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

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 addition, 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.     

Patterns of mineral lick visitation by spider monkeys and howler monkeys in Amazonia: are licks perceived as risky areas?

Mineral licks--also known as "salados," "saladeros," or "collpas"--are specific sites in tropical and temperate ecosystems where a large diversity of mammals and birds come regularly to feed on soil. Although the reasons for vertebrate geophagy are not completely understood, animals are argued to obtain a variety of nutritional and health benefits from the ingestion of soil at mineral licks. We studied the temporal patterns of mineral lick use by white-bellied spider monkey (Ateles belzebuth) and red howler monkey (Alouatta seniculus) in a lowland rain forest in Amazonian Ecuador. Using camera and video traps at four different mineral licks, combined with behavioral follows of one group of spider monkeys, we documented rates of mineral lick visitation by both primate species and the relative frequency and intensity of mineral lick use by spider monkeys. On the basis of 1,612 days and 888 nights of mineral lick monitoring, we found that A. belzebuth and A. seniculus both visit mineral licks frequently throughout the year (on average ～14% of days for both species), and mineral lick visitation was influenced by short-term environmental conditions (e.g. sunny and dry weather). For spider monkeys, the area surrounding the lick was also the most frequently and most intensively used region within the group's home range. The fact that spider monkeys spent long periods at the lick area before coming to the ground to obtain soil, and the fact that both species visited the lick preferentially during dry sunny conditions (when predator detectability is presumed to be relatively high) and visited simultaneously more often than expected by chance, together suggest that licks are indeed perceived as risky areas by these primates. We suggest that howler and spider monkeys employ behavioral strategies aimed at minimizing the probability of predation while visiting the forest floor at risky mineral lick sites.     

Geophagy in brown spider monkeys (Ateles hybridus) in a lowland tropical rainforest in Colombia

Spider monkeys and howler monkeys are the only Neotropical primates that eat soil from mineral licks. Not all species within these genera visit mineral licks, and geophagy has been restricted to populations of Ateles belzebuth belzebuth,Ateles belzebuth chamek and Alouatta seniculus in western Amazonian rainforests. With the aid of a camera trap we studied the visitation patterns of a group of brown spider monkeys (Ateles hybridus) to a mineral lick at Serrania de Las Quinchas, in Colombia. Spider monkeys visited the lick frequently throughout the year, with a monthly average of 21.7 ± 7.2 visits per 100 days of camera trapping (n = 14 months). Spider monkeys visited the mineral lick almost always on days with no rain, or very little (<3 mm) rain, suggesting that proximate environmental variables might determine spider monkeys' decisions to come to the ground at the licks. This study expands the geographical occurrence of mineral lick use by spider monkeys providing additional data for future assessments on the biogeographical correlates of mineral lick use by platyrrhines.     

红外相机技术在我国野生动物监测中的应用: 问题与限制

红外相机(camera traps)作为对野生动物进行“非损伤”性采样的技术, 已成为研究动物多样性、种群生态学及行为学的常用手段之一。其发展和普及为中国野生动物多样性和物种保育研究带来了诸多机会。如今, 国内大多数自然保护区都在运用红外相机技术开展物种监测工作。本文结合20年来已发表的相关研究, 从内容、实验设计以及发展趋势方面, 总结了目前红外相机技术在应用过程中出现的共性问题; 并就相机对动物的干扰性、影像识别、研究的适用范围及安全保障四个方面, 对该项技术在实践中存在的限制进行了探讨。最后结合红外相机技术未来的发展方向, 提出了建立技术规范、数据集成和共享、影像数据版权维护、提高监测效率等问题。     

Foraging,Food Choice,and Food Processing by Sympatric Ripe-Fruit Specialists: <Emphasis Type="Italic">Lagothrix lagotricha poeppigii</Emphasis> and <Emphasis Type="Italic">Ateles belzebuth belzebuth</Emphasis>

Studies of interspecific competition and niche separation have formed some of the seminal works of ecology. I conducted an 18-mo study comparing the feeding ecologies of 2 sympatric, closely-related ripe-fruit specialists, Humboldt's woolly monkeys (Lagothrix lagotricha poeppigii), and the white-bellied spider monkeys (Ateles belzebuth belzebuth) in Amazonian Ecuador. Woolly monkeys in the terra firme forest live at roughly triple the density of spider monkeys (31 versus 11.5 animals/km²). Woolly monkeys spend 17% of their time foraging, while spider monkeys spend only 1% of their time foraging. Spider monkeys alone fed on soil and termitaria, which are rich in phosphorus. Woolly monkeys are not hard-fruit specialists. Their fruit diet is significantly more diverse than that of spider monkeys. Dietary overlap between the 2 species is high, yet each specializes to some degree on a different set of fruit resources. Woolly monkeys visit more food sources per unit of time, feed lower in the canopy, visit more small food patches, and prey on more seeds. Spider monkeys feed on fewer, richer food sources and are more than twice as likely to return to a particular fruit source than woolly monkeys are. Spider monkeys maximize fruit pulp intake, carrying more intact seeds in their guts, while woolly monkeys minimize seed bulk swallowed through more careful food processing. Surprisingly, several preferred spider monkey foods with high fat content and large seeds are avoided by woolly monkeys. I outline the different ecological dimensions involved in niche separation between the 2 species and discuss the possible impetus for their evolutionary divergence.     

Trap style influences wild pig behavior and trapping success

Despite the efforts of many natural resource professionals, wild pig (Sus scrofa) populations are expanding in many areas of the world. Although many creative techniques for controlling pig populations are being explored, trapping has been and still is the most commonly used method of population control for many public and private land managers. We conducted an observational study to examine the efficiency of 2 frequently used trap styles: a small, portable box-style trap and a larger, semi-permanent, corral-style trap. We used game cameras to examine patterns of trap entry by wild pigs around each style of trap, and we conducted a trapping session to compare trapping success between trap styles. Adult female and juvenile wild pigs entered both styles of trap more readily than did adult males, and adult males seemed particularly averse to entering box traps. Less than 10% of adult male visits to box traps resulted in entries, easily the least percentage of any class at any style of trap. Adult females entered corral traps approximately 2.2 times more often per visit than box traps and re-entered corral traps >2 times more frequently. Juveniles entered and re-entered both box and corral traps at similar rates. Overall (all-class) entry-per-visit rates at corral traps (0.71) were nearly double that of box traps (0.37). Subsequent trapping data supported these preliminary entry data; the capture rate for corral traps was >4 times that of box traps. Our data suggest that corral traps are temporally and economically superior to box traps with respect to efficiency; that is, corral traps effectively trap more pigs per trap night at a lower cost per pig than do box traps. © 2011 The Wildlife Society.     

Occupancy Models for Monitoring Marine Fish: A Bayesian Hierarchical Approach to Model Imperfect Detection with a Novel Gear Combination

Occupancy models using incidence data collected repeatedly at sites across the range of a population are increasingly employed to infer patterns and processes influencing population distribution and dynamics. While such work is common in terrestrial systems, fewer examples exist in marine applications. This disparity likely exists because the replicate samples required by these models to account for imperfect detection are often impractical to obtain when surveying aquatic organisms, particularly fishes. We employ simultaneous sampling using fish traps and novel underwater camera observations to generate the requisite replicate samples for occupancy models of red snapper, a reef fish species. Since the replicate samples are collected simultaneously by multiple sampling devices, many typical problems encountered when obtaining replicate observations are avoided. Our results suggest that augmenting traditional fish trap sampling with camera observations not only doubled the probability of detecting red snapper in reef habitats off the Southeast coast of the United States, but supplied the necessary observations to infer factors influencing population distribution and abundance while accounting for imperfect detection. We found that detection probabilities tended to be higher for camera traps than traditional fish traps. Furthermore, camera trap detections were influenced by the current direction and turbidity of the water, indicating that collecting data on these variables is important for future monitoring. These models indicate that the distribution and abundance of this species is more heavily influenced by latitude and depth than by micro-scale reef characteristics lending credence to previous characterizations of red snapper as a reef habitat generalist. This study demonstrates the utility of simultaneous sampling devices, including camera traps, in aquatic environments to inform occupancy models and account for imperfect detection when describing factors influencing fish population distribution and dynamics.     

Mark-Recapture and Mark-Resight Methods for Estimating Abundance with Remote Cameras: A Carnivore Case Study

Abundance estimation of carnivore populations is difficult and has prompted the use of non-invasive detection methods, such as remotely-triggered cameras, to collect data. To analyze photo data, studies focusing on carnivores with unique pelage patterns have utilized a mark-recapture framework and studies of carnivores without unique pelage patterns have used a mark-resight framework. We compared mark-resight and mark-recapture estimation methods to estimate bobcat (Lynx rufus) population sizes, which motivated the development of a new "hybrid" mark-resight model as an alternative to traditional methods. We deployed a sampling grid of 30 cameras throughout the urban southern California study area. Additionally, we physically captured and marked a subset of the bobcat population with GPS telemetry collars. Since we could identify individual bobcats with photos of unique pelage patterns and a subset of the population was physically marked, we were able to use traditional mark-recapture and mark-resight methods, as well as the new “hybrid” mark-resight model we developed to estimate bobcat abundance. We recorded 109 bobcat photos during 4,669 camera nights and physically marked 27 bobcats with GPS telemetry collars. Abundance estimates produced by the traditional mark-recapture, traditional mark-resight, and “hybrid” mark-resight methods were similar, however precision differed depending on the models used. Traditional mark-recapture and mark-resight estimates were relatively imprecise with percent confidence interval lengths exceeding 100% of point estimates. Hybrid mark-resight models produced better precision with percent confidence intervals not exceeding 57%. The increased precision of the hybrid mark-resight method stems from utilizing the complete encounter histories of physically marked individuals (including those never detected by a camera trap) and the encounter histories of naturally marked individuals detected at camera traps. This new estimator may be particularly useful for estimating abundance of uniquely identifiable species that are difficult to sample using camera traps alone.     

Efficiency of flight interception traps for adult Colorado potato beetles (Coleoptera: Chrysomelidae)

Interception traps have been used to monitor and sample Colorado potato beetle, Leptinotarsa decemlineata (Say), populations in flight, but the efficiency of these traps was unknown. The efficiency of interception window traps is limited because flying adults avoid the traps and may bounce off the trap without being collected. All trap types tested were avoided in flight chamber tests, including those constructed of transparent Plexiglas or yellow wood boards. A larger screen trap and a harp trap designed to reduce detection were also avoided by the beetles in flight. None of the traps provide a direct estimate of the number of adults randomly flying in the trap area. The highest level of efficiency for window traps was obtained with the yellow trap, which caught 16% of the expected flying population. Harp and screen traps without frames intercepted 60-62% of the expected flying population. The presence of a frame did not increase significantly the avoidance of the screen and harp traps by beetles in flight. Recommendations are made to maintain or increase the efficiency of some traps.     

探讨基于红外相机技术对大型猫科动物及其猎物的种群评估方法

红外相机技术的发展促进了对东北虎(Panthera tigris altaica)、东北豹(Panthera pardus orientalis)及其猎物种群的研究。本研究以珲春保护区春化和马滴达两个区域的监测结果为例, 介绍利用该技术对我国长白山区东北虎、东北豹及其猎物的种群评估方法, 包括监测位点的选择、相机的架设方式及参数设置、数据筛选、东北虎和东北豹体侧花纹个体识别方法、物种相对丰富度的计算以及捕食者与猎物丰富度关系模型的构建。最后就东北虎、东北豹体侧花纹个体识别技术的适用性、红外相机监测与传统调查方法的差异, 相机监测的误差进行了讨论。研究表明, 利用红外相机技术进行密度预测以及东北虎、东北豹个体自动识别技术还需继续完善。1对/25 km²的相机架设密度基本上满足对于珲春保护区春化至马滴达区域虎豹的监测强度要求, 但对于有蹄类则需要另外的监测方案。     

The selfie trap: A novel camera trap design for accurate small mammal identification

Camera traps are a popular tool for monitoring wildlife though they can fail to capture enough morphological detail for accurate small mammal species identification. Camera trapping small mammals is often limited by the inability of camera models to: (i) record at close distances; and (ii) provide standardised photos. This study aims to provide a camera trapping method that captures standardised images of the faces of small mammals for accurate species identification, with further potential for individual identification. A novel camera trap design coined the ‘selfie trap’ was developed. The selfie trap is a camera contained within an enclosed PVC pipe with a modified lens that produces standardised close images of small mammal species encountered in this study, including: Brown Antechinus (Antechinus stuartii), Bush Rat (Rattus fuscipes) and Sugar Glider (Petaurus breviceps). Individual identification was tested on the common arboreal Sugar Glider. Five individual Sugar Gliders were identified based on unique head stripe pelage. The selfie trap is an accurate camera trapping method for capturing detailed and standardised images of small mammal species. The design described may be useful for wildlife management as a reliable method for surveying small mammal species. However, intraspecies individual identification using the selfie trap requires further testing.     

Assessing Initial Reintroduction Success in Long-Lived Primates by Quantifying Survival, Reproduction, and Dispersal Parameters: Western Lowland Gorillas (Gorilla gorilla gorilla) in Congo and Gabon

Postrelease monitoring is an important aspect of reintroduction projects, one outcome of which is to allow an assessment of the initial success of the reintroduction, often measured by quantifying survival and reproduction rates. In long-lived species, accurate estimations of demographic parameters are difficult to obtain, and therefore assessment of reintroduction success in such species is challenging. To assess the initial success of a reintroduction program for the long-lived, slow-reproducing, and critically endangered western lowland gorilla Gorilla gorilla gorilla, we analyzed postrelease monitoring data from 2 reintroduced populations, in the Batéké Plateau region of the Republics of Congo and Gabon, to quantify several demographic parameters, and compared our results with published data on wild gorilla populations. Annual survival rate of the 51 released gorillas was 97.4%, 9 females gave birth to 11 infants at an annual birth rate of 0.196 births per adult female, and first-year survival of the infants was 81.8%. Annual birth rate within the reintroduced populations is not significantly different from that given for wild western gorilla populations, and other demographic parameters fall within the range of published data for wild gorilla populations. Our analysis illustrates that the reintroduction program has been successful in terms of the initial measures of postrelease survival and reproduction, and our quantitative data should facilitate the development of a population model that can predict the probability of population persistence and therefore provide an indication of longer-term reintroduction success.     

利用红外相机视频数据进行库姆塔格沙漠地区野骆驼集群行为研究的可行性

野骆驼(Camelus ferus)生性机警, 且栖息于远离人迹、自然条件极端恶劣的荒漠、半荒漠地区, 其种群动态和行为生态学研究一直较为缺乏。本研究通过在库姆塔格沙漠地区进行不同季节的野外观测和连续水源地红外相机监测, 对野骆驼的集群行为进行了研究。2011-2013年, 在库姆塔格沙漠地区进行了8次野外调查, 共记录野骆驼64群, 个体430峰。非繁殖季节野骆驼集群大小平均为2.94±0.67峰; 而繁殖季节野骆驼集群大小平均为10.74±3.08峰。野外观测数据证明了野骆驼集群行为存在季节性差异, 倾向于冬季繁殖季节的集群。并于2012年10月至2013年9月期间, 在11个水源地设置11台红外相机, 共记录野骆驼281群745峰。与野外调查结果相比, 红外相机数据表明繁殖期间和非繁殖期间野骆驼集群大小没有显著差异(t = 0.322, P = 0.748)。水源地的地形因素、红外相机监测视角和监测时间的限制可能是造成这一差异的原因。但是两种方法的结果均表明野骆驼在阿尔金山北麓比西湖地区容易形成较大的集群; 同时, 繁殖季节野骆驼最大集群的规模要大于非繁殖季节。尽管利用红外相机进行动物集群行为研究存在一定的局限性, 但与传统基于野外调查的方法相比, 无论是经济上还是实用性方面, 利用红外相机都为我们开展动物行为学研究提供了新的手段。     

AnimalFinder: A semi-automated system for animal detection in time-lapse camera trap images

Although the use of camera traps in wildlife management is well established, technologies to automate image processing have been much slower in development, despite their potential to drastically reduce personnel time and cost required to review photos. We developed AnimalFinder in MATLAB® to identify animal presence in time-lapse camera trap images by comparing individual photos to all images contained within the subset of images (i.e. photos from the same survey and site), with some manual processing required to remove false positives and collect other relevant data (species, sex, etc.). We tested AnimalFinder on a set of camera trap images and compared the presence/absence results with manual-only review with white-tailed deer (Odocoileus virginianus), wild pigs (Sus scrofa), and raccoons (Procyon lotor). We compared abundance estimates, model rankings, and coefficient estimates of detection and abundance for white-tailed deer using N-mixture models. AnimalFinder performance varied depending on a threshold value that affects program sensitivity to frequently occurring pixels in a series of images. Higher threshold values led to fewer false negatives (missed deer images) but increased manual processing time, but even at the highest threshold value, the program reduced the images requiring manual review by ~ 40% and correctly identified > 90% of deer, raccoon, and wild pig images. Estimates of white-tailed deer were similar between AnimalFinder and the manual-only method (~ 1–2 deer difference, depending on the model), as were model rankings and coefficient estimates. Our results show that the program significantly reduced data processing time and may increase efficiency of camera trapping surveys.     

探讨我国森林野生动物红外相机监测规范

野生动物多样性是生物多样性监测与保护管理评价的关键指标, 因此对野生动物进行长期监测是中国森林生物多样性监测网络(CForBio)等大尺度生物多样性监测研究计划的一个重要组成部分。2011年以来, CForBio网络陆续在多个森林动态监测样地开展以红外相机来监测野生动物多样性。随着我国野生动物红外相机监测网络的初步形成, 亟待建立和执行基于红外相机技术的统一监测规范。基于3年来在我国森林动态监测样地红外相机监测的进展情况, 以及热带生态评价与监测网络针对陆生脊椎动物(兽类和鸟类)所提出的红外相机监测规范, 本文从监测规范和监测注意事项等方面探讨了我国森林野生动物红外相机监测的现状和未来。     

相机陷阱在野生动物种群生态学中的应用

种群参数估计及空间分布格局是动物生态学和保护生物学领域的重要目标之一.最近十几年来, 相机陷阱(camera trap)作为野外调查的一种非损伤性技术手段,在传统调查方法难以实现的情况下表现出极大优势,被广泛应用于野生动物生态学和保护学研究中.相机陷阱所获取的动物出现数据为野生动物种群提供了极其重要的定量信息.本文从相机陷阱工作原理出发,主要阐述了目前在种群生态学中较为成熟的两类针对具有或不具有天然个体标志物种的模型原理及应用: 1)种群密度和种群数量估计; 2)空间占据率估计.论文特别关注了模型发展的逻辑过程、依赖的假定、使用范围、仍然存在的问题以及未来发展方向.最后, 本文综合分析了相机陷阱在种群参数估计应用中还需注意的问题, 以及其在种群动态和生物多样性研究等方面的发展潜力.     

Comparison of statistical population reconstruction using full and pooled adult age-class data

Background

Age-at-harvest data are among the most commonly collected, yet neglected, demographic data gathered by wildlife agencies. Statistical population construction techniques can use this information to estimate the abundance of wild populations over wide geographic areas and concurrently estimate recruitment, harvest, and natural survival rates. Although current reconstruction techniques use full age-class data (0.5, 1.5, 2.5, 3.5, … years), it is not always possible to determine an animal''s age due to inaccuracy of the methods, expense, and logistics of sample collection. The ability to inventory wild populations would be greatly expanded if pooled adult age-class data (e.g., 0.5, 1.5, 2.5+ years) could be successfully used in statistical population reconstruction.

Methodology/Principal Findings

We investigated the performance of statistical population reconstruction models developed to analyze full age-class and pooled adult age-class data. We performed Monte Carlo simulations using a stochastic version of a Leslie matrix model, which generated data over a wide range of abundance levels, harvest rates, and natural survival probabilities, representing medium-to-big game species. Results of full age-class and pooled adult age-class population reconstructions were compared for accuracy and precision. No discernible difference in accuracy was detected, but precision was slightly reduced when using the pooled adult age-class reconstruction. On average, the coefficient of variation increased by 0.059 when the adult age-class data were pooled prior to analyses. The analyses and maximum likelihood model for pooled adult age-class reconstruction are illustrated for a black-tailed deer (Odocoileus hemionus) population in Washington State.

Conclusions/Significance

Inventorying wild populations is one of the greatest challenges of wildlife agencies. These new statistical population reconstruction models should expand the demographic capabilities of wildlife agencies that have already collected pooled adult age-class data or are seeking a cost-effective method for monitoring the status and trends of our wild resources.     

Diet and Travel Costs for Spider Monkeys in a Nonseasonal, Hyperdiverse Environment

I studied the effects of a nonseasonal environment with a high diversity of plant species in a community of white-bellied spider monkeys (Ateles belzebuth belzebuth) in the Yasuní National Park, Ecuador. During 10 2-wk follows of focal individuals across 1 yr, I collected 1268 h of observation data on ranging and foraging. The environment had strong effects on both the foraging and ranging behavior of the monkeys. Yasuní spider monkeys are similar to spider monkeys in more seasonal environments in that ripe-fruit consumption dominates the diet. However, Yasuní spider monkeys exhibit an extremely diverse diet that parallels the variety of foods available to them, consuming more than 238 species of fruits. The impressive dietary variety increased even more with increased observation time, as I had not previously observed in the spider monkeys’ diet 40% of the fruit species the subjects consumed during the final follow. Ripe fruits remain the most important item in the diet year-round, supplemented with decayed wood or leaf flush. Local rarity of plant species means that fruiting patches are an average of 420 m apart, and mean patch residence times are short, only 8.1 min. Visits to an average of 11.5 feeding patches/d lead to a mean daily path length of 3311 m, longer than reported for any other Ateles species, and long compared to most other primate species. The long daily paths of Yasuní spider monkeys reflect travel costs resulting from foraging in a hyperdiverse nonseasonal environment.     

The influence of trap type on evaluating population structure of the semifossorial and social rodent <Emphasis Type="Italic">Octodon degus</Emphasis>

Trap type may influence captures of individuals in different age-sex categories in small mammal studies, resulting in biased population and demographic information. We deployed 4 live trap types at burrow systems of the rodent, Octodon degus Molina, 1782, in central Chile to determine trap efficacy in capturing individuals of 6 demographic categories. We captured 2672 individuals in 17 709 trap days (15.1% trapping success). Tomahawks were the most efficient trap capturing half of individuals during both years, followed by mesh Sherman traps, large Sherman traps, and medium Sherman traps in 2005. All trap types equally sampled sexes. Large and medium Sherman traps provided similar demographic structure, where half of the individuals captured were pups; Tomahawk traps sampled more adults than pups. Relative captures of pups were similar across different trap types, suggesting that pups are equally sampled by each of the deployed trap types. Relative captures of adults were lower in Sherman traps, suggesting that this age class avoided solid-walled traps. For Octodon degus, the sole use of Tomahawk traps may produce sufficient, unbiased demographic data. Only 4 trap mortalities occurred (0.15%). Researchers may minimize trap mortality without compromising sufficient demographic sampling by trapping during peak animal activity.