (e.g. MacArthur et al., 1979) or the decreased heart rate of the alternate response to threat, commonly referred to as fear, or alarm, bradycardia (Jacobsen, 1979; Gabrielsen et al., 1985). Beavers are semi-aquatic mammals well known for their diving habits (Irving and Orr, 1935). Understanding the biological significance of diving bradycardia depends on heart rate investigations of freely diving animals, because the bradycardic response differs when animals are forcibly submerged (e.g. Butler and Woakes, 1979; Jones et al., 1982; Kanwisher et al., 1981; Gilbert and Gofton, 1982). Beavers dive as a means of escaping potential danger; however their reaction and accompanying heart rate response to threat when water is not accessible are not known. The objectives of the current research were to determine heart rates for various behaviors of beaver in free-ranging conditions. MATERIALS AND METHODS Beavers (Castor canadensis) were live-trapped
in Idaho and Washington and housed in the Furbearer Research Facility at Washington State Universitv. The facility provided bpen-air huts (2.1 x 2.4 x 3 m), each of which contained a nest box for a lodge, and a circular water tank
*Present address: Alaska Fish and Wildlife Research Center, 1101 E. Tudor Road, Anchorage, AK 99503, USA. tAuthor to whom all correspondence should be sent. 431
432
UNA G. SWAIN et al.
the light-sensitive video cameras. Air and water temperatures were recorded for each monitoring session and averaged for individual beavers. Heart rates were determined for as wide a range of behaviors as possible. These included swimming, diving, feeding, grooming, investigating, resting (both in and out of the water) and sleeping. Another category of resting behavior was defined as “alert resting”, which differed from “true resting” in the degree of activity displayed by the beaver while remaining stationary. Resting beavers were characterized by a total inactivity, whereas alert resting beavers were attentive to their surroundings, would commonly move both their heads and upper torsos, and would frequently rest solely on their hind legs as opposed to all four limbs. Feeding behavior included the handling of twigs and branches, which frequently accompanied this activity. The effect of temperature on heart rate was analysed by grouping together the heart rates of beavers exposed to similar temperatures. Two beavers were tested during the winter, while the other five beavers provided heart rate values at warmer temperatures. The heart rate response to threat was investigated when escape to water was prevented. The sight or sound of an approaching human provided the threatening stimulus. Heart rates for different types of dives were also investigated, but these results are presented in a separate paper (Swain et al., in review).* The dives reported in this paper occurred spontaneously. The data were analysed by measuring the time interval between each QRS complex, and instantaneous heart rates (IHR) were associated with each beat recorded. Each IHR represented the delay between individual heart beats expressed in beats/min. Artifacts caused by violent muscular movement were excluded from the data analysis. The IHRs were averaged for each behavioral episode, and the episode means were then averaged by behavioral category and by individual beavers. Only behavioral episodes lasting at least 15 set were analysed for heart rate. Furthermore, the first and last 5 set of an episode were excluded from average heart rate determinations to avoid any possible transitional phases in heart rate between different behaviors. Analysis of the first I5 set of a behavioral episode showed precursor behavior had no effect on the heart rate of subsequent behavior. Statistical significance was tested by t-tests and analyses of variance (completely random design and randomized complete block) (Steel and Torrie, 1980). Pairwise comparisons of means were effected with Fisher’s protected LSD test (P < 0.05). In the text and figures, data are reported as means f SE of seven beavers (N = 7) determined from n observations (n = number of behavioral episodes) unless otherwise stated. RESULTS
The more active behaviors of grooming (121 k 3 beats/min) (n = 848), investigating (118 + 3 beats/ min) (n = 376) and swimming (126 + 3 beats/min) (n = 747), as well as the behavior of resting in water (120 & 4 beats/min) (n = 328) showed no significant differences (P > 0.05, ANOVA) in heart rates when the results from all seven beavers were analysed. These behaviors resulted in significantly (P < 0.01) higher heart rates than resting on land (100 f 5 beats/min) (n = 143), whilst diving resulted in the lowest heart rate (61 + 6 beats/min) (n = 367). The heart rate for diving represented 48% of the swimming heart rate. Only behaviors in which all the *Swain U. G., Gilbert F. F. and Robinette Diving bradycardia in captive, free-ranging mitted to Physiol. Zoo/.)
J. D. (1988) beaver (sub-
beavers were represented were included in this analysis (P < 0.01, ANOVA). Beavers not only showed a bradycardic response during diving, but also when sleeping. The average sleeping heart rate was 75 f 5 beats/min (n = 41, Iv = 5), which was 75% of the resting heart rate (P < 0.01 paired r-test). Heart rates of both feeding (123 + 5 beats/min) (n = 40, N = 6) and alert resting (115 + 4 beats/min) (n = 421, N = 5) were comparable to heart rates of other active behaviors and that of resting in water (P > 0.05, ANOVA). Following diving, no transient recovery tachycardia was observed during the first 15 set of swimming, however the average swimming heart rate, as recorded for the entire episode, was higher after diving (127 f 3 beats/min) (n = 467) than after other precursor behaviors (123 + 3 beats/min) (n = 280) (P < 0.001 paired t-test). There was also an indication that swimming heart rates following diving were reflective of dive durations, with heart rates ranging from 124 k 3 beats/min after dives of less than 10 set (n = 191) to 134 ? 5 beatsjmin following dives exceeding 2 min (n = 40) (N = 4). Heart rates were determined at different ambient temperatures (Table 1). Active and resting in-water behaviors recorded at colder average air (- 1“C) and water (1’C) temperatures had a higher mean heart rate than behaviors at warmer average temperatures (21°C for air, 17°C for water) (P < 0.05 t-test). Although not significant, this trend of higher heart rates at colder temperatures was also observed for alert resting and sleeping. Resting proved the exception with heart rates being comparable at the different temperatures (P > 0.05). However, only 11 resting behavioral episodes were recorded for the two beavers monitored during the winter. Diving heart rates were excluded from the analysis because of their dependency on dive duration (Swain, 1985). Dives recorded for beavers at colder temperatures had a mean dive duration of 10 f 15 set (n = 119), whereas dives at warmer temperatures were considerably longer (P < 0.001) with a mean duration of 32 k 38 set (n = 675). Beavers exhibited a marked fear bradycardia (57 + 16 beats/min) (n = 22) (N = 5) when threatened on land. Heart rate dropped suddenly in response to threat and remained at low levels after removal of the stimulus (Fig. 1). The lowest heart rate recorded for an episode of fear bradycardia was 9 beats/min. The heart rate of fear bradycardia averaged 57% of the rate for resting behavior and was comparable to the bradycardia observed upon diving (I’ < 0.05, ANOVA). Analysis of individual behavioral episodes on an instantaneous heart rate basis indicated a sinus arrythmia (cf. Fig. 1). Respiration appeared as a wave form of successive IHRs and gave a mean resting respiration rate of 15 f 1 breaths/min. DISCUSSION determinations restrictive captive conditions unable to carry out natural The current research allowed ral activities in the beaver, Heart
rate
are often hampered by in which the animals are behavioral repertoires. the occurrence of natualthough it is suggested
Heart rate in the beaver
433
Table 1. Mean heart rate values (f SE) for free-ranging captive beaver monitored water (T,,,) temperatures Mean ambient Behavior* Diving Sleepingt Resting Alert restingt Resting in water Investigaling Grooming Feedingt Swimming
T, = - I ‘, T,,,, = I (N = 2) 57.2 f 8.41 (69) 81.5 + 6.9 (17) 97.1 i2.1g (II) 122.1 27.3 (157) 130.4 f 7.611 (51) 125.7 k 5.711 (109) 131.4+2.21l (200) 138.3 & 0.2 (7) 132.4* 5.911 (129)
temperatures
T,=21’,
at different air (T,) and
(‘C)
THlo=17
(N=5)
P’I
62.9 + 7.51 (298) 71.1 k7.6 (24, N=3) 101.0 k 2.e (132) 110.8 i 2.6 (264, N = 3) 115.9? I.311 (187) 115.8 + I.211 (267) 116.8 f 2.211 (648) 115.2* I.1 (33, N =4) 123.4 + 1.9 (618)
Number of behavioural episodes given in brackets. Number of animals (N) given in brackets when all beaver are not represented *Significant behavioral effects, F,,, = 59.51, Fo,20= 34.34. tBehavior not included in ANOVA. $$I1 within columns, heart rates with dlfferent letter subscripts are significantly l’significance levels of t-test for heart rates at different ambient temperatures.
that probably more time was spent in investigating and less in building than in the wild. Beaver heart rates varied with respect to the activity level of the behavior. Active behaviors may be distinguished from inactive behaviors on the basis of heart rate, but the wide ranges in heart rates of the more active behaviors preclude determination of individual active behaviors. Heart rate values for grooming, swimming and diving were similar to those reported for beavers by Gilbert and Gofton (1982). However, the resting heart rate they reported was comparable to the alert resting value in this study and probably reflects the more natural conditions of this study. The higher heart rate of resting in water, as compared to resting on land, was possibly due to the increased thermoregulatory cost in water. An increase in heart rate following diving can be interpreted as part of the physiological mechanisms
0.5 0.5 0.2 0.05 0.05 0.02 0.001 0.05
in behavior
different
mean.
at the 0.01 level.
initiated upon surfacing in response to the oxygen debt incurred during the dive (Irving and Orr, 1935; Scholander, 1940) or, in the case of cold water temperatures, hypothermia induced by diving. Beaver display no transient increase in heart rate during the first 5, 10 or 15 set following a dive; however the heart rate of the entire post- or inter-dive behavior is higher, indicating that beaver-like swamp rabbits (Syfvilugus aquaricus) (Smith and Tobey, 1983) and diving ducks (e.g. Aythya ferina, Aythya fiIigulu) (Butler and Woakes, 1979) have a recovery tachycardia following diving. In diving ducks, the tachycardia lasted l&15 set following a dive, whereas the time required for the heart rate to return to pre-dive levels in the beaver was longer. However, exact determination of the time course for recovery tachycardia was not undertaken. Diving ducks also portray a relationship between the magnitude of post-dive tachycardia
TIME IN SECONDS
Fig. I. Instantaneous threatening stimulus
heart rates for beaver Ai during an episode of fear bradycardia. Bar indicates of the approach of the investigator. Note the respiratory sinus arrythmia during the pre-stimulus behaviors.
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UNA G. SWAIN et al.
and the duration of the dive (Butler and Woakes, 1979). A similar situation was evident in beaver, where the longer dives elicited higher heart rates upon surfacing. Temperature is one of the many factors that may affect heart rate; however very few studies have investigated its influence on heart rate and, in particular, its influence on the diving heart rate. Hammel et al. (1977) have shown for the harbor seal (Phoca ritulina) that the usual vasoconstriction reflex observed during diving can be abolished if the preoptic area of the hypothalamus is artificially heated during submergence. Gilbert and Gofton (1982) found higher heart rates to be associated with all behaviors including diving in muskrat (Ondatra zibethicus) monitored at lower temperatures, while Thornton et al. (1978) recorded lower dive heart rates for muskrats in colder water temperatures. Gilbert (198 1) proposed that colder water temperatures may elevate base line heart rate values for diving in male beavers. Beavers at lower ambient temperatures displayed higher heart rates for most non-dive behaviors, probably reflecting the increased thermoregulatory costs. The lower critical temperature for beavers is given as -3°C (Coles, 1967, in Lancia et al., 1982). Behavioral observations have indicated a correlation between above-ice activity and ambient temperature (Wilsson, 1971; Lancia et al., 1982). The onset of above-ice activity occurred at air temperatures above -4°C to - lO”C, and activity increased with increasing temperatures. In the wild, the microenvironment of the lodge and frozen pond significantly moderate winter temperature extremes to near 0°C (Stephenson, 1969). Certain behavioral adaptations to cold temperatures were not feasible for the test beaver, as the study situation did not provide underwater access to the pool and hence, activity could not be restricted to below the ice during periods of subfreezing weather. Temperatures below - 3°C were common. Thus, it is likely that the beavers moving between the huts and the pool were exposed to colder ambient temperatures than they normally would have encountered in the wild, unless forced to forage on land for food when the food pile is inadequate (Gilbert, persona1 observation). The lack of emphasis placed on the influence of water temperature on diving physiology seems surprising, as any factor which may affect peripheral vasoconstriction during submergence might also be expected to alter the diving bradycardia. Definite conclusions about the effect of temperature on dive heart rates cannot be represented here, because of the effect of dive duration and because differences in heart rates may be masked when the same beavers are not represented at both temperature extremes. Both beavers monitored during the cold temperatures were females. Although the differences were not significant, dive heart rates were lower at lower temperatures. This, coupled with the observation that dives were shorter at lower ambient temperatures and should thus reflect higher heart rates (Swain, 1985), suggests that diving in colder water does elicit a deeper bradycardia in female beavers. Beavers have been shown to maintain a constant arterial blood pressure during submergence (Clausen and Ersland,
1970/71). McKean (1982) has shown that regional blood flow in beavers decreased to all organs except the adrenals, heart and lungs, and increased to the brain. It is likely that peripheral blood flow is altered to a greater degree in colder water (Thornton et al., 1978), hence the concomitant bradycardia might be expected to be of greater intensity in order to maintain a constant blood pressure (Andersen, 1966). Although our conclusions are speculative, they do point out that temperature should not be neglected in heart rate investigations. Emotional stimuli may act as strong modifying agents on heart rate. Many cases of bradycardia have been observed in non-diving situations, most of which involve an element of stress to the animal. Studies on terrestrial mammals and birds (e.g. Gabrielsen et al., 1977; Causby and Smith, 1981) suggest that the bradycardia observed in some situations has a fear component. The classic response to fear is increased heart rate and a general readiness for “flight or fight”. In those situations, however, in which the danger can be avoided more successfully by remaining motionless or hiding, bradycardia is elicited (Gabrielsen et al., 1977; Jacobsen, 1979; Smith and Woodruff, 1980). Many animals show what has been termed a “passive defence response” (Gabrielsen et al., 1985) to a threat source. Beavers display prone behavioral responses on land. They “freeze” when threatened both in the wild (personal observation) and in captivity, although if water were immediately accessible the response would be likely to be a dive. Beavers resemble incubating willow ptarmigan (Lagopus fagopus) threatened by intruders (Gabrielsen et al., 1977) white-tailed deer fawns (Odocoileus virginianus) (Jacobsen, 1979) and eastern grey squirrels (Sciurus carolinensis) (Smith and Johnson, 1984) approached by humans, and American opossums (Didelphis marsupialis) feigning death in response to a dog (Canis domesticus) (Gabrielsen and Smith, 1985). In all cases, the behavioral response was accompanied by a marked bradycardia. Studies on other diving species, such as seals, have shown that pain, abrupt noise or threatening gestures also can elicit bradycardia (Scholander, 1940). The onset of fear bradycardia was sudden in beaver and occurred immediately upon the animal’s awareness of threatening stimuli (Fig. I). The increase in heart rate observed for one of the beavers during 2 of the 4 episodes of threat is likely to be due to increased activity and movements which the investigator was unable to observe because the beaver was inside its nest box. In situations where there is no possibility of active escape, although probably rare for the beaver, fear bradycardia may enhance the prone behavioral responses which help conceal the animal and decrease the likelihood of being detected by a predator. Acknowledgements-The authors thank Dr L. Gallagher for his help with the surgical procedures and D. Douglas and J. Thomas for their technical assistance. Una Swain was the recipient of a Washington State University graduate research assistantship during part of the project. The study was supported by a grant to F. Gilbert from the International Fur Trade Federation.
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