Approaching birds with drones: First experiments and ethical guidelines

Abstract

Unmanned aerial vehicles, commonly called drones, are being increasingly used in ecological research, in particular to approach sensitive wildlife in inaccessible areas. Impact studies leading to recommendations for best practices are urgently needed. We tested the impact of drone colour, speed and flight angle on the behavioural responses of mallards Anas platyrhynchos in a semi-captive situation, and of wild flamingos (Phoenicopterus roseus) and common greenshanks (Tringa nebularia) in a wetland area. We performed 204 approach flights with a quadricopter drone, and during 80% of those we could approach unaffected birds to within 4 m. Approach speed, drone colour and repeated flights had no measurable impact on bird behaviour, yet they reacted more to drones approaching vertically. We recommend launching drones farther than 100 m from the birds and adjusting approach distance according to species. Our study is a first step towards a sound use of drones for wildlife research. Further studies should assess the impacts of different drones on other taxa, and monitor physiological indicators of stress in animals exposed to drones according to group sizes and reproductive status.

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Research
Cite this article: Vas E, Lescroe
¨l A, Duriez O,
Boguszewski G, Gre
´millet D. 2015 Approaching
birds with drones: first experiments and ethical
guidelines. Biol. Lett. 11: 20140754.
http://dx.doi.org/10.1098/rsbl.2014.0754
Received: 19 September 2014
Accepted: 13 January 2015
Subject Areas:
behaviour, ecology, environmental science,
bioengineering
Keywords:
animal behaviour, ecology, ornithology, robot,
stress, unmanned aerial vehicles
Author for correspondence:
David Gre
´millet
e-mail: david.gremillet@cefe.cnrs.fr
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rsbl.2014.0754 or
via http://rsbl.royalsocietypublishing.org.
Animal behaviour
Approaching birds with drones: first
experiments and ethical guidelines
Elisabeth Vas1,2,3, Ame
´lie Lescroe
¨l1, Olivier Duriez1, Guillaume Boguszewski2,3
and David Gre
´millet1,4,5
1
CEFE UMR 5175, CNRS - Universite
´de Montpellier - Universite
´Paul-Vale
´ry Montpellier - EPHE, 1919 route de
Mende, 34293 Cedex 05, Montpellier, France
2
Cyleone, Cap Omega, Rond-point Benjamin Franklin, CS 39521 34960 Montpellier Cedex 2, France
3
Labex NUMEV, 161 rue Ada, Campus Saint Priest UM2, 34095 Montpellier Cedex 05, France
4
OSU OREME UMS 3282 CNRS-UMS 223 IRD-Universite
´Montpellier 2, Place Euge
`ne Bataillon,
34095 Montpellier Cedex 05, France
5
FitzPatrick Institute and DST/NRF Excellence Centre, University of Cape Town, 7701 Rondebosch, South Africa
Unmanned aerial vehicles, commonly called drones, are being increasingly
used in ecological research, in particular to approach sensitive wildlife in
inaccessible areas. Impact studies leading to recommendations for best prac-
tices are urgently needed. We tested the impact of drone colour, speed and
flight angle on the behavioural responses of mallards Anas platyrhynchos
in a semi-captive situation, and of wild flamingos (Phoenicopterus roseus)
and common greenshanks (Tringa nebularia) in a wetland area. We per-
formed 204 approach flights with a quadricopter drone, and during 80%
of those we could approach unaffected birds to within 4 m. Approach
speed, drone colour and repeated flights had no measurable impact on
bird behaviour, yet they reacted more to drones approaching vertically.
We recommend launching drones farther than 100 m from the birds and
adjusting approach distance according to species. Our study is a first step
towards a sound use of drones for wildlife research. Further studies
should assess the impacts of different drones on other taxa, and monitor
physiological indicators of stress in animals exposed to drones according
to group sizes and reproductive status.
1. Introduction
Robots are still marginal as tools in ecological research, yet they have a tre-
mendous potential for biodiversity sampling, studies of population
dynamics and ecosystem functioning, experimental biology and behavioural
studies [1]. Recently, small unmanned aerial vehicles (hereafter ‘drones’)
have become increasingly affordable (i.e. a few hundred to a few thousand
US$), and this is currently leading to their widespread use for wildlife obser-
vations [2,3]. In ornithology, fixed-wing drones are already being widely used
for census work and observations [4,5], and dozens of videos available on the
Internet testify that researchers, and the general public, are keen to use
drones to approach birds. In a number of countries, air traffic regulations
strictly control the civil use of drones, yet no ethical guidelines exist with
respect to their potential impacts on animal welfare. This policy vacuum is
due to the paucity of research assessing the effect of drones on animal behav-
iour [6]. In this context, the aim of our study is to test the impact of
approaching drones on animals, and to provide users with guidelines. We
flew a small quadricopter drone, because this type of unmanned aerial
vehicle is currently the most affordable, and focused on three species of
waterbirds, because drones are already being extensively used for surveys
within wetland/coastal areas [7].
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2. Methods
We approached birds with drones in March and April 2014 in both
semi-captive and natural settings. The semi-captive setting was
located at the Zoo du Lunaret, Montpellier, France (N 4383803000;
E385203000), and the natural area at the Cros Martin, along
the brackish lagoon of the Etang de l’Or, Candillargues, France
(N 4383601800;E048301800). In the semi-captive setting, we
approached mallards (Anas platyrhynchos; 1.1 kg, 0.55 m length)
that were living in a zoo, but capable of flying in and out of
the premises. In the natural setting, we approached wild flamingos
(Phoenicopterus roseus, 3 kg, 1.25 m length) and common green-
shanks (Tringa nebularia, 0.2 kg, 0.35 m length).All birds were
non-breeding at the time of the experiments, and were resting or
feeding. They were either floating at the water surface (mallards)
or standing in shallow water (flamingos and greenshanks). Bird
groups included an average of 5 mallards (range 3–9), 35 flamin-
gos (range 5– 73) or 19 greenshanks (range 11– 27). Birds were
not individually marked, and we therefore cannot exclude that
we approached some of them more than once.
We used a Phantom drone designed by Cyleone (Montpellier,
France, http://cyleone.fr/). The device is a quadricopter with a
diagonal length of 350 mm, a mass of 1030 g, a pay load of
250 g, a maximum speed of 15 m s
21
, a vertical and horizontal
positioning accuracy of 0.8 and 2.5 m, respectively. Noise level is
60 dB at 2 m, and hence considered non-impacting [8]. The Phan-
tom came in three colours (white, black and blue), and was
equipped with a Hero3 GoPro camera (San Meteo, USA), which
relayed images in real time onto a portable screen (StudioSport,
France). The speed and position of the drone were determined
by an onboard GPS module. The position of the birds relative
to the observer and the drone was determined with a laser range-
finder (PCE-LRF 600, Strasbourg, France) held by the observer,
with an accuracy of 1 m. Light intensity was 40 000 Lx on average
during the trials, and never below 20 000 Lx. Visibility was at least
500 m, and wind speed (anemometer PCE-AM 81, Strasbourg,
France) never exceeded 22 km h
21
.
The drone was launched at a minimum distance of 50 and
100 m from the birds in the semi-captive and the wild situation,
respectively. These distances were chosen because pre-trials
revealed that they were adequate to launch the drone without
causing a reaction of the birds. While one operator was steering
the drone, a second observed the birds closely with 10 40 bin-
oculars and the rangefinder. From the take off point, the drone
ascended vertically (at 3 m s
21
) to 30 m, and then approached
the birds (figure 1). We varied the speed and angle of approach
according to four categories each (speed: 2, 4, 6 and 8 m s
21
;
angle: 208,308,608and 908from the horizontal—thus, the 908
trajectory involved the drone flying at 30 m to directly above
the birds before descending). When approaching close to the
ground (208), it is challenging to fly at 8 m s
21
, and hence for
this angle, we used only 2, 4 and 6 m s
21
. For all other angles
(308,608and 908), we used the speed categories 2, 6 and
8ms
21
. These combinations of angle and speed resulted in 12
categories, each of which was used for the three drone colours
(white, black, blue). Each of these 36 approach types was per-
formed once (66% of trials), or twice (33%) in mallards, once
(33% of trials) or twice (66%) in greenshanks, and twice (33%
of trials), three times (33%) or four times (33%) in flamingos.
Bird reactions were classified in three categories: (type 1) no reac-
tion; (type 2) brief head and tail movements followed by animal
movements away from the drone, either walking or swimming at
the water surface; (type 3) flying off. Approaches were pursued
until birds reacted, or stopped when the drone was 4 m from the
closest bird. We considered a bird group as ‘stressed’ as soon as
one individual showed a type 2 or type 3 response. Owing to
group dynamics, this individual reaction was always closely fol-
lowed by reactions of all group members. Two-minute breaks
were taken between each flight. Impacts of the different proto-
cols on bird behaviour were tested using variance analyses
conducted in R.
3. Results
We performed a total of 204 approaches in 8 days (24–36 per
day), 48 on mallards in a semi-captive situation, and 156 in
the wild on greenshanks (60 trials) and flamingos (96
trials). In mallards, no reaction was recorded in 35 cases
(72%), type 2 reactions in nine cases, and type 3 reactions
in four cases; those reactions occurred when the drone was
4–8 m from the birds. In flamingos, no reaction was recorded
in 75 cases (78%), type 2 reactions in 11 cases, and type 3 reac-
tions in 10 cases; those reactions occurred when the drone
was 5 – 30 m from the birds. In greenshanks, no reaction
was recorded in 53 cases (87%), type 2 reactions in five
cases, and type 3 reactions in two cases; those reactions
occurred when the drone was 4– 10 m from the birds.
Group size tended to influence reaction distance; with reac-
tions at 25– 30 m distance being observed only twice, for
the largest flamingo groups (more than 50 individuals). Our
sample size was nonetheless too limited to confirm this trend.
Results were largely consistent across all three species and
the semi-captive versus natural set-up, and bird behaviour
(resting/feeding) was a non-significant factor within all ana-
lyses: approach speed had no influence on bird reactions
(F
3,203
¼2.19, p¼0.09). Drone colour had no impact on bird
20°
altitude
30 m
30°
speed: 2, 4, 6 or 8 m s–1
60° 90°a:
a
Figure 1. Flight plan for approaching birds with the Phantom drone. The drone was first ascended to 30 m, and then moved at speeds of 2–4 – 6 or 8 m s
21
towards the birds at angles
a
of 208,308,608or 908. Drones of three colours were used (white, black and blue).
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reactions (F
2,203
¼1.27, p¼0.28). Successive approach flights
also had no significant cumulative impacts (no relation
between the rank-order of the trial per day and bird response;
F
1,203
¼0.90, p¼0.344). Conversely, approach angle had a
marked impact on bird reactions (F
3,203
¼136.33, p,0.0001;
figure 2): in mallards, birds showed no reaction for all
approaches conducted at angles of 208,308and 608, but
showed a reaction in eight cases of nine for approaches with
drones conducted at 908. Similarly, flamingos and greenshanks
never reacted for approaches at 208,308and 608, but reacted in
17 of 18 cases (flamingos) and five of nine cases (greenshanks)
for approaches at 908.
4. Discussion
Using a standardized protocol applied to three different
species of waterbirds across 204 approaches, we demonstrated
that in 80% of all cases one specific drone type could fly to
within 4 m of the birds without visibly modifying their behav-
iour. We also demonstrated that approach speed, drone colour
and repeated approaches did not have any significant impact
on bird reaction, butthat approach angles had marked impacts
across all three species. A Phantom drone approaching a bird
vertically was usually more disturbing, maybe because it
was associated with a predator attack. To test this hypothesis,
future studies should use ‘neutral’ quadricopters versus
fixed-wing drones mimicking the shape of avian predators
known to target the approached species.
It is surprising that we managed to fly so close (4 m) to
seemingly undisturbed birds, as in particular wild flamingos
and greenshanks are known for their extremely high sensi-
tivity to disturbance [9]. These results suggest that, when
carefully flown, drones may be used in ornithology for a
wide range of population censuses, measurements of biotic
and abiotic variables, and recordings of bird behaviour.
Those applications could be immensely useful, especially in
inaccessible areas such as mountains or large wetlands.
0
black
blue
white 90°
60°
30°
20°
approach angle
drone colour
20
% of successful approaches to 4m
40
60
80
100
0
black
blue
white
2ms–14ms–16ms–18ms–1
90°
60°
30°
20°
approach angle
drone colour
20
% of successful approaches to 4m
40
60
80
100
mallards
flamingos
approach speed
0
black
blue
white 90°
60°
30°
20°
approach angle
drone colour
20
% of successful approaches to 4m
40
60
80
100
greenshanks
Figure 2. Impacts of drone colour (white, blue, black), approach angle (8) and flight speed (m s
21
) on bird behaviour across 204 approach flights conducted in
three bird species. The impact is rated as the percentage of approaches to within 4 m of the birds during which animals did not show visible reactions. See Methods
and Results sections for details.
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Nevertheless, we are calling for much caution in the use
of drones for wildlife research. To take a precautionary
approach, we recommend launching drones farther than
100 m from the birds, not approaching them vertically, and
adjusting approaching distance according to species. We
also feel that our investigations should be followed by further
studies of the impacts of different types of drones (varying
size and noise levels) on a larger range of bird species.
Indeed, all three species investigated here feed on plants
and/or invertebrates, and it seems essential to also test the
reactions of omnivorous/predatory species to the presence
of drones. Notably, videos available on the Internet demon-
strate that birds of prey tend to attack drones, and this is
also likely for corvids and larids. Further, we recorded no be-
havioural changes in birds during most approaches, but this
does not mean that the drone presence was not stressful for
the animals. Indeed, numerous studies showed that disturb-
ance can lead to increased heart rates and/or corticosterone
levels in birds that do not react behaviourally [10]. It is there-
fore also essential to perform studies of drone impacts in
captive or wild birds for which physiological parameters
can be recorded along with behaviour patterns [11]. Such
stress levels should then be compared for birds censused
using drones versus other techniques (e.g. walking
humans). Finally, the incidence of bird group size and breed-
ing status (non-breeding, incubating, chick-rearing) on
reaction thresholds should also be thoroughly investigated.
In conclusion, our study of animal reaction to drones is
important in the context of the rapid development of drone
technologies for the monitoring of wild animals, particularly
in protected areas [12]. It is a first step towards a code of best
practices in the use of drones for ecological research, and calls
for further, detailed assessments of the wildlife impacts of
these new technologies.
Ethics statement. All experiments were performed under permits granted
from both the French veterinary services (permit no. 34-369) and
French environmental and aviation authorities (permit reference:
MAP CYLEONE edition no. 04-Amendment 1).
Data accessibility. Data used for all analyses are available as electronic
supplementary material. See also online video showing examples
of approach flights: http://youtu.be/t_WtxX6O0JI.
Acknowledgements. D.G. thanks the French Polar Institute (IPEV) for
support within the ADACLIM programme (no. 388). We are most
grateful to Luc Gomel and all staff at the Zoo du Lunaret for their
great help. We also warmly thank Luis de Sousa (DREAL-LR), Eve
Le Pommelet (SYMBO), Jonathan Fuster (CCPO) and Patrice
Cramm (CEN-LR) for their support. Thanks to Ewan McBride for
checking our English.
Authors’ contributions. E.V., D.G., A.L. and O.D. designed the study. E.V.,
G.B., D.G. and A.L. performed the study. E.V. and G.B. analysed
data. D.G. and E.V. wrote the manuscript, which was corrected by
all authors.
Funding statement. This study was supported by Cyleone and the labex
NUMEV, and supported by CNRS, IPEV and the OSU-OREME.
Competing interests. The authors have no competing interests.
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