Bears Show a Physiological but Limited Behavioral Response to Unmanned Aerial Vehicles

Report

Bears Show a Physiological but Limited Behavioral

Response to Unmanned Aerial Vehicles

Graphical Abstract

Highlights

d Cardiac biologgers reveal that bears exhibit a stress

response to UAV ﬂights

d Bears rarely display a behavioral response, measured by GPS

collars, to UAV ﬂights

d Magnitudes of heart rate spikes were correlated with wind

speed and proximity of UAV

Authors

Mark A. Ditmer, John B. Vincent,

Leland K. Werden, ..., Paul A. Iaizzo,

David L. Garshelis, John R. Fieberg

Correspondence

[email protected]

In Brief

Unmanned aerial vehicles (UAVs; i.e.,

‘‘drones’’) are increasingly popular tools

for ecological research. Ditmer et al. used

GPS collars and cardiac biologgers to

assess effects of UAV ﬂights on free-

roaming bears. All bears exhibited a

stress response to UAV ﬂights as

evidenced by elevated heart rates while

rarely exhibiting a behavioral response.

Ditmer et al., 2015, Current Biology 25, 2278–2283

http://dx.doi.org/10.1016/j.cub.2015.07.024

Current Biology

Report

Bears Show a Physiological but Limited

Behavioral Response to Unmanned Aerial Vehicles

Mark A. Ditmer,

John B. Vincent,

Leland K. Werden,

Jessie C. Tanner,

Timothy G. Laske,

4,5

Paul A. Iaizzo,

David L. Garshelis,

and John R. Fieberg

Department of Fisheries, Wildlife & Conservation Biology, University of Minnesota, St. Paul, MN 55108, USA

Plant Biological Sciences Graduate Program, University of Minnesota, St. Paul, MN 55108, USA

Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN 55108, USA

Atrial Fibrillation Solutions, Medtronic plc, Mounds View, MN 55112, USA

Department of Surgery, University of Minnesota, Minneapolis, MN 55455, USA

Minnesota Department of Natural Resources, Grand Rapids, MN 55744, USA

*Correspondence: [email protected]

http://dx.doi.org/10.1016/j.cub.2015.07.024

SUMMARY

Unmanned aerial vehicles (UAVs) have the potential

to revolutionize the way research is conducted in

many scientiﬁc ﬁelds [1, 2]. UAVs can access remote

or difﬁcult terrain [3], collect large amounts of data for

lower cost than trad itional aerial methods, and facil-

itate observations of species that are wary of human

presence [4]. Currently, despite large regulatory hur-

dles [ 5], UAVs are being deployed by researchers and

conservationists to monitor threats to biodiversity

[6], collect frequent aerial imagery [7–9], estimate

population abundance [4, 10], and deter poaching

[11]. Studies have examined the behavioral re-

sponses of wildlife to aircraft [12–20] (including

UAVs [21]), 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-roam-

ing individuals [22], and when linked to locational in-

formation, it can be used to determine events [19, 23,

24] or components of an animal’s environment [25]

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 indi-

vidual 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 physi-

ological 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.

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 (Fig-

ure 1; Movie S1). Nine ﬂights were conducted over two adult fe-

male 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 aver-

aged 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.

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 pre-

dicted values during UAV ﬂights (see Figure 2A for brief descrip-

tion 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 2B). Maximum HR anomalies were

the largest for the female with cubs, followed by the hibernating

adult female, and ﬁnally the young male (Figure 2C). 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 in-

terval associated with HRs 30 min prior to a given ﬂight, with me-

dian 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 ad-

renal glands (e.g., [26]).

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 associa-

tion), absolute altitude of the UAV (negative association), and an

interaction of the two (positive association, average multiple r

X = 0.84, SE = 0.05). HR anomalies were positively associated

with wind speed (Figure 3A) and negatively associated with the

distance between the UAV and the bear (Figure 3B). These rela-

tionships 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.

Despite signiﬁcant physiological reactions to UAV ﬂights,

movement rates (meters per hour) increased during or immedi-

ately following only one UAV ﬂight (12.5% of ﬂights with available

data, Figure S1). On this occasion, the bear increased its rate of

movement beyond all previous recorded movement rates for

that individual (Figure 4). The same ﬂight resulted in a maximum

displacement distance (maximum straight line distance [m] from

location 10 min prior to UAV to each location 40 min post-ﬂight)

of 576 m, which far exceeds maximum displacement distances

observed on days without a UAV ﬂight (ﬂight #8 in Figure S3 ).

No other ﬂight or set of ﬂights resulted in a displacement dis-

tance that differed from distances observed on days without

UAV ﬂights. However, the bear that exhibited the greatest in-

crease in HR (Figure S2) also responded behaviorally from the

same set of back-to-back ﬂights (two total instances of a behav-

ioral response; 11.1%). This bear moved at least 6.8 km within

28 hr of the ﬂight, into a neighboring collared female’s home

range where the individual had never previously been observed.

DISCUSSION

Our results support hypothesis #3: UAV ﬂights induced a physi-

ological response, but most bears did not respond behaviorally

by increasing movement rates or moving to a different location.

Prior to this study, little was known about the potential impacts of

UAV ﬂights on wildlife. Vas et al. [21] tested whether UAV ﬂights

triggered a behavioral response in three bird species. Birds ex-

hibited a response to 20% of UAV ﬂights, and the authors re-

marked about the ability to ﬂy their UAV as close as 4 m from

the birds typically without any detectable behavioral response.

Importantly, without the use of cardiac biologger technology,

we would also have concluded that bears rarely responded to

UAV ﬂights.

HRs returned to pre-ﬂight values relatively quickly after most

ﬂights. Bears in this population live in a highly human-altered

landscape (50% agriculture) and frequently encounter potential

stressors (e.g., roads and agricultural ﬁelds, with associated

noises from trafﬁc and farm equipment) and therefore may exhibit

lower stress responses and quicker recovery times than animals

in populations that encounter human-related stressors less

frequently [25]. Stress responses to UAVs are also likely to be

species speciﬁc, and the strength of the response may vary

among sex and age classes as our results suggest. Numerous

web-based videos demonstrate that some species react aggres-

sively toward UAV ﬂights. When stress responses are accompa-

nied by an extreme behavioral response, as we recorded twice

with our bears, individuals may become more vulnerable to sour-

ces of mortality (e.g., trafﬁc collisions when ﬂeeing, interactions

with bears in home ranges that they have encroached).

It has long been established that low-altitude ﬂights by heli-

copters and ﬁxed-wing aircraft can produce stress responses

in wildlife [19], yet we believe UAV ﬂights introduce a new and

unique stressor that has the potential to be more frequent and

induce higher levels of stress. UAVs can ﬂy extremely low

(some with maneuverability to ﬂy under a forest canopy) and

Figure 1. Illustration of Bear Movement and HR during a UAV Flight

(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 biologg er developed by Medtronic. We ﬂew unmanned

aerial vehicles over American black bears living in northwestern Minnesota

during September and October 2014.

See also Figure S3.

autonomous ﬂight. We used the APM Planner 2.0 software (http://planner.

ardupilot.com/) to program and ﬂy each ﬂight. In brief, each mission was ﬂown

according to the protocol below, but the re was some variation among ﬂight

plans due to weather conditions, distance to the animal, and the ability to

pinpoint the bear’s location (the only means to track the denning bear was

with VHF telemetry).

For each 5-min ﬂight, the UAV was programmed with a GPS ﬁx based on

the last known location of the focal bear obtained from the GPS collars or, in

the case of the VHF-collared bear, the triangulation of the bear’s location.

The UAV was launched and climbed to an altitude of 20 m, and then ﬂew

straight to the programmed GPS ﬁx. Upon reaching this point, the UAV loitered

in place for 1 min before initiating two consecutive large turns, each with a

radius of 20 m (1 min for each turn) around the GPS point. After completing

the turns, the UAV returned to the programmed ﬁx to loiter in place for 1 min.

After completing its mission over the bear, the UAV ﬂew back to the launch

point and automatically landed. Each mission was initiated by an FAA-certiﬁed

pilot who armed the quadcopter and increased the throttle to 50%. The pro-

gramed mission commenced automatically at this point, and each ﬂight was

ﬂown and landed fully autonomously with no further user input.

Following each ﬂight we downloaded the data logged by the UAV ﬂight com-

puter (Pixhawk) using APM Planner 2.0. We used PyMAVLink Tools (https://

pixhawk.org/dev/pymavlink) to extract the time stamps, GPS locations,

speed, and absolute altitude of the UAV (height of UAV above the ground)

throughout each ﬂight. These data are logged at 3–5 times per second by

the Pixhawk ﬂight computer. Following their extraction, these data were pro-

cessed so they could be linked with the HR and movement data from each

bear (see Statistical Methods).

Statistical Methods

All statistical analyses were carried out in R [29], an open source statistical pro-

gramming language. We ﬁt linear regression models to the HR data collected

1 hr prior to each UAV ﬂight, using natural cubic regression splines (ns function

in package: splines [29]) with 2 degrees of freedom to account for temporal

trends in the HR values. We used this model to predict the HR values occurring

during an 8-min window covering the time period of the UAV ﬂight and a few

minutes post-ﬂight (see Figure 2A). If two UAV ﬂights occurred over the

same individual, with less than 20 min between each ﬂight, we used the HR

values for the hour prior to the ﬁrst ﬂight to estimate the predicted values for

the second ﬂight. We formed HR anomalies, representing the increase in HR

beyond what might be expected given the trend in HR for the hour prior to

the ﬂight, as the difference between the observed and predicted HR values

during the 8-min window, divided by the SD of HR values from the hour prior

to the UAV ﬂight.

We generated control observations by repeating this process using HR data

from all dates without a UAV ﬂight (female with cubs of the year: 175 days;

young male: 181 days; hibernating adult female: 79 [winter hibernation days

only]) but collected during the same time of day as the UAV ﬂights. We formed

a null distribution for the empirical distribution function (ECDF), assuming no

effect of the UAV, by repeatedly subsampling these ‘‘control’’ data, keeping

the same number of observations per bear as in the original UAV-ﬂight dataset.

We calculated the ECDF for each of 10,000 subsampled control datasets and

created a 95% simulation envelope to compare to the ECDF of the HR anom-

alies associated with the UAV ﬂights (Figure 2B). An ECDF of the UAV HR ﬂight

data that did not fall within the 95% simulation envelope suggested that the

maximum HR anomaly values from control and experimental conditions

were drawn from two different distributions.

We calculated the recovery time of bear HRs post-ﬂight for each ﬂight and

reported the median and range for each individual. We deﬁned recovery

time as the number of minutes until HR returned to values below the upper

99% conﬁdence interval based on values from 30 min prior to each ﬂight. If

a set of ﬂights occurred such that the second ﬂight began prior to recovery af-

ter the ﬁrst ﬂight, we considered only recovery after the second ﬂight.

SUPPLEMENTAL INFORMATION

Supplemental Information includes Supplemental Experimental Procedures,

three ﬁgures, and one movie and can be found with this article online at

http://dx.doi.org/10.1016/j.cub.2015.07.024.

AUTHOR CONTRIBUTIONS

M.A.D. analyzed the data and wrote the paper. M.A.D., J.B.V., L.K.W., and

J.C.T. designed the study and performed the UAV ﬁeldwork. J.R.F. suggested

and helped develop the statistical approach. P.A.I. and T.G.L. performed the

biologger surgery and consulted on the physiological aspects of the study.

D.L.G. was the lead researcher for winter ﬁeldwork and consulted on interpre-

tation of bear behavior. All authors reviewed the ﬁnal version of the manuscript.

ACKNOWLEDGMENTS

The Institute on the Envi ronment (University of Minnesota) and the International

Association for Bear Research and Management provided ﬁnancial support.

We thank T. Baker, L. Dillard, and B. Taylor of the University of Minnesota

for advice and technical help. T. Iles, H. Martin, H. Severs-Wilkerson, and M.

McMahon assisted with ﬁeldwork. J. Huener and K. Arola of the Minnesota

Department of Natural Resources and G. Knutsen of the USFWS allowed us

to use their facilities for ﬁeldwork.

Received: June 1, 2015

Revised: July 7, 2015

Accepted: July 9, 2015

Published: August 13, 2015

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