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Advancing Primate Research and Conservation Through the Use of Camera Traps: Introduction to the Special Issue

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Effective conservation and management of primates depend on our ability to accurately assess and monitor populations through research. Camera traps are proving to be useful tools for studying a variety of primate species, in diverse and often difficult habitats. Here, we discuss the use of camera traps in primatology to survey rare species, assess populations, and record behavior. We also discuss methodological considerations for primate studies, including camera trap research design, inherent biases, and some limitations of camera traps. We encourage other primatologists to use transparent and standardized methods, and when appropriate to consider using occupancy framework to account for imperfect detection, and complementary techniques, e.g., transect counts, interviews, behavioral observation, to ensure accuracy of data interpretation. In addi-tion, we address the conservation implications of camera trapping, such as using data to inform industry, garner public support, and contributing photos to large-scale habitat monitoring projects. Camera trap studies such as these are sure to advance research and conservation of primate species. Finally, we provide commentary on the ethical considerations, e.g., photographs of humans and illegal activity, of using camera traps in primate research. We believe ethical considerations will be particularly important in future primate studies, although this topic has not previously been addressed for camera trap use in primatology or any wildlife species.
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Advancing Primate Research
and Conservation Through the Use of Camera
Traps: Introduction to the Special Issue
Paula A. Pebsworth &Marni LaFleur
#Springer Science+Business Media New York 2014
Abstract Effective conservation and management of primates depend on our ability to
accurately assess and monitor populations through research. Camera traps are proving
to be useful tools for studying a variety of primate species, in diverse and often difficult
habitats. Here, we discuss the use of camera traps in primatology to survey rare species,
assess populations, and record behavior. We also discuss methodological considerations
for primate studies, including camera trap research design, inherent biases, and some
limitations of camera traps. We encourage other primatologists to use transparent and
standardized methods, and when appropriate to consider using occupancy framework
to account for imperfect detection, and complementary techniques, e.g., transect counts,
interviews, behavioral observation, to ensure accuracy of data interpretation. In addi-
tion, we address the conservation implications of camera trapping, such as using data to
inform industry, garner public support, and contributing photos to large-scale habitat
monitoring projects. Camera trap studies such as these are sure to advance research and
conservation of primate species. Finally, we provide commentary on the ethical
considerations, e.g., photographs of humans and illegal activity, of using camera traps
in primate research. We believe ethical considerations will be particularly important in
future primate studies, although this topic has not previously been addressed for camera
trap use in primatology or any wildlife species.
Keywords Cameratrap.Conservationethics .Methods.Primat es.Remote photography
Int J Primatol
DOI 10.1007/s10764-014-9802-4
P. A. Pebsworth
Department of Anthropology, University of Texas, San Antonio, TX 78666, USA
e-mail: ppebsworth@mac.com
P. A. Pebsworth
Department of Soil Science, Stellenbosch University, Stellenbosch, South Africa
M. LaFleur (*)
Institute for Population Genetics, University of Veterinary Medicine, 1220 Vienna, Austria
e-mail: marni.lafleur@gmail.com
Introduction
At the XXIVth International Primatological Congress in Cancun, Mexico, a sympo-
sium entitled Advancing Primate Research and Conservation through the Use of
Camera Trapsbrought primatologists together to discuss how camera trapping facil-
itates the study, management, and conservation of nonhuman primates. The symposium
organizers (Marni LaFleur and Chia L. Tan) gathered information on the current state of
camera trap applications in primate research and promoted the standardization of
qualitative and quantitative methods. This forum provided camera trap users and
would-be users the opportunity to discuss relevant topics, such as selecting the best
hardware and accessories for ones project needs and budget, overcoming technical and
methodological difficulties, and making reliable inferences from camera trap data. This
special issue highlights some of the camera trap research presented at the IPS sympo-
sium in Cancun, and also addresses some of the discussion points that followed, e.g.,
data interpretation and standardized methods.
In this special issue editorial, we review a variety of camera trap applications that
have been used in primatology: surveying rare species, assessing primate populations,
and recording behavior. Next, we provide primatologists with methodological consid-
erations for their camera trap studies. We then discuss how camera traps can be used to
determine the conservation status of primate species and as a means promoting and
protect primates. Finally, we address some of the ethical concerns that may arise when
using camera traps in primate research, such as recording illegal activity and
(potentially) protecting human anonymity. Surprisingly, given the extent of human
wildlife conflict on the global scale, ethical considerations and camera trap use are not
discussed in any wildlife research that we are aware, but could be particularly important
in cases of animal poaching and trafficking. We base our editorial on the information
presented at the IPS symposium, the articles within the special issue, and the literature
to date on camera trap use in primatology.
Camera Trap Applications
Surveying Rare Species
Natural resource, e.g., water, land, plants, management decisions are heavily influenced
by the abundance and distribution of rare species (Thompson 2004). Unfortunately, by
their very nature, rare species are a challenge to study because their populations may be
clumped or sparsely distributed over a large range, and/or their behavior may be elusive
(Thompson 2004). Rare species may also reside in remote areas where field conditions
are difficult and traditional survey methods, e.g., direct observation, capture/recapture,
are likely to be ineffective or impractical (Kierulff et al.2004;Tanet al.2013). In these
instances, camera traps have proved to be an effective tool for surveying primates,
without the need to observe the individuals directly or physically trap them (Fig. 1).
Camera traps can record presence/absence of a rare or elusive species (Bezerra et al.
2014;Gerberet al.2014), establish habitat requirements (Head et al.2012;Numata
et al.2005), and document geographical range (Easton et al.2011). To optimize the
likelihood of capturing the focal subject, researchers have used lures (Bezerra et al.
P.A. Pebsworth, M. LaFleur
2014;Kierulffet al.2004), strategically placed camera traps near critical resources,
such as natural canopy bridges (Gregory et al.2013), bamboo zones (Easton et al.
2011), and natural licks (Lhota et al.2012). Additional methods of careful and targeted
placement are described by Loken et al.(2013), Olson et al.(2012), and Tan et al.
(2013).
Assessing Primate Populations
Primates are among the most threatened taxa, with almost half of the worldsprimate
species in danger of extinction from habitat destruction, illegal wildlife trade, and
commercial bushmeat hunting (Mittermeier et al.2009). Primatologists need to monitor
endangered populations, so that they can inform the public of a populations plight,
encourage governments to conserve these species, and raise the necessary funds to
introduce and implement critical conservation measures. Camera traps offer the possi-
bility of continually monitoring a population indefinitely (or nearly indefinitely) and
Fig. 1 (a) A very rare photo of a silky sifaka (Propithecus candidus) on the ground at the Anjanaharibe forest
site in the Makira Natural Park, Madagascar. (b) An aye-aye (Daubentonia madagascariensis) at the
Farankarina protected area near Masoala National Park, Madagascar. (Photos by Zach J. Farris.).
Use of Camera Traps: Introduction
can be used to assess primate demographic patterns (Fig. 2). For example, long-term
camera trap projects can reconstruct group composition, including births, disappear-
ances, and interbirth intervals (Galvis et al.2014). In addition to demographic patterns,
camera traps can be used to record specific primate behaviors, which are addressed
next.
Recording Primate Behavior
Focal animal follows provide a wealth of data and information, as they document all
behaviors of interest and primatesuse of various resources (Altmann 1974). However,
following animals in this way requires habituation, which is not always feasible or
advisable (Jack et al.2008; Souza-Alves and Ferrari 2010), as doing so may be
detrimental to their health and wellbeing (Bezerra et al.2014; Boyer-Ontl and Pruetz
2014;Butynski2001; Williamson and Feistner 2003,2011). Camera traps may provide
a viable data collection alternative, in situations where animal follows and habituation
Fig. 2 (a) Ring-tailed lemurs (Lemur catta) with an infant at the Tsimanampetsotse National Park, Mada-
gascar. (Photo by Marni LaFleur.) (b) Chacma baboons (Papio cynocephalus ursinus)congregatetodrink
water and eat soil at the Wildcliff Nature Reserve, South Africa. (Photo by Paula Pebsworth.).
P.A. Pebsworth, M. LaFleur
are not advisable. Primate studies have capitalized on camera trapsability to monitor
fixed locations where a specific behavior or resource use occurs, as well as interactions
among and between species, as addressed in more detail next.
One of the first camera trap applications for recording behavior was geophagy, i.e.,
the deliberate consumption of earth materials (Fig. 3). Camera trap studies have
documented which species frequent geophagy sites (Link et al.2011;Matsubayashi
et al.2007), patterns of consumption (Galvis et al.2014;Pebsworthet al.2012), and
possible seasonal effects of geophagy (Blake et al.2010). Because geophagy sites are
important contributors to a primates overall health and they can be monitored with
relative ease, these sites should be considered conservation priorities and target areas
for gathering camera trap data (Matsubayashi et al.2007; Pebsworth et al.2012).
Other primate resources, such as foods, can also be monitored using camera traps.
Studies focusing on the consumption of masting fruit resources (Miura et al.1997;
Prasad et al.2010), seed dispersal (Miura et al.1997), and of primates dropping or
knocking off fruits that terrestrial animals then eat (Prasad et al.2010), have informed
Fig. 3 (a) Diademed sifaka (Propithecus diadema) at a geophagy site in the Maromizaha Forest, Madagascar.
(Photo from San Diego Zoo Global/University of Turin/GERP.) (b) Adult female chacma baboon (Papio
cynocephalus ursinus) eating soil at the Wildcliff Nature Reserve, South Africa. (Photo by Paula Pebsworth.).
Use of Camera Traps: Introduction
researchers on how primates contribute to forest ecology. Moreover, video camera
trapping showed that seasonal fruit abundance may influence interspecific competition
between common chimpanzees (Pan troglodytes troglodytes), gorillas (Gorilla gorilla
gorilla), and forest elephants (Loxodonta cyclotis)(Headet al.2012). Camera trap
research on habitat use patterns by sympatric chimpanzees and gorillas reflect the
speciesdietary preferences, in that chimpanzees are frugivorous and prefer montane
forests and gorillas are folivores and are distributed across habitat types (Nakashima
et al.2013).
Unlike primate resources, predation events and predators are notoriously diffi-
cult to monitor. However, if you are extremely lucky, camera traps can be useful in
documenting predation events (Fig. 4). Moreover, owing to the relative length of
time camera traps are deployed, when compared with the amount of time one can
spend observing, and the fact that observer presence can influence predator
behavior, camera traps are also useful for detecting predators (Fig. 5) and under-
standing how primates react to their presence. Predator avoidance strategies have
been detected via camera trap photos in white-bellied spider monkeys (Ateles
belzebuth)andredhowlers(Alouatta seniculus)(Blakeet al.2010;Linket al.
2011), and the authors suggest that these primates are more likely to use geophagy
sites when they know where their predators are, even if the predators are
nearby. Simlairly, ring-tailed lemurs (Lemur catta) stay in trees for longer
periods when their largest aerial predators, Madagascar harrier hawks
(Polyboroides radiata), are also present in the trees (LaFleur unpubl. data).
This is likely because the hawks have large wingspans and cannot attack
between branches (LaFleur unpubl. data).
Camera traps can also be used to assess other forms of behavioral plasticity.
Loken et al.(2013) used camera traps to assess whether canopy connectivity
influences terrestrial behavior in orangutans (Pongo pygmaeus morio), a predom-
inately arboreal primate. This species of orangutan is native to Borneo, where
habitat destruction and fragmentation have altered primate habitat (van Schaik
et al.2009). Camera traps documented that terrestriality is common in this
population of orangutans and represents a locomotion strategy to overcome loss
of canopy connectivity. Further, these results suggest orangutans may have more
ecological flexibility than once thought.
Camera trap studies have shown that activity patterns vary more than traditional
views, in such species as ring-tailed lemurs (Lemur catta:LaFleuret al.2014), gray
snub-nosed monkeys (Rhinopithecus brelichi:Tanet al.2013), and savannah chim-
panzees (Pan troglodytes versus: Boyer-Ontl and Pruetz 2014)(Fig.6). Each of these
primates has been traditionally classified as diurnal (Kirk and Kay 2004;cf.Donati
et al.2013 and Traina 2001 for Lemur catta). Nighttime activity in these primates has
been attributed to avoiding extremely high daytime temperatures (Boyer-Ontl and
Pruetz 2014) and exploiting ephemeral resources (LaFleur et al.2014;Tanet al.
2013). Moreover, some of the nocturnal behaviors documented by camera traps have
been novel, such as cave use and pool soaking by unhabituated groups of Pan
troglodytes verus (Pruetz 2007). Such unexpected animal activity may have important
implications for our understanding of species ecology, including activity budget, food
intake, and predator avoidance, and highlights the behavioral flexibility of these
primate species.
P.A. Pebsworth, M. LaFleur
Methods
Many different camera traps are available, and a researchers site, objectives, and
budget determine which camera is most appropriate. Camera trap technology is
changing rapidly, so we do not discuss specific makes or models but offer some
considerations for selecting a remotely triggered camera and how to determine whether
it will be appropriate for a research site and objectives.
Flash Type and Intensity
Camera traps with infrared flash take color daytime and monochromatic nighttime
photos, while camera traps with white flash take color photos regardless of light levels.
Nighttime color photographs can be critical for conducting a faunal inventory and
studies requiring individual recognition, but white flash may frighten target subjects
Fig. 4 (a) Madagasc ars largest terrestrial predator, the fossa (Crypropracta ferox), entering the nest of the
largest aerial predator, the Madagascar harrier hawk (Polyboroides radiata). (b) Six minutes later the fossa
leaves with a hawk in its mouth. (Photos taken at the Tsimanampetsotse National Park, Madagascar by Marni
LaFleur.).
Use of Camera Traps: Introduction
and alter detection probabilities. In addition to flash type, researchers studying noctur-
nal primates may want to consider whether the camera automatically adjusts flash
intensity based on the distance to the primate. This feature maximizes the probability of
detecting primates while minimizing visible or audible cues that potentially alter
behavior.
Trigger Speed and Sensitivity
How much time passes between camera activation and when a photograph is taken is
critical to many studies. Most cameras employ a passive infrared sensor that activates at
some time after it detects a difference in heat motion between the fore- and background
temperature. Cameras with a short trigger delay (<1 s) are ideal for capturing relatively
fast-moving, small, or solitary primates, whereas a longer trigger delay (>1 s) may be
better for slow-moving, large, or group-living primates. False negative images, i.e., a
Fig. 5 (a) A Cape leopard (Panthera pardus) which shares its range with chacma baboons (Papio
cynocephalus ursinus), and (b) a Madagascar harrier hawk (Polyboroides radiata), which shares its range
with ring-tailed lemurs (Lemur catta). (Photos taken at Wildcliff Nature Reserve, South Africa by Paula
Pebsworth and Tsimamampetsotse National Park, Madagascar by Marni LaFleur.).
P.A. Pebsworth, M. LaFleur
primate triggered the sensor but moved out of the frame before the photograph was
taken, result from a trigger speed that is too slow, but cameras with fast trigger speed
are often more expensive.
The sensitivity, or the cameras ability to detect heat motion, decreases when
ambient temperature is low, or when the difference between ambient temperature and
the subjects body temperature is small (i.e., <2.7°C) (Meek 2012). Decreased sensi-
tivity can result in failure to trigger the camera trap. Alternatively, in very hot
environments the camera can be highly sensitive and triggered more easily by nontarget
movements, e.g., wind or moving vegetation (Gregory et al.2013;Roveroet al.2013).
Sensitivity can be adjusted on most cameras.
Detection Zone
Detection area varies between camera models and is an important determinant in the
number of photos taken. Some cameras use a conical detection zone, while others use
Fig. 6 (a) Ring-tailed lemur (Lemur catta) nighttime activity at the Tsimanampetsotse National Park,
Madagascar. (Photo by Marni LaFleur.) (b) Senegalese chimpanzee (Pan troglodytes versus) nighttime
activity. (Photo by Kelly Boyer Ontl.).
Use of Camera Traps: Introduction
horizontal bands and vertical axis zones (Rovero et al.2013). Obviously, a larger
detection zone allows a larger area to be monitored. The detection zones of some
cameras are wider than their field of view, which can be useful in capturing fast-moving
primates. However, wide detection zones may produce a surplus of blank photographs
taken when primates enter the cameras detection zone but not the field of view.
Cameras with narrower detection zones produce fewer blank photographs but may
also fail to detect primates that move quickly or are not well centered in front of the
camera.
Memory
Most camera traps are digital and require secure digital memory cards. Larger card
sizes, e.g., 432 GB, allow for longer deployment time, a large number of photographs,
or video recording.
Security
Camera traps are expensive and may be difficult to replace once in the field. To
prevent or discourage theft, they can be attached to trees or other substrates
with security cables. Cameras can also be housed in external metal security
boxes, which have the extra protection of being tamper-proof and can also be
locked and securely attached.
Effects of Climate
Moisture and extreme temperatures affect image quality and power. Researchers
combat high humidity and precipitation by placing an internal desiccant inside the
camera housing to prolong dry conditions (Blake et al.2010;Miuraet al.1997). In
addition, covering the camera in a thin transparent polyethylene bag or wrap can act as
a barrier to moisture and debris (Numata et al.2005). Intense sunlight can also impact
camera performance, as it degrades plastic lenses.
In addition to image quality, camera trap performance declines with extreme tem-
peratures, e.g., <0°C and >30°C. In very cold temperatures, alkaline batteries quickly
discharge, so lithium or nickel metal hydride (NiMH) rechargeable batteries are the best
option. NiMH rechargeable batteries fail sooner in hot weather (when temperatures
exceed 32°C), and alkaline and lithium batteries are preferable.
Small portable solar panels with built-in lithium polymer batteries are also available
for camera traps. These are safe for use in extreme temperatures and are automatically
chosen as the main power source for the cameras, although we recommend internal
batteries as backup to solar power.
Trap Days and Camera Placement
Camera trap days are the number of 24-h periods that cameras are employed, multiplied
by the number of cameras in operation (Blake et al.2010; Rovero et al.2013). The
research goals determine the number of camera trap days necessary for data collection.
For example, LaFleur et al.(2014) determined in less than a month that Lemur catta
P.A. Pebsworth, M. LaFleur
frequently engaged in nighttime activity. However, rare behaviors or infrequently
seen species will likely require extended periods of monitoring. In species inven-
tory studies, an accumulation curve can be used to assess if the duration of
sampling has sufficiently captured species present (Tobler et al.2008). In this
case, time needed to carry out a survey is inversely proportional to the number of
camera traps used. The more camera traps used, the more quickly the accumula-
tion curve will level off. However, the distance between cameras may be impor-
tant, as cameras that are placed nearby one another may not produce photographs
that are independent events. This also applies to the time lag between photo-
graphs. Researchers must think carefully about how and why they consider
photographs independent, as this will influence the results (LaFleur et al.2014;
Tan et al.2013).
Camera traps can be placed strategically or systematically. Systematic placement
involves determining set intervals for cameras. In this case, camera placement may be
based on a grid (Gerber et al.2012;Headet al.2012), in convenient areas such as on
trails (Farris et al.2014;Headet al.2012), or randomly (Nakashima et al.2013).
Random sampling aims to meet certain statistical requirements, to achieve independent
sampling (Nakashima et al.2013).
Assessment Biases
All sampling methods have biases, and camera traps are no exception. Images
captured can be biased by species-specific characteristics, as camera trap detec-
tion is higher in gregarious species that forage and travel together than solitary
individuals (Treves et al.2010) and they are also more effective at detecting
smaller, solitary, and nocturnal species than wildlife patrol units (Burton 2012).
Population assessments using camera traps can also be affected by anthropo-
genic disturbances and human presence. For example, Gray and Phan (2011)
reported that camera trap detection was lower in areas within a dayswalkfrom
human settlement and that even after 750 nights of surveys, camera traps failed
to capture all species known to exist within the Phnom Prich Wildlife
Sanctuary.
Correcting Camera Trap Biases
When possible, researchers should compare sampling methods to determine
whether their data are biased. Ideally, biased camera trap data should be
corrected or offset by using an occupancy framework (Gerber et al.2014),
and/or combining camera trap surveys with complementary methods. Many
established methods have been used in combination with camera trap surveys
to improve data reliability, e.g., direct observation and spot counts (Galvis et al.
2014;Pickleset al.2011; and line transects, Farris et al.2014), although other
methods also have inherent biases such as variation in detection, small sample
size, and low precision (Gerber et al.2014). When camera traps and direct
observation fails to establish species presence, indirect observation (spoor, feces,
nest, carcasses) can be employed (Nakashima et al.2013;RossandReeve2003;
Stevens et al.2011).
Use of Camera Traps: Introduction
Implications for Primate Conservation
Primatologists are concerned with the survival of their research taxa (Setchell 2013).
Baseline analyses and environmental monitoring are essential components of conser-
vation management, and camera traps are effective tools both alongside and apart from
traditional habitat and animal monitoring programs (Ahumada et al.2013;Galviset al.
2014). For example, camera trap monitoring and surveillance of Peruvian primates
showed that trap success and encounter rates dramatically decreased immediately after
land clearance and gas pipeline installation; however, animals resumed use of land
bridges after construction (Gregory et al.2013). These data were used to inform gas
and oil developers, who continued to maintain corridors when clearing forested areas
(Gregory et al.2013). Another camera trap study documented Gorilla gorilla diehli for
the first time in Cameroons Kagwene Gorilla Sanctuary (Wildlife Conservation
Society, 2012). This elusive species has rarely been viewed directly, and researchers
and conservation organizations discourage habituation because of potential hunting
pressures. The Wildlife Conservation Society used these data as part of community and
public awareness campaigns, and footage served to inspire local people, governments,
and the global community to protect and conserve this Critically Endangered great ape.
Data such as these can enable conservation planners to assess and progress toward
conservation goals and to target and design interventions (Gregory et al.2013;OBrien
et al.2010; Wegge et al.2004).
The largest globally coordinated camera trap monitoring project, Tropical Ecological
Assessment & Monitoring Network (TEAM), also provides opportunities for primate
conservation planning through camera trap data (www.teamnetwork.org). TEAM
report activities of terrestrial vertebrates and currently monitor 16 tropical forest sites
across Africa, Asia, and Latin America. Camera trap data are collected according to
strict protocols, and all researchers can access the data via an online database.
Primatologists can also contribute data to this project but must adhere to guidelines
including the use of a minimum of 60 camera traps per project. More information on
TEAM can be found on their website (www.teamnetwork.org).
Ethical Considerations
Field primatologists face a complex array of issues related to primate subjects, which
often stem from the competing need for resources by wild primates and humans, and/or
the management of habitat by local governments or officials (Wolfe 2005). Several
excellent publications have resulted from the recent initiative to highlight the ethical
dilemmas faced by field primatologists (Fedigan 2010; MacKinnon and Riley 2010;
Malone et al.2010), but the use of camera traps has not been addressed directly. In fact,
to our knowledge, ethical concerns of camera trapping have not been addressed in the
wildlife literature.
Some of the ethical considerations of using camera traps are the same as those
encountered by conducting fieldwork in general, such as potentially witnessing illegal
activity, while others are unique to camera traps, including what constitutes informed
consent by humans that are photographed. Inevitably, whether intentional or not,
researchers employing camera traps will capture photographs of humans. We thus need
P.A. Pebsworth, M. LaFleur
to determine under what circumstances, if any, these photos are used. Human activities
could, of course, be the focus of our research, as we may want to document human
presence or human impact on nonhuman primate habitats. In these instances, permis-
sion from the researchers Institutional Review Board (IRB) or similar for human
subjects is likely to be necessary. However, if photographs of people are merely a
by-productof data collection, what should we do with these unintended data, and
should we still seek IRB approval?
Ethnographers generally provide copies of data to all informants and go to great
lengths to protect informant identity (Murchison 2010). Should we adopt similar
policies? One could imagine providing photos to each person captured by cameras
quickly becoming unmanageable. Alternatively, it may be more suitable to provide
information, rather than actual photographs, to local people with reference to the
location of cameras and goals of research. Along these lines, and similar to some of
the concerns of sociocultural anthropologists, we also need to consider data storage
policies and decide who will have access to these images. What should we do if local
authorities request (or demand) copies of our camera trap images as a condition of our
research, or even after the research has taken place? Can we protect the anonymity of
the people in our photos, and, with reference to illegal activities, do we want to? Illegal
activity is likely to be the most ethically difficult (and common) potential scenario
researchers will face with camera trap studies. In some instances, providing photo-
graphic documentation to local authorities on illegal harvesting of forest resources,
hunting, or capturing animals could aid forest protection and prosecution of wrong-
doers. Yet, in other cases, this information may do little to further our conservation
agendas and could act to alienate local people and threaten our future research and
conservation prospects.
There are no simple answers to these complex issues, but we hope to initiate a
discussion on some of the ethical conundrums primatologists may face when using
camera traps and encourage forethought related to the conflicts that may arise when
using camera traps in primate research.
Conclusion
The articles in this special issue reflect a variety of primate studies that employed
camera traps and collectively provide a summary of the applications primatologists
are using. Camera traps are proving to be an effective tool in the documentation of
primate ecology and spatial distribution patterns. Further, as human activity con-
tinues to alter primate habitat and behavior, we suggest camera traps can monitor
primate populations that should not be habituated or whose behavior would be
greatly altered by human presence. However, camera traps are not a research
panacea and have inherent biases. We encourage primate researchers to test and
acknowledge these limitations and to use corrective and complementary techniques
when they are warranted. We also recommend that researchers adhere to method-
ological protocols and report qualitative and quantitative methods accurately to
facilitate intersite and -species comparisons. We particularly encourage further
research into the ethical concerns raised by using camera traps in primatological
field research.
Use of Camera Traps: Introduction
Acknowledgments We thank the editor of International Journal of Primatology, Dr. Joanna Setchell, for
help and assistance in the production of this special issue and particularly this editorial. In addition, we thank
our co-guest editor, Chia Tan, and Keith Riggle for their support, suggestions, and reviews of earlier versions
of the manuscript. We thank the symposium participants (Advancing Primate Research and Conservation
through the Use of Camera Traps) and attendees for their contributions and thought-provoking discussion
points. Funding was provided by the Austrian Academy of Science (M. LaFleur) and Wilderness Wildlife
Trust (P. A. Pebsworth).
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... Camera traps provide a potential alternative. They are relatively cheap, require little expertise to set up and maintain, and can be deployed for long periods of time while recording data day and night, seven days a week, which is difficult for researchers to achieve through observation (Pebsworth & LaFleur, 2014). Some animals crop-forage by night (Gunn et al., 2014;Krief et al., 2014), behavior which is particularly challenging to study through observation. ...
... However, where camera traps have been used to assess crop-foraging in the past, what they can and cannot measure is often assumed. There has been little effort to date to establish whether camera traps can reliably record patterns of crop-foraging, as characteristics of species, such as body size or gregariousness, may create systematic biases in camera trap data leading to erroneous conclusions (Kolowski & Forrester, 2017;Pebsworth & LaFleur, 2014;Treves et al., 2010). ...
... Lower detection of smaller primate species has also been observed in other studies (Wallace, 2010). Biases in camera trap detection may explain their poorer ability to predict vervet crop-foraging; larger groups are more likely to be detected by cameras, as are larger bodied animals (Kolowski & Forrester, 2017;Pebsworth & LaFleur, 2014;Treves et al., 2010). ...
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Foraging by wildlife on anthropogenic foods can have negative impacts on both humans and wildlife. Addressing this issue requires reliable data on the patterns of anthropogenic foraging by wild animals, but while direct observation by researchers can be highly accurate, this method is also costly and labor‐intensive, making it impractical in the long‐term or over large spatial areas. Camera traps and observations by guards employed to deter animals from fields could be efficient alternative methods of data collection for understanding patterns of foraging by wildlife in crop fields. Here, we investigated how data on crop‐foraging by chacma baboons and vervet monkeys collected by camera traps and crop guards predicted data collected by researchers, on a commercial farm in South Africa. We found that data from camera traps and field guard observations predicted crop loss and the frequency of crop‐foraging events from researcher observations for crop‐foraging by baboons and to a lesser extent for vervets. The effectiveness of cameras at capturing crop‐foraging events was dependent on their position on the field edge. We believe that these alternatives to direct observation by researchers represent an efficient and low‐cost method for long‐term and large‐scale monitoring of foraging by wildlife on crops. Understanding anthropogenic foraging by researcher observation is costly and labor‐intensive. We investigated whether camera traps and crop guard records could give the same insights as researcher observation into patterns of crop‐foraging by baboons and vervet monkeys. Camera and guard data predicted data from researchers for baboons, and to an extent, vervets, and therefore present a viable alternative to researcher observation allowing for large‐scale and long‐term monitoring of crop‐foraging.
... It has been shown widely among animal taxonomic groups that individuals can be visually identified based on their natural, external phenotypic characteristics, including fur or skin marks and patterns (Karanth & Nichols 1998;K€ uhl & Burghardt 2013;Gardiner et al. 2014). Photographic identification based on these features has been used as an effective, non-invasive technique of capture-mark-recapture, as images of an individual's unique features can be cross-matched within photo-libraries for detection of recapture events (Williams et al. 2002;Pebsworth & LaFleur 2014). With the increased use and accessibility of smartphone devices, individuals can now be photographed with sufficient quality, even under field conditions, and differentiated with very little associated costs or expertise (Wagner et al. 2008;Haddock et al. 2013;Pebsworth & LaFleur 2014). ...
... Photographic identification based on these features has been used as an effective, non-invasive technique of capture-mark-recapture, as images of an individual's unique features can be cross-matched within photo-libraries for detection of recapture events (Williams et al. 2002;Pebsworth & LaFleur 2014). With the increased use and accessibility of smartphone devices, individuals can now be photographed with sufficient quality, even under field conditions, and differentiated with very little associated costs or expertise (Wagner et al. 2008;Haddock et al. 2013;Pebsworth & LaFleur 2014). As such, smartphone photography now offers a reliable alternative to artificial marking techniques that are expensive, possibly physically harmful to the individual and require extended handling times (Reisser et al. 2008;Sacchi et al. 2010). ...
Article
Individuals within amphibian populations are commonly identified using artificial marking techniques, such as toe clipping and microchipping. However, many species in this group may be strong candidates for visual identification from photographs given intraspecific variability in skin features. We investigated the potential for dorsal skin patterns to be used as natural markers for the photo-identification of both juveniles and adults of the green and golden bell frog (Litoria aurea). This is a threatened species that has come under intense population monitoring using capture-mark-recapture procedures primarily involving the use of artificial markers, with no apparent investigation of the potential for natural markers to be used instead. We collected photographs of marked individuals to determine the level of intraspecific variability in dorsal patterning within a population. This photo-database was subsequently used to create an online survey in which participants were asked to match separate images of query frogs from small image pools by comparing dorsal patterns. Photographs were taken on a smartphone device under field conditions to test whether this technique could be applied to the study of wild populations with little cost or expertise required. We showed that dorsal patterns are clear and distinct among L. aurea individuals and easily visualised from field-acquired images to detect recapture events by eye with a low error rate. While an overwhelming majority of adults possessed dorsal patterning that can be easily distinguished by eye, juveniles often showed a complete absence of patterning, suggesting that photo-identification may be more effective for adult stages. Nevertheless, we highlight the feasibility of collecting visual information on the natural markings of a threatened anuran, providing evidence that it may be used as a supplementary form of identification alongside more traditional techniques, highlighting a potential direction for the future monitoring of this species.
... Animal biometrics is an emerging field that involves the identification of species or individuals based on their external phenotypic characteristics, including natural markings or color patterns (Kühl & Burghardt, 2013). It has been used as an effective technique for data collection in ecological procedures such as capture-mark-recapture (CMR), as photographic images of an individual's unique markings can be cross-matched within a photo-database for detection of recapture events (Williams, Nichols & Conroy, 2002;Pebsworth & Lafleur, 2014). This process has been particularly useful for monitoring species that cannot be easily captured or artificially tagged for identification purposes (Frisch & Hobbs, 2007;Arandjelović & Zisserman, 2011;Hughes & Burghardt, 2015), and has been applied to a diverse number of taxa including mammals (Karanth & Nichols, 1998), large fish (Arandjelović & Zisserman, 2011;Hughes & Burghardt, 2015), crustaceans (Frisch & Hobbs, 2007), and herpetofauna (Gardiner et al., 2014). ...
... This process has been particularly useful for monitoring species that cannot be easily captured or artificially tagged for identification purposes (Frisch & Hobbs, 2007;Arandjelović & Zisserman, 2011;Hughes & Burghardt, 2015), and has been applied to a diverse number of taxa including mammals (Karanth & Nichols, 1998), large fish (Arandjelović & Zisserman, 2011;Hughes & Burghardt, 2015), crustaceans (Frisch & Hobbs, 2007), and herpetofauna (Gardiner et al., 2014). With the increased affordability and use of smartphone devices that are equipped with cameras, as well as the advent of camera trapping technology, individuals can now be photographed under field conditions and differentiated with very little cost, logistics or expertise required (Wagner et al., 2008;Haddock, Kim & Mukai, 2013;Pebsworth & Lafleur, 2014). Photo-identification is thus becoming an increasingly important ecological tool that is also providing greater opportunities for the use of citizen science in animal monitoring programs (Dickinson, Benjamin & David, 2010). ...
Article
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Among amphibians, adults have traditionally been identified in capture-mark-recapture studies using invasive marking techniques with associated ethical, cost and logistical considerations. However, species in this group may be strong candidates for photo-identification based on natural skin features that removes many of these concerns, with this technique opening up opportunities for citizen scientists to be involved in animal monitoring programs. We investigated the feasibility of using citizen science to distinguish between individuals of an Australian anuran (the sandpaper frog, Lechriodus fletcheri ) based on a visual analysis of their natural skin features. We collected photographs of marked individuals in the field over three breeding seasons using a smartphone device. This photo-database was used to create an online survey to determine how easily members of the general public could photo-match individuals by a comparison of two facial skin features; black banding that runs horizontally above the tympanum and a background array of tubercles present in this region. Survey participants were provided with 30 closed, multiple choice questions in which they were asked to match separate images of a query frog from small image pools of potential candidate matches. Participants were consistently able to match individuals with a low matching error rate (mean ± SD of 26 ± 5) despite the relatively low quality of photographs taken from a smartphone device in the field, with most query frogs being matched by a majority of participants (mean ± SD of 86.02 ± 9.52%). These features were found to be unique and stable among adult males and females. Thus, photo-identification is likely to be a valid, non-invasive method for capture-mark-recapture for L. fletcheri , and likely many anurans that display similar facial skin features. This may become an important alternative to artificial marking techniques, with the challenges of manual photo-matching reduced by spreading workloads among members of the public that can be recruited online.
... Through habituation, researchers can spend more time with the study animals and approach them at the distance necessary for detailed behavioral observations. Although telemetry and camera traps may offer appealing alternatives (Boyer-Ontl & Pruetz, 2014;Crofoot et al., 2010;Pebsworth & LaFleur, 2014), habituation often is still necessary to collect detailed behavioral information on the study subjects (Alcayna-Stevens, 2016;Bertolani & Boesch, 2007;Blom et al., 2004;Doran-Sheehy et al., 2007;McLennan & Hill, 2010;Narat et al., 2015;Souza-Alves & Ferrari, 2010;Tutin & Fernandez, 1991;Van Krunkelsven et al., 1999). ...
Article
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When studying animal behavior in the wild, some behaviors may require observation from a relatively short distance. In these cases, habituation is commonly used to ensure that animals do not perceive researchers as a direct threat and do not alter their behavior in their presence. However, habituation can have significant effects on the welfare and conservation of the animals. Studying how nonhuman primates react to the process of habituation can help to identify the factors that affect habituation and implement habituation protocols that allow other researchers to speed up the process while maintaining high standards of health and safety for both animals and researchers. In this study, we systematically described the habituation of two groups of wild moor macaques (Macaca maura), an Endangered endemic species of Sulawesi Island (Indonesia), to assess the factors that facilitate habituation and reduce impact on animal behavior during this process. During 7 months, we conducted behavioral observations for more than 7,872 encounters and an average of 120 days to monitor how macaque behavior toward researchers changed through time in the two groups under different conditions. We found that both study groups (N = 56, N = 41) became more tolerant to the presence of researchers during the course of the habituation, with occurrence of neutral group responses increasing, and minimum distance to researchers and occurrence of fearful group responses decreasing through time. These changes in behavior were predominant when macaques were in trees, with better visibility conditions , when researchers maintained a longer minimum distance to macaques and, unexpectedly, by the presence of more than one researcher. By identifying these factors , we contribute to designing habituation protocols that decrease the likelihood of fearful responses and might reduce the stress experienced during this process.
... Future field work, however, may be constrained by the ongoing security concerns in the area, which continue to frustrate Zombitse-Vohibasia's significant research potential (Goodman et al., 2018;Siers, 2007). This may necessitate less resource-intensive, remote alternatives to line transects, including camera trapping (Olson et al., 2012;Pebsworth & LaFluer, 2014), thermal infrared drone surveys (Zhang et al., 2020) and passive acoustic monitoring (Hending et al., 2017(Hending et al., , 2020Marques et al., 2012). ...
Article
en Zombitse-Vohibasia National Park harbours a species-rich but understudied lemur community in southwestern Madagascar. Local population estimates are dated or absent for its four sympatric species of Cheirogaleidae: the grey mouse lemur (Microcebus murinus), Coquerel's giant mouse lemur (Mirza coquereli), fat-tailed dwarf lemur (Cheirogaleus medius) and pale fork-marked lemur (Phaner pallescens). To provide local density and encounter rate estimates for these cheirogaleids, we conducted line transect surveys in the Zombitse sector of the National Park over a three-week period in December 2018–January 2019. We calculated densities of 37.4 Mir. coquereli individuals/km² (95% CI = 20.4–68.6) and 230.8 C. medius individuals/km² (95% CI = 172.6–308.6). Our results highlight the conservation importance of Zombitse-Vohibasia as a stronghold for these restricted and threatened species. The sample sizes for Mic. murinus and P. pallescens were insufficient for generating population estimates. Considering that Microcebus spp. are typically amongst the most abundant mammals at a given site, further studies are needed to investigate and verify this apparent scarcity. Résumé fr Le parc national de Zombitse-Vohibasia, situé au sud-ouest de Madagascar abrite une communauté de lémuriens riche en espèces, mais peu étudiée. Les estimations portant sur la population locale de quatre espèces sympatriques de Cheirogaleidae (le microcèbe [Microcebus murinus], le lémurien nain géant Coquerels [Mirza coquereli], le lémurien nain à grosse queue [Cheirogaleus medius] et le lémurien à fourche pâle [Phaner pallescens] sont obsolètes ou inexistantes. Nous avons réalisé des études par transects en ligne dans le secteur Zombitse du parc national sur une période de trois semaines, de décembre 2018 à janvier 2019 afin de fournir des estimations de la densité locale et du taux de rencontre de ces chéirogaléidés. Nous avons calculé des densités de 37,4 individus Mir. Coquereli au km² (IC à 95 % = de 20,4 à 68,6) et de 230,8 individus C. medius au km² (IC à 95 % = de 172,6 à 308,6). Nos résultats mettent en évidence l'importance de la conservation du parc national de Zombitse-Vohibasia en tant que bastion pour ces espèces restreintes et menacées. La taille des échantillons de Mic. murinus et de P. pallescens était insuffisante pour produire des estimations de la population. Étant donné que l’espèce Microcebus est généralement classée parmi les espèces de mammifères les plus abondantes sur un site donné, d'autres études sont nécessaires afin d’étudier cette situation apparemment rare.
... The ability of remote sensing tools to incidentally (or deliberately, in the case of poachers) reveal the location, movement, and behavior of individuals raises concerns about informed consent, privacy, civil liberties, and fear of arrest. To our knowledge, there is no standard for determining when images or sounds captured from remote sensing can be shared or used (Pebsworth and LaFleur 2014), despite the growing need for universal agreements on these and related contexts that require formal guidance. A recent discussion of the ethical issues related to camera trapping, for example, laid out recommendations for a basic code of conduct (Sharma et al. 2020). ...
Article
Full-text available
Observing and quantifying primate behavior in the wild is challenging. Human presence affects primate behavior and habituation of new, especially terrestrial, individuals is a time-intensive process that carries with it ethical and health concerns, especially during the recent pandemic when primates are at even greater risk than usual. As a result, wildlife researchers, including primatologists, have increasingly turned to new technologies to answer questions and provide important data related to primate conservation. Tools and methods should be chosen carefully to maximize and improve the data that will be used to answer the research questions. We review here the role of four indirect methods—camera traps, acoustic monitoring, drones, and portable field labs—and improvements in machine learning that offer rapid, reliable means of combing through large datasets that these methods generate. We describe key applications and limitations of each tool in primate conservation, and where we anticipate primate conservation technology moving forward in the coming years.
... Camera traps are an effective tool to capture baseline natural history data on understudied primates, especially for nonhabituated or hunted populations in difficult environments (Alempijevic et al., 2021;Li et al., 2015;Pebsworth & LaFleur, 2014;Tan et al., 2013;Yang et al., 2018). Camera traps proved to be a useful tool to document the ontogenetic pelage pattern of dryas monkeys and conduct a preliminary assessment of the dryas monkey population in Lomami National Park and buffer zone. ...
Article
Full-text available
The natural history and taxonomic status of two central African primates, Cercopithecus dryas and Cercopithecus salongo have long been in question. Recent studies confirmed that C. dryas is a basal member of the savanna monkey clade, and that it prefers dense undergrowth in lowland rainforest. While these studies advanced our knowledge of this enigmatic species, key aspects of its natural history remain poorly documented. Furthermore, the lack of a field study that documents pelage patterns of both sexes and different age classes of C. dryas has led to a disagreement over the validity of C. salongo as a sister taxon to C. dryas. Using the results of two multi‐strata camera trap surveys in Lomami National Park (Democratic Republic of the Congo) and its buffer zone, we conducted a third survey in the understory of degraded forest to accumulate videos of C. dryas/salongo. We used these videos to test the hypothesis that C. dryas and C. salongo are synonymous, and to assess the species' group composition, density, behavior and vocalizations. Camera traps revealed an ontogenetic change in pelage pattern that supports the view that C. salongo is the adult of C. dryas. Videos revealed that adult males develop a blue perineum and scrotum, and a red subcaudal patch, similar to other savanna monkeys. We provide a preliminary assessment of C. dryas' group composition, density, behavior, and vocalizations. This long‐overlooked monkey is an exceptional member of the Chlorocebus clade, and all aspects of its biology require further investigation. Research Highlights • Camera trap videos support that two described species, Cercopithecus dryas and Cercopithecus salongo, are conspecific. • Male dryas monkeys develop a red subcaudal patch, blue perineum, and white caudal ruff that forms an elaborate display, similar to the red, white, and blue displays of savanna monkeys.
... Recently, camera traps have become an important tool for terrestrial species surveys, in particular for mammal surveying (Andresen et al., 2018;Blake & Loiselle, 2018;McShea et al., 2009;Srivastava & Kumar, 2018;Widness & Aronsen, 2018). The method has also been used to either research or study such as the effects of human disturbance and environmental change on mammals (Vanthomme et al., 2013), the conservation of species that are rare and endangered, for animal monitoring in human landscapes, and in behavior studies of nonhuman primates (Pebsworth & LaFleur, 2014;Rabinowitz & Nottingham, 1989;Saito & Koike, 2013), to document the use of specific habitats by animals (Fiderer et al., 2019;Granados et al., 2016). ...
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A comprehensive and practical guide to ethnographic research, this book guides you through the process, starting with the fundamentals of choosing and proposing a topic and selecting a research design. It describes methods of data collection (taking notes, participant observation, interviewing, identifying themes and issues, creating ethnographic maps and tables and charts, and referring to secondary sources) and analyzing and writing ethnography (sorting and coding data, answering questions, choosing a presentation style, and assembling the ethnography). Although content is focused on producing written ethnography, many of the principles and methods discussed here also apply to other forms of ethnographic presentation, including ethnographic film. Designed to give basic hands-on experience in the overall ethnography research process, Ethnography Essentials covers a wealth of topics, enabling anyone new to ethnography research to successfully explore the excitement and challenges of field research.
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