Unmanned aerial vehicles (UAVs) have the potential to revolutionize the way research is conducted in many scientific fields []. UAVs can access remote or difficult terrain [], collect large amounts of data for lower cost than traditional aerial methods, and facilitate observations of species that are wary of human presence []. Currently, despite large regulatory hurdles [], UAVs are being deployed by researchers and conservationists to monitor threats to biodiversity [], collect frequent aerial imagery [], estimate population abundance [], and deter poaching []. Studies have examined the behavioral responses of wildlife to aircraft [] (including UAVs []), but with the widespread increase in UAV flights, it is critical to understand whether UAVs act as stressors to wildlife and to quantify that impact. Biologger technology allows for the remote monitoring of stress responses in free-roaming individuals [], and when linked to locational information, it can be used to determine events [] or components of an animal’s environment [] that elicit a physiological response not apparent based on behavior alone. We assessed effects of UAV flights on movements and heart rate responses of free-roaming American black bears. We observed consistently strong physiological responses but infrequent behavioral changes. All bears, including an individual denned for hibernation, responded to UAV flights with elevated heart rates, rising as much as 123 beats per minute above the pre-flight baseline. It is important to consider the additional stress on wildlife from UAV flights when developing regulations and best scientific practices.

Results

We investigated the influence of unmanned aerial vehicle (UAV) flights on the behavior and physiology of free-roaming American black bears (Ursus americanus) in northwestern Minnesota by capturing their location and movement with Iridium satellite GPS collars and heart rate (HR) in beats per minute (bpm) using cardiac biologgers developed for human use (Medtronic, Reveal XT Model 9529). Both GPS collars and biologgers recorded values at 2-min intervals, so it was possible to discern how individual bears responded, at fine temporal and spatial scales, to short-duration UAV flights. We flew a small quadcopter UAV (3D Robotics) using a fully autonomous mission plan that loitered and circled approximately 20 m over the location of the bear (pre-programmed just before takeoff) during the course of a 5-min flight. We hypothesized that bears would respond to the UAV in one of four ways: (1) no discernable behavioral or physiological response, (2) behavioral response only (i.e., increased movement rates and/or moving away from the area of the UAV), (3) no behavioral response, but a physiological response (measurable increase in HR), and (4) both a behavioral response and physiological response.

Figure 1 Illustration of Bear Movement and HR during a UAV Flight Show full caption (A) Movement rates (meters per hour) of an adult female black bear with cubs of the year as estimated using 2 min GPS locations prior to, during, and after a UAV flight (gray bar). (B) The corresponding HR in bpm during the same day and time measured using a remote cardiac biologger developed by Medtronic. We flew unmanned aerial vehicles over American black bears living in northwestern Minnesota during September and October 2014. See also Figure S1 and Movie S1 We conducted 18 UAV flights above or near four bears from September 21, 2014 to October 12, 2014. For 17 of these flights, we were able to collect associated HR and location data ( Figure 1 Movie S1 ). Nine flights were conducted over two adult female bears with cubs (eight over one and one over the other), three flights were conducted over a 1-year-old male bear, and six flights were conducted over an adult female bear that entered a den for winter hibernation 2 days prior to the first UAV flight. Flight times averaged 5 min 3 s (SE = 16.7 s). Absolute altitude (height above ground) was influenced by vegetation and averaged 21.0 m per flight (SE = 1.45) including takeoff and landing. The minimum distance between the UAV and the target bear averaged 43 m (SE = 5.67). On average, the UAV was launched 215 m (range: 184–245) from the targeted location of the bear.

26 von Borell E.

Langbein J.

Després G.

Hansen S.

Leterrier C.

Marchant-Forde J.

Marchant-Forde R.

Minero M.

Mohr E.

Prunier A.

et al. Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals -- a review. Figure 2 Method and Results of Bear Maximum HR Anomalies during UAV Flights Show full caption (A) Method for calculating HR anomalies during an 8-min period starting at the takeoff of UAV flights and on days without UAV flights during the same time period. We fit a linear regression model to HR data collected 1 hr prior to the flight (or control observation window), using natural cubic regression splines with 2 degrees of freedom to account for temporal trends in the HR values. We used the fitted model to predict HR values during the subsequent 8-min period. We measured the physiological response to the UAV flight (and also control measurements) as the maximum difference between observed and predicted values, divided by the SD of the observed values (from the hour prior to the flight or control observation window). (B) The empirical cumulative distribution function (ECDF) for the HR anomalies associated with UAV flights and the median and 95% simulation envelope calculated using controls taken from days without UAV flights. (C) Maximum HR anomaly data for non-UAV flight times are shown as boxplots along with the values associated with UAV flight times (red dots) for the three individual bears with HR data. See also Figure S2 Bears responded to UAV flights with elevated HRs in all 17 flights with corresponding HR data ( Figure S1 ). We calculated the “maximum HR anomaly” for bears by comparing the observed differences between maximum bear HRs and predicted values during UAV flights (see Figure 2 A for brief description or Experimental Procedures for full description). The maximum HR anomalies associated with UAV flight times were significantly higher than the maximum HR anomalies during days without flights ( Figure 2 B). Maximum HR anomalies were the largest for the female with cubs, followed by the hibernating adult female, and finally the young male ( Figure 2 C). The maximum difference between observed and predicted HR values during UAV flights was 123 bpm for a female with cubs ( Figure S2 ), 56 bpm for the hibernating adult female, and 47 bpm for the 1-year-old male. Bear HRs recovered after the completion of every UAV flight to within the 99% confidence interval associated with HRs 30 min prior to a given flight, with median recovery times of 10 min (range: 2–204 min), 16 min (range: 4–20 min), and 5 min (range: 4–6 min) for the female with cubs of the year, hibernating adult female, and young male, respectively. These durations in HR elevations were likely associated with sympathetic activations of catecholamine releases from the adrenal glands (e.g., []).

2: X ¯ = 0.84, SE = 0.05). HR anomalies were positively associated with wind speed ( Figure 3 Factors Influencing Bear HRs during UAV Flights Show full caption (A and B) Relationships, including an ordinary-least-squares regression line, between the maximum HR anomaly values (see Figure 2 A) and ambient wind speed (mph) (A), and minimum distance (m) (B) between the UAV and the bear during each flight. UAV flights occurred above or near American black bears located in northwestern Minnesota during September and October 2014. During controlled test flights in different habitats (forest, shrub, open) and different wind speed conditions (methods found in Supplemental Information ), variation in ambient noise (dB(A)) was largely explained by distance to the UAV (negative association), absolute altitude of the UAV (negative association), and an interaction of the two (positive association, average multiple r= 0.84, SE = 0.05). HR anomalies were positively associated with wind speed ( Figure 3 A) and negatively associated with the distance between the UAV and the bear ( Figure 3 B). These relationships suggest that stress responses were stronger when UAV flights involved an element of surprise: bears likely could not hear the approach of the UAV in windier conditions, so they were more startled.