A Novel Use of Camera Traps to Study Demography and Life History in Wild Animals: A Case Study of Spider Monkeys (Ateles belzebuth)

Demographic and life history data from wild populations of long-lived primate species are difficult to acquire but are critical for evaluating population viability and the success of conservation efforts. Camera trapping provides an opportunity for researchers to monitor wild animal populations indirectly and could help provide demographic and life history data in a way that demands fewer person-hours in the field, is less disruptive to the study population because it requires less direct contact, and may be cost effective. Using data on group composition collected concurrently though both direct observation and camera trap monitoring, we evaluate whether camera traps can provide reliable information on population dynamics (births, disappearances, interbirth intervals, and other demographic variables) for a wild population of white-bellied spider monkeys (Ateles belzebuth), an Endangered species. We placed camera traps focused on the sole access point used by the monkeys to visit a geophagy site located roughly in the center of one group’s home range, and we reviewed all of the photos collected at that site over a roughly 3-yr period to identify the individual monkeys recorded in the pictures. Group composition based on 2947 photos containing 3977 individual monkey images matched perfectly data collected concurrently through direct observation. The camera traps also provided estimates of the dates when individuals disappeared from the study group, and of infant births during the study. We conclude that long-term camera trap monitoring of wild populations of white-bellied spider monkeys—and other animals that are individually recognizable and that regularly visit predictable resources—can be a useful tool for monitoring their population dynamics indirectly.     

基于标记-重捕模型开展野生动物红外相机种群监测的方法及案例

红外相机技术的广泛应用推动了动物种群生态学研究方法的发展和革新, 特别是基于标记-重捕模型框架通过非损伤取样方式对物种数量和密度等种群参数的可靠估计, 为保护濒危物种和评估保护成效提供了有力的科学依据。对于身体上具有独特天然标记的动物(如多数猫科动物), 可依据红外相机拍摄身体上的独特斑点或条纹鉴别个体, 再运用标记-重捕模型, 估计动物种群数量、密度等参数。本文概述了标记-重捕模型的基本原理、特点以及国内外的应用, 特别是近年来发展出的空间标记-重捕模型。总结了从相机布设到数据分析的具体流程、操作原则, 并以青城山家猫为实例, 展示了应用红外相机数据通过空间标记-重捕模型估计种群密度和数量的基本步骤。最后展望了该模型在种群动态、景观廊道设计、资源选择等方面的应用和发展趋势。     

Take Only Photographs,Leave Only Footprints: Novel Applications of Non-Invasive Survey Methods for Rapid Detection of Small,Arboreal Animals

The development of appropriate wildlife survey techniques is essential to promote effective and efficient monitoring of species of conservation concern. Here, we demonstrate the utility of two rapid-assessment, non-invasive methods to detect the presence of elusive, small, arboreal animals. We use the hazel dormouse, Muscardinus avellanarius, a rodent of conservation concern, as our focal species. Prevailing hazel dormouse survey methods are prolonged (often taking months to years to detect dormice), dependent on season and habitat, and/or have low detection rates. Alternatives would be of great use to ecologists who undertake dormouse surveys, especially those assessing the need for mitigation measures, as legally required for building development projects. Camera traps and footprint tracking are well-established tools for monitoring elusive large terrestrial mammals, but are rarely used for small species such as rodents, or in arboreal habitats. In trials of these adapted methods, hazel dormice visited bait stations and were successfully detected by both camera traps and tracking equipment at each of two woodland study sites, within days to weeks of installation. Camera trap images and footprints were of adequate quality to allow discrimination between two sympatric small mammal species (hazel dormouse and wood mouse, Apodemus sylvaticus). We discuss the relative merits of these methods with respect to research aims, funds, time available and habitat.     

Camera Traps Can Be Heard and Seen by Animals

Camera traps are electrical instruments that emit sounds and light. In recent decades they have become a tool of choice in wildlife research and monitoring. The variability between camera trap models and the methods used are considerable, and little is known about how animals respond to camera trap emissions. It has been reported that some animals show a response to camera traps, and in research this is often undesirable so it is important to understand why the animals are disturbed. We conducted laboratory based investigations to test the audio and infrared optical outputs of 12 camera trap models. Camera traps were measured for audio outputs in an anechoic chamber; we also measured ultrasonic (n = 5) and infrared illumination outputs (n = 7) of a subset of the camera trap models. We then compared the perceptive hearing range (n = 21) and assessed the vision ranges (n = 3) of mammals species (where data existed) to determine if animals can see and hear camera traps. We report that camera traps produce sounds that are well within the perceptive range of most mammals’ hearing and produce illumination that can be seen by many species.     

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。     

Changing use of camera traps in mammalian field research: habitats,taxa and study types

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Determining the efficacy of camera traps,live capture traps,and detection dogs for locating cryptic small mammal species

Metal box (e.g., Elliott, Sherman) traps and remote cameras are two of the most commonly employed methods presently used to survey terrestrial mammals. However, their relative efficacy at accurately detecting cryptic small mammals has not been adequately assessed. The present study therefore compared the effectiveness of metal box (Elliott) traps and vertically oriented, close range, white flash camera traps in detecting small mammals occurring in the Scenic Rim of eastern Australia. We also conducted a preliminary survey to determine effectiveness of a conservation detection dog (CDD) for identifying presence of a threatened carnivorous marsupial, Antechinus arktos, in present‐day and historical locations, using camera traps to corroborate detections. 200 Elliott traps and 20 white flash camera traps were set for four deployments per method, across a site where the target small mammals, including A. arktos, are known to occur. Camera traps produced higher detection probabilities than Elliott traps for all four species. Thus, vertically mounted white flash cameras were preferable for detecting the presence of cryptic small mammals in our survey. The CDD, which had been trained to detect A. arktos scat, indicated in total 31 times when deployed in the field survey area, with subsequent camera trap deployments specifically corroborating A. arktos presence at 100% (3) indication locations. Importantly, the dog indicated twice within Border Ranges National Park, where historical (1980s–1990s) specimen‐based records indicate the species was present, but extensive Elliott and camera trapping over the last 5–10 years have resulted in zero A. arktos captures. Camera traps subsequently corroborated A. arktos presence at these sites. This demonstrates that detection dogs can be a highly effective means of locating threatened, cryptic species, especially when traditional methods are unable to detect low‐density mammal populations.     

Comparing the Use of Camera Traps and Farmer Reports to Study Crop Feeding Behavior of Moor Macaques (<Emphasis Type="Italic">Macaca maura</Emphasis>)

Investigating crop feeding patterns by primates is an increasingly important objective for primatologists and conservation practitioners alike. Although camera trap technology is used to study primates and other wildlife in numerous ways, i.e., activity patterns, social structure, species richness, abundance, density, diet, and demography, it is comparatively underused in the study of human–primate interactions. We compare photographic (N?=?210) and video (N?=?141) data of crop feeding moor macaques (Macaca maura) from remote sensor cameras, functioning for 231 trap days, with ethnographic data generated from semistructured interviews with local farmers. Our results indicate that camera traps can provide data on the following aspects of crop feeding behavior: species, crop type and phase targeted, harvesting technique used, and daily and seasonal patterns of crop feeding activity. We found camera traps less useful, however, in providing information on the individual identification and age/sex class of crop feeders, exact group size, and amount of crops consumed by the moor macaques. While farmer reports match camera trap data regarding crop feeding species and how wildlife access the gardens, they differ when addressing crop feeding event frequency and timing. Understanding the mismatches between camera trap data and farmer reports is valuable to conservation efforts that aim to mitigate the conflict between crop feeding wildlife and human livelihoods. For example, such information can influence changes in the way certain methods are used to deter crop feeding animals from damaging crops. Ultimately, we recommend using remote-sensing camera technology in conjunction with other methods to study crop feeding behavior.     

Software for minimalistic data management in large camera trap studies

The use of camera traps is now widespread and their importance in wildlife studies is well understood. Camera trap studies can produce millions of photographs and there is a need for a software to help manage photographs efficiently. In this paper, we describe a software system that was built to successfully manage a large behavioral camera trap study that produced more than a million photographs. We describe the software architecture and the design decisions that shaped the evolution of the program over the study's three year period. The software system has the ability to automatically extract metadata from images, and add customized metadata to the images in a standardized format. The software system can be installed as a standalone application on popular operating systems. It is minimalistic, scalable and extendable so that it can be used by small teams or individual researchers for a broad variety of camera trap studies.     

An approach to rapid processing of camera trap images with minimal human input

1. Camera traps have become an extensively utilized tool in ecological research, but the manual processing of images created by a network of camera traps rapidly becomes an overwhelming task, even for small camera trap studies.
2. We used transfer learning to create convolutional neural network (CNN) models for identification and classification. By utilizing a small dataset with an average of 275 labeled images per species class, the model was able to distinguish between species and remove false triggers.
3. We trained the model to detect 17 object classes with individual species identification, reaching an accuracy up to 92% and an average F1 score of 85%. Previous studies have suggested the need for thousands of images of each object class to reach results comparable to those achieved by human observers; however, we show that such accuracy can be achieved with fewer images.
4. With transfer learning and an ongoing camera trap study, a deep learning model can be successfully created by a small camera trap study. A generalizable model produced from an unbalanced class set can be utilized to extract trap events that can later be confirmed by human processors.

     

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。     

Protein variations and primatology

We summarize work based on electrophoretic screening for protein variation within and between primate species. We consider serum proteins—albumins, haptoglobins, transferrins—and red cell proteins—carbonic anhydrases, hemoglobins. Using hemoglobin, cytochrome-c, and fibrinopeptides as examples, we discuss the value of using molecular data, i.e. protein structures, in evolutionary studies and in primatology.     

Toward reliable population density estimates of partially marked populations using spatially explicit mark–resight methods

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Recommended guiding principles for reporting on camera trapping research

Camera traps are used by scientists and natural resource managers to acquire ecological data, and the rapidly increasing camera trapping literature highlights how popular this technique has become. Nevertheless, the methodological information reported in camera trap publications can vary widely, making replication of the study difficult. Here we propose a series of guiding principles for reporting methods and results obtained using camera traps. Attributes of camera trapping we cover include: (i) specifying the model(s) of camera traps(s) used, (ii) mode of deployment, (iii) camera settings, and (iv) study design. In addition to suggestions regarding best practice data coding and analysis, we present minimum principles for standardizing information that we believe should be reported in all peer-reviewed papers. Standardised reporting enables more robust comparisons among studies, facilitates national and global reviews, enables greater ease of study replication, and leads to improved wildlife research and management outcomes.     

Estimation of population density of European pine marten in central Italy using camera trapping

Evaluating presence and abundance of small carnivores is essential for their conservation. In Italy, there is scarce information on European pine marten distribution, and no data are published on its abundance. Camera traps have been widely used to estimate population density applying capture–recapture models for species in which individual recognition is possible. Here we estimate the abundance of European pine martens in central Italy using camera trapping and a model that allows the estimation of population density without the need for individual recognition Rowcliffe et al. (Anim Conserv 11:185–186, 2008). Camera trapping was also used to evaluate habitat use patterns by martens. Fifteen camera traps were deployed in 90 placements for 15 days each, for a total of 1,334 camera days. Pine martens were captured in 24% of camera trap placements with a mean trap success rate of 0.33 photographs per camera placement. Estimated pine marten population density in the study area was 0.34 individuals km⁻². Marten trap rate was not strongly associated with any habitat type, although there were trends towards lower probability of records at locations with high coverage of cultivated fields and higher probability of records at locations with high coverage of human-made woodland. The results suggest that pine martens in this area are not confined to wooded habitat. To our knowledge, this study is the first application of the Rowcliffe et al. (Anim Conserv 11:185–186, 2008) method to a wild carnivore population and, furthermore, the first estimation of population density of pine martens in Italy.     

Accuracy of identifications of mammal species from camera trap images: A northern Australian case study

Camera traps are a powerful and increasingly popular tool for mammal research, but like all survey methods, they have limitations. Identifying animal species from images is a critical component of camera trap studies, yet while researchers recognize constraints with experimental design or camera technology, image misidentification is still not well understood. We evaluated the effects of a species’ attributes (body mass and distinctiveness) and individual observer variables (experience and confidence) on the accuracy of mammal identifications from camera trap images. We conducted an Internet‐based survey containing 20 questions about observer experience and 60 camera trap images to identify. Images were sourced from surveys in northern Australia and included 25 species, ranging in body mass from the delicate mouse (Pseudomys delicatulus, 10 g) to the agile wallaby (Macropus agilis, >10 kg). There was a weak relationship between the accuracy of mammal identifications and observer experience. However, accuracy was highest (100%) for distinctive species (e.g. Short‐beaked echidna [Tachyglossus aculeatus]) and lowest (36%) for superficially non‐distinctive mammals (e.g. rodents like the Pale field‐rat [Rattus tunneyi]). There was a positive relationship between the accuracy of identifications and body mass. Participant confidence was highest for large and distinctive mammals, but was not related to participant experience level. Identifications made with greater confidence were more likely to be accurate. Unreliability in identifications of mammal species is a significant limitation to camera trap studies, particularly where small mammals are the focus, or where similar‐looking species co‐occur. Integration of camera traps with conventional survey techniques (e.g. live‐trapping), use of a reference library or computer‐automated programs are likely to aid positive identifications, while employing a confidence rating system and/or multiple observers may lead to a collection of more robust data. Although our study focussed on Australian species, our findings apply to camera trap studies globally.     

Giving the Forest Eyes: The Benefits of Using Camera Traps to Study Unhabituated Chimpanzees (Pan troglodytes verus) in Southeastern Senegal

Habituation has been the standard methodology used to study the natural history of great apes and other primates. Habituation has invaluable strengths, particularly in quantity and diversity of data collected, but along with these come substantial weaknesses, i.e., costs both in time and effort, health risks, and potential exposure of subjects to poaching. With new technologies, we are able to extend our studies beyond the limitations of habituation; camera traps are one technology that can be used to study unhabituated primate groups. In this study we used eight camera traps over the course of 2 yr (1542 camera trap days) to capture thousands of still images of West African savanna chimpanzees (Pan troglodytes verus) in the Falémé region of southeastern Senegal. Images corroborated behavioral observations from habituated chimpanzees at the Fongoli site, where researchers have observed nocturnal activity and cave use. The cameras also captured interspecies interactions at water sources during the dry season and allowed us to determine demographic composition and minimum community size. The photographs provide data on local fauna, including predators (Panthera pardus pardus, Panthera leo senegalesis, and Crocuta crocuta), potential prey, and competitor species (Papio papio, Cercopithecus aethiops, and Erythrocebus patas). As primate habitat across Africa is further threatened and human–wildlife conflict increases, camera trapping could be used as an essential conservation tool, expanding studies of primates without exacerbating potential threats to the species.     

Divergent effects of lure on multi-species camera-trap detections and quality of photos

The use of attractants to increase detection of target species, such as carnivores, in camera trap studies must be tested for its effectiveness and be carefully planned, as it can lead to misleading comparisons among species. We analyzed a five-year multi-species camera trap dataset of lured and control stations in a protected area in the Amazon rainforest. We aimed to identify the lure effect on a wider range of species and assess whether its use is an efficient strategy to increase the number and the quality of carnivore records. From the 14 vertebrate species analyzed, we found that the use of lures had a negligible effect on nine species, and did not improve the number of records or the detection probability of the carnivores. On the other hand, lured stations attracted omnivores and scavengers (common opossum, black-and-white tegu, and turkey vulture) while had the opposite effect on potential prey species (Black-capped capuchin and Northern Amazon squirrel). We detected a stronger effect of the lure when considering the number of records (relative abundance models) than the probability of detection (occupancy models). The lure increased the proportion of high-quality photos, suitable for individual recognition of jaguars, but only for the first weeks, when the lure was fresh. Therefore, we suggest that the sardine and egg-based lures should be refreshed every-two weeks to ensure greater effectiveness in the quality of photos for jaguar individualization. However, it is important to consider that lure renewing will imply a significant increase in field-related costs and it’s likely to bias other species studies. Thus, we advise that lures should only be used if researchers are certain that the focus is only to increase carnivore data at the expense of using non-target species. Camera traps survey design must be carefully planned a priori and the cost-benefit of lure use and refreshment should be weighed in the study context.     

Studying Large Mammals With Imperfect Detection: Status and Habitat Preferences of Wild Cattle and Large Carnivores in Eastern Cambodia

Studying large mammal species in tropical forests is a conservation challenge with species’ behavior and ecology often increasing the probability of non‐detection during surveys. Consequently, knowledge of the distribution, status, and natural history of many large mammal species in Southeast Asia is limited. I developed occupancy models from camera‐trapping data, thereby accounting for imperfect detection at sampling sites, to clarify the status and habitat requirements of four globally threatened or near threatened large mammals (banteng Bos javanicus, gaur Bos gaurus, dhole Cuon alpinus, and leopard Panthera pardus) in Mondulkiri Protected Forest, eastern Cambodia. Camera traps were operational for >3500 trap nights with 202 photographic encounters of the four study species. Model averaged occupancy estimates were between 5 percent (leopard) and 140 percent (gaur) higher than naive estimates (i.e., proportion of camera‐trap sites species recorded from) thus highlighting the importance of accounting for detectability during conservation surveys. I recommend the use of an occupancy framework when using camera‐trap data to study the status, ecology, and habitat preferences of poorly known and elusive species. The results highlight the importance of mixed deciduous and semi‐evergreen forest for wild cattle in eastern Cambodia and I emphasize that these habitats must be considered in conservation planning across the Lower Mekong Dry Forest Ecoregion.     

Evolutionary and ecological traps for brown bears Ursus arctos in human‐modified landscapes

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