Forest loss due to land conversion for agriculture and pasture is one the principal threats facing biodiversity in the Neotropics [1
]. As a result, animal populations across the region are threatened with extinction. Forest loss is accompanied by forest fragmentation and degradation, processes that may strongly affect arboreal species due to changes in canopy connectivity and loss of aerial pathways. To protect the remaining habitat, the species residing in them, and the ecosystem services they provide, conservation practitioners need accurate and precise information on the distribution and abundance of species [4
]. Arboreal mammals can be difficult to survey, as many species are nocturnal, live in the canopy or flee before they have been detected by observers on the ground [4
]. Due to these challenges, along with the cost of accessing large swaths of forest, there is a lack of population information for a wide range of arboreal species.
Spider monkeys (Ateles
spp.) are large-bodied arboreal primates and widely distributed in the Neotropics [7
]. Due to anthropogenic pressures (mainly hunting and deforestation), all species are categorised as Endangered or Critically Endangered on the International Union for the Conservation of Nature (IUCN) red list [8
]. Conservation management therefore requires frequent, accurate, and precise information on presence as well as population density throughout the species’ range. As with many other arboreal mammal species, data on presence and/or population density have been collected during general biodiversity surveys or surveys focused on particular species [9
], traditionally by counting individuals along line transects on foot [12
]. Although methods exist to determine presence and abundance, there are large gaps in our knowledge of spider monkey distribution and density [14
]. This is partially due to spider monkeys being notoriously difficult to survey due to their high degree of fission–fusion dynamics (i.e., group members split into subgroups whose size, membership, and spatial cohesion vary greatly over time [15
]), fast arboreal movements, and large home ranges, and they may thus remain unsurveyed at sites where they occur [16
]. Additionally, the wide distribution of the species and the costs of conducting ground surveys are further hindering factors [14
]. The need for frequent surveys due to the rapid land-use changes that are occurring across their range only exacerbates this problem. There is thus an urgent need to test alternative methods to obtain data on presence and density at a pace that is comparable to the pace of land-use change.
Relatively recently, researchers have started to use drones to obtain data on animals and their habitats (reviewed in Reference [17
]). In most studies, standard visual spectrum (RGB) cameras have been mounted on drones to obtain data on species presence due to the relatively large areas that drones can cover rapidly; in fewer studies, they were used to determine population density [17
]. Although using the visual spectrum has been successful, there are several limitations [18
]. First, the relatively limited bandwidth of the visual spectrum (0.39–0.7 µm) means that the reflectance of all objects is relatively close to each other, which can hamper differentiation. Second, using the visual spectrum does not allow for the detection of animals when there is low light, or it is dark. Thus, for species that are nocturnal or species where detection of animals at dawn and dusk is important, there is a need to explore detection opportunities with other sensors. Thermal infrared (TIR) cameras, which use a different part of the electromagnetic spectrum (8–13.5 µm), have recently been used to detect a variety of animals (e.g., deer, seals, koalas, kinkajous, monkeys, and rhinoceros [19
There have been only a few drone studies to detect primates, which mostly focused on nests built by apes (Pan troglodytes
]; Pongo abelii
]). Kays et al., 2019 [23
] found that a TIR camera mounted to a drone can be used to survey arboreal mammals, including monkeys (Ateles geoffroyi
and Alouatta palliata
). They concluded that ground surveys are more effective in counting monkeys than drone surveys, as dense canopy vegetation may mask individuals that are found in lower layers of the vegetation strata. However, these results are based on only two surveys where drone and ground counts were compared, and although the same overall area was surveyed, the drone and human observers did not follow the exact same paths. Further studies using a larger number of surveys are therefore necessary to corroborate these results and determine whether using drones with TIR cameras is an alternative or complementary method to ground surveys for spider monkeys.
In this study, we assessed the effectiveness of using drones with a TIR camera for surveying Geoffroy’s spider monkeys (A. geoffroyi
). First, we examined whether we can detect the presence of spider monkeys in their sleeping trees using a TIR camera mounted to a drone. Second, we compared simultaneous ground and aerial counts of spider monkeys at their sleeping sites to determine the agreement between the two methods. Third, we compared the number of spider monkeys counted during ground and drone surveys depending on flight type (grid and hover flights) and time of day (morning and evening). Primate ground surveys become less reliable when encountering larger groups, as individuals are more likely to be missed [27
]. Drone surveys using a TIR camera might therefore produce more reliable counts than ground surveys when monkeys are found in large numbers due to a greater area covered and the ease of detecting individuals in the top of the canopy that might be missed from the ground.
Accurate and precise counts of animal populations form the basis of conservation decisions and actions; however, they are lacking for the majority of arboreal species due to difficulties and costs of performing ground surveys. To overcome these difficulties, recent studies have fitted drones with TIR cameras to monitor primate populations (howler monkeys and spider monkeys [23
]; orangutans [42
]). Here, we demonstrated that a TIR camera fitted to a drone can be successfully employed to determine the presence and count the number of spider monkeys in a closed-canopy forest. Spider monkeys were easy to detect in the TIR footage due to their relatively high temperature compared to their surroundings. Since they spend a large amount of time at the top of the forest canopy [43
] and tend to sleep on terminal branches, an aerial viewpoint offers distinct advantages over ground-based observations. Spider monkey movement in the canopy aided the differentiation between monkeys and other objects with a similar heat image, especially in the afternoon when the heat stored from the sun during the day still illuminated the branches in the TIR footage. In addition to spider monkeys, the Yucatan Peninsula is home to black howler monkeys (Alouatta pigra
), but they are very rare in Los Arboles Tulum. Other animals of similar size to spider monkeys (e.g., coatis, small cats) occupy lower vegetation layers and will therefore be more difficult to detect in TIR drone footage [23
]. None of these species were observed near the monkeys during our ground observations. It is therefore unlikely that we misidentified spider monkeys during our ground and drone surveys. During the dry season, many tree species in the Yucatan Peninsula lose their leaves, which may aid visibility and facilitate detection of arboreal mammals. Our study was performed at the start of the rainy season, when tree foliage is extensive, suggesting that drones fitted with TIR cameras can be used to survey spider monkeys in sites where foliage cover is high year-round.
The drone surveys produced counts similar to those produced using traditional ground surveys for subgroups containing <10 monkeys, and the two counts were shown to be statistically consistent with each other. For larger subgroups (>10 monkeys), the number of individuals counted was higher for drone than ground surveys in 92% of the cases. Drone surveys may offer an advantage over ground surveys when observing large subgroups, as they provide greater visibility because vegetation does not obscure some of the monkeys, and the footage can be replayed multiple times to aid visual identification. In addition, in TIR footage, the monkeys appear as bright objects (during cooler times of the day), whereas they are the same brightness as their surroundings when viewed with the naked eye. In our study, visibility made counting monkeys from the ground difficult in some cases. For example, 75% of large subgroups where ground observers missed individuals occurred at sleeping site B, where monkeys tend to sleep in an emergent tree whose canopy is largely obscured from view from the ground by other vegetation.
Conversely to our findings, Kays et al., 2019 [23
] found that ground counts were higher than drone counts. However, they compared counts from only two flights, whereas we compared counts from 28 flights. Kays et al., 2019 [23
] also used a lower resolution TIR camera than ours, and TIR camera resolution has been shown to strongly affect the detectability of animals from a drone [32
]. As our study was performed at sleeping sites, most monkeys were relatively stationary and therefore potentially easier to detect on TIR footage as mobile individuals may go in and out of view while moving through the canopy. Ground surveys are often carried out when primates are most active (i.e., in the early morning and late afternoon), as their movement through the canopy can aid detection [44
]. Ground surveys may therefore be more accurate than TIR drone surveys during hours of the day when primates are active, but their surroundings have started to heat up, minimising thermal contrast. Kays et al., 2019 [23
] performed surveys when spider monkeys were more active and thus more difficult to detect on TIR footage, potentially explaining differences in results between the studies.
Kays et al., 2019 [23
] reported heating of the canopy to be a major issue in using TIR to detect and identify animals in their study. Time of day is an important consideration when flying drones with TIR cameras. To maximise thermal contrast, drone flights should be performed at the time of day that the difference in temperature between the animal of interest and its surroundings is greatest [23
]. Therefore, flying a drone with a TIR camera over a forested area during most of the day would make detecting large-bodied arboreal primates such as spider monkeys extremely difficult as tree leaves and branches have become heated by the sun [23
]. Likewise, distinguishing different species of similar size becomes nearly impossible at this time of day. To minimise this effect, we performed our surveys at times of the day when the heat from the surroundings would differ the most in relation to the heat of the monkeys (Figure 3
]). The results of our study and that of Kays et al., 2019 [23
] highlight the importance of understanding the environment and planning observations accordingly when using thermal drones to survey wildlife. As many countries have regulatory frameworks in place that restrict flying drones at night or before sunrise [46
], surveyors will also have to adjust their study design to align with local regulations.
The purpose of the four hover flights was to examine whether TIR images from these flights led to a pattern regarding the comparison with ground counts similar to that of grid flights. Therefore, the fact that more monkeys were counted from TIR footage obtained from hover flights than from grid flights was simply due to the bias in the relative locations where the two types of flights were performed. We performed hover flights above sleeping trees where we knew that many monkeys slept together, thereby biasing towards higher monkey counts. In fact, 80% of the subgroups counted from the ground during the four hover flights were large, whereas only 26% of the subgroups counted from the ground during 24 grid flights were large.
The number of additional monkeys detected in TIR drone footage outside of the visual field of ground observers ranged from zero to 12 (Table A1
), a mean increase of 49% in the number of monkeys detected compared to ground counts, suggesting that ground counts may underestimate the number of individuals in an area. In this study, we were unable to confirm whether either ground or drone counts provide the true number of monkeys in an area. However, given that drone surveys can cover a larger area and allow counts to be performed at a more leisurely pace post-flight while replaying the footage to identify monkeys in different areas, we suggest that drone surveys provide counts that are closer to the true number of animals inhabiting the area.
Appropriate survey design and analysis may allow researchers to scale up and extrapolate the results from surveys performed in small areas to an overall area of interest. However, population counts may be biased if factors affecting population size such as vegetation or climate are heterogenous across the overall area and are not controlled for. If the use of drones and TIR cameras can be validated to provide accurate and precise population counts, large areas can be surveyed and bypass the need for extrapolation. Whereas a more thorough understanding on the completeness of drone-based counts is necessary, our findings provide a base for validating the accuracy and precision of this technology for surveys of spider monkeys and indicate that this technology can offer important information to conservation practitioners.
As discussed above, one source of potential confusion when using TIR cameras is heat given off by objects in the general environment [47
]. Tree branches, hard earth, concrete surfaces, and bodies of water can retain heat for many hours after they stop receiving solar heating. Even when performing flights during the cooler times of day, we found that heat from the surroundings did occasionally lead to missing individual monkeys that were counted by ground observers. We found more spider monkeys were counted at the same sleeping site in the morning than the previous evening from TIR footage, likely because they appeared brighter and easier to identify in early-morning TIR footage given that the surroundings cooled off during the night.
The behaviour of the monkeys may explain why more individuals were detected from the ground than from TIR footage for 29% (10 out of 35) of monkey subgroups. For instance, spider monkey females tend to huddle together with juveniles in sleeping trees and could have been mistakenly counted as a single individual from TIR footage. From the ground, observers have more time and can change position to assess whether there are huddling individuals, whereas in most of our flights, the drone flies over the monkeys in a preprogrammed grid without hovering over the sleeping trees to allow better identification. Interestingly, for all hover flights, drone counts were higher than ground counts.
The behavioural reaction of the spider monkeys to the drone flying overhead was of short duration for grid flights but more pronounced for hover flights. This is in line with a recent review of animal responses to drone flights [48
]. The behaviours shown by the monkeys during our drone flights were similar to the behaviours of unhabituated spider monkeys encountered during line-transect surveys performed on the ground: Monkeys move away, alarm call or display by throwing branches at the human observers (Denise Spaan, personal observation). The similarity in behaviours leads us to suggest that performing drone surveys is not more invasive or stressful than performing line-transect surveys on the ground. Drone surveys on unhabituated populations of spider monkeys are needed to corroborate our assertion, as we surveyed monkeys habituated to humans.
Although the lightweight multirotor drone we used to perform this study is not ideal to cover large areas due to its short flight-time, our results support the use of drones fitted with TIR cameras as a successful method to detect and count spider monkeys at their sleeping sites. Fitting a TIR camera to a fixed-wing drone or a vertical take-off and landing (VTOL) drone would remove the need for large open take-off and landing space, thus enabling surveyors to cover larger areas within relatively little time. Flying at night when the temperature difference between the monkeys and their surroundings is greatest would enable researchers to detect and count spider monkeys in their sleeping sites in areas where they are not known to occur. As fixed-wing drones can be flown at high altitudes, the combination with a high resolution TIR camera would ensure minimal noise disturbance to the spider monkeys. As such, the use of drones with TIR cameras can potentially offer a huge advance in population monitoring of spider monkeys in forested environments. Automating the detection of species in TIR footage or images obtained from drone flights would further aid its usefulness by reducing the time taken to analyse footage post-flight. Full implementation of the use of drones for population monitoring is technologically feasible, but at present, the regulatory framework in most countries does not allow for beyond visual line of sight (BVLOS) flights [46
] nor flying at night and thus poses a challenge for surveys of large remote areas. A risk-based approach to the distance from the pilot at which drones would be allowed to fly could facilitate such BVLOS flights and allow for more opportunities for surveys in low-risk areas [49