R404 Current Biology 26, R387–R407, May 23, 2016 © 2016 Elsevier Ltd.
moved around and sat near the site for
about 2 minutes, after which he left with
the rest of the group.
This report complements accounts
of responses to dying and dead
individuals in four other wild primate
species (Table S2). Multiple factors
probably contribute to the variable
nature of responses recorded, including
the cause and context of death, quality
of the social relationships between the
deceased and other group members
[7,8], and possibly species-typical social
organization. The snub-nosed monkey
DM migrated into ZBD’s unit in October
2010. The strong bond between DM
and ZBD over the subsequent three-
year period (DM gave birth to one infant
in March 2012) likely underpinned the
caretaking behaviors shown by the
male toward the dying female, recalling
similar behavior in chimpanzees [4,8]
and a male marmoset .
Both ZBD and other members of his
OMU uttered alarm calls and contact
calls as the female lay dying. Alarm
calls are usually given in response
to danger (such as the approach of
a dog) on the ground. Conceivably,
DM’s sudden fall from the tree and
her unusual behavior as she lay
dying aroused some degree of fear or
anxiety in the monkeys, as reported
in other cases of sudden, traumatic
deaths [5,9]. ‘Unexplained’ deaths
and deaths resulting from obvious
injury elicit different responses in
No individuals other than members
of her own OMU contacted the
dying female. In another species
characterized by OMUs — geladas — a
dying adult female also received only
passing visual attention from other
OMU members . Furthermore,
although afﬁ liative acts toward the dying
DM were seen in all members of the
focal OMU, only the adult male tended
her after she died, further supporting
the expression of compassion by an
individual with a strong bond to the
deceased. His responses included
exploration, attempts to elicit a
response from the female, and afﬁ liative
acts including embracing (Table S3).
These observations, combined with
others in the literature, suggest that
compassionate caretaking is not unique
to humans and great apes [2–5], at least
when dying individuals and survivors
share an emotional bond.
Supplemental Information includes Experimen-
tal Procedures and three Tables and can be
found with this article online at http://dx.doi.
The study was supported by the Key Program
of National Natural Science Fund ( 31130061),
National Natural Science Foundation of China
( 31572278, 31270442,31470456,31501872),
Special Foundation of Shaanxi Academy of
Sciences, China ( 2014K-29). The funding
organizations had no role in study design, data
collection and analysis, decision to publish,
or preparation of the manuscript. We thank
Zhouzhi National Nature Reserve for permission
to carry out this study. We greatly appreciate our
ﬁ eld assistants for indispensable support during
this study, especially students from the Primate
Research Center of Northwest University China .
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K., and Li, B.G. (2011). Sexual interference in
the golden snub-nosed monkey (Rhinopithecus
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8. Stewart, F.A., Piel, A.K., and O’Malley, R.C.
(2012). Responses of chimpanzees to a recently
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1Shaanxi Key Laboratory for Animal
Conservation, Shaanxi Institute of Zoology,
Shaanxi Academy of Sciences, Xi’an 710032,
China. 2Department of Psychology, Kyoto
University Graduate School of Letters, Kyoto
606-8501, Japan. 3Shaanxi Key Laboratory
for Animal Conservation, and College of Life
Sciences, Northwest University, Xi’an 710069,
China. 4Co-ﬁ rst authors.
to wildlife in
biological ﬁ eld
Jarrod C. Hodgson* and Lian Pin Koh
The use of unmanned aerial vehicles
(UAVs), colloquially referred to as
‘drones’, for biological ﬁ eld research is
increasing [1–3]. Small, civilian UAVs are
providing a viable, economical tool for
ecology researchers and environmental
managers. UAVs are particularly useful
for wildlife observation and monitoring
as they can produce systematic data
of high spatial and temporal resolution
. However, this new technology could
also have undesirable and unforeseen
impacts on wildlife, the risks of which
we currently have little understanding
[5–7]. There is a need for a code of best
practice in the use of UAVs to mitigate or
alleviate these risks, which we begin to
Different wildlife populations can
respond idiosyncratically to a UAV
in proximity depending on a variety
of factors, including the species,
environmental and historical context, as
well as the type of UAV and its method
of operation. While we do not presently
have sufﬁ cient information on how these
factors might affect wildlife to develop
prescriptive policies for UAV use, we
could draw from existing guidelines for
ensuring the ethical treatment of animals
in research [8,9]. For example, the
ARRIVE (Animals in Research: Reporting
In Vivo Experiments) guidelines detail
the minimum information all scientiﬁ c
publications reporting research using
laboratory animals should include ,
which may serve as a good starting point
for the UAV context.
Considering the growing popularity of
UAVs as a tool among ﬁ eld biologists, we
advocate for the precautionary principle
to manage these risks. Speciﬁ cally, we
provide a suite of recommendations as
the basis for a code of best practice in
Current Biology 26, R387–R407, May 23, 2016 R405
the use of UAVs in the vicinity of animals
or for the purpose of animal research,
which supplement current standards in
animal ﬁ eld research and reporting.
Adopt the precautionary principle
in lieu of evidence. When researchers
cannot make informed decisions about
minimum wildlife disturbance ﬂ ight
practices for their environment or study
species, they should exercise caution,
particularly if endangered species
or ecologically sensitive habitats are
involved. While reported observations of
animal responses to UAVs are increasing,
there is a need for more empirical
evidence across a range of animals and
environments. Experiments that ethically
quantify disturbance using captive and
wild animals to ﬁ ll this knowledge gap
are necessary to inform minimum wildlife
disturbance practices. As an interim
measure, expert advice on species and
UAV monitoring should be obtained
for operations involving taxa whose
responses to UAVs are poorly quantiﬁ ed
Utilise the institutional animal
ethics process to provide oversight
to UAV-derived animal observations
and experiments. UAV monitoring
that involves animals will beneﬁ t
from ensuring all UAV methods are in
accordance with approved institutional
ethics permits. We encourage UAV users
to seek this approval when appropriate
and explain the anticipated beneﬁ t of
using UAV technology in their situation.
Ethics committees should evaluate these
claims relative to comparative traditional
techniques (e.g. ground surveys or
remotely sensed data from an alternative,
higher altitude platform such as manned
aircraft or satellites).
Adhere to relevant civil aviation rules
and adopt equipment maintenance
and operator training schedules.
UAV operations need to comply with all
relevant civil aviation rules which may
include restrictions on ﬂ ying beyond
visual line of sight, above a deﬁ ned
altitude, at night and near people or in
the vicinity of important infrastructure
and prohibited areas. In countries
where rules are not present or are still
evolving, operators are encouraged to
exercise caution. UAV equipment should
be regularly serviced to ensure good
working order, and maintenance recorded
appropriately. Experienced operators
should be utilised for UAV operations
(formal accreditation is necessary in
some countries). Where appropriate,
approval for ﬂ ight should be sought from
Select appropriate UAV and sensor
equipment. UAVs should be selected
to minimise visual and audio stimulus to
target and non-target organisms, while
remaining capable of satisfying study
objectives. Consideration should be
given to the way different units move
(e.g. the gliding motion of a ﬁ xed-wing
unit) as well as their shape, volume and
colour relative to the study environment.
In some cases, it may be beneﬁ cial to
modify UAVs to mimic non-threatening
wildlife, e.g. a bird that is not a predator
of the target species. Sensors should be
optimised (e.g. focal length) to enable
collection of suitable data from a UAV
operated, typically, as high or as far as
possible from the subjects.
Exercise minimum wildlife
disturbance ﬂ ight practices. Particular
attention should be given to siting launch
and recovery sites away from animals
(out of sight if possible) and maintaining
a reasonable distance from animals at all
times during ﬂ ight. Potentially threatening
approach trajectories and sporadic ﬂ ight
movements should be avoided. Species-
speciﬁ c protocols, including optimum
ﬂ ight altitude, should be developed and
implemented wherever possible.
Cease UAV operations if they
are excessively disruptive. Animal
responses should be measured during
UAV operations (and before and after if
possible). Monitoring stress response at
a physiological level is encouraged, as is
the use of tracking technology to quantify
potential displacement. Operations
should be aborted if excessive
disturbance results, especially in cases
when quantiﬁ cation of UAV disturbance
is not a research interest. The methods
for such studies should be reviewed and
only resumed with a reﬁ ned protocol if
Detailed, accurate reporting of
methods and results in publications.
UAV speciﬁ cations and ﬂ ight practices
should be reported accurately and
in full. Thorough results should be
reported to ensure ﬁ ndings can be
integrated in future research. Notes of
animal responses (see above) should be
included in published studies to generate
an evidence base for reﬁ ned guidelines.
We encourage authors to be proactive
in sharing suggestions for improving
UAV best practices in biological ﬁ eld
research and also to guide the regulation
of recreational use. Importantly, such
reports should include both positive
and negative observations, including
accidents during operations and
incidents of excessive disturbances to
animals. Publishers may wish to consider
minimum reporting requirements for
manuscripts that involve UAV operations.
Promoting the awareness,
development and uptake of a code of
best practice in the use of UAVs will
improve their suitability as a low impact
ecological survey tool. We consider this
code to be a ﬁ rst and guiding step in
the development of species-speciﬁ c
protocols that mitigate or alleviate
potential UAV disturbance to wildlife.
J.C.H. and L.P.K. conceived and wrote the paper.
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research and management methods in the
21st century: Where do unmanned aircraft ﬁ t in?1.
J. Unmanned Vehicle Systems 3, 137–155.
2. Watts, A.C., Perry, J.H., Smith, S.E., Burgess,
M.A., Wilkinson, B.E., Szantoi, Z., Ifju, P.G., and
Percival, H.F. (2010). Small unmanned aircraft
systems for low-altitude aerial surveys. J. Wildlife
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3. Anderson, K., and Gaston, K.J. (2013).
Lightweight unmanned aerial vehicles will
revolutionize spatial ecology. Front. Ecol. Environ.
4. Linchant, J., Lisein, J., Semeki, J., Lejeune, P.,
and Vermeulen, C. (2015). Are unmanned aircraft
systems (UASs) the future of wildlife monitoring?
A review of accomplishments and challenges.
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5. Vas, E., Lescroel, A., Duriez, O., Boguszewski, G.,
and Gremillet, D. (2015). Approaching birds with
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Biol. Lett. 11, 20140754.
6. Ditmer, M.A., Vincent, J.B., Werden, L.K., Tanner,
J.C., Laske, T.G., Iaizzo, P.A., Garshelis, D.L., and
Fieberg, J.R. (2015). Bears show a physiological
but limited behavioral response to unmanned
aerial vehicles. Curr. Biol. 25, 2278–2283.
7. Pomeroy, P., O’Connor, L., and Davies, P. (2015).
Assessing use of and reaction to unmanned aerial
systems in gray and harbor seals during breeding
and molt in the UK1. J. Unmanned Vehicle
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8. Sikes, R.S., Gannon, W.L., and Mammalogists,
A.S. (2011). Guidelines of the American Society
of Mammalogists for the use of wild mammals in
research. J. Mammal. 92, 235–253.
9. National Health and Medical Research Council
(2013). Australian code for the care and use
of animals for scientiﬁ c purposes. 8th Edition
(Canberra: National Health and Medical Research
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Emerson, M., and Altman, D.G. (2010). Improving
bioscience research reporting: the ARRIVE
guidelines for reporting animal research. PLoS
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School of Biological Sciences, The University
of Adelaide, SA 5005, Australia.