Monitoring the wild black bear's reaction to human and environmental stressors
© Laske et al; licensee BioMed Central Ltd. 2011
Received: 25 January 2011
Accepted: 17 August 2011
Published: 17 August 2011
Bears are among the most physiologically remarkable mammals. They spend half their life in an active state and the other half in a state of dormancy without food or water, and without urinating, defecating, or physical activity, yet can rouse and defend themselves when disturbed. Although important data have been obtained in both captive and wild bears, long-term physiological monitoring of bears has not been possible until the recent advancement of implantable devices.
Insertable cardiac monitors that were developed for use in human heart patients (Reveal® XT, Medtronic, Inc) were implanted in 15 hibernating bears. Data were recovered from 8, including 2 that were legally shot by hunters. Devices recorded low heart rates (pauses of over 14 seconds) and low respiration rates (1.5 breaths/min) during hibernation, dramatic respiratory sinus arrhythmias in the fall and winter months, and elevated heart rates in summer (up to 214 beats/min (bpm)) and during interactions with hunters (exceeding 250 bpm). The devices documented the first and last day of denning, a period of quiescence in two parturient females after birthing, and extraordinary variation in the amount of activity/day, ranging from 0 (winter) to 1084 minutes (summer). Data showed a transition toward greater nocturnal activity in the fall, preceding hibernation. The data-loggers also provided evidence of the physiological and behavioral responses of bears to our den visits to retrieve the data.
Annual variations in heart rate and activity have been documented for the first time in wild black bears. This technique has broad applications to wildlife management and physiological research, enabling the impact of environmental stressors from humans, changing seasons, climate change, social interactions and predation to be directly monitored over multiple years.
KeywordsElectrophysiology Hibernation Cardiac Physiology
Data loggers (archival tags) that are attached or surgically implanted in animals to collect and store or relay information about activity, movements, physiology, and the local environment are becoming increasingly sophisticated and useful to biologists [1, 2]. Such devices have been used to monitor heart rate and activity of free-ranging reptiles, birds, and mammals [3–5]. With rapid advancements in electronics over the past decade, data logger packages have become smaller and less invasive while the period of monitoring has increased from days to months, and rarely up to 1 year [6, 7]. With the aid of these devices, biologists have been able to study critical changes in animal physiology related to their natural history (e.g., migration, foraging dives, fasting) or in response to human disturbance [8–11].
One of the most profound changes in physiology is hibernation, and one of the most physiologically remarkable hibernators is the bear. Smaller hibernators have bouts of arousal and survive the winter in secluded burrows where risks of predation are minimal. By contrast, bears pass the winter in a state of shallow hypothermia without bouts of active arousal [12, 13]. However, because of their large mass, they are often in partially-exposed dens with associated higher risks for predation and/or external disturbance [14, 15]. Although they have depressed metabolic functions during this period, we have commonly noted defensive posturing and high respiratory rates by bears within a very short period (seconds) of being disturbed. Bears have limited loss of skeletal muscle protein and strength during winter [16–18]. Likewise, their heart is able to revert from the quiescent state of hibernation, conserving energy for up to 6 months of fasting, to supporting a burst of activity in a very short interval. In this respect, the black bear's heart function may be unique among mammals.
Earlier studies reported significant reductions in bears' heart rates, contractility, mass, and output when comparing summer and winter [19–21]. Additional work indicated that cardiac wall thickness and function (electrophysiological parameters) were maintained during the period of hibernation . We previously observed winter heart rates as low as 4.5 bpm, with a dramatic respiratory sinus arrhythmia (RSA) enabling the heart to rest between inspirations . We hypothesized that the RSA is an adaptive mechanism to conserve energy while maintaining adequate cardiac perfusion over winter to sustain the "fight or flight" response.
Previous findings about the seasonal adaptations of ursid hearts were based upon data obtained at a limited number of discrete time intervals from animals that were either chemically anesthetized or hand-reared and trained for these procedures [19–22]. Recent advances in implantable devices applied to the management of human clinical patients have the potential to remove the current barriers associated with long-term monitoring in the wild. In this study we sought to document for the first time annual trends in heart rate and activity from continuous monitoring of free-ranging bears. By studying undisturbed bears in the wild, we sought to elucidate both the physical and environmental situations (seasonal changes, entering/emerging from hibernation, changes in the availability of food, birthing of cubs) and mechanisms (interaction of heart rate, respiration rate, and activity) that motivate their physiological and behavioral changes.
Additional file 1:Hibernating female bear video 1. Hibernating female bear with cubs prior to tranquilization March 2008. (AVI 16 MB)
In addition to storing the timing of each heartbeat and daily activity over the three year life of the device, the device memory can store up to 22.5 min of ECG recordings from patient-activated episodes and up to 27 min of ECG recordings from automatically detected arrhythmias. The devices also report daytime heart rate (HR) (08:00-20:00; referencing a 24 hour clock) and nighttime HR (0:00-04:00). For human patients, the ICM records cardiac information in response to both automatically detected arrhythmias and patient activation using a hand held device prescribed at the time of device implantation. Although designed for activation by a clinical patient during symptomatic episodes, the device can be activated by researchers and clinicians to record electrocardiograms during periods of interest. Arrhythmias that can be selected for automatic detection include: atrial tachyarrhythmias/atrial fibrillation (AT/AF), bradyarrhythmias (slow heart rates), asystole (long periods without a heart beat), and ventricular tachyarrhythmias (high heart rates).
We programmed devices after implantation in bears using a portable programmer, and used the same programmer to download data through the skin of bears visited at winter dens a year later. Devices were implanted in March 2009 and 2010, and follow-up visits were made the following December and March. In addition to continuously recording heart rates and activity, the devices were programmed to automatically detect and store the ECG for episodes in which: 1) a heart rate of at least 167 beats per minutes (bpm) was sustained for at least 16 beats ("tachycardia"), 2) a heart rate of less than 31 bpm was sustained for at least 4 beats ("bradycardia"), and 3) pauses of at least 4.5 seconds between consecutive heart beats ("asystole"). For purposes of data analyses, the period of winter inactivity (essentially the period of winter hibernation) was defined as the interval from when activity dropped below 1 hour/day in the fall to the time when activity of over 3 hours/day was sustained in the spring. Studies were conducted in conjunction with the Minnesota Department of Natural Resources and were approved by the University of Minnesota's Animal Care and Use Committee. All statistical analyses were performed using the non-parametric Mann-Whitney U-test. Normality was evaluated using a Shapiro-Wilk test. P-values less than or equal to 0.05 were considered significant.
Data were retrieved from 7 of 14 devices implanted in wild Minnesota black bears (Ursus americanus), and also from a bear that was kept in captivity over winter and released in spring. Annual HR and activity data were successfully retrieved from 6 bears and partial data sets were retrieved from 2 bears shot by hunters in the fall. The data from the other 7 devices were lost when bears were shot by hunters and not retrieved or when rejected by bears due to a foreign body response (as has been previously reported for other devices implanted in wild bears) [7, 24]. The devices that remained implanted showed no evidence of inflammation or irritation. All sutures had been absorbed and the subcutaneous insertion sites (an incision of 1.5 cm) were no longer detectable. For the devices that were rejected, the implantation site was no longer detectable and could only be located via the patch of hair that had been shaved at the time of implant. The animals from which annual datasets were successfully collected included: two adult males, two females with cubs that denned with them during the subsequent winter as yearlings, a female with yearlings that became pregnant and gave birth to two cubs during the winter study period, and a female for which two consecutive years of data were obtained, who denned with yearlings during one winter and gave birth to cubs the second year.
Summary of heart rate and activity data recorded over a 12 month period in wild black bears.
Implant Date (Den Visits)
Heart Beats per Year#
Minimum Average Daily HR
Maximum Average Daily HR
Daytime HR Higher
Minimum Average Nighttime HR
Maximum Average Nighttime HR
Nighttime HR Higher
Minimum Daily Activity
Maximum Daily Activity
Duration of Winter Inactivity@
Longest Sinus Pause Confirmed by ECG
Maximum HR Confirmed by ECG
Denning with cubs 2008-9, and yearling in 2009-2010
27.5 × 106
Apr-May (< 0.0001)
July-Sep (< 0.0001)
(6X: 02-Dec to 11-Feb)
(5X: 17-Dec-09 to 3-Feb-10)
Denning with yearlings 2008-9, and birthing cubs in 2009-2010
23.5 × 106
May-Sep (< 0.0001)
(4X: 13-Jan-10 to 1-Feb-10)
(18-Dec-09, 05-Mar-10, 05-Mar-11)
Denning with cubs 2008-9, and yearlings in 2009-2010
24.9 × 106
June-July (< 0.0001)
(26-Nov, 27-Nov, 8-Dec)
(34X: 26-Oct to 26-Feb)
(18-Dec-09, 05-Mar-10, 05-Mar-11)
Denning with yearlings 2009-2010 and birthing cubs in 2010-2011
25.9 × 106
Jun-July (< 0.0001)
(5X: 7-Jan to 13 Jan)
23.4 × 106
(4X: 20-22-Dec, 16-Feb)
(13X: 24-Nov to 16-Feb)
Sep (< 0.0001)
Denning in rescue facility. Released 7-May.
June-Aug (< 0.0001)
Yearling that denned with mother
May-Aug (< 0.0001)
(3X: 11-Dec, 16-Dec, 20-Dec)
Mar (< 0.0001)
Nov (< 0.0001)
(8X: 19-Nov to 21-Dec)
Aug-Sep (< 0.0001)
Denning with cubs in 2009-2010 and yearlings in 2010-2011
25.3 × 106
Apr-July (< 0.0001)
Sep (< 0.0001)
(51X: 14-Nov to 7-Mar)
980 min (19-Jul)
A sharp decline in both HR and activity occurred in September and October, with the first day of denning evident from a dramatic drop in activity (Figures 1, 2 and 3). The duration of winter inactivity (including 2 winters for bear 3) was 176 ± 20 days (range: 148 to 195 days) with only 24 ± 6% of heart beats occurring during this period. A sharp increase in heart rate was evident in late December for all bears, corresponding to the winter den visit by the research team; this elevated rate was sustained for 1-2 days after our disturbance. During our March visit to the den of the female with newborn cubs (bear 2), there were fresh wolf tracks near the den entrance. This encounter resulted in only a subtle increase in activity and heart rate, as there were no large spikes in the record. A sharp cessation of activity in mid-January preceded by a period of elevated heart rate is seen in the expanded plot for bear 2 (Figure 1) and in the second year for bear 3, corresponding to the birth of cubs. The mother may have remained in a more stationary position immediately after birthing so as not to crush the altricial cubs, which stay warm underneath her, and to provide them constant access to milk. Changes in mid-winter activity were not observed for the females with yearlings (which do not nurse during winter). The ICM in bear 4 (an adult male) ceased collecting activity data in early June during the height of the breeding season. The cause of the data loss is not yet known because the device remains implanted, but we suspect that the activity circuitry may have been damaged since cessation of data collection correlated to a period of high heart rate and activity. The device lies just under the skin, so is potentially vulnerable to damage from high impact.
The trend data for one of two bears legally shot by a hunter is shown in the lower panel of Figure 3 (bear 5). The general trends in heart rate and activity are similar to bears 1-4 with the exception of the late winter/springtime data during which time this bear was housed outdoors in a wildlife rescue facility. Although the activity levels (physical movement) of bear 5 were very limited and appeared to be similar to the other bears in late hibernation, the bear's heart rate was substantially elevated until it was released into the wild (May 7). The data from bear 5 were included here because they demonstrate the physiological reaction to the hunt and also highlight the disparity in heart rates between captive and free-ranging bears.
This is the first investigation of continuous annual heart rhythms and associated body acceleration activities recorded from bears in the wild. In addition, we believe this to be the first recording of physiological parameters from an animal hunted in the wild. The ICMs yielded 24 hour data throughout a 12 month period, providing contrasts between periods of hibernation and non-denning activity, and a record of the transitions between the two. The devices provided valuable insights into the otherwise non-obvious influence on the bear's physiology and behavior during data collection activities, as well as behaviors associated with birthing, cub-rearing, hunting, and natural seasonal variations. Although the general trends seen in heart rhythms during summer and winter data collection intervals were similar to those reported in previous studies, we documented natural extremes in both high and low heart rates that exceeded any previously recorded in either wild or captive bears [7, 19–22]. Our observation of bears becoming more nocturnal in fall is consistent with activity data collected from radio-collared black bears in Minnesota and elsewhere, and may be related to a change in the types of food eaten, thermoregulatory responses to increased body mass, and/or avoidance of hunters [27, 28].
The effects of environmental changes on animals like bears are often assessed by investigating movements, habitat use, and stress hormones, but these techniques have a number of limitations [29–33]. We suggest that implantable heart and activity monitors that are made for use in humans, and thus seeing rapid technological improvement, are readily adapted for monitoring behavioral and physiological changes in wild animals. The device used in this study enabled the collection of cumulative annual activity and number of annual heart beats, allowing for the longitudinal assessments of the physiological stress imposed by such factors as human encroachment and climate change on wild cohorts. To date, we have not yet fully exploited the opportunities offered by this technique. A future step might entail a comparison of heart rates with ambient temperature, which varied from -30 to 42°C during this study. Additionally, the study bears all had radio-collars with GPS units that stored locational data that can be matched to habitat. Thus, we expect to be able to ultimately investigate heart rhythms and activity patterns as bears moved from dense forest to open fields, crossed roads, came near houses, and fed in agricultural fields. Our study site is at the extreme western edge of the bear range for the eastern United States, and contains a patchwork of small woodlots interspersed with agriculture. Much of the day-to-day variation in average heart rates exhibited over the course of the active season (Figures 1, 2 and 3) was likely due to bears moving across this patchwork of habitats, probing the limits of their range, and at some level, interacting with anthropogenic aspects of their environment. Novel insights into how they react biologically to this environment are likely to be gained through a complete record of their heart beats. We thus suggest that ICMs may be a useful addition to the burgeoning field of conservation physiology . New devices, applications, and procedures for heart rate monitoring will continue to advance the growing body of literature investigating effects of human activities and other environmental stressors on wildlife [35–40].
We thank Karen Noyce and Brian Dirks of the Minnesota Department of Natural Resources and Mark Ditmer of the University of Minnesota for assistance in the field work, Paul Krause, Joseph DePalo, and Kyle Berndt of Medtronic for technical assistance with the Reveal® XT, and M.A. Mahre for assistance with manuscript preparation. This work was supported by the Minnesota Department of Natural Resources, University of Minnesota Institute for Engineering in Medicine and Department of Surgery, and Medtronic, Inc.
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