MN Black Bear Research

Black bears (Ursus americanus) typically remain inactive during hibernation, during which time their body temperatures only drop to 1-3°C below normal and they typically do not eat, drink, urinate, or defecate. Yet, during hibernation, these bears can return to apparently normal systemic function within seconds of arousal: a perceived threat in their environment (a fight or flight response). It is hypothesized that their cardiovascular functions during hibernation are conservative in terms of overall energy expenditure, but are also capable of supporting rapid arousal in the events of predatorial threats. Such observed reductions in cardiovascular function without some innate protective mechanisms; if these dramatic reduced functions occurred in other large mammals (including humans), within hours such would result in irreversible ischemic tissue damage and/or clotting. Note, many large mammals will elicit some energy conservation mechanisms.

Along with their research partners at the Minnesota DNR and Medtronic, the VHL has studied the annual cardiovascular performances of free-ranging black bears using implantable data recorders. Additionally, during den visits, the periodic collections of echocardiographic and electrocardiographic (12-lead) assessments are used to show that both cardiac mass and electrical behaviors are conserved during hibernation [1]. Dramatic heart rate modulations, known as “respiratory sinus arrhythmias”, i.e., from exceptionally low resting heart rate values of 5 to 10 beats/min, then accelerating up to 60-70 beats/min only during inspiration (for ~ 2-3 beats). It is hypothesized that this behavior aids to minimize energy expenditures while maintaining adequate brain, heart, and other tissue perfusions as well as oxygen delivery. Interestingly, during expiration a given bear’s heart may elicit pauses between 5 to 30 seconds and this behavior can be recorded throughout hibernation. Of interest a human will typically pass out if they do not have a heartbeat for ~6 seconds. Can bear’s elicit normal sleep during hibernation if they do not have normal brain function? One of our proposed hypotheses, is that normal sleep behaviors are not elicited during hibernation and thus requires several weeks for such to return after early den emergence.

Fig. Electrocardiograms from hibernating wild black bears. Thirty second traces with low heart rates (left) and respiratory sinus arrhythmias (RSA, right) are shown for four different bears. Electrical data were captured with implanted data recorders during mid-winter. RSAs were seen in all animals and were identified by an increase in heart rate and a modulation of the electrogram amplitude corresponding with chest expansion and relaxation. The respiration rates that elicited the RSA identified in the right panels for Bears 1–4 are two, six, four, and two breaths/minute, respectively. Electromyographic activity (EMG) is noted in the right epochs for Bears 1 and 2 and the left epoch for Bear 4. (Laske et. al., 2010).

It is hypothesized that these adaptive cardiovascular behaviors could have broad implications for human medicine (e.g., how to better treat Seasonal Affective Disorder, heart failure, or post-myocardial infarction or a heart attack) and possibly space travel, since it would allow for prolonged periods of lower activities while maintaining both cardiac capacity and abilities to rapidly return to alertness. Note, that some non-hibernating mammals will elicit greater degrees of respiratory arrythmias and reduced heart rates through the year.

From a conservation biology standpoint, we have used the data collected from the implanted biologgers to provide insights relative to black bear behaviors during non-hibernation active periods. 

For example, roadways may negatively impact wildlife species through vehicular-related mortality and spatial displacement or obstruction. In one study, we investigated physiological responses to provide insights into a given animal’s perception of its environment. We deployed Global Positioning System (GPS)-collars in combination with implanted cardiac biologgers on American black bears (Ursus americanus; 18 bear-years) in areas with differing road densities across Minnesota. We tested whether bears exhibited acute stress responses, as defined by significant increases in heart rate (HR), associated with road crossings. Maximum HR between successive telemetry locations were, on average, 13 bpm higher when bears were known to cross a road. They crossed a road, on average, once per day. Different demographic groups (males, females with and without cubs) responded similarly. We found stronger HR responses when crossing high-traffic roads relative to low-traffic in half of the bear-year combinations we sampled. Bears crossed high-traffic roads mainly at night, but low traffic roads during daylight hours. Bear HRs first became elevated when they were approximately 70−180 m away from roadways. Our findings suggested that roadways act as an acute stressor, but the magnitudes of the stress responses appeared to be mild. Elevated HRs may reflect an increased vigilance and recognitions of threat when preparing to cross a road. We considered that a given bear’s recognition and alertness to human-related threats is adaptive for living in human-altered landscapes.

In an interesting series of studies, unmanned aircraft systems (drones) were used to visualize some of our free-ranging bears during summer months. We utilized unmanned aircraft systems (UAS; i.e. ‘drones’) as means to provide new opportunities for data collection in ecology, wildlife biology and/or conservation.

Several previous studies by others have documented behavioral or physiological responses to close-proximity UAS flights. In our research, we experimentally tested whether American black bears (Ursus americanus) habituate to repeated UAS exposure and whether tolerance levels persist during an extended period without UAS flights. Using implanted cardiac biologgers, we measured heart rates (HRs) of five captive bears before and after the first of five flights each day. Spikes in HR, a measure of stress, diminished across the five flights within each day and over the course of 4 weeks of twice-weekly exposure. We halted flights for 118 days, and when we resumed, HR responses were similar to those recorded at the end of the previous trials. Our findings highlight the capacity of a large mammal to become and remain habituated to a novel anthropogenic stimulus in a relatively short time (3–4 weeks). However, such habituation to mechanical noises may reduce their wariness of other human threats. Also, whereas cardiac effects diminished, frequent UAS disturbances may have other chronic physiological effects that were not measured. We caution that the rate of habituation may differ between wild and captive animals: while the captive bears displayed large initial spikes in HR changes (albeit not as large as wild bears), these animals were accustomed to regular exposures to humans and mechanical noises that may have hastened habituations to the UAS.

References:

1. Laske TG, Harlow HJ, Werder JC, Marshall MT, Iaizzo PA: High capacity implantable data recorders: system design and experience in canines and denning black bears. Journal of Biomechanical Engineering 127:964-971, 2005.
2. Laske TG, Harlow HJ, Garshelis DL, Iaizzo PA: Extreme respiratory sinus arrhythmia enables overwintering black bear survival—physiological insights and applications to human medicine. Journal of Cardiovascular Translational Research 3:559-569, 2010. DOI: 10.1007/s12265-010-9185-7.
3. Laske TG, Garshelis DL, Iaizzo PA: Monitoring the wild black bear’s reaction to human and environmental stressors. BMC Physiology 11:13, 2011. DOI: 10.1186/1472-6793-11-13.
4. Laske TG, Garshelis DL, Iaizzo PA: Big data in wildlife research: remote web-based monitoring of hibernating black bears. BMC Physiology 14:13, 2014. DOI: 10.1186/s12899-014-0013-1.
5. Iles TL, Laske TG, Garshelis DL, Iaizzo PA: Blood clotting behavior is innately modulated in Ursus americanus during early and late denning relative to summer months. Journal of Experimental Biology 220 (Pt 3):455-459, 2017. DOI: 10.1242/jeb.141549.
6. Laske TG, Iaizzo PA, Garshelis DL: Six years in the life of a mother bear—the longest continuous heart rate recordings from a free-ranging mammal. Scientific Reports 7:40732, 2017. DOI: 10.1038/srep40732.
7. Laske TG, Evans AL, Arnemo JM, Iles TL, Ditmer MA, Fröbert O, Garshelis DL, Iaizzo PA: Development and utilization of implantable cardiac monitors in free-ranging American black and Eurasian brown bears: system evolution and lessons learned. Animal Biotelemetry. 6:13, 2018. DOI: 10.1186/s40317-018-0157-z.
   Ditmer MA, Vincent JB, Werden LK, Tanner, JC, Laske TG, Iaizzo PA, Garshelis DL, Fieberg JR: Bears show a physiological but limited behavioral response to unmanned aerial vehicles. Current Biology 25: 2278-2283, 2015. DOI: 10.1016/j.cub.2015.07.024.
8. Ditmer MA, Garshelis DL, Noyce KV, Laske TG, Iaizzo PA, Burk TE, Forester JD, Fieberg JR: Behavioral and physiological responses of American black bears to landscape features within an agricultural region. Ecosphere 6:Article 28 (Open access, 2015). DOI: 10.1890/ES14-00199.1.
9. Ditmer MA, Rettler SJ, Fieberg JR, Iaizzo PA, Laske TG, Noyce KV, Garshelis DL: American black bears perceive the risks of crossing roads. Behavioral Ecology 29:667-675, 2018. DOI:10.1093/beheco/ary020.

*graphic image below

Hibernating black bears (Ursus americanus) elicit profound abilities to resolve injuries while mildly hypothermic (30-35ºC) and not eating, drinking, urinating, or defecating. We continue to perform investigative studies on free-ranging black bears during denning in early winter and again in late winter. To date, three methods have been employed to induce small cutaneous wounds during three consecutive winters on 10 different bears, two of which were studied for more than one winter. Tissue samples were processed by routine histological methods and evaluated by light microscopy. All sites healed with remodeling of the dermal layers, reduced expression of scarring, and limited regrowth of hair. Even significant injuries that were incurred prior to hibernation, but which had not begun to heal at the time of hibernation, were completely resolved in 1-2 months. This unique healing ability is a clear survival advantage for bears, as those unable to heal while hibernating could suffer loss of body fluids, greatly increased metabolic demands, and/or toxicity from infection. Other hibernating mammals, however, appear to lack this ability. These observations may provide new insights, and further investigation may uncover new biological materials for treating wounds with little or no scarring in humans, especially in patients who are malnourished, hypothermic, diabetic, or elderly.

Fig. (a) Injury incurred before denning (Bear 2081), first observed in December (left) and after healing 12 weeks later (right). This animal’s core body temperature was 35.4°C in December and 32.8°C in March.

Fig. (b) Paired infrared images from those shown in (a), with the temperature scale of 25°C (black) to 35°C (white). Subsequent to initial December photos (a, left), a local subcutaneous injection of lidocaine was administered along the injury border, the injury was debrided, and single sutures were used to close the skin edges (approximately 1 cm spacing).

Fig. (c) Close-up view before (left) and after (center) suturing, as well as after a healing period (right). In the late winter photos (right), a small line of new hair can be detected (1–3 mm wide), just along the line where the skin was sutured.

Reference

• Iaizzo PA, Laske TG, Harlow HL, McClay CB, Garshelis DL: Wound healing during hibernation by black bears (Ursus Americana) in the wild: elicitation of reduced scar formation, Integrative Zoology, 7:48-60, 2012.

Wound Formation, Treatment, and Healing

The occurrence of pressure ulcers among the elderly and in hospitalized patients has an extensive impact on patients and health care providers in terms of decreased quality of life, loss of productivity, and high cost of treatment. Various studies indicate that 50-60% of all pressure ulcers in acute hospital populations develop after admission and thus are deemed preventable (i.e., more frequent risk assessment, treatment plans, specialty devices, etc.). Although extensive literature exists concerning pressure ulcers, there remains no clear consensus regarding the etiology of such wounds. Rather, several factors are known to contribute to the formation and persistence of pressure-related wounds, including elevated pressure over extended time, shear, elevated pressure augmented by elevated temperature, age, poor nutrition, incontinence, fractures, paralysis or lack of sensation, arterial insufficiency, venous stasis, and diabetes. Specifically, there are few detailed reports about the thresholds of wound formation with respect to pressure, temperature, and duration of application, and lack of clear consensus about the proper form of treatment. Clinicians use a variety of visual methods to evaluate the status of skin tissue, however these methods lack precision, and quantification of slow or subtle changes may be difficult. Accurate determination of the extent and depth of subsurface injuries would allow for appropriate and timely therapeutic intervention.

Related studies in our lab include the following:

• Development of a porcine model to facilitate investigation of pressure ulcer formation, healing, and prevention (Figures 1 and 2). This model allows for easy, independent modulation of pressure, temperature, and duration parameters to create specific classes of wounds [1].
• Investigation of the effects of duration of applied pressure and applied temperature on wound formation, as well as the threshold temperature below which focalized cooling will minimize the potential for wound formation using a porcine model. The benefits of focal cooling were evident at an extended duration and at deep tissue layers, and suggest future clinical applications for pressure ulcer prevention and therapy [2].
• Examination of the use of cutaneous reactive hyperemia as a means for noninvasive assessment of wound severity of newly formed temperature-modulated pressure injuries in a porcine model. This study employed color image analysis to determine the severity of wounds and infrared imaging/computer image processing to detect differences in skin temperature. Both techniques correlated with the severity of injuries as determined by a histologic assessment of biopsied tissue, however infrared imaging provided the better means to assess wound depth [3].
• Critical assessment of potential methodologies for noninvasive wound evaluation using a color imaging system, development of a method for quantifying histological readings, and testing these techniques on a porcine model of wound formation. Color analyses enabled statistically significant differentiation of mild, moderate, and severe injuries within 30 minutes after application of the injury, and again when the wounds were 5-7 days old; this technique could be adapted for assessing and tracking wound severity in humans in a clinical setting [4].
• Explicit definition of critical thresholds of applied pressure, duration, and temperature in the formation of pressure ulcers or cutaneous burns in a porcine model. Pathological changes in pressure ulcers were found to begin at the deep muscle and progress upward into the cutaneous layers with increasing pressure and/or duration of contact; muscle degeneration was also observed after 5 hours of ischemia (Figure 3). Thresholds for all four cutaneous layers increased with a decrease in applied temperature, suggesting that these deep tissue changes could be lessened or prevented with appropriate focal cooling. Such predictions of thresholds for injury causation could provide a predictive basis for the design and development of support surfaces and patient turning schedules for the prevention of tissue injury [5].
• Noninvasive assessment of the severity and depth of pressure injuries in dermal and subdermal tissue using infrared thermography in a porcine model. Two techniques were investigated: 1) thermographic evaluation of wounds at thermal equilibrium with normal room temperature surroundings, and 2) observation of temperature changes that occurred to the wound area after application of focal cooling. Deep tissue injuries were easily distinguished from shallow wounds by their thermal response to focal cooling, suggesting clinical utility for detecting abscessed areas of skeletal muscle that are concealed by a healthy epidermal or dermal bridge (6).

Fig 1. Cluster of 4 discs was designed to apply pressure to preselected wound sites. Temperature modulation was facilitated with a micro-processor-controlled unit; cooling was provided by a water bath and heating by electrical resistance wire. Temperatures were maintained within ±0.5°C.

Fig 2. Disc application and subsequent assessment sites

Fig 3. Illustrative representation of tissue damage at combinations of pressure, temperature, and duration that resulted in tissue alterations

References:

• Kokate JY, Leland KJ, Held AM, Hansen GL, Kveen GL, Johnson BA, Wilke MS, Sparrow EM, Iaizzo PA: Temperature-modulated pressure ulcers: a porcine model. Archives of Physical Medicine and Rehabilitation, 76:666-673, 1995.
• Iaizzo PA, Kveen GL, Kokate JY, Leland KJ, Hansen GL, Sparrow EM: Prevention of pressure ulcers by focal cooling: histological assessment in a porcine model. Wounds: A Compendium of Clinical Research and Practice, 7:161-169, 1995.
• Hansen GL, Sparrow EM, Kammamuri R, Iaizzo PA: Assessing wound severity using color and infrared imaging of reactive hyperemia. Wound Repair and Regeneration, 4:386-392, 1996.
• Hansen GL, Sparrow EM, Kokate JY, Leland KJ, Iaizzo PA: Wound status evaluation using color image processing. IEEE Transactions on Medical Imaging, 16:78-86, 1997.
• Kokate JY, Leland KJ, Sparrow EM, Iaizzo PA: Critical thresholds for pressure ulcer formation in a porcine model. Wounds: A Compendium of Clinical Research and Practice, 9:111-121, 1997.
• Hansen GL, Sparrow EM, Kalieta AL, Iaizzo PA: Using infrared imaging to assess the severity of pressure ulcers. Wounds: A Compendium of Clinical Research and Practice, 10:43-53, 1998.