Prof Dr Anna Nekaris is a Professor in Anthropology and Primate Conservation and is the University Lead for Public Engagement of Research. She is the Subject Lead for the highly acclaimed MSc Primate Conservation and MRes Primatology and Conservation. She is Director of the Development Office's Slow Loris Fund, through which she directs the Little Fireface Project. She is also Convenor of the Nocturnal Primate Research Group and member of the Ecology and Evolution Research Group and the Centre for Functional Genomics.
I have supervised approximately 30 PhD students to completion. I regularly am the Director of Studies of 2 postdocs, 5 PhD students and 4 MSc students.I am currently Director of Studies for the following:
Grace Foreman: Impact of social media on animal conservation
Leah Fitz: Assembling the genome of the only venomous primate – the slow loris
Angelina Wilson: Using a conservation education approach to mitigate online wildlife trade amongst UK teenagers
Primate Factoids: Efficacy of visual literature in teaching young children about ecology and conservation
Dr Penthai Siriwat
‘Wildlife Trade in the Digital Age: The role of the Internet in monitoring the trade in wild plants and animals in Thailand
Dr Miguel de Guinea Luengo
Navigating in Rainforests: Movement patterns in a neotropical primate the Black Howler Monkey.
Dr Kathleen Reinhardt
Ecophysiology of a wild nocturnal primate the Javan Slow Loris (Nycticebus Javanicus)
Dr Jaima Smith
An examination and assessment of current conservation practices for Javan gibbons (Hylobates moloch) in West Java, Indonesia
Dr Michela Balestri
Ecology and conservation of the southern woolly lemur (Avahi meridionalis) in the Tsitongambarika Protected Area, south-eastern Madagascar
Dr Stephanie Poindexter
Navigating the Night: Spatial Cognition. Locomotor and ranging behaviour in Nycticebus species
Dr Camille Coudrat
Ecology and conservation of docu monkeys (Pygathrix spp.) in Cambodia, Laos and Vietnam: a comparative study
Working in the wild, zoos, museums, rescue centres and in the lab, Anna's main focus is on the conservation of Asian nocturnal animals, especially slow and slender lorises. Her primate conservation work extends to African nocturnal primates, lemurs, colobines, and macaques.
Research topics include:
ecology and evolutionary adaptations related to mammalian venom
behavioural ecology using radio tracking and biologgers
behavioural adaptations to climate change
conservation value of agroforestry systems
socioecological impacts of Wildlife Friendly farming
With nearly 30 years of research in 11 range countries, Anna is known as a leading expert in Asia's slow and slender lorises. Of her more than 70 postgraduate students, over 50 of Anna’s MSc, MRes, MPhil and PhD students, including from range countries, have completed research on lorises. Anna also regularly welcomes postdoctoral researchers into her lab.
Anna has a world-wide association with rescue centres, field stations, and zoos with need of advice regarding taxonomic identification, captive care, and ecological advice regarding Asian lorises and African pottos. Anna’s advice has also been sought when illegal social media videos of pet slow lorises, which violate international legislation, became viral reaching millions of hits, leading to warning captions of such material on Facebook and Instagram. She led campaigns leading to some of these videos being removed.
Anna was the lead scientist involved in the transfer of all slow lorises to CITES Appendix 1 (Convention on International Trade in Endangered Species). She also worked with the Japanese Government via the Japan Wildlife Conservation Society to change legislation so that CITES I listed species' import documentation must be linked to a microchip.
Anna works with zoos and rescue centres worldwide improving captive diets, especially providing irrefutable scientific evidence that slow lorises are gum-feeding specialists and slender lorises are specialist insectivores. These findings have led to dramatic changes in captive management and wefare.
Anna appears regulalry in documentaries that increase awareness of the plight of lorises and other species, including UK BBC's The Natural World and Life of Mammals, USA Animal Planet's Frontier Earth, Japan NHK's Here comes Darwin, Singapore MediaCorp's Beyond the Viral Video and Korea EPS's Our Seoul Earth. She also regularly appears in documentaries providing a scientific perspective to the field of cryptozoology.
Projects as Principal Investigator, or Lead Academic if project is led by another Institution
Factors affecting childhood exposures to urban particulates (led by University of Durham) (30/04/2020 - 29/04/2023), funded by: UK Research and Innovation (UKRI), funding amount received by Brookes: £0
As road infrastructure networks rapidly expand globally, especially in the tropics, previously continuous habitats are being fragmented, resulting in more frequent wildlife–vehicle collisions (WVC). Primates are widespread throughout many sub-/tropical countries, and as their habitats are fragmented, they are increasingly at risk of WVC. We created the Global Primate Roadkill Database (GPRD), the largest available standardized database of primate roadkill incidents. We obtained data from published papers, un-published and citizen science databases, anecdotal reports, news reports, and social media posts. Here, we describe the collection methods for the GPRD and present the most up-to-date version of the database in full. For each primate roadkill incident, we recorded the species killed, the exact location, and the year and month the roadkill was observed. At the time of publication, the GPRD includes 2862 individual primate roadkill records from 41 countries. As primates range in more than twice as many countries, the absence of data from these countries is not necessarily indicative of a lack of primate vehicular collisions. Given the value of these data for addressing both local and global research questions, we encourage conservationists and citizen scientists to contribute to the GPRD so that, together, we can better understand the impact road infrastructure has on primates and evaluate measures which may help mitigate risk-prone areas or species.
The worldwide pandemic caused by SARS-CoV-2 challenged conservation organizations. The lack of tourism has benefited or negatively affected wildlife organizations in various ways, with several primate sanctuaries struggling to cope with the COVID-19 crisis and to keep providing for their inhabitants. In addition, the genetic similarity between great apes and humans puts them at higher risk than any other species for the transmission of COVID-19. PASA is a non-profit organization comprising 23 sanctuaries, and cares for many species of primate, including African great apes. In light of the pandemic, we aimed to understand the direct effects of COVID-19 on PASA management throughout three time periods: before (2018–2019), at the start of (2019–2020), and during (2020–2021) the pandemic. We collected data via annual surveys for PASA members and ran Generalized Linear Mixed Models to highlight any significant differences in their management that could be linked to COVID-19. Our findings demonstrated no particular impact on the number of primates rescued, employees, or expenses. However, revenues have been decreasing post-COVID-19 due to the lack of income from tourism and volunteer programs. Nonetheless, our results reveal a form of resilience regarding the sanctuaries and the strategy applied to maintain their management. Consequently, we emphasize the specific impacts of the COVID-19 outbreak and its repercussions for conservation work. We discuss the difficulties that sanctuaries have faced throughout the crisis and present the best measures to prevent future outbreaks and protect biodiversity.
Quarles LF, Feddema K, Campera M, Nekaris KAI, 'Normal redefined: Exploring decontextualization of lorises (Nycticebus & Xanthonycticebus spp.) on social media platforms' Frontiers in Conservation Science 4 (2023)
Introduction: Decontextualization is a concept from psychology whereby new words are learned outside of the context of the here-and-now. Decontextualized language is used for discussing abstract concepts and is crucial to the development of academic language. When it comes to images, a dearth of context can lead to a lack of clarity, such as the use of ambiguous decontextualized images in environmental communication, leading to the promotion of greenwashing. Here we refer to decontextualization as the removal of wildlife from their wild ecological context. Images and videos of globally threatened species are increasingly popular on social media. Showing such taxa alongside humans may impact public perceptions of their abundance and need for conservation and can increase illegal trade. One group of animals that are particularly popular on social media platforms are the slow and pygmy lorises (Nycticebus spp., Xanthonycticebus spp.).
Methods: Here, we examined 100 videos from three popular social media platforms (YouTube, TikTok, and Giphy) to calculate how often and in which ways these videos remove slow lorises from their natural ecological and behavioural context. We also examined views and likes to determine viewer engagement trends. We used relevant content from each site to assess the presence of decontextualization using five conditions.
Results: In all but two videos, conditions of decontextualization were present and 77% of all videos had four to five conditions of decontextualization. Using Spearman correlation, we found a significant effect of decontextualization scores on the number of views and likes for YouTube and TikTok videos. Views were significantly higher when videos presented animals in anthropogenic settings (i.e., in human-made structures or in proximity of human artefacts). Additionally, views on TikTok and YouTube were significantly higher when animals displayed signs of stress or ill health and when they were in unnatural conditions.
Discussion: Our case study of lorises provides an example of the danger of decontextualizing wild animals on social media. Public preference for imagery where animals are neglected is indicative that better guidelines need to be put in place and policed by social media platforms. Additionally, conservationists need to develop strategies to promote wild imagery and further explore decontextualization if we are to understand and address the drivers of the rampant illegal wildlife trade online.
Al-Razi H, Campera M, Hasan S, Marjan M, Nijman V, Nekaris KA-I., 'Influence of Agricultural Expansion and Human Disturbance on the Encounter Rates of Nocturnal Mammals in Tropical Hill Forests in Bangladesh' Ecologies 4 (1) (2023) pp.195-208
Agricultural expansion has had a detrimental effect on tropical forests and the animal communities that depend on them. Agroforestry systems, however, with their more complex tree and plant communities, have been shown to be important habitats for a range of globally threatened species, including nocturnal animals. Here, we present novel data on the encounter rates of seven species of nocturnal mammals in relation to agroforestry systems within four national parks and associated plantations in Bangladesh to examine if encounter rates were influenced by the human population density, presence of plantations, and human access as represented by a Human Influence Index of anthropogenic disturbance. We walked 70.3 km of transects with only semi-natural forest, 26.9 km of transects with semi-natural forest and gardens, and 21.7 km of transects with semi-natural forest and monocultures over 55 nights from 2017–2019. Of the seven species of nocturnal mammals we detected, all were present in Satachari National Park, whereas six occurred in Lawachara National Park, Rajkandi Forest Range, and Rema-Kalenga Wildlife Sanctuary. Within these national parks, three species (Bengal slow loris, large Indian civet, particolored flying squirrel) were more frequently recorded in areas with human disturbance, especially agroforestry plantations. With declining forest cover in Bangladesh, we highlight here the potential of agroforestry systems as emerging important habitats for these species. We encourage long-term studies of these lesser-studied taxa to understand fully the capacity of agroforestry systems in order to support their long-term conservation.
Nijman V, Nekaris KAI, Shepherd CR, Vigne L, Ardiansyah A, Imron MA, Ni Q, Hedger K, Campera M, Morcatty TQ, 'Potential Mammalian Vector-Borne Diseases in Live and Wet Markets in Indonesia and Myanmar' Microbiology Research 14 (1) (2023) pp.116-131
Vector-borne diseases spread from wild animals and their associated ectoparasites to humans and domesticated animals. Wildlife markets are recognized as important areas where this transfer can take place. We assessed the potential for spreading vector-borne diseases in two live and wet markets in Myanmar (Mong La, on the Myanmar-China border) and Indonesia (Sukahaji in Bandung on the island of Java) by making an inventory of all live and freshly killed wild mammals for sale. For eight mammal families, we quantified the number of animals on offer, and we used a heatmap cluster analysis to map vector-borne diseases that these families may carry. In Myanmar, we observed large numbers of wild pigs and deer (potentially carrying West Nile and various encephalitis viruses) whereas in Indonesia we observed Old World fruit bats (potentially carrying Chikungunya and encephalitis viruses) and squirrels (potentially carrying West Nile and encephalitis viruses). The trade in Indonesia was dominated by live mammals offered for sale as pets, and only Old World fruit bats and squirrels traded for traditional Asian medicine were killed in the markets. The trade in Myanmar was more geared towards wild meat (e.g., wild pigs, deer, primates) and traditional Asian medicine (squirrels). The combined risks of vector-borne diseases spreading from traded animals to human health highlight the need for an integrated approach protecting public health, economic interests and biodiversity.
Campera M, Balestri M, Phelps M, Besnard F, Mauguiere J, Rakotoarimanana F, Nijman V, Nekaris KAI, Donati G, 'Depth of Edge Influence in a Madagascar Lowland Rainforest and Its Effects on Lemurs’ Abundance' Land 12 (1) (2022)
Edge effects result from interactions between adjacent habitats, which can modify abiotic and biotic conditions and produce various negative effects on biodiversity. Given the high degree of forest fragmentation in Madagascar, understanding lemur responses to edges is a conservation priority. We aim to determine the depth of edge influence in a continuous low-land rainforest of south-eastern Madagascar and identify the response of six lemur species. We surveyed lemur abundance along nine 1 km transects from May 2015 to July 2016 totaling 112.2 km of survey effort during the day and 88.5 km at night. We characterized the habitat structure via 33 plots centered along the line transects. We used Generalized Additive Models and Generalized Linear Models to test the effect of distance from the forest edge on vegetation parameters and animal encounter rates. Edge effect on the vegetation structure can be detected up to around 100 m in terms of tree diversity and density. We found a negative edge response for Madame Fleurette’s sportive lemurs (Lepilemur fleuretae) and collared brown lemurs (Eulemur collaris), and a positive edge response for Anosy mouse lemurs (Microcebus tanosi), Southern bamboo lemurs (Hapalemur meridionalis) and Southern woolly lemurs (Avahi meridionalis). Since around half of the forested areas in Madagascar are within 100 m of forest edge, taking into account edge effect is vital when producing estimates of population sizes and informing conservation management.
Morcatty TQ, Pereyra PER, Ardiansyah A, Imron MA, Hedger K, Campera M, Nekaris KA-I, Nijman V, 'Risk of Viral Infectious Diseases from Live Bats, Primates, Rodents and Carnivores for Sale in Indonesian Wildlife Markets' Viruses 14 (12) (2022)
Southeast Asia is considered a global hotspot of emerging zoonotic diseases. There, wildlife is commonly traded under poor sanitary conditions in open markets; these markets have been considered ‘the perfect storm’ for zoonotic disease transmission. We assessed the potential of wildlife trade in spreading viral diseases by quantifying the number of wild animals of four mammalian orders (Rodentia, Chiroptera, Carnivora and Primates) on sale in 14 Indonesian wildlife markets and identifying zoonotic viruses potentially hosted by these animals. We constructed a network analysis to visualize the animals that are traded alongside each other that may carry similar viruses. We recorded 6725 wild animals of at least 15 species on sale. Cities and markets with larger human population and number of stalls, respectively, offered more individuals for sale. Eight out of 15 animal taxa recorded are hosts of 17 zoonotic virus species, nine of which can infect more than one species as a host. The network analysis showed that long-tailed macaque has the greatest potential for spreading viral diseases, since it is simultaneously the most traded species, sold in 13/14 markets, and a potential host for nine viruses. It is traded alongside pig-tailed macaques in three markets, with which it shares six viruses in common (Cowpox, Dengue, Hepatitis E, Herpes B, Simian foamy, and Simian retrovirus type D). Short-nosed fruit bats and large flying foxes are potential hosts of Nipah virus and are also sold in large quantities in 10/14 markets. This study highlights the need for better surveillance and sanitary conditions to avoid the negative health impacts of unregulated wildlife markets.
Nekaris KAI, Balestri M, El Bizri HR, Dewi T, Hedger K, Morcatty TQ, Nijman V, Weldon AV, Campera M, 'From International to Local: Promoting Local Volunteer Tourism to Guarantee the Persistence of Wildlife Conservation Projects in the Post-COVID-19 Era' COVID 2 (9) (2022) pp.1287-1302
Volunteer tourists, often foreigners, collect essential data in wildlife conservation projects worldwide. Due to the COVID-19 pandemic, international tourism activities reduced drastically, forcing many conservation projects to shut down. Using a nine-year (2013–2021) case study in Indonesia, we examine how local and foreign tourists construct the meaning of their volunteer experiences in the light of COVID-19. We aim to highlight the potential benefits of local volunteer tourism to face the travel limitations posed by COVID-19, and to show an example of how conservation projects can overcome the challenges of the current and potential future pandemics. We recruited 117 volunteers (49 Indonesians, 68 foreign; 73 females, 44 males; mean age: 24.2 ± SD 4.7) that collected 50.8% of the total amount of data collected by the project over the same period. Of the 117 volunteers, 81 of them (38 Indonesians, 43 foreigners) filled in a feedback form at the end of their stay. Via logistic regressions, we found that Indonesian volunteers declared more positive feedback on the logistics at the research station (p = 0.047). Via Bayesian structural equation models, we found that Indonesian volunteers reported significantly more frequently than foreign volunteers that they learned new skills (89% Credible Interval = 0.017–0.351) and that they gained personal wisdom, growth and maturity (89% Credible Interval = 0.891–1.003) from the volunteer experience. The volunteer program evolved from being 100% foreign volunteers in 2013 to 100% Indonesian volunteers by 2020 at the peak of the pandemic, which helped maintain the continuity of the research and conservation activities. We presented the positive implications of shifting towards local volunteer tourists in a long-term conservation project. We suggest that promoting local volunteer tourism through training new generations of nationals in conservation projects is key to guarantee the persistence of such initiatives in the post-COVID-19 Era.
Fourage A, Shepherd C, Campera M, Nekaris KAI, Nijman V, 'It's a sign: Animal welfare and zoo type are predictors of animal identification signage usage and quality at zoo exhibits' Zoo Biology 42 (2) (2022) pp.283-295
Conservation education programs are listed as priority actions for almost every threatened species on the International Union for Conservation of Nature Red List. Zoos play an important role in delivering such programs, yet evidence of zoo education in many non-western countries is limited. Here, we evaluate animal identification signage prevalence and quality at zoo exhibits and investigate whether animal welfare, zoo type (accredited, government, and private), admission fee, zoo size, and proximity to urban centers are influencing factors. We used hornbills (Bucerotidae) as a model taxon, surveyed hornbill signage, and conducted welfare assessments of hornbill exhibits. We developed scoring frameworks and applied content analysis to analyze signage quality. Our results show that out of 18 zoos that displayed hornbills, 15 had hornbill signage. However, of the 106 hornbill exhibits in these zoos, 33% had no signage. We also found that signage presence or absence at individual zoos and signage quality is strongly correlated with animal welfare quality. Zoo type is a key factor in predicting signage and welfare quality, with accredited zoos scoring highest for both signage and welfare, followed by government and private zoos. Private zoos charged higher admission than other zoo types, and zoo size and proximity to urban centers did not influence signage or welfare scores. Overall, we conclude that in our study, signage usage and quality are inadequate, highlighting the importance of compliance with robust zoo standards to improve education and welfare within zoos to support global conservation goals.
Manson S, Campera M, Hedger K, Ahmad N, Adinda E, Nijman V, Budiadi B, Imron MA, Lukmandaru G, Nekaris KAI, 'The effectiveness of a biopesticide in the reduction of coffee berry borers in coffee plants' Crop Protection 161 (2022)
Crop pest outbreaks are expected to become more frequent and unpredictable due to climate change, posing risks to ecosystem health and farmers’ livelihoods. At the same time, there is growing evidence that chemical pesticides can persist in the landscape and contribute to land degradation. The use of natural pesticides in place of chemical pesticides is hoped to manage pest outbreaks while also restoring pollinator populations and improving the quality of arable land. During the 1970s, many countries committed to promoting and legislating Integrated Pest Management (IPM) strategies (encouraging natural and holistic approaches to pest management), often including using natural pesticides, known as biopesticides.
We assessed the effectiveness of a biopesticide on coffee berry borer (CBB; Hypothenemus hampei) presence in 57 small-holder coffee home gardens in West Java, Indonesia across three years.
Prior to the application of the biopesticide, we randomly chose ten coffee plants from each field and recorded the proportion of healthy berries per plant (berries without pest infestation) as a control. In April 2020, we distributed the biopesticide in each of the 57 coffee home gardens and repeated the above experiment. The biopesticide was redistributed in October 2020 and April 2021. We repeated the experiment for the last time in April 2021.
Results and conclusions
We found that CBB presence significantly decreased, with an inverse relationship between distance to natural forest and CBB presence and a positive relationship between shade cover and CBB presence. We also interviewed farmers in April 2021 to investigate their perception of the effectiveness of the biopesticide and 87% of farmers thought it was more effective than conventional pesticides.
We contribute to the growing literature on the effectiveness of natural pesticides through assessing farmers’ perceptions of these methods and providing empirical evidence for their effectiveness in remedying CBB infestation. We hope that this study will empower farmers to make conscious land-use choices and provide government authorities with evidence to support increased accessibility to biopesticides.
Campera M, Balestri M, Stewart AN, Nekaris KAI, 'Influence of Moon Luminosity, Seasonality, Sex and Weather Conditions on the Activity Levels of the Nocturnal Javan Slow Loris' Ecologies 3 (3) (2022) pp.257-266
The activity patterns of mammals depend on environmental changes (e.g., moon luminosity, food availability, weather) and endogenous rhythms. Behavioral observations are traditionally used to estimate the activity patterns of animals, but low visibility and the cryptic nature of some species entail that, in certain conditions, the animal is visible only for around 60% of the time. Recent advances in technology allow automatic data collection on the activity levels of animals. We used five years of data collected via accelerometers to understand how moon luminosity, seasonality, sex, and weather conditions influence the activity levels of the nocturnal and cryptic Javan slow loris. We collected 9589 h on six females and 7354 h on six males. Via Generalized Additive Mixed Models, we found that lorises are lunarphobic; they reduce activity levels during cold nights, they have higher activity levels when the relative humidity is close to 100%, and they have high peaks of activity between December and February and between June and August. The activity levels are thus influenced by avoidance of predators, food availability, consumption of insects and nectar, physiological, and behavioral adaptations to cold temperatures and energy requirements during reproductive stages. We highlight the importance of using bio-loggers for cryptic animals as with behavioral observations only, and the observer might underestimate active behaviors and overestimate inactivity.
For over 100 years, non-human primates (primates) have been a part of the now hundred-billion-dollar global film industry in a variety of capacities. Their use in the film industry is of concern due to the negative welfare effects on individuals, the potential for increased pet trade, and the conservation impacts of public perception. While the effects on human perception of using live primates in film have been studied, little research has been performed on their appearance in animation and none in computer-generated imagery (CGI). We aimed to investigate how the portrayal of primates varied between depiction medium types and how this related to the films’ performance with critics and in the box office. We observed 151 primates in 101 different English-speaking films that debuted between 2000 and 2019. For each appearance we recorded aspects of primate portrayals based on accuracy, anthropomorphism, environment, and agency displayed, along with the depiction medium. We used structural equation models to depict the highest likelihood of the portrayal aspects on the medium’s relationship to the films gross profit worldwide and film critic consensus scores. We found that over the 20-year time frame, use of live primates has decreased, CGI has increased, and animations have remained relatively steady. While animation had no significant relationship to gross profit or critic consensus, both were significantly lower for films that used live primates and were significantly higher for films that used CGI primates. Due to the steady increase in the use of the CGI medium and its positive relationship with gross profit and critic consensus, it could have great effects on people’s perceptions of primates and implications for conservation efforts.
Gnanaolivu SD, Campera M, Nekaris KAI, Nijman V, Satish R, Babu S, Singh M, 'Medicine, black magic and supernatural beings: Cultural rituals as a significant threat to slender lorises in India' People and Nature 4 (4) (2022) pp.1007-1019
1. Trade of wildlife for use in traditional medicines, rituals, magical spells and cul-tural practices occurs globally and has been studied mostly in Africa and Asia.
2. The grey slender loris Loris lydekkerianus is used for both medicinal and ritual purposes, but little information is available on how the user is meant to extract their medicinal properties, or the potential impact these practices have on the species' populations.
3. From 2014– 2021, we used open- ended interviews with 293 informants in three slender loris range states in Southern India to collect qualitative information on peo-ple's beliefs regarding the use of slender lorises in traditional medicine, black magic rituals and other cultural practices. To understand this further, we analysed data on 139 live slender loris rescues from three rescue and rehabilitation centres and one government organization in Bengaluru, India collected over an 18- year period.
4. We found that 116/139 live individuals had been involved in black magic rituals, including piercing, or burning the body and the eyes. These ritual practices occurred more often to female slender lorises and during the new moon. Data from 293 inter-views revealed that astrologers regularly use live lorises for fortune- telling or for ward-ing off evil. Slender loris body parts are used to make traditional folk medicine, develop black magic potions that bring people harm, hypnotize people or to thwart evil.
5. Habitat loss and anthropogenic pressures, coupled with the existing slender loris trade for cultural practices, are a cause for grave concern. Numerous deep- rooted superstitious beliefs and rituals continue to thrive in modern India, and this is potentially one of the major threats to India's already imperilled slender loris population. More research into the prevalence of loris use for black magic is needed to assess the impact on species sustainability.
Campera M, Budiadi B, Bušina T, Fathoni BH, Dermody J, Nijman V, Imron MA, Nekaris KAI, 'Abundance and richness of invertebrates in shade‑grown versus sun‑exposed coffee home gardens in Indonesia' Agroforestry Systems 96 (2022) pp.829-841
Complex agroforestry systems are suggested as a possible solution to reduce the effects of deforestation in the tropics while enhancing the livelihoods of local human populations. Coffee (Coffea spp.) is one of the most important commodity crops in the world that can easily be cultivated in complex agroforestry systems. Coffee agroforestry systems usually sustain higher biodiversity levels than sun-exposed fields while keeping similar levels of productivity considering the several benefits of growing coffee under a complex system. We aim to explore the richness and abundance of invertebrates in coffee home gardens in West Java, Indonesia by comparing 14 sun-exposed and 14 shade-grown gardens. We collected data in March/April 2019 via pitfall traps, pan traps, and beating tray in each field. We ran generalised linear models to assess whether the number of species and the number of individuals of insects differed between sun-exposed vs. shade-grown coffee gardens, and tested associations between main taxa. Overall, there was no difference in the richness (sun-exposed: 19.86 ± SE1.19; shade-grown: 19.71 ± SE1.19; Z-value = 0.12, p value = 0.904) and abundance (sun-exposed: 141.93 ± SE 3.18; shade-grown: 139.93 ± SE3.16; Z-value = 0.35, p value = 0.706) of invertebrates in coffee gardens, although taxa specific differences were present. Sun-exposed fields had a higher abundance of invertebrates considered as pests (Blattodea: Rhinotermitidae, Ectobiidae; Coleoptera: Scarabaeidae, Lycidae and Tenebrionidae; Diptera: Anisolabididae, Drosophilidae and Sarcophagidae). Camponotus spp. were the most dominant ants in shade-grown gardens while Dolichoderus spp. and Myrmicaria spp. were more abundant in sun-exposed gardens. Despite the fact that sun-exposed coffee fields registered higher abundance of invertebrate pests than shade-grown coffee fields, the richness of invertebrates did not substantially vary between sun-exposed and shade-grown coffee, suggesting that the matrix of gardens offers advanced ecosystem services. It is important to keep the complexity of agroforestry systems that provide key habitats for biodiversity.
Balestri M, Campera M, Beaman E, Bell D, Pink R, Nekaris KAI, 'Let’s get virtual! Reinventing a science festival during a pandemic: limitations and insights' International Journal of Science Education, Part B: Communication and Public Engagement 12 (3) (2022) pp.193-202
Non-formal, yet educative, activities such as science festivals can positively influence the public regarding their attitude towards Science, Technology, Engineering and Math (STEM) subjects and students’ willingness to pursue STEM-related careers. We evaluate the changes made to adapt the Oxford Brookes Science Bazaar, a science festival that has been delivered face-to-face since 2008, to a virtual format in 2021 due to the COVID-19 pandemic. The online festival included 28 pre-recorded and 12 live activities of different types (hands-on, demonstration, games, lectures, podcasts, virtual tours). Hands-on activities and virtual tours had the highest number of unique viewers, while lectures and podcasts were the least watched. The videos were watched also after the advertised date of the festival and reached a broader audience than the physical events. The number of participants, the holding time, and the proportion of people who filled the feedback forms, however, were lower in the online than the physical events. STEM organisations should consider hybrid events, with both virtual and in-person contents, to reach a broader audience and to create more inclusive events. We provide recommendations on how to maximise the benefit of virtual formats, including expanding blended virtual activities to reach a wider variety of age groups.
Romdhoni H, Perwitasari-Farajallah D, Iskandar E, Hedger K, Campera M, Birot H, Nekaris KAI, 'The Influence of Sex and Weather on the Activity Budget of Javan Slow Lorises (Nycticebus javanicus) in Garut Regency, West Java' Journal of Tropical Biodiversity and Biotechnology 7 (1) (2022)
The Javan slow loris (Nycticebus javanicus) is a nocturnal primate endemic to Java. Previous studies on slow loris activity are limited to general daily activity, and there is a lack of research on the potential sex differences in slow loris activity. This study aims to analyze differences in the daily activity of the Javan slow loris based on sex. From August to December 2018, the daily activity of six wild Javan slow lorises was recorded using behavioral observations with instantaneous point sam-pling at 5-minute intervals. Differences in male and female slow loris activity were analyzed using the Generalized Linear Mixed Model (GLMM). We set sex and weather as fixed factors and individuals as random effects. The results of this study showed that females spent more time feeding and less time resting than males. In addition, the Javan slow loris behavior was affected by temperature and humidity like other slow loris species.
It is challenging to disentangle the legal and illegal aspects of wild-caught animals that are traded in wildlife markets or online, and this may diminish the value of conducting wildlife trade surveys. We present empirical studies on the trade in birds (ducks, owls, songbirds, non-passerines) in Indonesia (2005 to 2021). Based on visits to wildlife markets, wholesale traders, and monitoring of an Instagram account, we examine if five specific pieces of legislation (domestic and international) are adhered to: (1) protected species, (2) harvest quota, (3) welfare, (4) provincial transport restrictions, and (5) illegal import of CITES-listed species. Our five distinctly different case studies showed that in each case, certain rules and regulations were adhered to, whilst others were violated to varying degrees. When trade involved non-protected species, there was frequently a lack of harvest quotas or trade occurred above these allocated quotas. Basic welfare provisions were regularly and habitually violated. Visiting wildlife markets and recording first-hand what is openly offered for sale is a highly reliable, verifiable, and valuable method of data collection that can give insight in numerous aspects of the animal trade. Our research provides support for recognising the urgency for the government to take appropriate action to curb all the illegal aspects of the bird trade in Indonesia.
Manson S, Nekaris KAI, Hedger K, Balestri M, Ahmad N, Adinda E, Budiadi B, Imron MA, Nijman V, Campera M, 'Flower Visitation Time and Number of Visitor Species Are Reduced by the Use of Agrochemicals in Coffee Home Gardens' Agronomy 12 (2) (2022)
Pollination services, from both wild and managed populations of insect pollinators, have degraded as a result of agricultural intensification. Whilst 75% of economically important crops depend on insect pollinators for cultivation, 40% of insect pollinator species are threatened with extinction. Pollination services must be preserved if there is to be enough food for a global population whose demand is expected to double, if not triple, by 2050. Pollinator diversity and pollinator efficiency have been found to increase as a result of wildlife-friendly farming practices (i.e., natural chemicals and fertilizers and agroforestry). We evaluated the presence of insect pollinators in 42 coffee home gardens in West Java, Indonesia. Via generalized linear mixed models, we found that number of visitor species (β = 0.418 ± SE 0.194, p = 0.031) and visitation time (β = 0.845 ± SE 0.308, p = 0.006) decreased as farms were more intensely managed, (i.e., used chemical pesticides), compared to fields using organic practices. As knowledge of pollination services is widespread amongst smallholder farmers in Indonesia and beyond due to the long-held tradition of beekeeping, these results will add to their existing knowledge and empower farmers to enhance resources for pollinator species through agroforestry and natural pest management. Although we found significant differences in pollination services provided in intensely managed and wildlife-friendly farms, chemical use can affect farms far beyond a particular area of production. Therefore, pollinator conservation must be applied at a landscape level and involve all stakeholders, including farmers, when making effective policies.
Nekaris KA-I, Campera M, Chimienti M, Murray C, Balestri M, Showell Z, 'Training in the Dark: Using Target Training for Non-Invasive Application and Validation of Accelerometer Devices for an Endangered Primate (Nycticebus bengalensis)' Animals 12 (4) (2022)
Accelerometers offer unique opportunities to study the behaviour of cryptic animals but require validation to show their accuracy in identifying behaviours. This validation is often undertaken in captivity before use in the wild. While zoos provide important opportunities for trial field techniques, they must consider the welfare and health of the individuals in their care and researchers must opt for the least invasive techniques. We used positive reinforcement training to attach and detach a collar with an accelerometer to an individual Bengal slow loris (Nycticebus bengalensis) at the Shaldon Wildlife Trust, U.K. This allowed us to collect accelerometer data at different periods between January–June 2020 and January–February 2021, totalling 42 h of data with corresponding video for validation. Of these data, we selected 54 min where ten behaviours were present and ran a random forest model. We needed 39 15-min sessions to train the animal to wear/remove the collar. The accelerometer data had an accuracy of 80.7 ± SD 9.9% in predicting the behaviours, with 99.8% accuracy in predicting resting, and a lower accuracy (but still >75% for all of them apart from suspensory walk) for the different types of locomotion and feeding behaviours. This training and validation technique can be used in similar species and shows the importance of working with zoos for in situ conservation (e.g., validation of field techniques).
Nijman V, Campera M, Imron MA, Ardiansyah A, Langgeng A, Dewi T, Hedger K, Hendrik R, Nekaris KA-I, 'The Role of the Songbird Trade as an Anthropogenic Vector in the Spread of Invasive Non-Native Mynas in Indonesia' Life 11 (8) (2021)
The wildlife trade has facilitated the introduction of invasive non-native species, which may compete with native species for resources and alter ecosystems. Some of these species have great potential to become invasive if released or escaped from captivity. Here we studied the pet trade in a group of open countryside birds, the mynas (Acridotheres spp.) in Indonesia, and identified the areas that are at high risk of facing the establishment of these species. Mynas are among the most invasive birds in Southeast Asia. Once established in a new area, they are almost impossible to eradicate and can have strong negative impacts on the ecosystem. Preventing their introduction is therefore essential. Yet, invasive non-native mynas continue to be traded openly. We present data on the trade in seven species of mynas on Java, Bali and Lombok, with three species being native to parts of one or two of these islands, but not to the remainder, and four that are non-native to the region. From 2016 to 2021 we conducted 255 surveys of 30 animal markets. We recorded over 6000 mynas that were offered for sale outside their native range. Areas most at risk because of their high prevalence in specific animal markets, are Greater Jakarta, eastern Java, Bali and Lombok. The number of invasive non-native mynas recorded was positively related to the size of the animal market. Indonesia is signatory to several international agreements (CBD, ASEAN) that have policies and guidelines to prevent the introduction of invasive non-native species, but compliancy is weak. Annually hundreds and possibly thousands of invasive non-native mynas are released by Indonesian conservation authorities in regions that are outside their native range. Effective management of, and regulation of trade in, potential invasive non-native birds in Indonesia falls short and inadvertently greatly aids both their introduction and establishment.
Nekaris KAI, Handby V, Campera M, 'Impact of weather conditions, seasonality and moonlight on the use of artificial canopy bridges by nocturnal arboreal mammals' Biodiversity and Conservation 30 (2021) pp.3633-3645
Natural and artificial canopy bridges can be used to mitigate the effects of habitat fragmentation. Understanding the ecological factors that influence bridge use is imperative to the effective design and placement of this potential conservation intervention. Moonlight, seasonality and weather may influence the cost and risk of using bridges, potentially reducing their effectiveness. We installed five artificial waterline bridges and, between 2017 and 2019, monitored via camera trapping their use by Javan palm civets Paradoxurus musanga javanicus and Javan slow lorises Nycticebus javanicus. We used a weather station to record microclimate data (temperature and relative humidity) and calculated the illumination percentage of the moon. We tested the influence of moon luminosity, relative humidity, seasonality (Julian day) and temperature on the frequency of bridge use via Generalised Additive Models. Camera traps captured 938 instances of bridge use by civets, which was significantly lower than the reference value at moon luminosity > 90%, temperatures > 20 °C, humidity > 90%, and during the drier period (May–July). Camera traps captured 1036 instances of bridge use by lorises, which was significantly lower than the reference value during the drier period and higher than the reference value at temperatures > 20 °C. Lorises showed peaks in bridge use close to sunset and sunrise whereas civets showed peaks around 2 h after sunset and 2 h before sunrise. Our study illustrates the utility of simple-to-construct bridges by two sympatric nocturnal mammals facing severe habitat loss, with bridge use differing between those species according to abiotic factors. In particular, less use by both taxa during the drier season could suggest modifying placement of bridges or providing another intervention during that time. Camera traps were an excellent mechanism to record these differences and to validate the importance of the bridges, including during inclement weather and dark nights, when observations would be more difficult for human observers. By understanding the influence that abiotic factors have on the use of artificial bridges, we can improve bridge placement and construction to encourage use by a variety of species, particularly those threatened by habitat fragmentation.
Campera M, Hedger K, Birot H, Manson S, Balestri M, Budiadi B, Imron MA, Nijman V, Nekaris KAI, 'Does the Presence of Shade Trees and Distance to the Forest Affect Detection Rates of Terrestrial Vertebrates in Coffee Home Gardens?' Sustainability 13 (15) (2021)
Complex agroforestry systems can host similar biodiversity levels to adjacent continuous forests and can offer important ecosystem services for wildlife. Species inhabiting adjacent forests, as well as species that prefer agroforestry systems, can benefit from this habitat matrix. It is necessary, however, to understand the species-specific adaptability to such a complex matrix. Indonesia is a biodiversity hotspot and hosts many endemic species that are threatened with extinction. Its human population relies heavily on agriculture, meaning that finding a balance between crop productivity and biodiversity is key for the long-term sustainability of local communities and wildlife. We aim to determine the influence of the presence of shade trees and distance to the forest on the detection rates of wildlife in coffee home gardens. In West Java, Indonesia, we monitored 23 gardens between April 2018 and March 2021 via camera traps, totalling 3856 days of monitoring in shade-grown and 3338 days in sun-exposed gardens. We also collected data in the nearby montane rainforest, totalling 1183 days of monitoring. We used Generalized Additive Models to estimate the influence of shade cover and distance to the forest on the detection rates of wildlife. The Sunda leopard cat Prionailurus javanensis was found more frequently in shade-grown gardens and used both the forest and agroforest matrix. Wild boars Sus scrofa mostly occurred in gardens adjacent to the forest, while barred buttonquails Turnix suscitator were associated with gardens far (>1 km) from the forest. Several species (civets Viverricula indica and Paradoxus musangus javanicus, Horsfield’s treeshrew Tupaia javanica, Javan ferret badger Melogale orientalis, Javan mongoose Herpestes javanicus) were not influenced by shade cover and distance to the forest, suggesting they are well adapted to the agroforestry system. Still, species of high conservation importance, such as Javan leopard Panthera pardus melas, Sunda porcupine Hystrix javanica, and grizzled langur Presbytis comata, were present in the forest but not in the agroforest, suggesting that the replacement of the forest by the agroforestry matrix is still detrimental. Nevertheless, it is important to maintain the complexity of the agroforestry system and connectivity with the neighbouring continuous forest to favour the long-term sustainability of this environment and the conservation of endemic species.
In mammals, colouration patterns are often related to concealment, intraspecific communication, including aposematic signals, and physiological adaptations. Slow lorises (Nycticebus spp.) are arboreal primates native to Southeast Asia that display stark colour contrast, are highly territorial, regularly enter torpor, and are notably one of only seven mammal taxa that possess venom. All slow loris species display a contrasting stripe that runs cranial-caudally along the median sagittal plane of the dorsum. We examine whether these dorsal markings facilitate background matching, seasonal adaptations, and intraspecific signaling. We analyzed 195 images of the dorsal region of 60 Javan slow loris individuals (Nycticebus javanicus) from Java, Indonesia. We extracted greyscale RGB values from dorsal pelage using ImageJ software and calculated contrast ratios between dorsal stripe and adjacent pelage in eight regions. We assessed through generalized linear mixed models if the contrast ratio varied with sex, age, and seasonality. We also examined whether higher contrast was related to more aggressive behavior or increased terrestrial movement. We found that the dorsal stripe of N. javanicus changed seasonally, being longer and more contrasting in the wet season, during which time lorises significantly increased their ground use. Stripes were most contrasting in younger individuals of dispersal age that were also the most aggressive during capture. The dorsal stripe became less contrasting as a loris aged. A longer stripe when ground use is more frequent can be related to disruptive colouration. A darker anterior region by younger lorises with less fighting experience may allow them to appear larger and fiercer. We provide evidence that the dorsum of a cryptic species can have multimodal signals related to concealment, intraspecific communication, and physiological adaptations.
Providing a natural diet is a key component to improving animal welfare and potentially reducing stereotypic behaviours in captivity. Wild slow lorises (Nycticebus spp.) are threatened by illegal wildlife trade, and in Thailand, confiscations from trade have led to a large number of Bengal (Nycticebus bengalensis) and greater slow lorises (N. coucang) in rescue centers such as Bang Phra Wildlife Domestic Research Station (Bang Phra). Due to limited enclosure space and availability of natural food items, welfare may be compromised for these confiscated animals. Slow lorises in most rescue centres including Bang Phra are mainly fed with fruit and vegetables rather than their natural diet of exudates, nectar and insects. Our project aimed to increase wild-type activities and reduce stereotypic behaviours in captive slow lorises at Bang Phra by modifying the diet (especially adding exudates of gum Arabic) using environmental enrichment devices. From May to August 2019, we implemented four diet conditions on 30 individuals: baseline, gum presented in two feeding devices and insects presented in a box. Diet conditions changed individual behaviours, with more time spent feeding and foraging, less time spent resting, and less stereotypic behaviours. Fixed gum was the most successful device to encourage increased feeding (40.4 % vs ∼ 3.5 % during baseline conditions) and foraging (16.3 % vs ∼2.5 % during baseline conditions), whilst significantly decreasing stereotypic behaviours (3.2 % vs ∼16.5 % during baseline conditions). Animals with small body sizes are often placed in small cages in rescue centres despite their needs in the wild. At the same time, species with specialist diets may not thrive in rescue centres that lack the funds or infrastructure to procure food items perceived to be specialised. With wild numbers declining rapidly, rescue centres must provide adequate space and wild type diets to ensure the health and well-being of these globally threatened primates.
Campera M, Balestri M, Besnard F, Phelps M, Rakotoarimanana F, Nijman V, Nekaris KAI, Ganzhorn JU, Donati G
, 'The Influence of Seasonal Availability of Young Leaves on Dietary Niche Separation in Two Ecologically Similar Folivorous Lemurs' Folia Primatologica 92 (3) (2021) pp.139-150
Traditional socio-ecological models consider that folivorous primates experience limited feeding competition due to the low quality, high abundance, and even distribution of leaves. Evidence from several folivorous species that experience similar constraints to frugivores does not support this hypothesis. The sympatric lemur genera Avahi (Indriidae) and Lepilemur (Lepilemuridae) are good models to understand how food availability constrains folivores since they are both nocturnal, folivorous, and have a comparable body mass. Here we investigate how two nocturnal folivorous primates, Avahi meridionalis and Lepilemur fleuretae, living in the lowland rain forest of Tsitongambarika, South-East Madagascar, partition their dietary niche and are influenced by seasonality of young leaves. To account for food availability, we collected annual phenological data on 769 trees from 200 species. We also collected behavioural data on 5 individuals per lemur species from August 2015 to July 2016 via continuous focal sampling. We found the phenological profile to be seasonal with peaks of leaf flushing, flowering, and fruiting occurring in the austral summer. The two species showed limited dietary overlap (37% rich period, 6% lean period), and A. meridionalis showed higher feeding time and longer daily distances travelled during the rich period. L. fleuretae showed a dietary shift during the lean period, relying more on mature leaves (73.3% during the lean period, 13.5% during the rich period) but maintaining similar activity levels between seasons. The time spent feeding on food items by A. meridionalis was positively correlated with the nitrogen content and negatively correlated with polyphenols in food items during the rich period. We highlighted a clear effect of the seasonality of young leaves on the diet, nutritional content, activity patterns, and daily distances travelled by two folivorous species, which can be linked to nutrient balancing and time-minimising versus energy-maximising strategies.
Campera M, Balestri M, Manson M, Hedger K, Ahmad N, Nijman V, Budiadi B, Imron MA, Nekaris KAI, 'Shade trees and agrochemical use affect butterfly assemblages in coffee home gardens' Agriculture, Ecosystems and Environment 319 (2021)
Agroforestry systems have been recognised as a possible refuge for biodiversity especially when bordering intact landscapes. The intensification of crop management to increase yields is usually associated with a reduction of shade trees and heavy use of chemicals, typically correlated with a decrease in biodiversity. The relationship between intensity of crop management and biodiversity, however, is not clear-cut and is dependent on environmental and geographical differences. We assessed the influence of different shade cover, shade tree richness, richness of other crops, distance from the forest, and use of chemicals on the diversity, richness and abundance of butterflies, a bioindicator in coffee home gardens. We collected data in 42 coffee home gardens in West Java, Indonesia, via Pollard transects, totalling 15.1 km (July-August 2019 and July-August 2020). We found 54 species of butterflies in the gardens. Via Generalised Additive Mixed Models, we found that the use of chemicals negatively influenced the abundance (p = 0.001) and richness (p = 0.039) of butterflies, while shade tree richness positively influenced the abundance (p
Nijman V, Campera M, Ardiansyah A, Balestri M, Bizri HRE, Budiadi B, Dewi T, Hedger K, Hendrik R, Imron MA, Langgeng A, Morcatty TQ, Weldon AV, Nekaris KAI, 'Large-Scale Trade in a Songbird That Is Extinct in the Wild' Diversity 13 (6) (2021)
Indonesia is at the epicenter of the Asian Songbird Crisis, i.e., the recognition that the cage bird trade has a devastating impact on numerous imperiled bird species in Asia. The Javan pied starling Gracupica jalla, only in the last five years recognized as distinct from the pied starlings of mainland Southeast Asia, has been declared extinct the wild in 2021. Up until the 1980s, it used to be one of the most common open countryside birds on the islands of Java and Bali, Indonesia. From the early 2000s onwards, the species is commercially bred to meet the demand from the domestic cagebird trade. We conducted 280 market surveys in 25 bird markets in Java and Bali between April 2014 and March 2020, with 15 markets being surveyed at least six times. We recorded 24,358 Javan pied starlings, making it one of the most commonly observed birds in the markets. We established that, conservatively, around 40% of the birds in the market were sold within one week and used this to estimate that at a minimum ~80,000 Javan pied starlings are sold in the bird markets on Java and Bali. The latter represents a monetary value of USD5.2 million. We showed that prices were low in the 1980s, when all birds were sourced from the wild. It became more varied and differentiated in the 2000s when a combination of now expensive wild-caught and cheaper captive-bred birds were offered for sale, and prices stabilized in the 2010s when most, if not all birds were commercially captive-bred. Javan pied starlings are not protected under Indonesian law, and there are no linked-up conservation efforts in place to re-establish a wild population on the islands, although small-scale releases do take place.
Nijman V, Smith JH, Foreman G, Campera M, Feddema K, Nekaris KAI, 'Monitoring the Trade of Legally Protected Wildlife on Facebook and Instagram Illustrated by the Advertising and Sale of Apes in Indonesia' Diversity 13 (6) (2021)
Apes continue to be trafficked to meet the demand for pets or zoos. Indonesia, the most diverse country in terms of ape species, has been implicated in the global trade in gibbons, orangutans and, to a lesser degree, chimpanzees. Recently trade has shifted to online platforms, a trend that may have been amplified by the Covid-19 pandemic and partial lockdowns. We assessed the availability of legally protected apes for sale on Facebook and Instagram over two 16-months periods (2017–2018 and 2020–2021). Despite Facebook and Instagram explicitly banning the sale of endangered animals, and Facebook not allowing the sale of live animals, we found 106 gibbons, 17 orangutans and four chimpanzees for sale on five Facebook pages and 19 Instagram accounts. All orangutans and chimpanzees and 70% of the gibbons were infants or juveniles. We did not record any obvious responses of vendors to the Covid-19 pandemic. Facebook and Instagram accounts were linked (similar names, cross-referencing each other and announcing new accounts on existing ones), names were altered (e.g., “petshop” to “pethsop”) and new vendors emerged for short periods. Facebook and Instagram’s policy of not allowing the sale of live and/or endangered wildlife on their platforms is not effectively implemented in Indonesia.
Barrett M, Campera M, Morcatty TQ, Weldon AV, Hedger K, Maynard KQ, Imron MA, Nekaris KAI, 'Risky Business: The Function of Play in a Venomous Mammal—The Javan Slow Loris (Nycticebus javanicus)' Toxins 13 (5) (2021)
Immature mammals require opportunities to develop skills that will affect their competitive abilities and reproductive success as adults. One way these benefits may be achieved is through play behavior. While skills in developing use of tusks, antlers, and other weapons mammals have been linked to play, play in venomous animals has rarely been studied. Javan slow lorises (Nycticebus javanicus) use venom to aid in intraspecific competition, yet whether individuals use any behavioral mechanisms to develop the ability to use venom remains unclear. From April 2012 to December 2020, we recorded 663 play events and studied the factors influencing the frequency of play and the postures used during play in wild Javan slow lorises. Regardless of the presence of siblings, two thirds of play partners of young slow lorises were older and more experienced adults. Young lorises engaged in riskier behaviors during play, including using more strenuous postures and playing more in riskier conditions with increased rain and moonlight. We found that play patterns in immature lorises bear resemblance to venom postures used by adults. We suggest that play functions to train immature lorises to deal with future unexpected events, such as random attacks, as seen in other mammalian taxa with weapons. Given the importance of venom use for highly territorial slow lorises throughout their adult lives and the similarities between venom and play postures, we cannot rule out the possibility that play also prepares animals for future venomous fights. We provide here a baseline for the further exploration of the development of this unique behavior in one of the few venomous mammals.
China plays a critical role in global biodiversity conservation, as both a biodiversity hotspot and for its role in international and domestic animal trade. Efforts to promote wildlife conservation have sparked interest in the attitudes held by Chinese citizens towards animals. Using a questionnaire, we sought to investigate the attitudes of 317 Chinese nationals across provincial-level administrative units regarding their uses of animals, their perceived emotional capacities and views on exotic pets. We reduced the variables related to perceived uses of animals via Principal Component Analysis and ran Generalised Linear Models and Structural Equation Modelling to test relationships between questionnaire-derived variables. Perceptions of animals were divided into two Kellert categories — Utilitarian and Humanistic uses — and 97% of participants believed in animals’ capacities to have and express emotions. We found few interactions, with exotic pets, ie playing with or taking photographs, but the acceptability of owning an exotic pet influenced the likelihood of purchasing one. A belief that animals express emotions encouraged people to look for them as pets but thinking that pets make people happy made exotic pet ownership less acceptable. The shift in attitudes to include humanistic perceptions of animals, a belief in animals as emotive beings and understanding of terminology changed from the previous utilitarian views of pre-reform China, suggesting a readiness to embrace further conservation efforts in China. This deeper understanding of Chinese attitudes towards animals and drivers of the exotic pet trade within China may enable conservation efforts to better target future campaigns.
Van Hamme G, Svensson MS, Morcatty TQ, Nekaris KAI, Nijman V, 'Keep your distance: Using Instagram posts to evaluate the risk of anthroponotic disease transmission in gorilla ecotourism' People and Nature 3 (2) (2021) pp.325-334-334
1. Mountain gorilla Gorilla beringei beringei trekking is a substantial source of revenue for the conservation of this threatened primate and its habitat. Trekking, however, may pose a threat of human-to-gorilla disease transmission that could have disastrous effects on wild gorillas.
2. We used 858 photographs posted on Instagram in 2013–2019 to analyse the proximity of tourists visiting mountain gorillas in the wild. We classified photographs of the encounters according to the distance between the closest gorilla and human, the age class of the gorilla, the trekking location and presence of a surgical face mask on the tourist. We ran a generalised linear mixed model to test whether these variables influenced the distance between the human and the wild gorillas in the photographs, and to test whether these distances have changed over time.
3. Most sampled photographs (86%) showed tourists within a critical 4 m of the gorillas, with 25 incidents of physical contact between a tourist and a gorilla, and only 3% at the recommended distance of 7 m or more. We only were able to record face mask use in the Democratic Republic of Congo, where these were present in 65% of uploaded photos.
4. Tourists and immature gorillas tended to get closer to each other than tourists and adult gorillas, and this is more pronounced in female tourists than male tourists. The mean distance between human and wild gorillas decreased by ~1 m between 2013 and 2019.
5. The results indicate that existing rules are not enforced and raise attention to this unsustainable aspect of mountain gorilla trekking as it is practiced today. These ever-growing tourist attractions in the range countries pose risks of disease transmission in both directions between tourists and wildlife. The popularity of photograph-based social media may stimulate closer contacts and influence people into risky behaviours.
6. We advocate the establishment and reinforcement of regulations relating to the distance between animals and tourists in any in situ wildlife ecotourism context,as well as campaigns to raise awareness regarding the risks of anthroponosis, and fines applied in case of non-compliance.
Campera M, Budiadi B, Adinda E, Ahmad N, Balestri M, Hedger K, Imron MA, Manson S, Nijman V, Nekaris K, 'Fostering a Wildlife-Friendly Program for Sustainable Coffee Farming: The Case of Small-Holder Farmers in Indonesia' Land 10 (2) (2021)
There is an urgent need for a global transition to sustainable and wildlife-friendly farming systems that provide social and economic equity and protect ecosystem services on which agriculture depends. Java is home to 60% of Indonesia’s population and harbors many endemic species; thus, managing agriculture alongside human well-being and biodiversity is vital. Within a community of ~400 coffee farmers in the province of West Java, we assessed the steps to develop a wildlife-friendly program until reaching certification between February 2019 and October 2020. We adopted an adaptive management approach that included developing common objectives through a process of stakeholder consultation and co-learning. We firstly investigated via interviews the expectations and the issues encountered by 25 farmers who converted to organic production in 2016. Their main expectations were an increase in income and an increase in coffee quality, while they had issues mainly in finding high quality fertilizers, reducing pests, and increasing productivity. We used this information to establish a problem-solving plan for the transition to community-wide wildlife-friendly practices. As part of the adaptive evaluation, we assessed the quality of coffee plantations before and after the implementation of coproduced actions. The quality of coffee significantly improved after our interventions to reduce the coffee berry borer, especially in the fields that started as inorganic and converted to organic. We uncovered additional issues to meet the standards for certification, including banning hunting and trapping activities and increasing coffee quality for international export. We describe the coproduced actions (agroforestry, conservation education, local law, organic alternatives) and phases of the program and discuss the potential barriers. We provide novel evidence of adaptive management framework successfully used to implement management actions and reach shared goals.
Keely Q. Maynard1,2, Hélène Birot2, Marco Campera1,2, Muhammad Ali Imron3, Cristina Jasso del Toro1, Stephanie A. Poindexter1,4, K.A.I. Nekaris1,2, 'Slow learning of feeding skills in a nocturnal extractive forager' Animal Behaviour 173 (2021) pp.1-7
A long developmental period in animals is often needed to learn skills for adult reproduction and survival, including feeding behaviour. The nocturnal Javan slow loris, Nycticebus javanicus, is unusual in that it consumes a specialized diet of difficult to extract resources, as well as disperses up to a year after sexual maturity. Here, we examined the ontogeny of its feeding behaviour to understand whether learning to feed on difficult resources, including by co-feeding, is related to delayed dispersal. We collected feeding and proximity data on developing and adult wild slow lorises at a long-term field site in Cipaganti, West Java from 2012 to 2018. To determine whether acquisition of insects, exudates, nectar and flowers varied by age, we ran logistic generalized additive mixed models. We found that intake of insects and exudates occurred significantly more in the early stages, and feeding on nectar significantly more in the later stages, of development. Co feeding occurred for all food types, with insects showing the most co-feeding events during early development, and co-feeding on exudates remaining high throughout development. Social learning via co-feeding is a potentially important factor in transmission of dietary information from older individuals, including siblings and parents, to young slow lorises. Differences between immature and adult diets levelled off after sexual maturity and before average dispersal. Together these factors suggest that the period required to learn to forage on difficult items could help explain the delayed dispersal patterns seen in mammals with similar foraging strategies.
Wildlife trade has been widely discussed as a likely origin of the COVID-19 pandemic. It remains unclear how the main actors in the wildlife trade chain responded to these discussions and to the campaigns advocating wildlife trade bans. We analyzed the content of ~20,000 posts on 41 Facebook groups devoted to wild pet trade and ran a breakpoint and a content analysis to assess when and how the COVID-19 pandemic was incorporated into the discourse within trade communities. Only 0.44% of advertisements mentioned COVID-19, mostly after WHO declared COVID-19 a pandemic. No traders discussed the role of trade in spreading diseases; instead, posts stimulated the trade in wild species during lockdown. COVID-19 potentially offers persuasive arguments for reducing wildlife trade and consumption. This effect was not demonstrated by on-the-ground actors involved in this market. Bans in wildlife trade will not be sufficient and additional strategies are clearly needed.
Nekaris KAI, Campera M, Nijman V, Birot H, Rode-Margono EJ, Fry BG, Weldon A, Wirdateti W, Imron MA, 'Slow lorises use venom as a weapon in intraspecific competition' Current Biology 30 (20) (2020) pp.R1252-R1253
Animals have evolved an array of spectacular weapons, including antlers, forceps, proboscises, stingers, tusks and horns [ 1 ]. Weapons can be present in males and females of species needing to defend critical limiting resources, including food (rhinoceros beetles, Trypoxylus) and territories (fang blennies, Meiacanthus) [ 1 , 2 , 3 ]. Chemicals, including sprays, ointments and injected venoms, are another defence system used by animals. As with morphological weapons, venom can serve multiple purposes, including to facilitate feeding, in predation, and in defence when attacked [ 4 ]. Although rare, several taxa use venom for agonistic intraspecific competition (e.g. ghost shrimp, Caprella spp.; sea anemones, Actinia equina; cone snails, Conidae; male platypus, Ornithorhynchus anatinus) [ 4 , 5 , 6 ]. Another group of venomous mammals are the nocturnal slow lorises ( Nycticebus) [ 7 ]. Slow loris bites often result in dramatic diagnostic wounds characterised by necrotic gashes to the head and extremities. Although these bites are the major cause of death of lorises in captivity, the function of this aggressive behaviour has never been studied in the wild [ 7 ]. Here, through an 8-year study of wounding patterns, territorial behaviour, and agonistic encounters of a wild population of Javan slow lorises ( Nycticebus javanicus), we provide strong evidence that venom is used differentially by both sexes to defend territories and mates.
Nekaris KAI, Handby V, Campera M, Birot H, Hedger K, Eaton J, Imron MAI, 'Implementing and Monitoring the Use of Artificial Canopy Bridges by Mammals and Birds in an Indonesian Agroforestry Environment' Diversity 12 (10) (2020)
Deforestation is a major threat to biodiversity, particularly within tropical forest habitats. Some of the fastest diminishing tropical forest habitats in the world occur in Indonesia, where fragmentation is severely impacting biodiversity, including on the island of Java, which holds many endemic species. Extreme fragmentation on the western part of the island, especially due to small-scale agriculture, impacts animal movement and increases mortality risk for mainly arboreal taxa. To mitigate this risk in an agroforest environment in Garut District, West Java, we installed 10 canopy bridges and monitored them through camera trapping between 2017 and 2019. Five of the monitored bridges were made of waterlines and five of rubber hose. We recorded Javan palm civets using the waterline bridges 938 times, while Javan slow lorises used the waterlines 1079 times and the rubber bridges 358 times. At least 19 other species used the bridges for crossing or perching. Our results demonstrate that relatively simple and cost-effective materials can be used to mitigate the effects of habitat fragmentation. We also recommend the use of camera traps to monitor the effectiveness of these interventions.
Tavares AS, Mayor P, Loureiro LF, Gilmore MP, Perez-Peña P, Bowler M, Lemos LP, Svensson MS, Nekaris KAI, Nijman V, Valsecchi J, Queiroz Morcatty T., 'Widespread use of traditional techniques by local people for hunting the yellow-footed tortoise (Chelonoidis denticulatus) across the Amazon' Journal of Ethnobiology 40 (2) (2020) pp.268-280
Understanding the repertoire of hunting techniques used by traditional peoples in tropical forests is crucial for recognizing the role of traditional knowledge in hunting activities, as well as assessing the impact of harvests on game species. We describe the hunting techniques used across Amazonia by Indigenous and non-Indigenous peoples for hunting yellow-footed tortoises (Chelonoidis denticulatus), one of the most consumed species in the biome. We interviewed 178 local people in 25 communities living in seven study areas in the Peruvian and Brazilian Amazon. We used a Principal Coordinate Analysis (PCoA) and Analysis of Similarity (ANOSIM) to compare the hunting techniques between ethnic groups and the ages of the interviewees. Four different techniques were reported: (1) trapping with bait (46%; n = 122); (2) hunting with dogs (35%; n = 92); (3) active searching (14 %; n = 37); and (4) visiting fruiting trees (5%; n = 14). Trapping with bait was alleged to be the most cost-effective technique by 67% of the interviewees. Among the baits used, 93% involved the use of wild species as rotten meat. Hunting with dogs was also frequently cited and involved eight different methods of training. The hunting techniques recorded were not significantly different among ethnic groups or generations. The consonance among the technique repertoire likely reflects a shared knowledge still in use across different cultural groups. There is a potential for applying the hunting techniques to large scale community-based monitoring and management programs, but the impact on additional species affected, such as species intentionally captured to be used as bait, should be considered. Local assessments and community-based management plans that incorporate traditional ecological knowledge are recommended to guarantee the maintenance of livelihoods and ensure the species' conservation in Amazonia.
Morcatty T, Bausch Macedo JC, Nekaris KAI, Ni Q, Durigan C, Svensson MS, Nijman V, 'Illegal trade in wild cats and its link to Chinese‐led development in Central and South America' Conservation Biology 34 (6) (2020) pp.1525-1535
Seizures of hundreds of jaguar heads and canines in Central and South America from 2014 to 2018 resulted in worldwide media coverage suggesting that wildlife traffickers are trading jaguar body parts as substitutes for tiger parts to satisfy the demand for traditional Asian medicine. We compiled a data set of >1000 seized wild cats (jaguar [Panthera onca], puma [Puma concolor], and ocelot [Leopardus pardalis]) from 19 Central and South American countries and China. We ran generalized additive mixed models to detect trends in wild-cat seizures from 2012 to 2018 and assess the effects of socioeconomic factors of source countries and between those countries and China on the number of wild cats seized. Jaguar seizures increased over time, and most of the seized jaguar pieces were canines (1991 of 2117). Around 34% (32 of 93) of the jaguar-part seizure reports were linked with China, and these seizures contained 14-fold more individuals than those intended for domestic markets. Source countries with relatively high levels of corruption and Chinese private investment and low income per capita had 10-50 times more jaguar seizures than the remaining sampled countries. The number of Chinese residents in Central and South America was not significantly related to the number of jaguars seized. No socioeconomic factors influenced the seizures of puma and ocelots. Legal market chains may provide structure for the illegal chain; thus, the influx of illegal jaguar products is potentially a side effect of the economic partnership between Central and South American countries and China. Poverty and high levels of corruption in the source countries may motivate local people to engage in illegal activities and contribute to the growth of this trade. Supply-side interventions to curb this threat to Neotropical wild cats may include improved training for officials and promotion of governance and the value of protecting these animals to local people.
Scheib H, Nekaris KAI, Rode-Margono EJ, Baumann K, Dobson J, Ragnarsson-McGrath L, Baumann K, Dobson JS, Wirdateti W, Nouwens A, Nijman V, Martelli P, Ma R, Lewis RJ, Kwok HF, Fry BG, 'The toxicological intersection between allergen and toxin: a structural comparison of the cat dander allergenic protein Fel d1 and the slow loris brachial gland secretion protein.' Toxins 12 (2) (2020)
Slow lorises are enigmatic animal that represent the only venomous primate lineage. Their defensive secretions have received little attention. In this study we determined the full length sequence of the protein secreted by their unique brachial glands. The full length sequences displayed homology to the main allergenic protein present in cat dander. We thus compared the molecular features of the slow loris brachial gland protein and the cat dander allergen protein, showing remarkable similarities between them. Thus we postulate that allergenic proteins play a role in the slow loris defensive arsenal. These results shed light on these neglected, novel animals.
Campera M, Brown E, Imron MA, Nekaris KAI, 'Unmonitored releases of small animals? The importance of considering natural dispersal, health, and human habituation when releasing a territorial mammal threatened by wildlife trade' Biological Conservation 242 (2020)
Unmonitored release is a common practice, especially in small animals, that present a series of adverse conditions if not well-planned. Small research centers and non-governmental organizations in developing countries often receive animals that are then subject to unmonitored releases. We explored the patterns of post-release and natal dispersal in the Javan slow loris, a Critically Endangered venomous and territorial mammal that is highly threatened by wildlife trade. We then determined the importance of health status and human habituation for the survival of translocated and natally dispersing animals. We collected data from 2012 to 2018 on pre-release and pre-dispersal health conditions and human habituation, post-release and post-dispersal presence of wounds, behavior, and ranging patterns of 11 translocated and 11 natally dispersing individuals and compared them with 12 stable resident individuals. Translocated animals had a larger home range size (15.9 ± 4.1 ha) and higher wound presence during recaptures (0.47 ± 0.13) than stable resident individuals (3.2 ± 3.0 ha; 0.10 ± 0.06) but they did not differ from natally dispersing individuals (13.8 ± 3.7 ha; 0.28 ± 0.11). Both translocated and natally dispersing individuals can move to a different habitat type compared to their release area or natal range. The fate of both translocated and natally dispersing individuals was influenced by their health state (p
Brown E, Imron MA, Campera M, Nekaris KAI , 'Testing efficacy of a multi-site environmental education program in an ethnically diverse biodiversity hotspot using social scientific analyses. ' Environmental Conservation 47 (1) (2020) pp.60-66
Creating and assessing relatively broad conservation education curricula is important when trying to reach a variety of students. We used a curriculum centred around a storybook in 12 schools in four separate areas of Indonesia, reaching 529 students. We visited each school twice, and taught the ecology and importance of the target taxa, Indonesia’s seven threatened slow loris species (Nycticebus spp.). Through cultural consensus analyses and structural equation modelling, we found that students from all regions showed improvements in knowledge, and that the distance from the forest to where children lived, teachers’ use of given education materials, and students’ use of the storybook all affected student performance in drawing and essay accuracy. Here we make suggestions for creating and evaluating multi-site environmental education programmes. We recommend creating curricula that are not inclusive of any particular community; providing teachers with materials to supplement a conservation intervention; giving each child their own copy of any visual materials used in the lessons; following up with students and teachers about the use of such materials; and interviewing teachers and students regarding their experience with and attitudes towards the study subject. Furthermore we suggest practitioners share their materials and have confidence in adapting them for other species and locations.
Campera M, Santini L, Balestri M, Nekaris KAI, Donati G, 'Elevation gradients of lemur abundance emphasise the importance of Madagascar’s lowland rainforest for the conservation of endemic taxa' Mammal Review 50 (1) (2020) pp.25-37
Elevation gradients correlate with changes in several environmental conditions and are known to be related to animal abundance. Animals in regions with a naturally limited extent of lowland rainforest are expected to have evolved adaptations to intermediate elevations that provided a stable environment during their evolution.
Since the lowland rainforest of Madagascar has a limited extent and suffers from increasing anthropogenic pressure, it is essential to understand how well species tolerate intermediate and high elevations. In this study, we aim to quantify the relationship between lemur abundance and elevation in the eastern rainforest of Madagascar.
We correlated abundance data on 26 lemur species (10 genera), including 492 records from 26 studies, with elevation. We analysed the consistency of correlations across species with a meta‐analytical approach. We controlled for species’ body mass, elevational range and median elevation. We then ran generalised linear mixed models to determine whether lemur abundance was related to elevation, body mass, plant productivity and anthropogenic disturbance.
Overall, the abundance of lemur species in Malagasy rainforests was negatively correlated with elevation, and species occupying broader elevational ranges showed stronger correlations. Body mass was not related to species’ tolerance of high elevations. Even though several lemur species are able to occupy the entire elevation gradient, the few remaining patches of lowland rainforests host lemur species at greater abundances than other sites. Abundance across species was negatively related to body mass, elevation and seasonality in plant productivity and positively related to plant productivity.
Despite the ecological flexibility of many lemur species, the remnant patches of lowland rainforests host the highest levels of lemur abundance and are key to lemur conservation. It is crucial to preserve this priority habitat both for biodiversity conservation and for our understanding of lemur adaptations.
Birot H, Campera M, Imron MA, Nekaris KAI, 'Artificial canopy bridges improve connectivity in fragmented landscapes: the case of Javan slow lorises in an agroforest environment' American Journal of Primatology 82 (4) (2019)
Canopy bridges are increasingly used to reduce fragmentation in tropical habitats yet monitoring of their impact on the behavior of primates remains limited. The Javan slow loris (Nycticebus javanicus) is endemic to Java, Indonesia, where the species most often occurs in human-dominated, highly patchy landscapes. Slow lorises cannot leap, are highly arboreally adapted, and are vulnerable on the ground. To increase arboreal connectivity, as part of a long-term conservation project in Cipaganti, West Java, we built and monitored seven slow lorises bridges of two types – waterline or rubber – and monitored their use by seven adult individuals from 2016-2017. Motion triggered camera traps collected data for 195 ± SD 85 days on each bridge. We collected 341.76 hours (179.67 h before and 162.09 h after the installation of bridges) of behavioral and home range data via instantaneous sampling every 5-min, and terrestrial behavior (distance and duration of time spent on the ground) via all occurrences sampling. We found that slow lorises used bridges on average 12.9 ± SD 9.7 days after their instalment mainly for travelling. Slow lorises showed a trend towards an increase in their home range size (2.57 ha before, 4.11 ha after; p=0.063) and reduced ground use (5.98 s/h before, 0.43 s/h; p=0.063) after implementation of bridges. Although the number of feeding trees did not change, new feeding trees were included in the home range, and the proportion of data points spent travelling and exploring significantly decreased (p=0.018). Waterline bridges serve a purpose to irrigate the crops of local farmers who thus help to maintain the bridges, and also ascribe value to the presence of slow lorises. Other endemic mammal species also used the bridges. We advocate the use and monitoring of artificial canopy bridges as an important supplement for habitat connectivity in conservation interventions.
Fox G, Preziosi R, Antwis R; Combe F, Harris E, Hartley I, Kitchener A, de Kort S, Nekaris KAI, Serrato M, Rowntree J, 'Multi-individual Microsatellite identification: a multiple genome approach to microsatellite design (MiMi)' Molecular Ecology Resources 19 (6) (2019) pp.1672-1680
Bespoke microsatellite marker panels are increasingly affordable and tractable to researchers and conservationists. The rate of microsatellite discovery is very high within a shotgun genomic data set, but extensive laboratory testing of markers is required for confirmation of amplification and polymorphism. By incorporating shotgun next‐generation sequencing data sets from multiple individuals of the same species, we have developed a new method for the optimal design of microsatellite markers. This new tool allows us to increase the rate at which suitable candidate markers are selected by 58% in direct comparisons and facilitate an estimated 16% reduction in costs associated with producing a novel microsatellite panel. Our method enables the visualisation of each microsatellite locus in a multiple sequence alignment allowing several important quality checks to be made. Polymorphic loci can be identified and prioritised. Loci containing fragment‐length‐altering mutations in the flanking regions, which may invalidate assumptions regarding the model of evolution underlying variation at the microsatellite, can be avoided. Priming regions containing point mutations can be detected and avoided, helping to reduce sample‐site‐marker specificity arising from genetic isolation, and the likelihood of null alleles occurring. We demonstrate the utility of this new approach in two species: an echinoderm and a bird. Our method makes a valuable contribution towards minimising genotyping errors and reducing costs associated with developing a novel marker panel. The Python script to perform our method of multi‐individual microsatellite identification (MiMi) is freely available from GitHub (https://github.com/graemefox/mimi).
Geerah RD, O'Hagan RP, Wirdateti W, Nekaris KAI, 'The use of ultrasonic communication to maintain social cohesion in the Javan slow loris (Nycticebus javanicus)' Folia Primatologica 90 (2019) pp.392-403
Only a handful of primate taxa use ultrasonic vocalisations (those ≥20 kHz) to communicate. The extent and uses of ultrasonic communication remain poorly understood, potentially ranging from echolocation, advertisement of reproductive status and resource availability, social cohesion, to predator avoidance. Here, using active acoustics whereby the study subjects were observed throughout their activity period, we describe the first purely ultrasonic call from a strepsirrhine primate (family Lorisidae), recorded in a completely wild setting, and hypothesise about its function. We identified one type of ultrasonic call, the doublet click, from 14 Javan slow lorises (Nycticebus javanicus) produced by males and females of juvenile, subadult and adult ages within their social groups (n = 791, mean = 46.0 kHz). We ran quadratic discriminant function analysis, finding dominant frequency and doublet click duration as the key parameters for identifying individuals’ sex and age. Significantly more vocalisations were produced during affiliative social behaviour, suggesting that the call serves a social cohesion function. Considering the range of other cryptic behaviours, including slow and silent locomotion, and the high degree of territoriality associated with venomous attacks on conspecifics, the call may also serve as a safety strategy, allowing family members to regulate distance from other slow lorises and to communicate cryptically whilst avoiding predators.
Among primates, the suborder Haplorhini is considered to have evolved a consolidated monophasic sleep pattern, with diurnal species requiring a shorter sleep duration than nocturnal species. Only a few primate species have been systematically studied in their natural habitat where environmental variables, including temperature and light, have a major influence on sleep and activity patterns. Here we report the first sleep study on a nocturnal primate performed in the wild. We fitted seven wild Javan slow lorises (Nycticebus javanicus) in West Java, Indonesia with accelerometers that collected activity data, and installed climate loggers in each individual’s home range to collect ambient temperature readings (over 321 days in total). All individuals showed a strictly nocturnal pattern of activity and displayed a striking synchronisation of onset and cessation of activity in relation to sunset and sunrise. The longest consolidated rest episodes were typically clustered near the beginning and towards the end of the light period, and this pattern was inversely related to daily fluctuations of the ambient temperature. The striking relationship between daily activity patterns, light levels and temperature suggests a major role of the environment in shaping the daily architecture of waking and sleep. We concluded that well-known phenotypic variability in daily sleep amount and architecture across species may represent an adaptation to changes in the environment. Our data suggest that the consolidated monophasic sleep patterns shaped by environmental pressures observed in slow lorises represent phylogenetic inertia in the evolution of sleep patterns in humans.
The rise of palm oil as the world’s most consumed vegetable oil has coincided with exponential growth in palm oil research activity. Bibliometric analysis of research outputs reveals a distinct imbalance in the type of research being undertaken, notably a disproportionate focus on biofuel and engineering topics. Recognizing the expansion of oil palm agriculture across the tropics and the increasing awareness of environmental, social, and economic impacts, we seek to reorientate the existing research agenda toward one that addresses the most fundamental and urgent questions defined by the palm oil stakeholder community. Following consultation with 659 stakeholders from 38 countries, including palm oil growers, government agencies, non-governmental organizations, and researchers, the highest priority research questions were identified within 13 themes. The resulting 279 questions, including 26 ranked as top priority, reveal a diversity of environmental and social research challenges facing the industry, ranging from the ecological and ecosystem impacts of production, to the livelihoods of plantation workers and smallholder communities. Analysis of the knowledge type produced from these questions underscores a clear need for fundamental science programmes, and studies that involve the consultation of non-academic stakeholders to develop “transformative” solutions to the oil palm sector. Stakeholders were most aligned in their choice of priority questions across the themes of policy and certification related themes, and differed the most in environmental feedback, technology and smallholder related themes. Our recommendations include improved regional academic leadership and coordination, greater engagement with private and public stakeholders in Africa, and Central and South America, and enhanced collaborative efforts with researchers in the major consuming countries of India and China.
Campera M, Balestri M, Chimienti M, Nijman V, Nekaris KAI, Donati G, 'Temporal niche separation between the two ecologically similar nocturnal primates Avahi meridionalis and Lepilemur fleuretae' Behavioral Ecology and Sociobiology 73 (2019)
Time is considered a resource in limited supply, and temporal niche separation is one of the most common strategies that allow ecologically similar species to live in sympatry. Mechanisms of temporal niche separation are understudied especially in cryptic animals due to logistical problems in gathering adequate data. Using high-frequency accelerometers attached to radio-collars, we investigated whether the ecologically similar lemurs Avahi meridionalis and Lepilemur fleuretae in the lowland rainforest of Tsitongambarika, south-eastern Madagascar, show temporal niche separation. Accelerometers stored data with a frequency of 1 Hz for a total of 71 days on three individuals of A. meridionalis and three individuals of L. fleuretae. We extrapolated motor activity patterns via the unsupervised learning algorithm expectation maximisation and validated the results with systematic behavioural observations. Avahi meridionalis showed peaks of activity at twilights with low but consistent activity during the day, while L. fleuretae exhibited more activity in the central hours of the night. Both lemur species had their activity pattern entrained by photoperiodic variations. The pair-living A. meridionalis was found to be lunarphilic while the solitary-living L. fleuretae was lunarphobic. We suggest that these activity differences were advantageous to minimise feeding competition, as an anti-predator strategy, and/or for dietary-related benefits. These findings demonstrate a fine-tuned temporal partitioning in sympatric, ecologically similar lemur species and support the idea that an activity spread over the 24-h, defined here as cathemerality sensu lato, is more common than previously thought in lemurs.
Ecologically similar species may exhibit temporal niche partitioning and separate their peaks of activity when co-occurring in an area. We show for the first time that the mainly nocturnal genus Avahi can exhibit high crepuscular activity with low but consistent bouts of activity (up to 44.6% of daily activity) during the day. We defined this activity as cathemerality sensu lato as opposed to the cathemerality sensu stricto observed in Eulemur sp. We suggest that this flexible activity may be advantageous for the species to minimise feeding competition and predatory pressure, and/or to provide dietary-related benefits. This finding in the secondary nocturnal genus Avahi supports the idea that activity patterns in lemurs are graded and traditional categorisations are inadequate.
Environment and diet are key factors which shape the microbiome of organisms. There is also a disparity between captive and wild animals of the same species, presumably because of the change in diet. Being able to reverse the microbiome to the wild type is thus particularly important for the reintroduction efforts of Critically Endangered animals. The Javan slow loris (Nycticebus javanicus) is a suitable model, being kept in the thousands within rescue centres throughout Southeast Asia. With next-generation sequencing, we show how a naturalistic diet impacts the gut microbiome of captive slow lorises (Primates: Nycticebus). A comparison of the microbiome of wild animals with captive animals that had been fed a standard captive or improved diet reveals strong microbiome differences between wild and captive animals; however, diet changes failed to alter the microbiome of captive populations significantly. Bifidobacterium was the most abundant genus in wild animals (46.7%) while Bacteroides (11.6%) and Prevotella (18.9%) were the most abundant in captive animals fed the captive and improved diets, respectively. Correlation analyses of nutrients with microbial taxa suggest important implications in using nutrition to suppress potential pathogens, with soluble fibre and water-soluble carbohydrates both being associated with opposing microbiome profiles. The improved diet significantly increased microbe diversity, which exemplifies the importance of high fibre diets; however, wild individuals had lower diversity, which contradicts recent studies. Detection of methanogens appeared to be dependent on diet and whether the animals were living in captivity or in the wild. This study highlights the potential of nutrition in modulating the microbiome of animals prior to release. Unexpectedly, the results were not as significant as has been suggested in recent studies.
The function of colouration in animals includes concealment, communication and signaling, such as the use of aposematism as a warning signal. Aposematism is unusual in mammals, and exceptions help us to understand its ecology and evolution. The Javan slow loris is a highly territorial venomous mammal that has a distinctive facial mask and monochromatic vision. To help understand if they use aposematism to advertise their venom to conspecifics or predators with different visual systems, we studied a population in Java, Indonesia. Using ImageJ, we selected colours from the facial masks of 58 individuals, converted RBG colours into monochromatic, dichromatic and trichromatic modes, and created a contrast index. During 290 captures, we recorded venom secretion and aggressiveness. Using Non-metric Multidimensional Scaling and generalised additive models for location, scale and shape, we found that young slow lorises differ significantly from adults, being both more contrasting and more aggressive, with aggressive animals showing fewer wounds. We suggest aposematic facial masks serve multiple purposes in slow lorises based on age. Change in colouration through development may play a role in intraspecific competition, and advertise toxicity or aggressiveness to competitors and/or predators in juveniles. Aposematic signals combined with intraspecific competition may provide clues to new venomous taxa among mammals.
Ni Qingyong, Wang Yu, Weldon Ariana, Xie Meng, Xu Huailiang, Yao Yongfang, Zhang Mingwang, Li Ying, Li Yan, Zeng Bo, Nekaris KAI, 'Conservation implications of primate trade in China over 18 years based on web news reports of confiscations' PeerJ – the Journal of Life & Environmental Sciences 6 (2018)
Primate species have been increasingly threatened by legal and illegal trade in China, mainly for biomedical research or as pets and traditional medicine, yet most reports on trade from China regard international trade. To assess a proxy for amount of national primate trades, we quantified the number of reports of native primate species featuring in unique web news reports from 2000 to 2017, including accuracy of their identification, location where they were confiscated or rescued, and their condition upon rescue. To measure temporal trends across these categories, the time span was divided into three sections: 2000–2005, 2006–2011 and 2012–2017. A total of 735 individuals of 14 species were reported in 372 news reports, mostly rhesus macaques (n = 165, 22.5%, Macaca mulatta) and two species of slow lorises (n = 487, 66.3%, Nycticebus spp.). During the same period, live individuals of rhesus macaques were recorded 206 times (70,949 individuals) in the Convention on International Trade in Endangered Species of Wild Fauna and Flora Trade Database, whereas slow lorises were only recorded four times (nine individuals), indicating that the species originated illegally from China or were illegally imported into China. Due to their rescued locations in residential areas (n = 211, 56.7%), most primates appeared to be housed privately as pets. A higher proportion of ‘market’ rescues during 2006–2011 (χ2 = 8.485, df = 2, p = 0.014), could be partly attributed to an intensive management on wildlife markets since the outbreak of severe acute respiratory syndrome (SARS) in 2003. More than half (68.3%, 502 individuals) of the primate individuals were unhealthy, injured or dead when rescued. Thus, identification and welfare training and capacity-building should be provided to husbandry and veterinary professionals, as well as education to the public through awareness initiatives. The increase in presence of some species, especially slow lorises, with a declining population in restricted areas, also suggests the urgent need for public awareness about the illegal nature of keeping these taxa as pets.
Luhrs AM, Svensson MS, Nekaris KAI, 'Comparative ecology and behaviour of eastern potto Perodicticus ibeanus and central potto P. edwardsi in Angola, Cameroon, Kenya, Nigeria, Rwanda and Uganda' Journal of East African Natural History 107 (1) (2018) pp.17-30
Comparative behavioural research reveals both intra- and inter-species diversity among primates. Few long-term behavioural studies have been conducted on African nocturnal primates. Here we describe and compare behavioural and ecological observations on two species of pottos (Perodicticus ibeanus and P. edwardsi) across ten sites. We observed a total of 51 P. edwardsi and 28 P. ibeanus. We recorded all 21 postures within an established lorisid ethogram, as well as 42 of 50 behaviours. Eating, locomotion, freezing, resting and sniffing were the most common behaviours. We recorded behaviours not previously described for perodicticines, including bark chewing and unique vocalisations. Three species of pottos are now recognised, with potentially more species to be revealed within this cryptic and nocturnal genus. Although there are similarities among potto species, we show that unique ecological adaptations and behaviours may further elucidate their diversity.
Svensson MS, Nekaris KAI, Bearder SK, Bettridge C, Butynski T, Cheyne SM, Das N, de Jong Y, Luhrs AM, Luncz L, Maddock ST, Perkin A, Pimley E, Poindexter SA, Reinhardt KD, Spaan D, Stark DJ, Starr CR, Nijman V, 'Sleep patterns, daytime predation and the evolution of diurnal sleep site selection in lorisiforms' American Journal of Physical Anthropology 166 (3) (2018) pp.563-577
Objectives: Synthesize information on sleep patterns, sleep site use, and daytime predation at sleep sites in lorisiforms of Asia and Africa (ten genera, 36 species), and infer patterns of evolution of sleep site selection. Materials and methods: We conducted fieldwork in twelve African and six Asian countries, collecting data on sleep sites, timing of sleep and predation during daytime. We obtained additional information from literature and through correspondence. Using a phylogenetic approach, we establish ancestral states of sleep site selection in lorisiforms and trace their evolution. Results: The ancestral lorisiform was a fur-clinger and used dense tangles and branches/forks as sleep sites. Use of tree holes and nests as sleep sites emerged ~22 Mya (range 17-26 Mya) in Africa, and use of bamboo emerged ~11 (7-14) Mya in Asia and later in Africa. Nests are commonly used by Galagoides, Paragalago, Galago and Otolemur, tree holes by Galago, Paragalago, Sciurocheirus and Perodicticus, tangles by Nycticebus, Loris, Galagoides, Galago, Euoticus, Otolemur, Perodicticus and Arctocebus, and all but Sciurocheirus and Otolemur additionally sleep on branches/forks. Daytime predation may affect sleep site selection and sleep patterns in some species of Nycticebus, Galago, Galagoides, Otolemur and Perodicticus. Most lorisiforms enter their sleep sites around sunrise and leave around sunset; several are active during twilight or, briefly, during daytime. Conclusion: Variations in sleep behavior, sleep patterns and vulnerability to daytime predation provide a window into the variation that was present in sleep in early primates. Overall, lorisiforms use the daytime for sleeping and no species can be classified as cathemeral or polycyclic.
It has been suggested that strepsirrhines (lemurs, lorises, and galagos) retain the more primitive left hand preference, whilst monkeys and apes more regularly display a right hand preference at the individual-level. We looked to address questions of laterality in the slow loris (Nycticebus spp.) using spontaneous observations of seven wild individuals, unimanual tests in six captive individuals, and photos of 44 individuals in a bilateral posture assessing handedness at the individual- and group-level. During the unimanual reach task, we found at the individual-level, only four slow lorises showed a hand use bias (R: 3, L:1), Handedness index (HI) ranged from -0.57-1.00. In the wild unimanual grasp task we found at the individual-level two individual showed a right-hand bias, the HI ranged from -0.19-0.70. The bilateral venom pose showed a trend toward a right hand dominant grip in those photographed in captivity, but an ambiguous difference in wild individuals. There are many environmental constraints in captivity that wild animals do not face, thus data collected in wild settings are more representative of their natural state. The presence of right-handedness in these species suggest that there is a need to re-evaluate the evolution of handedness in primates.
Gardiner M, Weldon A, Poindexter SA, Gibson N, Nekaris KAI, 'Survey of practitioners handling slow lorises (Primates: Nycticebus): an assessment of the harmful effects of slow loris bites' Journal of Venom Research 9 (2018) pp.1-7
Slow lorises (Nycticebus spp.) are one of six venomous mammals, and the only known venomous primate. In the wild envenomation occurs mainly during conspecific competition for mates and territory, but may also be used as an application against parasites or for predator defense. Envenomation in humans is documented, with the most extreme accounts detailing near-fatal anaphylactic shock. From September 2016 – August 2017, we received questionnaire responses from 80 wild animal practitioners working with Nycticebus spp. in zoos, rescue centres and in the wild. We identified 54 practitioners who had experience of being bitten or were otherwise affected by slow loris venom, and an additional 26 incomplete entries. No fatalities were reported. Fifteen respondents noted that medical intervention was required, 12 respondents indicated no reaction to being bitten (9 of these indicated they were wearing gloves). Symptoms for those affected
included: anaphylactic shock, paraesthesia, haematuria, dyspnoea, extreme pain, infection
and general malaise. Impact of slow loris bites ranged from instantaneous to long-persisting
complications, and healing time ranged from 1 day to >8 months. Extremities, including hands and arms, were mostly affected from the bites. Six of nine species of slow loris were reported to bite, with N. pygmaeus being the most common in our sample. We make suggestions regarding the use of these highly threatened yet dangerous primates as unsuitable tourist photo props and zoo animal ambassadors. We discuss the medical complications experienced in relation to protein sensitisation, and bacterial pathogenesis. We recommend future work to ascertain the protein content of slow loris venom to aid in enabling mitigation of risks posed.
Hofner AN, Jost Robinson CA, Nekaris KAI, 'Preserving Preuss’s red colobus (Piliocolobus preussi); an analysis of hunting and changing perceptions of primates in Ikenge-Bakoko, Cameroon' International Journal of Primatology 39 (5) (2018) pp.895-917
The futures of nonhuman primate species and human communities in shared landscapes rely on our ability to engage with and understand the complex histories and multiscalar aspects of human–animal relationships. We use the Critically Endangered Preuss’s red colobus (Piliocolobus preussi) as a case study to examine the important ways in which histories of multiscalar human–primate interactions play out in the village of Ikenge-Bakoko, Korup National Park, Cameroon. We contextualize ethnographic and catchment data from adult men (N = 32) and women (N = 31) within long-term diurnal primate monitoring datasets to better understand the relationships among hunting practices, local perceptions of diurnal primates, populations of P. preussi, and conservation management. Our data indicate a disconnect between local cultural definitions of “hunter” and Western assumptions as to the makeup and nature of this and other categories. We show that such contradictions can have negative outcomes for conservationists seeking to turn the science of establishing accurate off-take rates of prey species into practical management solutions. Using a single village as a focal point, we highlight the importance of an ethnoprimatological approach to understanding the intricate entanglements among conservation histories, subsistence strategies, and human and nonhuman primate lives. The application of ethnoprimatology is critical for twenty-first century primatologists who must navigate conservation concerns while also acknowledging and valuing the experiences of the human communities living alongside the primates we study.
Slow loris (Nycticebus spp.) captive diets have been based on routine and anecdotes rather than scientific fact. The growing body of evidence contradicts the high fruit diet supported by such anecdotes. Non-human primate nutrient requirements are grouped into new (based on the common marmoset Callithrix jacchus) or old world (based on rhesus macaques Macaca mulatta) primates. Slow lorises are known to suffer from many health ailments in captivity such as dental disease, obesity, wasting and kidney issues all of which have been linked to diet. This study aimed to estimate nutrient intake from free-ranging slow lorises and to determine whether this intake can be used as nutrient recommendations. We collected data of nutrient intake, food passage rate and digestibility of captive slow lorises on three diet treatments 1: current captive type diet which is mostly fruits, 2: wild-type diet made only of food items from their natural diet, 3: new diet made to reflect wild slow loris nutrient intake. In order to validate our nutrient recommendations, diets 2 and 3 would have to be significantly different to Diet 1 in terms of nutrients, but not different from each other. Captive diets were significantly higher in soluble carbohydrates and lower in minerals and fibre fractions than both diets 2 and 3. Diets 2 and 3 led to a significantly increased food passage time and to more effective fibre and calcium digestion compared to Diet 1. We also observed obese individuals lost weight and underweight individuals gained weight. Our nutrient recommendations have been validated by our trials, and new or old world monkey nutrient recommendations are not consistent with our results. Diets should be high in protein and fibre and low in soluble carbohydrates and fats.
Illegal harvesting and trade are major forces behind population declines of wild slow lorises (genus Nycticebus). The impacts of the wildlife trade on individual slow lorises have not been as well described. In this article, we describe quantitatively the consequences of the wildlife trade for 77 greater slow lorises, N. coucang, who were confiscated en masse and brought to Cikananga Wildlife Center in Indonesia. Medical records indicated that in total, 28.6% of the slow lorises died within the first 6 months, mostly due to traumatic injury, and all the infants died. The greatest sources of morbidity were external wounds (33.1% of 166 total medical events) and dental problems (19.3%). Of the surviving individuals, 25.4% displayed abnormal behavior. Behavioral observations indicated that healthy adults (n = 3) spent 48.2% of their active period performing stereotypies. These data illustrate the physical and behavioral impacts of the illegal wildlife trade on the welfare of slow lorises. We suggest that sharing these individual stories may help generate empathy and educate the public about the impacts of the exotic companion-animal (pet) trade on nonhuman animal welfare.
Miard Priscillia, Nekaris K. A. I., Ramlee Hatta, 'Hiding in the Dark: Local Ecological Knowledge about Slow Loris in Sarawak Sheds Light on Relationships between Human Populations and Wild Animals' Human Ecology 45 (2017) pp.823-831
Local ecological knowledge (LEK) increases understanding of certain species and the threats they face, especially little-studied taxa for which data on distribution and conservation are often lacking. We conducted 111 semi-structured interviews in Sarawak, Malaysia, to collect local knowledge about the behavior and distribution of the Philippine slow loris (Nycticebus menagensis) from two ethnic groups, the Iban and the Penan. Our study revealed that male Penan respondents, generally hunters, who frequently go into the forest were better at identifying animals from pictures. Overall, the Penan have a more detailed knowledge of slow loris behaviors, habitat, and distribution than the Iban. The two ethnic groups have different attitudes towards slow loris as the Penan hunt, eat, or keep them as pets while the Iban consider them sacred and signifiers of good luck. We advocate the use of LEK for providing complementary information to scientific methods in the study of cryptic animals.
Donati G, Santini L, Eppley TM, Arrigo-Nelson SJ, Balestri M, Boinski S, Bollen A, Bridgeman LL, Campera M, Carrai V, Chalise MK, Derby Lewis A, Hohmann G, Kinnaird MF, Koenig A, Kowalewski M, Lahann P, McLennan MR, Nekaris AKI, Nijman V, Norscia I, Ostner J, Polowinsky SY, Schülke O, Schwitzer C, Stevenson PR, Talebi MG, Tan C, Tomaschewski I, Vogel ER, Wright PC, Ganzhorn JU, 'Low levels of fruit nitrogen as drivers for the evolution of Madagascar’s primate communities' Scientific Reports 7 (2017)
The uneven representation of frugivorous mammals and birds across tropical regions – high in the New World, low in Madagascar and intermediate in Africa and Asia – represents a long-standing enigma in ecology. Several hypotheses have been proposed to explain these differences but the ultimate drivers remain unclear. Here, we tested the idea that fruits in Madagascar contain insufficient nitrogen to meet primate metabolic requirements, thus constraining the evolution of frugivory. We performed a global analysis of nitrogen in fruits consumed by primates, as collated from 79 studies. Our results showed that average frugivory among lemur communities was lower compared to New World and Asian-African primate communities. Fruits in Madagascar contain lower average nitrogen than those in the New World and Old World. Nitrogen content in the overall diets of primate species did not differ significantly between major taxonomic radiations. There is no relationship between fruit protein and the degree of frugivory among primates either globally or within regions, with the exception of Madagascar. This suggests that low protein availability in fruits influences current lemur communities to select for protein from other sources, whereas in the New World and Old World other factors are more significant in shaping primate communities.
Cabana F, Dierenfeld E, Wirdateti W, Donati G, Nekaris KAI, 'Slow lorises (Nycticebus spp.) really are slow: A study into food passage rates' International Journal of Primatology 38 (5) (2017) pp.900-913
The characteristics of food ingested by a primate affect its assimilation of energy by modulating food passage rate. In general, digestive time increases in folivorous primates and decreases in frugivorous primates when they are fed higher fibre diets but this relationship is understudied in exudativorous primates. We compared the food passage rate of five slow loris species. We studied 34 wild-caught slow lorises (15 Nycticebus coucang, 15 N. javanicus, and four N. menegensis) in an Indonesian rescue centre and four captive-born slow lorises (two N. bengalensis and two N. pygmaeus) in a UK institution. We fed the Indonesian animals two different diets: a captive-type diet comprising fruits, vegetables and insects, and a wild-type diet formulated to be similar in nutrients to that consumed by slow lorises in the wild, consisting of gum, insects, vegetables and nectar. We fed the UK animals a diet of gum, vegetables, insects and hard-boiled eggs. We formulated this diet to mimic the wild diet, with notably higher fibre fractions and lower soluble sugars than the previous diet. We measured two variables: the transit time (TT) and the mean retention time (MRT). We mixed 1 tsp of glitter in bananas or gum as our markers and fed them to the slow lorises immediately prior to their main diet. We noted the date and time of feeding and of appearances of the marker in faeces. We weighed food given and left over for each animal to calculate ingested foods and nutrients. We found that TTs were not affected by diet treatment but MRTs were significantly longer for all species fed the wild type diet. Our results show that Nycticebus spp. have long MRTs for their body weight, and N. pygmaeus may have the slowest MRT of all primates in relation to body mass. The digestive flexibility of exudativorous primates should allow them to maximise fermentation opportunities when they ingest more (appropriate) fibre by increasing the amount of time the fibre substrate stays in the large intestine. Exudativorous primates appear to have plastic digestive strategies that may be an adaptation to cope with relatively nutrient-poor staple food sources such as gum. The provision of gum in a captive setting may therefore provide benefits for gut health in slow lorises.
Conservation professionals recognize the need to evaluate education initiatives with a flexible
approach that is culturally appropriate. Cultural-consensus theory (CCT) provides a
framework for measuring the extent to which beliefs are communally held and has long been
applied by social scientists. In a conservation-education context, we applied CCT and used
free lists (i.e., a list of items on a topic stated in order of cultural importance) and domain
analysis (analysis of how free lists go together within a cultural group) to evaluate a
conservation education program in which we used a children’s picture book to increase
knowledge about and empathy for a critically endangered mammal, the Javan slow loris
(Nycticebus javanicus). We extracted free lists of keywords generated by students (n=580 in
18 schools) from essays they wrote before and after the education program. In 2 classroom
sessions conducted approximately 18 weeks apart, we asked students to write an essay about
their knowledge of the target species and then presented a book and several activities about
slow loris ecology. Prior to the second session, we asked students to write a second essay. We
generated free lists from both essays, quantified salience of terms used, and conducted
minimal residuals factor analysis to determine presence of cultural domains surrounding slow
lorises in each session. Students increased their use of words accurately associated with slow
loris ecology and conservation from 43% in initial essays to 76% in final essays . Domain
coherence increased from 22% to 47% across schools. Fifteen factors contributed to the
domain slow loris. Between the first and second essays, factors that showed the greatest
change were feeding ecology and slow loris as a forest protector, which increased 7-fold, and
the humancentric factor, which decreased 5-fold. As demonstrated by knowledge retention
and creation of unique stories and conservation opinions, children achieved all six levels of
Bloom’s taxonomy of learning domains. Free from the constraints of questionnaires and
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surveys, CCT methods provide a promising avenue to evaluate conservation education
Balestri M, Campera M, Nekaris KAI, Donati G, 'Assessment of long-term retention of environmental education lessons given to teachers in rural areas of Madagascar' Applied Environmental Education and Communication 16 (4) (2017) pp.298-311
Assessing the retention of knowledge is the first step of environmental education programs. The low education level in rural areas is one factor influencing habitat loss in Madagascar. We tested whether environmental education lessons given to teachers from a municipality, Iaboakoho, in a priority area for lemur conservation were retained after one year. Questionnaires were given to teachers from Iaboakoho and from other three neighbouring municipalities (control groups). Teachers from Iaboakoho had higher scores than the others. Knowledge gained was retained and might be transferred to children. Increasing proenvironmental attitudes and behaviours is the next step to reduce environmental exploitation.
Animals of all ages need to access essential food resources, either on their own or with the assistance of conspecifics. Rapid physical and behavioural development is one strategy to help young animals reach adulthood. Specialized gum-feeding mammals exploit a food type that is relatively difficult to access and digest and must possess the appropriate adaptions to access large vertical substrates, i.e. tree trunks. Unlike other gum feeding mammals, the Javan slow loris (Nycticebus javanicus) lacks physical structures, such as keeled nails or claws, which animals commonly use to secure themselves to large vertical substrates. To understand how slow lorises of all ages exploit gum, we examined their vertical gouging posture, locomotor behaviour, habitat use during feeding, and their morphometric measures across three age classes (adult, sub-adult, juvenile). Using data collected in Cipaganti, Java, Indonesia between April 2012 and April 2016, we found that individuals of N. javanicus rely on their hand, foot, and limb morphology to maintain vertical gouging postures, in place of claws or keeled nails. Locomotor behaviour, position in tree, and tree DBH showed no significant difference across age classes while feeding. Juveniles were indistinguishable from adults and sub-adults in regards to limb proportion indices, lower leg length, hand span and foot span. Some morphometric measures scaled isometrically e.g. arm length, but those highlighted during prolonged vertical postures scaled allometrically e.g. leg, hand, and foot measures. These findings suggest that the rapid behavioural and physical development of key features may act as an ontogenetic adaptation to facilitate access to a stable food resource at a young age. The Javan slow loris exemplifies the complex relationship that exists between an animal’s diet and the specializations that facilitate access to these food resources.
Hundreds of species of wild-caught birds are offered for sale in the bird markets of Java and Bali, Indonesia, to meet the demand for the largely-domestic pet and songbird trade. In the past, owls were offered only in very small numbers in these bird markets but since the release of the Harry Potter series in Indonesia in the early 2000s their popularity as pets has increased. Whereas in the past owls were collective known as Burung Hantu (“Ghost birds”), in the bird markets they are now commonly referred to as Burung Harry Potter (“Harry Potter birds”). We made a retrospective quantitative assessment of the abundance of owls in the bird markets (1979–2010) and conducted 109 surveys in 20 bird markets in 2012–2016 to quantify owls in trade. In the 1980s, 1990s and early 2000s owls were rarely recorded in Indonesia's bird markets, typically one or two and up to five per survey, and frequently no owls were recorded at all. The trade was largely confined to small scops owls. In the late 2000s more species were offered for sale, including barn and bay owls, and larger owl species such as wood-owls, eagle-owls and fish-owls; typically 10 + owls were observed per survey. In recent years, the number of owl species increased even more, and on average we recorded 17 owls per survey, yielding a total of 1810 owls, and in >90% of the surveys owls were present. In the larger bird markets in Jakarta and Bandung typically 30 to 60 owls are on offer of up to 8 species at a time. The number of owls as a proportion of all birds in the markets increased from <0.06% prior to 2002 to >0.43% post 2008, suggesting a delayed Harry Potter effect. Over this period, common species have become cheaper and less common ones have become more expensive. The owls are largely, if not exclusively, wild-caught and are sold into the domestic pet market. The release of Harry Potter films and novels in Indonesia coincided with the rise of the Internet and social media and, with some delay, the emergence of pet owl interest groups on Java and Bali, thus preventing us to demonstrate a causal Harry Potter effect on the owl trade. The overall popularity of owls as pets in Indonesia has risen to such an extent that it may imperil the conservation of some of the less abundant species. Inclusion of owls on Indonesia's protected species list, alongside all diurnal raptors, may be a first step to mitigate the negative effects of this emerging trend.
Lemurs, lorises, and tarsiers are socially and ecologically diverse primates that include some of the most endangered mammals. We review results of long-term studies of 15 lemur species from 7 sites in Madagascar and 1 species each of loris and tarsier in Indonesia. We emphasize that the existence of long-term study populations is a crucial prerequisite for planning and conducting shorter studies on specific topics, as exemplified by various ecophysiological studies of lemurs. Extended studies of known individuals have revealed variation in social organization within and between ecologically similar species. Even for these primates with relatively fast life histories, it required more than a decade of paternity data to characterize male reproductive skew. The long-term consequences of female rank on reproductive success remain poorly known, however. Long-term monitoring of known individuals is the only method to obtain data on life-history adaptations, which appear to be shaped by predation in the species covered here; long-term studies are also needed for addressing particular questions in community ecology. The mere presence of long-term projects has a positive effect on the protection of study sites, and they generate unique data that are fundamental to conservation measures, such as close monitoring of populations.
Los lémures, lorises y tarseros son grupos de primates, muy diversos social y ecológicamente, que incluyen algunas de las especies de mamíferos más amenazadas. Se revisaron los resultados de estudios a largo plazo de 15 especies de lémures en 7 áreas de estudio en Madagascar y una especie de loris y otra de tarsero, en Indonesia. Se resalta la importancia de las áreas de estudio a largo plazo como prerrequisito esencial para planear y llevar a cabo estudios de menor duración sobre temas especificos, como lo ejemplifican varios estudios eco-fisiológicos en lemurs. Estudios a largo plazo de individuos conocidos, han revelado variacion en la organizacion social dentro y entre especies ecologicamente similares. Incluso en estos primates, con un ciclo de vida relativamente corto, se necesita recopilar más de una década de datos de paternidad para determinar el sesgo reproductivo de los machos. Sin embargo, aún se sabe poco de las consecuencias a largo plazo que la posición de las hembras en la jerarquía social puede tener en su éxito reproductivo. El monitoreo a largo plazo de individuos conocidos es el unico metodo para obtener datos sobre adaptaciones en su history natural, las cuales aparentemente son moduladas en function de la predacion a las especies estudiadas en este trabajo. Estos estudios a largo plazo son tambien necesarios para afrontar temas específicos sobre la ecología de estas comunidades. La simple presencia de proyectos a largo plazo tienen un efecto positive en la proteccion de los lugares de studio, como asi tambien generan datos unicos que son fundamentals para apoyar medidas de conservacion tales como el monitoreo de poblaciones.
Nekaris KAI, Poindexter S, Reinhardt KD, Sigaud M, Cabana F, Wirdateti W, Nijman V, 'Coexistence between Javan Slow Lorises (Nycticebus javanicus) and Humans in a Dynamic Agroforestry Landscape in West Java, Indonesia' International Journal of Primatology 38 (2) (2017) pp.303-320
In a world increasingly dominated by human demand for agricultural products, we need to understand wildlife’s ability to survive in agricultural environments. We studied the interaction between humans and Javan slow lorises (Nycticebus javanicus) in Cipaganti, Java, Indonesia. After its introduction in 2013, chayote (Sechium edule), a gourd grown on bamboo lattice frames, became an important cash crop. To evaluate people’s use of this crop and to measure the effect of this increase on slow loris behavior, home ranges, and sleep sites, we conducted interviews with local farmers and analysed the above variables in relation to chayote expansion between 2011 and 2015. Interviews with farmers in 2011, 2013, and 2015 confirm the importance of chayote and of bamboo and slow lorises in their agricultural practices. In 2015 chayote frames covered 12% of land in Cipaganti, occupying 4% of slow loris home ranges, which marginally yet insignificantly increased in size with the increase in chayote. Slow lorises are arboreal and the bamboo frames increased connectivity within their ranges. Of the sleep sites we monitored from 2013 to 2016, 24 had disappeared, and 201 continued to be used by the slow lorises and processed by local people. The fast growth rate of bamboo, and the recognition of the value of bamboo by farmers, allow persistence of slow loris sleep sites. Overall introduction of chayote did not result in conflict between farmers and slow lorises, and once constructed the chayote bamboo frames proved to be beneficial for slow lorises.
Cabana F, Dierenfeld ES, Wirdateti, Donati G, Nekaris KAI, 'Exploiting a readily available but hard to digest resource: A review of exudativorous mammals identified thus far and how they cope in captivity' Integrative Zoology 13 (1) (2017) pp.94-111
Gum is a widely available carbohydrate, composed mainly of non-digestible structural carbohydrates. No mammalian enzymes can digest gum, therefore a mammal ingesting gum must rely on microbial fermentation in order to access the energy it possesses. Gums are known as relatively nutrient poor. Despite this, some mammals have evolved to exploit this food resource. We aim to review the literature for all mammal species which have been recorded to ingest gum, whether quantified or not and discuss this in context of their evolutionary adaptations. We also investigated the recommended captive diets for these species to look at if gum is recommended. We conducted a literature search on ISI Web of Knowledge to tabulate all mammal species observed ingesting gum and classify them as obligate, facultative or opportunistic feeders. We encountered 94 mammal species which eat gum in the wild (26 obligate feeders, 35 facultative feeders and 33 opportunistic feeders). Obligate feeders have entirely evolved to exploit this resource but were found to not be given gum in captivity, which may explain why they are failing to thrive, as opposed to facultative feeders which have fewer issues. Gum may be necessary for the health of obligate feeders in captivity. Future research should focus on the physiological effects that gum ingestion poses on different digestive systems.
Svensson MS, Bersacola E, Mills MSL, Munds RA, Nijman V, Perkin A, Masters JC, Couette S, Nekaris KAI, Bearder SK, 'A giant among dwarfs: a new species of galago (Primates: Galagidae) from Angola' American Journal of Physical Anthropology 163 (1) (2017) pp.30-43
Objectives. Based on vocalization recordings of an unknown galago species, our main objectives were to compare morphology and call structure with known closely-related taxa and describe a new species of galago.
Materials and methods. We conducted field surveys in three forest habitats along the escarpment region in western Angola (Kumbira Forest, Bimbe Area, and Northern Scarp Forest), and examined galago specimens from museums worldwide. We digitized and analyzed calls using Avisoft SASLab Pro software. We also compared museum specimens from Angola with other Galago and Galagoides specimens, and conducted comparative analyses (ANOVA and between group principle component analysis) based on a set of twelve linear measurements of skulls and teeth.
Results. We describe the new species to which we give the name Angolan dwarf galago, Galagoides kumbirensis sp. nov. The new species has a loud and characteristic crescendo call, used by other Galagoides spp. (sensu stricto) in West Africa to attract companions and repel rivals. However, this call shows species-typical differences from its closest relatives. Galagoides kumbirensis sp. nov. is also distinguished by differences in the skull morphology, pelage color and facial markings, as well as a larger body size, similar to that of Galago moholi, which is not known to be sympatric.
Conclusion. This discovery points to the importance of Angolan forests as refuges for endemic biodiversity. These forests are under severe threat from overexploitation, and there is an urgent need to establish conservation measures and designate protected areas.
Raptors are confirmed predators of Asian slow lorises (Nycticebus spp.), the only primates with a toxic bite. A possible function of this venom is to protect against predators. Slow lorises release volatile chemicals when threatened, thus potentially communicating their venomous status towards predators. Crested Serpent-eagles (Spilornis cheela) and Changeable Hawk-eagles (Nisaetus cirrhatus) are known to prey on venomous snakes and small mammals and are potential predators of slow lorises. We tested the anti-predator potential of slow loris venom by presenting pieces of chicken combined with swabs of Greater Slow Loris (Nycticebus coucang) venom to 10 Changeable Hawk-eagles and 5 Crested Serpent-eagles. The eagles showed few behavioural responses in reaction to slow loris venom, examining swabs with venom or control scents equally. Both eagle species did show higher rates of face-rubbing behaviour following consumption of foods paired with venom compared with control scents. Our data suggest that slow loris venom does not function to repel avian predators, but may have an anti-predator defence function. While the eagles are not repelled by the smell of slow lorises, contact with their venom causes discomfort, potentially limiting the palatability of slow lorises to eagles.
Cabana F, Dierenfeld E, Wirdateti W, Donati G, Nekaris KAI, 'The seasonal feeding ecology of the Javan slow loris (Nycticebus javanicus)' American Journal of Physical Anthropology 162 (4) (2017) pp.768-781
Objectives. To describe the strategy employed by exudativorous primates during seasonal shifts in food abundance using the Javan slow loris as a model. Males and females may cope differently as well as exploit fallback foods in different proportions.
Materials and methods. Observing 15 free ranging Javan slow lorises over a year, we quantified their seasonal diet and nutrient intake using intake rates. For gum intake rates, we conducted a trial with 10 captive Javan slow lorises measuring the length of time it took for them to ingest 10 g of gum. We monitored phenology in our field site over five plots that were assessed monthly. We weighed our free-ranging animals every six months. We analyzed all food items slow lorises ingested for macronutrients using the nutritional geometry framework.
Results. The slow loris diet consisted of eight food categories, with gum and insects being the major food sources in terms of wet weight intake. The captive gum trials resulted in an intake rate of 0.021 g/s. All food items eaten by wild Javan slow lorises were available in the wet season and were restricted in the dry season. Males and females reacted differently to seasonal abundances with females ingesting more protein, gum, fruits and flowers and males ingesting more fiber.
Conclusions. The strategy used by the Javan slow lorises during periods of lower food availability were similar to folivorous primates and included increased dependence on lower quality foods. The reproductive costs of gestation and lactation may place a burden on females that requires them to alter their foraging strategy during the dry season to ensure enough protein and overall energy is ingested. The overall strategy used by these exudativorous primates is one of nutrient maximization as no nutrient was clearly preferred over another.
Svensson M S, Shanee S, Shanee N, Bannister FB, Cervera L, Donati G, Huck M, Jerusalinsky L, Juarez CP, Maldonado AM, Martinez Molinedo J, Méndez-Carvajal PG, Molina Argandoña MA, Mollo Vino A D, Nekaris KAI, Peck M, Rey-Goyeneche J, Spaan D, Nijman V, 'Disappearing in the night: an overview on trade and legislation of night monkeys in South and Central America' Folia Primatologica 87 (5) (2017) pp.332-348
The international trade in night monkeys (Aotus spp.), found throughout Central and South America, has been regulated by the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) since 1975. We present a quantitative analysis of this trade from all 9 range countries, over 4 decades, and compare domestic legislation to CITES regulations. Night monkeys were exported from 8 of the 9 habitat countries, totalling 5,968 live individuals and 7,098 specimens, with trade of live individuals declining over time. In terms of species, the most commonly traded was Aotus nancymaae (present in Brazil, Colombia, Peru) followed by A. vociferans (Brazil, Colombia, Ecuador, Peru) and A. zonalis (Colombia, Panama). There was no significant correlation between levels of trade and species' geographic range size or the number of countries in which a species occurs. Five countries have legislation that meets CITES requirements for implementation, whereas the other 4 countries' legislation showed deficiencies. Research conducted in Colombia, Peru, and Brazil suggests significant cross-border trade not captured in official international trade registers. Although international trade has diminished, current trends suggest that populations of rarer species may be under unsustainable pressure. Further research is needed to quantify real trade numbers occurring between habitat countries.
Estrada A, Garber P A, Rylands A B, Roos C, Fernandez-Duque E, Di Fiore A , Nekaris K A-I, Nijman V, Heymann E W , Lambert J E, Rovero F, Barelli C, Setchell J M, Gillespie T R, Mittermeier R A, Verde Arregoitia L, de Guinea M, Gouveia S, Dobrovolski R, Shanee S, Shanee N, Boyle S A, Fuentes A, MacKinnon K C, Amato K R, Meyer A L S, Wich S, Sussman R W, Pan R, Kone I, Li B, 'Impending extinction crisis of the world’s primates: Why primates matter' Science Advances 3 (1) (2017)
Non-human primates, our closest biological relatives, play important roles in the livelihoods, cultures and religions of many societies, and offer unique insights into human evolution, biology, behavior and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. The most recent compilation of primate taxonomy lists 504 species, 197 subspecies and 79 genera distributed in the Neotropics, mainland Africa, Madagascar and Asia. Alarmingly, ~60% of primate species are now threatened with extinction as a result of unsustainable human activities, including illegal hunting and those resulting in extensive land-cover changes: industry driven agricultural production, deforestation, livestock and cattle ranching, oil and gas drilling, mining, dam building, climate change, and poor governance. Although drivers of primate decline vary by region, it is clear that decreasing the per capita demand of industrialized nations, lowering human birth rates and population growth, improving health, reducing poverty and gender biases in education, developing sustainable land-use initiatives, and preserving traditional livelihoods in primate range countries are all part of a comprehensive solution. Despite the existing threats to primate survival, we are adamant that primate conservation is not yet a lost cause. We still have the opportunity to reduce the human impact to primates and their habitats, but that demands raising greater local, regional and global public awareness of the plight of the world’s primates and the costs of their loss to ecosystem health, human culture and ultimately human survival.
Joint impacts of anthropogenic disturbance and climate change are of pressing concern for modern conservationists. Climate change patterns have various diminishing effects on the biodiversity of an ecosystem, requiring an understanding of a species’ ability to adapt. Agricultural practices are expanding at an altitudinal gradient on the Indonesian island of Java, forcing endemic species to range at increased elevation with lower temperatures, and in human-populated areas. One example is the Critically Endangered Javan slow loris (Nycticebus javanicus), which finds itself increasingly restricted to montane regions with extreme climate patterns and habitat disturbance. We observed wild N. javanicus in a highly fragmented, montane agroforest area to determine if climate variables and forest connectivity influence activity budget and behavior. Lorises ranged at different altitudes (1275 m above sea level (asl)—1570 m asl) and were observed for six months in Cipaganti, West Java. Using multinomial regression analyses, we found loris individuals were most likely to engage in increased foraging, feeding and travelling behavior than resting when relative humidity increases and in habitats with greater forest connectivity. Regression analyses found effects of relative humidity and forest connectivity to be the most significant predictors of N. javanicus foraging behavior (P = 0.001, P = 0.030). We suggest that future-climate shifts and increased anthropogenic disturbance will detrimentally influence wild populations of N. javanicus, requiring immediate plans for mitigation in conserving these already scarce wild populations. We also suggest the altering of reintroduction protocols in relation to climate and geographic region.
Videos, memes and images of pet slow lorises have become increasingly popular on the Internet. Although some video sites allow viewers to tag material as ‘animal cruelty', no site has yet acknowledged the presence of cruelty in slow loris videos. We examined 100 online videos to assess whether they violated the ‘five freedoms' of animal welfare and whether presence or absence of these conditions contributed to the number of thumbs up and views received by the videos. We found that all 100 videos showed at least 1 condition known as negative for lorises, indicating absence of the necessary freedom; 4% showed only 1 condition, but in nearly one third (31.3%) all 5 chosen criteria were present, including human contact (57%), daylight (87%), signs of stress/ill health (53%), unnatural environment (91%) and isolation from conspecifics (77%). The public were more likely to like videos where a slow loris was kept in the light or displayed signs of stress. Recent work on primates has shown that imagery of primates in a human context can cause viewers to perceive them as less threatened. Prevalence of a positive public opinion of such videos is a real threat towards awareness of the conservation crisis faced by slow lorises.
Tropical marine molluscs are traded globally. Larger species with slow life histories are under threat from over-exploitation. We report on the trade in protected marine mollusc shells in and from Java and Bali, Indonesia. Since 1987 twelve species of marine molluscs are protected under Indonesian law to shield them from overexploitation. Despite this protection they are traded openly in large volumes.
We collected data on species composition, origins, volumes and prices at two large open markets (2013), collected data from wholesale traders (2013), and compiled seizure data by the Indonesian authorities (2008–2013). All twelve protected species were observed in trade. Smaller species were traded for <USD1.00 whereas prices of larger species were USD15.00–40.00 with clear price-size relationships. Some shells were collected locally in Java and Bali, but the trade involves networks stretching hundreds of kilometres throughout Indonesia. Wholesale traders offer protected marine mollusc shells for the export market by the container or by the metric ton. Data from 20 confiscated shipments show an on-going trade in these molluscs. Over 42,000 shells were seized over a 5-year period, with a retail value of USD700,000 within Indonesia; horned helmet (Cassis cornuta) (>32,000 shells valued at USD500,000), chambered nautilus (Nautilus pompilius) (>3,000 shells, USD60,000) and giant clams (Tridacna spp.) (>2,000 shells, USD45,000) were traded in largest volumes. Two-thirds of this trade was destined for international markets, including in the USA and Asia-Pacific region.
We demonstrated that the trade in protected marine mollusc shells in Indonesia is not controlled nor monitored, that it involves large volumes, and that networks of shell collectors, traders, middlemen and exporters span the globe. This impedes protection of these species on the ground and calls into question the effectiveness of protected species management in Indonesia; solutions are unlikely to be found only in Indonesia and must involve the cooperation of importing countries.
Nijman V, Spaan D, Rode-Margono EJ, Wirdateti, Nekaris KAI, 'Changes in the primate trade in Indonesian wildlife markets over a 25-year period: fewer apes and langurs, more macaques and slow lorises' American Journal of Primatology 79 (11) (2015)
Indonesia has amongst the highest primate species richness, and many species are included on the country's protected species list, partially to prevent over-exploitation. Nevertheless traders continue to sell primates in open wildlife markets especially on the islands of Java and Bali. We surveyed 13 wildlife markets in 2012–2014 and combined our results with previous surveys from 1990–2009 into a 122-survey dataset with 2,424 records of 17 species. These data showed that the diversity of species in trade decreased over time, shifting from rare rainforest-dwelling primates traded alongside more widespread species that are not confined to forest to the latter type only. In the 1990s and early 2000s orangutans, gibbons and langurs were commonly traded alongside macaques and slow lorises but in the last decade macaques and slow lorises comprised the bulk of the trade. In 2012–2014 we monitored six wildlife markets in Jakarta, Bandung and Garut (all on Java), and Denpasar (Bali). During 51 surveys we recorded 1,272 primates of eight species. Traders offered long-tailed macaque (total 1,007 individuals) and three species of slow loris (228 individuals) in five of the six markets, whereas they traded ebony langurs (18 individuals), and pig-tailed macaques (14 individuals) mostly in Jakarta. Pramuka and Jatinegara markets, both in Jakarta, stood out as important hubs for the primate trade, with a clear shift in importance over time from the former to the latter. Slow lorises, orangutans, gibbons and some langurs are protected under Indonesian law, which prohibits all trade in them; of these protected species, only the slow lorises remained common in trade throughout the 25-year period. Trade in non-protected macaques and langurs is subject to strict regulations—which market traders did not follow—making all the market trade in primates that we observed illegal. Trade poses a substantial threat to Indonesian primates, and without enforcement, the sheer volume of trade may mean that species of Least Concern or Near Threatened may rapidly decline.
Trade in primates is considered a major impediment to primate conservation globally. The bushmeat trade in West and Central Africa is considered largely unsustainable and represents one of the main threats to biodiversity. Furthermore, the use of primates in traditional practices and medicine includes a third of the African primate species. Little is known about the trade in the African mainland lorisiforms; pottos, angwantibos and galagos. Aiming to fill this knowledge gap we created an online survey, conducted a literature review, and analyzed CITES trade records, focusing on the last two decades. We obtained 188 questionnaire responses from researchers and people working in 31 different countries in sub-Saharan Africa. We found a total of 33 publications reporting on trade in African lorisiforms, and CITES records indicate that almost 2000 lorisiforms were traded internationally from African range countries. Fifty-three percent of respondents provided meaningful details about aspects of the trade in African lorisiforms from 50% of the range countries. Galagos were reported by respondents in larger numbers than pottos and angwantibos, and mainly occurred in the pet trade. Pottos were the most frequently mentioned taxon in the literature, when all trade types were combined. Across all of the sources (online survey, literature and CITES database), trade in pottos and angwantibos was reported from 12 countries, and galagos from 23 countries. Trade was reported to occur mainly within rural settings (64%), potentially indicating that demand is not high enough to fuel long distance trading. However, as seen in the Asian lorisiforms, once quantitative studies were conducted, the threat that trade posed became alarmingly apparent and is now considered a major impediment to their conservation. Our insight into the trade of African lorisiforms should be followed up with concerted studies, with an emphasis on quantifying trade to the species level.
Venom delivery systems (VDS) are common in the animal kingdom, but rare amongst mammals. New definitions of venom allow us to reconsider its diversity amongst mammals by reviewing the VDS of Chiroptera, Eulipotyphla, Monotremata, and Primates. All orders use modified anterior dentition as the venom delivery apparatus, except Monotremata, which possesses a crural system. The venom gland in most taxa is a modified submaxillary salivary gland. In Primates, the saliva is activated when combined with brachial gland exudate. In Monotremata, the crural spur contains the venom duct. Venom functions include feeding, intraspecific competition, anti-predator defense and parasite defense. Including mammals in discussion of venom evolution could prove vital in our understanding protein functioning in mammals and provide a new avenue for biomedical and therapeutic applications and drug discovery.
Pozzi L, Nekaris KAI, Perkin A, Bearder SK, Pimley ER, Schulze H, Streicher U, Zischler H, Bruford M, Zinner D, Roos C, 'Remarkable Ancient Divergences Amongst Neglected Lorisiform Primates' Zoological Journal of the Linnean Society 175 (3) (2015) pp.661-674
Lorisiform primates (Primates: Strepsirrhini: Lorisiformes) represent almost 10% of the living primate species and are widely distributed in sub-Saharan Africa and South/South-East Asia; however, their taxonomy, evolutionary history, and biogeography are still poorly understood. In this study we report the largest molecular phylogeny in terms of the number of represented taxa. We sequenced the complete mitochondrial cytochrome b gene for 86 lorisiform specimens, including ∼80% of all the species currently recognized. Our results support the monophyly of the Galagidae, but a common ancestry of the Lorisinae and Perodicticinae (family Lorisidae) was not recovered. These three lineages have early origins, with the Galagidae and the Lorisinae diverging in the Oligocene at about 30 Mya and the Perodicticinae emerging in the early Miocene. Our mitochondrial phylogeny agrees with recent studies based on nuclear data, and supports Euoticus as the oldest galagid lineage and the polyphyletic status of Galagoides. Moreover, we have elucidated phylogenetic relationships for several species never included before in a molecular phylogeny. The results obtained in this study suggest that lorisiform diversity remains substantially underestimated and that previously unnoticed cryptic diversity might be present within many lineages, thus urgently requiring a comprehensive taxonomic revision of this primate group.
Flagship species are traditionally large, charismatic animals used to rally conservation efforts. Accepted flagship definitions suggest they need only fulfil a strategic role, unlike umbrella species that are used to shelter cohabitant taxa. The criteria used to select both flagship and umbrella species may not stand up in the face of dramatic forest loss, where remaining fragments may only contain species that do not suit either set of criteria. The Cinderella species concept covers aesthetically pleasing and overlooked species that fulfil the criteria of flagships or umbrellas. Such species are also more likely to occur in fragmented habitats. We tested Cinderella criteria on mammals in the fragmented forests of the Sri Lankan Wet Zone. We selected taxa that fulfilled both strategic and ecological roles. We created a shortlist of ten species, and from a survey of local perceptions highlighted two finalists. We tested these for umbrella characteristics against the original shortlist, utilizing Maximum Entropy (MaxEnt) modelling, and analysed distribution overlap using ArcGIS. The criteria highlighted Loris tardigradus tardigradus and Prionailurus viverrinus as finalists, with the former having highest flagship potential. We suggest Cinderella species can be effective conservation surrogates especially in habitats where traditional flagship species have been extirpated.
Japan’s involvement in the wildlife trade is widely recognised. We investigated the extent and legitimacy of trade of slow lorises, Nycticebus spp., as pets in Japan. We collected data from online videos, pet shops, and selected informants between May and July 2014 in Japan, and supplemented these with data from CITES Trade Database and confiscation records. We recorded 114 slow lorises in 93 Japanese online videos, and across 20 pet shops we recorded the sale of 74 individuals of six threatened species, including 12 Critically Endangered N. javanicus and two hybrids, each costing USD 3,290-8,650, with animals displayed with falsified CITES permits. From 1985 to 2013, CITES data specify that Japan imported more slow lorises than any other country (n=633), and 400 individuals were confiscated entering Japan, between 2000 and 2013. Penalties imposed on law breakers are weak and our investigations highlight inadequacies in Japan’s enforcement of national law and CITES regulation. To combat the illegal trade and demand for wildlife as pets, we emphasise the need for: stronger penalties,
improved legislative regulation, provision of educational materials and training programs to border control staff and the public. Finally, we strongly urge the continued monitoring of the slow loris trade in Japan.
Grow N, Wirdateti, Nekaris KAI, 'Does toxic defence in Nycticebus spp. relate to ectoparasites? The lethal effects of slow loris venom on arthropods' Toxicon: An Interdisciplinary Journal on the Toxins Derived from Animals, Plants and Microorganisms 95 (2014) pp.1-5
The venom produced by slow lorises (Nycticebus spp.) is toxic both intra- and inter-specifically. In this study we assessed the ecoparasite repellent properties of their venom. We tested venom from two Indonesian slow loris species: Nycticebus javanicus and Nycticebus coucang. Arthropods directly exposed to brachial gland secretions mixed with saliva from both species were immediately impaired or exhibited reduced activity (76%), and often died as a result (61%). We found no significant difference in the result of 60-min trials between N. coucang and N. javanicus [X2(1, n = 140) = 2.110, p = 0.3482]. We found evidence that the degree of lethality of the venom varies according to the arthropod taxa to which it is exposed. While most maggots (84%) were initially impaired from the venom after 10 min, maggots died after a 1 h trial 42% of the time. In contrast, at the end of 1 h trial, spiders died 78% of the time. For all arthropods, the average time to death from exposure was less than 25 min (M = 24.40, SD = 22.60). Ectoparasites including ticks, members of the arachnid order, are known to transmit pathogens to hosts and may be an intended target of the toxic secretions. Our results suggest that one function of slow loris venom is to repel parasites that affect their fitness, and that their topical anointing behaviour may be an adaptive response to ectoparasites.
With the number of threatened species in rescue centres rising, scientific reports on the functioning and success of such centres is essential. Compassionate conservation tries to bridge the gap between animal welfare advocates and conservation biologists, recognising the benefits of preserving a species and its individuals. A case in point is that of Indonesia’s threatened slow lorises Nycticebus spp., where illegal trade is decimating wild populations of these primates. We present 4 yr of data from Ciapus Primate Centre in Indonesia, which received 180 slow lorises between 2008 and 2011. We show that >85% of these primates were unsuitable for reintroduction; 23 slow lorises that were deemed suitable for reintroduction were released to the wild between 2010 and 2013 and were followed with radio tracking. Eleven of them died (on average 76 d post-release), 1 was recaptured (148 d post-release), 6 are no longer being monitored (after, on average, 263 d post-release) and their status is unknown, and 5 are still being monitored (average 226 d post-release, as of December 2013). The challenges posed by work with slow lorises in the Ciapus Primate Centre over these 4 yr, with release success highly variable, show that even with concerted effort, rescue centres need to consider alternative options. We review such options, considering the pros and cons of euthanasia, life in captivity and reintroduction to the wild. We conclude that in today’s global conservation crisis, it can only be beneficial to combine the expertise of animal welfare practitioners and conservation biologists.
Predation pressure, food availability, and activity may be affected by level of moonlight and climatic conditions. While many nocturnal mammals reduce activity at high lunar illumination to avoid predators (lunarphobia), most visually-oriented nocturnal primates and birds increase activity in bright nights (lunarphilia) to improve foraging efficiency. Similarly, weather conditions may influence activity level and foraging ability. We examined the response of Javan slow lorises (Nycticebus javanicus Geoffroy, 1812) to moonlight and temperature. We radio-tracked 12 animals in West Java, Indonesia, over 1.5 years, resulting in over 600 hours direct observations. We collected behavioural and environmental data including lunar illumination, number of human observers, and climatic factors, and 185 camera trap nights on potential predators. N. javanicus reduced active behaviours in bright nights. Although this might be interpreted as a predator avoidance strategy, animals remained active when more observers were present. We did not find the same effect of lunar illumination on two potential predators. We detected an interactive effect of minimum temperature and moonlight, e.g. in bright nights slow lorises only reduce activity when it is cold. Slow lorises also were more active in higher humidity and when it was cloudy, whereas potential predators were equally active across conditions. As slow lorises are well-adapted to avoid/defend predators by crypsis, mimicry and the possession of venom, we argue that lunarphobia may be due to prey availability. In bright nights that are cold, the combined effects of high luminosity and low temperature favour reduced activity and even torpor. We conclude that Javan slow lorises are lunarphobic – just as the majority of mammals.
For endangered species management it is imperative that there is a shared understanding of the different beliefs, opinions and factual knowledge about different aspects of the conservation programme. To allow this to be taken into account, detailed assessments need to be made of these views, how they differ between individuals, and crucially, what beliefs and views are shared. These assessments require tools from both the natural and the social sciences. Here we focus on the beliefs, opinions and knowledge about Javan slow lorises in 12 Sundanese communities of West Java, Indonesia. Javan slow lorises are small, nocturnal, venomous primates that are threatened by habitat loss and over-exploitation for the illegal pet trade. Based on detailed interviews with 79 informants, and using cluster and cultural domain analyses, we identify and document five different topics, i.e. Trade and exploitation, Taboos against disturbing or capturing, Venomous primates, Blood myths and Mystical powers. The most salient topics were factual (activity pattern, habitat use) and the taboo on collecting or disturbing slow lorises. In communities where there were strong traditions, taboos and beliefs in place, slow lorises were found in seemingly unlikely habitats, in or adjacent to the villages; where these were absent slow lorises were less known to the communities and the slow lorises were either less abundant or absent. We conclude that it is imperative that any management programme or species action plan implemented in West Java has to take into account the traditions, beliefs and taboos regarding slow lorises.
Few primate species are known to excavate plant sources to procure exudates and other foods via active gouging. It is now apparent that slow lorises belong to this rare guild of obligate exudativorous primates. We investigate the diet of the pygmy loris (Nycticebus pygmaeus) in a mixed deciduous forest in the Seima Protection Forest, Eastern Cambodia, and attempted to determine the importance of this resource in their diet. Feeding behaviors of six females and seven males were observed using radio-tracking to facilitate follows, and nine fecal samples were collected in February–May and January–March in 2008 and 2009 respectively. We observed 168 feeding bouts, during which the animals ate exudates (76); fruits (33); arthropods (27); flower parts (21); fungi (3); parts of bamboo culms (7); and reptiles (1). We filmed 19 bouts of exudativory, and observed animals consuming exudates in an orthograde posture, or standing quadrupedally over the exudate source. Pygmy lorises also gouged bamboo to collect lichen and fungi, or broke open dead culms to access invertebrates. Feeding occurred on terminal tree branches (24), tree trunks (21), bamboo (13), the middle of branches (7), and the undergrowth (1). The fecal samples contained plant parts, small-sized arthropods (primarily Coleoptera and Lepidoptera), reptile scales, animal bones, and animal hairs. Pygmy slow lorises are morphologically specialized for processing and digesting exudates, displaying small body sizes, specialized dentitions, elongated, and narrow tongues, large caecums, short duodenums, expanded volar pads, and modified hindlimbs. These features, combined with the prevalence of exudates in their diet across seasons, and ill health when exudates are missing from their diet in captivity, points to this species being an obligate exudativore.
Neilson E, Nijman V, Nekaris KAI, 'Conservation Assessments of Arboreal Mammals in Difficult Terrain: Occupancy Modeling of Pileated Gibbons (Hylobates Pileatus)' International Journal of Primatology 34 (2013) pp.823-835
Long-term monitoring programs, wildlife surveys, and other research involving species population assessment require reliable data on population status. Given the logistically challenging nature of some species’ habitats and cryptic behaviors, collecting these data can prove to be a considerable barrier. We used detection/nondetection data from pileated gibbons (Hylobates pileatus) in the Cardamom Mountains of southwest Cambodia to estimate their population occupancy and detectability. We modeled occupancy using elevation, tree height, tree density, tree diversity, and disturbance covariates. Modeling demonstrated that 83% of the sites are occupied by Hylobates pileatus and that the detectability of the species varies positively with elevation. No clear relationship between habitat quality covariates and occupancy of Hylobates pileatus emerged. Effort analysis based on model estimates demonstrated that at high elevations, less than half the number of site visits is needed to attain the same detectability estimate precision as across all elevations. We suggest that human activities at low elevations, which affect forest composition, are the central factors impacting the detectability and occupancy of Hylobates pileatus. Longer sampling durations and/or a higher number of site visits, especially at lower elevations, increase precision of the occupancy estimator for the least effort. For effective future monitoring and research for this and similar species, using this relatively simple method, applied with repeat site visits, would allow a longitudinal comparison of detection at sites in difficult terrain.
Linking predator avoidance and social organisation predicts that large groups are favoured under heavy predation pressure but that small, inconspicuous groups may do equally well by avoiding detection altogether. We explored the relationships between antipredator behaviour (vocalisation, concealment, fleeing), detectability (colouration, group size) and social organisation in arboreal langurs. Three clear antipredation conditions emerged: (1) exemplified by Presbytis melalophos--brightly-coloured species (red, yellow) with contrasting colours, living in large unimale-multifemale groups (>10 individuals), that vocalised frequently and that flee loudly through the canopy; (2) exemplified by P. comata--greyish species (some contrasting colours), living in intermediate, unimale-multifemale or 1-male-1-female groups (approx. 7 individuals), that vocalise infrequently and that flee through the middle forest layers; (3) exemplified by P. frontata--dull-coloured species without contrast, living in small unimale-multifemale or 1-male-1-female groups (<5 individuals), that may freeze upon detection, and that may vocalise mainly during the night. Crypsis as an antipredator strategy is restricted to taxa that occur in 1-male-1-female groups. This wide range of antipredator strategies within a monophyletic taxon living in the same general area with a similar suite of predators facing similar predator pressures appears to be unique among the order Primates.
More species of nocturnal primates are now recognized than in the past, because many are cryptic species. Subtle morphological disparities, such as pelage pattern and color variation, vocal cues, and genetics have aided in elucidating the number of diagnosable species in a genus. The slow lorises (genus Nycticebus) once included only two species, but recent taxonomic studies resulted in the description of three additional species; further incompletely explored variability characterizes each of the currently described species. The Bornean loris in particular is characterized by pelage and body size variation. In this study, we explored facemask variation in the Bornean loris (N. menagensis). Differing facemask patterns, particularly influenced by the amount of white on the face, significantly clustered together by geographic regions, separated by notable geographic boundaries. Our results support the recognition of four species of Bornean lorises: N. menagensis, N. bancanus, N. borneanus, and N. kayan. Genetic studies are required to support these findings and to refine further our understanding of the marked variability within the Bornean loris populations.
Nekaris KA-I, Campbell N, Coggins TG, Rode EJ, Nijman V, 'Tickled to Death: Analysing Public Perceptions of ‘Cute’ Videos of Threatened Species (Slow Lorises – Nycticebus spp.) on Web 2.0 Sites' PLoS ONE 8 (7) (2013)
The internet is gaining importance in global wildlife trade and changing perceptions of threatened species. There is little data available to examine the impact that popular Web 2.0 sites play on public perceptions of threatened species. YouTube videos portraying wildlife allow us to quantify these perceptions.
Focussing on a group of threatened and globally protected primates, slow lorises, we quantify public attitudes towards wildlife conservation by analysing 12,411 comments and associated data posted on a viral YouTube video ‘tickling slow loris’ over a 33-months period. In the initial months a quarter of commentators indicated wanting a loris as a pet, but as facts about their conservation and ecology became more prevalent this dropped significantly. Endorsements, where people were directed to the site by celebrities, resulted mostly in numerous neutral responses with few links to conservation or awareness. Two conservation-related events, linked to Wikipedia and the airing of a television documentary, led to an increase in awareness, and ultimately to the removal of the analysed video.
Slow loris videos that have gone viral have introduced these primates to a large cross-section of society that would not normally come into contact with them. Analyses of webometric data posted on the internet allow us quickly to gauge societal sentiments. We showed a clear temporal change in some views expressed but without an apparent increase in knowledge about the conservation plight of the species, or the illegal nature of slow loris trade. Celebrity endorsement of videos showing protected wildlife increases visits to such sites, but does not educate about conservation issues. The strong desire of commentators to express their want for one as a pet demonstrates the need for Web 2.0 sites to provide a mechanism via which illegal animal material can be identified and policed.
Field primatologists search the archaeological record of tool-using primates to gain insight into their cultures and traditions. Similarly, researchers of primate communication have set up a linguistic framework to investigate its intricacies in the context of the evolution of human language and music.
Starr C, Nekaris K, Streicher U, Leung L, 'Field surveys of the vulnerable pygmy slow loris Nycticebus pygmaeus using local knowledge in Mondulkiri Province, Cambodia' Oryx: The International Journal of Conservation 45 (2011) pp.135-142
The pygmy slow loris Nycticebus pygmaeus is a little-studied primate endemic to Vietnam, Laos, southern China and eastern Cambodia. Our study aimed to gain local knowledge on the distribution and ecology of, and threats to, the species by interviewing hunters, traders and wildlife protection staff, and to verify this information using a spotlighting survey in three major reserves in Mondulkiri Province, Cambodia. Encounter rates of pygmy loris were assessed along 29 transects (129.5 km), yielding observations of 26 individuals. Mean encounter rates were 0.40 km-1 in Seima Protection Forest, 0.10 km-1 in Phnom Prich Wildlife Sanctuary and 0.00 km-1 in Mondulkiri Protected Forest. Informants had knowledge of where populations occurred, their diet, sociality and habitat preferences. Widespread large population declines were reported and informants linked this to high hunting pressure, particularly in 2001 and 2002. In late 2008 and 2009 we resurveyed three transects that had high encounter rates in early 2008 and failed to detect any lorises. Local informants reported high hunting pressure during the previous wet season in two of these sites, and a gold mine development was underway in the third site. Urgent actions are required to address these population declines and to assess the conservation status of pygmy lorises throughout eastern Cambodia.
Rode E, Nekaris K, Schwitzer C, Hoffman M, 'Mirza Zaza - preliminary conservation status assessment for the Data Deficient northern giant mouse lemur' Lemur News : the Newsletter of the Madagascar Section of the IUCN/SSC Primate Specialist Group (2011) pp.11-12
Trade in primates is seen as a significant impediment to their conservation. Primates are traded both domestically and internationally, in order to supply, amongst others, biomedical industries and pharmaceutical markets, the entertainment business, or pet markets. Primate meat is consumed globally, whereas body parts are used as ingredients in traditional medicine or sold as curios. All international trade in primates is regulated through the Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES), to which all but 2 primate range countries are signatory. The last 15 years has seen a linear increase in the export of live primates (each year 3500 more individuals are exported), with China being, numerically, the largest exporter. While the trade in live primates worldwide involves tens, if not hundreds, of thousands of individuals a year, the trade in dead primates involves millions of animals a year. We introduce here a series of studies dealing with various aspects of the primate trade. We hope that these studies will urge others to quantify the extent of trade in primates alive and dead in both domestic and international contexts, allowing us to find ways to mitigate the consequences of this trade to the conservation of primates.
Original habitat of animal species is being destroyed at an accelerating rate. This is usually associated with an alteration of the remaining habitat, which becomes degraded and/or fragmented. In many regions, forests are cleared to make way for plantations or other agricultural use, and animal species are forced to coexist with humans. In some countries, forests are in the process of being restored for wildlife. As even long-established and well-protected areas typically comprise mosaics of habitats with different degrees of degradation, the future conservation of many species will depend on the capacity of such altered habitats to support their populations. During the last 15 yr, more and more studies have addressed the way that different species respond to the human-induced change of their habitats. These responses are varied, and range from population decline to adaptation and development of new behavioural strategies. Whereas some species rely heavily on intact primary forests, others can adapt to secondary forests and forest-agriculture mosaics. Habitat change has been shown to affect many aspects of the ecology and behaviour of animals. Changes in dietary composition and diversity, population density, group size and adult sex ratio in groups are some examples. This Theme Section of Endangered Species Research collates a number of case studies on how animals, and particularly primates, respond to the alteration of their habitat.
The resolution of the ambiguity surrounding the taxonomy of Aotus means data on newly classified species are urgently needed for conservation efforts. We conducted a study on the Panamanian owl monkey (Aotus zonalis) between May and July 2008 at three localities in Chagres National Park, located east of the Panama Canal, using the line transect method to quantify abundance and distribution. Vegetation surveys were also conducted to provide a baseline quantification of the three habitat types. We observed 33 individuals within 16 groups in two out of the three sites. Population density was highest in Campo Chagres with 19.7 individuals/km2 and intermediate densities of 14.3 individuals/km2 were observed at Cerro Azul. In la Llana A. zonalis was not found to be present. The presence of A. zonalis in Chagres National Park, albeit at seemingly low abundance, is encouraging. A longer‐term study will be necessary to validate the further abundance estimates gained in this pilot study in order to make conservation policy decisions.
Nijman V, Nekaris K, 'Effects of deforestation on attitudes and levels of tolerance towards commensal primates (Cercopithecidae) in Sri Lanka' International Journal of Pest Management 56 (2) (2010) pp.153-158
Attitudes of people to wildlife, particularly to animals that live in close proximity to them, are an important element of conservation efforts and management. Attitudes may vary according to age and levels of conflict. We assessed the influence of proximity of forest on the attitudes of people towards two commensal primates, the purple-faced langur and the toque macaque. Data were collected in Sri Lanka by interviews in three villages where there is no continuous forest remaining and in three villages with adjacent forest. We found high levels of tolerance towards commensal primates, but significantly higher levels of negative perceptions in villages where forest was no longer present. Perceptions were not related to age or sex. The total disappearance of forest, with primates being dependent on fruit crops and living permanently on the village grounds, inevitably leads to conflict. These changing views have important management implications. Animals surviving in a human-dominated landscape may become more common, and the experiences in Sri Lanka may provide insight into what the future holds for other sites.
Nekaris K, Shepherd C, Starr C, Nijman V, 'Exploring cultural drivers for wildlife trade via an ethnoprimatological approach: a case study of slender and slow lorises (Loris and Nycticebus) in South and Southeast Asia' American Journal of Primatology 72 (10) (2010) pp.877-886
Illegal and unsustainable trade in wildlife is a major conservation challenge. For Asian primates, economic and cultural traditions, and increased forest access mean that trade may have become detrimental for certain species. Slow and slender lorises (Nycticebus and Loris) are primates particularly prevalent in trade, determined until now by focused counts of lorises in regional markets. Here, we use international trade statistics and a participant-observer approach to assess culturally specific drivers for trade in lorises in South and Southeast Asia, to provide a broader context to help mitigate this practice. Analysis of international records for the last 30 years revealed that live animal trade was more prevalent than trade in body parts (slow lorises, 86.4%; slender lorises, 91.4%), with Laos, Cambodia, and Thailand the largest exporters. We then examine drivers of international and domestic trade based on long-term data from 1994-2009 in Sri Lanka, Cambodia, and Indonesia. We show that slender lorises are important in Sri Lankan folklore, but their use as pets and for traditional medicine is rare. Trade in Bengal slow and pygmy lorises in Cambodia for use in traditional medicines, a practice with deeply historical roots, is widespread. Despite its own set of myths about the magical and curative properties of lorises, trade in Javan, Bornean, and greater slow lorises in Indonesia is largely for pets. Conservation practices in Asia are often generalized and linked with the region's major religions and economies. We show here that, in the case of wildlife trade, culturally specific patterns are evident among different ethnic groups, even within a country. Revealing such patterns is the foundation for developing conservation management plans for each species. We suggest some participatory methods for each country that may aid in this process.
Moore R, Nekaris K, Eschmann C, 'Habitat use by western purple-faced langurs Trachypithecus vetulus nestor (Colobinae) in a fragmented suburban landscape' Endangered Species Research 12 (3) (2010) pp.227-234
As natural habitats around the globe disappear, humans and non-human primates become increasingly engaged in complex interactions, both peaceful and hostile. Sri Lanka" s endemic western purple-faced langur Trachypithecus vetulus nestor persists in the majority of its range in complete sympatry with humans. Listed as Critically Endangered by the IUCN and one of the world" s top 25 most endangered primates, their survival appears dependent on the tolerance of humans with whom they coexist. Our aims were to augment the limited information on T. v. nestor focusing on group composition and behavioural adaptations in relation to its heavily fragmented habitat. Research was carried out in Talangama Wetlands, Sri Lanka in 2007. The 5 groups varied in size from 11 to 19 individuals Monkeys regularly used fences, rooftops, power lines, and agricultural trees. Two groups of 19 and 16 individuals had home ranges of 3.06 and 2.86 ha respectively. They consumed a variety of foods including fruits, showing dietary flexibility; the fruits and leaves of Arctocarpus heterophyllus were the langurs" most frequently consumed foods. The langurs seem to be adapting to these human-modified environments. Notwithstanding, areas for concern include potentially fatal dangers when crossing between fragments, increasing human-primate conflict and inter-group conflict, and permanent genetic isolation.
Crop-raiding by primates is increasingly known to cause conflict between humans and primates, and due to their opportunism, adaptability, intelligence and manipulative abilities, primates can be significant agricultural pests. Levels of crop-raiding are dependent on time of year, crop type, size and location of the farm, and primate species involved, making it difficult for farmers to predict susceptibility to crop-raiding accurately. We use a simple method for calculating the likelihood of crop damage by primates using crop susceptibility to predict the frequency of crop damage for individual farms. The method relies on calculating incidence rates of crop-raiding for individual crops using pooled data from all farms in the sample, and summing these rates as to reach a farm's risk value (RV) to primate crop-raiding. From 273 farms in southwestern Sri Lanka data were collected on crop-raiding by two species of primate, the arboreal folivorous purple-faced langur and the terrestrial frugivorous toque macaque. Data from 93 farms were used to calculate crop-raiding incidence rates for seven commonly grown crops, and we tested the applicability of the model using the remainder of the dataset. Incidence rates of raiding for crops differed for the two species of primate, albeit not in a uniform manner. Farms appear to be more susceptible to crop-raiding by langurs than by macaques, with higher RVs for langurs than for macaques: this is not related to the behaviour of the farmer as for both species four-fifth of the farmers that experience crop-raiding actively chase primates away. Our model using RVs works well for predicting crop-raiding in langurs as crop-raided farms have significantly higher RVs. It works less well for macaques, which may be related to their terrestriallity allowing them to range over larger areas and raid farms opportunistically.
Starr C, Nekaris K, Streicher U, Leung L, 'Traditional use of slow lorises Nycticebus bengalensis and N. pygmaeus in Cambodia: an impediment to their conservation' Endangered Species Research 12 (1) (2010) pp.17-23
In Cambodia, periodic reports since the 1990s have identified the sale of large numbers of dried pygmy Nycticebus pygmaeus and northern slow lorises N. bengalensis in traditional medicine stores. We used interviews and questionnaires to identify the uses and users of lorises, elucidate factors affecting selection of loris medicines, and determine whether access to alternative therapies may reduce the use of loris medicines. Pygmy lorises were found to be the most commonly requested animal from traditional medicine stores in Cambodia" s capital Phnom Penh, and the primary users recalled by sellers were women between the ages of 25 and 45 from middle to upper class backgrounds. Slow lorises were predominantly used in a tonic for women after childbirth, stomach problems, healing wounds and broken bones, and in the treatment of sexually transmitted diseases. Lorises were reported to be sourced from provinces with large protected areas within their distribution ranges. Market values of both species more than doubled from 1997 to 2007; however, the majority of respondents expressed reluctance to substitute loris medicines with alternatives, indicating that promotion of alternatives would be an inappropriate conservation tool. Education and enhanced law enforcement are vital to conserve slow lorises in Cambodia.
Thorn J S, Smith D, Nijman V, Nekaris K A I, 'Ecological niche modelling as a technique for assessing threats and setting conservation priorities for Asian slow lorises (Primates: Nycticebus)' Diversity and Distributions 15 (2) (2009) pp.289-298
Aim: Data on geographical ranges are essential when defining the conservation status of a species, and in evaluating levels of human disturbance. Where locality data are deficient, presence-only ecological niche modelling (ENM) can provide insights into a species' potential distribution, and can aid in conservation planning. Presence-only ENM is especially important for rare, cryptic and nocturnal species, where absence is difficult to define. Here we applied ENM to carry out an anthropogenic risk assessment and set conservation priorities for three threatened species of Asian slow loris (Primates: Nycticebus). Location: Borneo, Java and Sumatra, Southeast Asia. Methods: Distribution models were built using maximum entropy (MaxEnt) ENM. We input 20 environmental variables comprising temperature, precipitation and altitude, along with species locality data. We clipped predicted distributions to forest cover and altitudinal data to generate remnant distributions. These were then applied to protected area (PA) and human land-use data, using specific criteria to define low-, medium- or high-risk areas. These data were analysed to pinpoint priority study sites, suitable reintroduction zones and protected area extensions. Results: A jackknife validation method indicated highly significant models for all three species with small sample sizes (n = 10 to 23 occurrences). The distribution models represented high habitat suitability within each species' geographical range. High-risk areas were most prevalent for the Javan slow loris (Nycticebus javanicus) on Java, with the highest proportion of low-risk areas for the Bornean slow loris (N. menagensis) on Borneo. Eighteen PA extensions and 23 priority survey sites were identified across the study region. Main conclusions: Discriminating areas of high habitat suitability lays the foundations for planning field studies and conservation initiatives. This study highlights potential reintroduction zones that will minimize anthropogenic threats to animals that are released. These data reiterate the conclusion of previous research, showing MaxEnt is a viable technique for modelling species distributions with small sample sizes.
In this study we describe tree hole characteristics and use by the hairy-eared dwarf lemur (Allocebus trichotis) to determine habitat needs, potential functions of tree holes and sleeping group composition. We radio-tracked 6 adult individuals between April and November 2007 in the Analamazaotra Special Reserve. Tree holes were 1-9 m high (median: 7 m), in living trees measuring 26-54 cm in diameter at breast height (median: 32 cm), and could be a limiting resource. Each individual used 4 or 5 tree holes and had high nest fidelity. Animals most often slept socially in mixed-sex groups of 2-6 individuals and occasionally shared a tree hole with white-tailed tree rats (Brachytarsomys albicauda). We identified two sleeping groups: one composed of 2 adult males, 2 adult females and 2 juveniles; one composed of at least 2 adult females and 2 juveniles. Although tree holes were generally group exclusive, some intergroup sleeping was observed. Tree holes could have antipredator and thermoregulatory functions. Further research into sleeping hole availability, nest use and the degree of niche separation or competition between sympatric Cheirogaleidae and other tree hole users (e.g. endemic rodents) is needed to assess better the conservation needs of these species.
Smith D, Thompson S, Nekaris K, 'An assessment of conservation initiatives and priorities, and the habitat risks of human land use to the primates (colobinae, hylobatidae and pongidae) of Kalimantan' Folia Primatologica 79 (5) (2008) pp.385-386
ISSN: 0015-5713 eISSN: 1421-9980
Nekaris K, Nijman V, 'Attention for Sri Lanken monkey paints a bleak picture yet gives a glimmer of hope' Oryx: The International Journal of Conservation 42 (2008) pp.487-488
Eschmann C, Moore R, Nekaris K, 'Calling patterns of Western purple-faced langurs (Mammalia: Primates: Cercopithecidea: Trachypithecus vetulus nestor) in a degraded human landscape in Sri Lanka' Contributions to Zoology 77 (2) (2008) pp.57-65
The study of calling patterns is a useful non-invasive method for determining population densities and the taxonomic relationships of rare or cryptic animal species. The Western purple-faced langur Trachypithecus vetulus nestor, endemic to Sri Lanka" s lowland rainforests, is severely impacted by forest fragmentation, with most remaining populations living almost completely in home gardens. Due to their shy nature, little is known about the behaviour of this subspecies; analysing the regular loud calls emitted by these langurs could allow for improvement of census techniques, clarification of their taxonomy, and an understanding of the impact of forest destruction on their behaviour. In 2007, we recorded the calling patterns of five male T. v. nestor at Talangama Wetlands. Time, duration, weather conditions, and stimulant of 253 calls were noted. Loud calls comprised three structural units: harsh barks, whoops and residuals. The average call contained 4 phrases and 3.8 residuals, was 38 seconds in length, had an average maximum frequency of 3.5 kHz, a formant frequency of 0.36 kHz, and a fundamental frequency of 0.2 kHz. Significant differences were found between individuals for the number of phrases and residuals within a call, two different phrase lengths, the formant frequency and the fundamental frequency. The earliest call occurred at 05:27 hrs, while the latest was made at 17:57 hrs. The greatest percentage of calls (73.5%) was heard in the morning (05:00-09:59 hrs), mostly stimulated by territorial battles with neighbouring troops. These results show that vocalisations can be used to distinguish individual males; as langurs are more often heard than seen, and most troops contain only a single adult male, vocalisations may be used to determine the number of troops in an area. Calls of this taxon also differed from the other subspecies, suggesting that they may be used to distinguish subspecies and their boundaries. Finally, calling behaviour differed from other subspecies. Deforestation may be a direct cause of different calling patterns. These baseline data form a valuable starting point for further studies of this Critically Endangered primate.
Nekaris K A I, Blackman G, Nijman V, 'Conservation implications of low encounter rates of five nocturnal primate species (Nycticebus spp.) in Asia' Biodiversity and Conservation 17 (4) (2008) pp.733-747
Five species of slow lorises were once considered to comprise a single strongly polymorphic species, Nycticebus coucang, ranging throughout South and Southeast Asia. The cryptic nature of these nocturnal primates has led to a lack of understanding of their distribution patterns and abundance. In short surveys, often few if any lorises are detected, meaning that the few available density estimates are from long-term studies. Based on new research in Sebangau National Park, Borneo, and compilation of survey data from other areas, we provide the first comparative abundance estimates for all five slow loris species: N. coucang occurred in significantly higher abundances (median encounter rate 0.80/km: n = 15), than N. bengalensis (0.26/km; n = 12), or N. javanicus (0.11/km: n = 2), N. menagensis (0.02/km: n = 3), and N. pygmaeus (0.13/km: n = 4). Abundance estimates in Sebangau (0.19/km) did not increase with increasing survey effort, but for all species and studies combined, study duration was positively correlated with abundance estimates. We did not find a relation between abundance and body mass, nor between abundance and latitude. Long-term studies are more likely to be conducted at sites where the species of interest is particularly plentiful. The data suggest that slow lorises occur at low abundances throughout much of their range, and some in larger social groups than previously assumed. We recommend taking into account the species" heterogeneous distribution (potentially requiring larger survey effort), their social structure, the use of red lights as opposed to white lights whilst surveying, and to make use of their vocalisations when surveying slow lorises.
Aldrich B, Molleson L, Nekaris K, 'Vocalizations as a conservation tool: an auditory survey of the Andean titi monkey Callicebus oenanthe Thomas, 1924 (Mammalia: Primates: Pitheciidae) at Tarangue, Northern Peru' Contributions to Zoology 77 (1) (2008) pp.1-6
Titi monkeys (Callicebus), morphologically cryptic primates, have been difficult to survey using traditional sighting-based line transect methods. Callicebus-species regularly engage in loud, ritualized singing bouts, which could allow for the use of alternate, potentially more accurate call-based survey methods to monitor populations. The Andean titi monkey, C. oenanthe, is endemic to a small region of northern Peru, an area subject to widespread and rapid deforestation and human colonization. We conducted a call-based survey of C. oenanthe at Tarangue, a 74 ha private reserve near Moyobamba. Triangulation of calls was used to map groups of titi monkeys on and around the reserve. 73 mapped calls were used to estimate the presence of between three and six groups per listening area - a total of 23 groups entirely or partially within the borders of Tarangue, yielding an estimated population density of 1.41 individuals per ha. Observations were much greater than those resulting from a visually-based survey conducted at Tarangue three years earlier. These higher estimates are probably not only due to this more suitable survey method; incessant destruction of habitat occurring in the area surrounding Tarangue may have caused the reserve to become a refuge for displaced individuals, with diminished opportunities for dispersal and establishment of new territories. Immediate measures to prevent further fragmentation within the Andean titi monkey" s geographic range are essential in order to allow the species to persist. We recommend the use of triangulation of calls for future surveys of titi monkeys.
Parker L, Nijman V, Nekaris K, 'When there is no forest left: fragmentation, local extinction, and small population sizes in the Sri Lankan western purple-faced langur' Endangered Species Research 5 (1) (2008) pp.29-36
The western purple-faced langur Trachypithecus vetulus nestor is a Critically Endangered primate endemic to Sri Lanka according to the International Union for Conservation of Nature (IUCN). Its population decline is inferred mainly due to vast habitat loss. Few recent data are available regarding its distribution or abundance. The aim of our study was to assess the conservation status of T. v. nestor throughout its known historical range by establishing presence/absence and correlating these data with semi-structured interviews determining human perceptions and threats. Twenty-six sites were investigated, with presence of T. v. nestor being confirmed at 11 and indicated through questionnaires only at 2 additional sites. The present distribution of T. v. nestor is severely fragmented both locally and regionally. More than half of the populations comprised 1 or 2 groupsonly and, being isolated in a matrix of urban landscapes, are close to unviable. Conflicts between local people and T. v. nestor were identified at such sites, where reports of troops crop-raiding gardensand plantations were associated with negative perceptions. Consequences for crop-raiding langurs ranged from shouting to (infrequently) shooting and killing by dogs. Negative views towards T.v. nestor were significantly related to the length of time they spent in anthropogenic landscapes, while more positive views were significantly associated with the length of time T. v. nestor spent in forested areas. Evidence of local extinctions means that the remaining, yet increasingly fragmented habitat of the highly arboreal T. v. nestor is critical for survival. Intervention to manage this human-wildlife conflict is vital. An integrated approach using international and local conservation authorities is highly recommended.
The unique slow-climbing quadrupedalism of Asian lorises has been the subject of numerous studies; however, qualitative observations of more rapid locomotion have occasionally been reported. Field studies of the red slender loris have revealed the habitual use of unexpectedly high-speed locomotion by the so-called -œsloth of the primate world.- Novel video footage permitted the first quantitative kinematic analysis of rapid quadrupedalism in wild lorises. Observations revealed that this previously unexplored behavior is far from infrequent, with 26% of red slender loris locomotor activity being dedicated to high-velocity arboreal quadrupedalism. This locomotor pattern may represent a primitive retention of the rapid, scrambling quadrupedalism that is observed in other strepsirhines, or it may constitute a more recent specialization of this smallest loris taxon.
Since the 1950s, Sundaland (Borneo, Java, Sumatra and their surrounding islands) was thought to be inhabited by a single slow loris species, the greater slow loris Nycticebus coucang. Early taxonomies as well as recent morphological and genetic studies, however, point to at least three species native to this region: N. coucang, N. menagensis, and N. javanicus. In the light of this taxonomy, all Sundaland slow lorises, previously considered Least Threatened, have been listed as Vulnerable or Endangered. Of particular concern is the fact that slow lorises are the
most common protected primate species in the rampant Southeast Asian pet trade, resulting in their recent transferral to CITES Appendix I precluding all international commercial trade. Due to lack of knowledge regarding morphological differences between the three species, they are still managed as one, with potential serious affects to wild populations, as hard-release of individuals of unknown geographic origin is common. This paper examines morphological variability of 34 live slow lorises, all of
which were rescued from the wildlife trade in Java, Indonesia. Morphometric data and diagnostic images were collected, various species descriptions were considered and statistical analyses were conducted and compared with other taxonomists" classifications. A discriminant function analysis provided support for four distinct groupings: Nycticebus coucang and N. javanicus, as well as evidence for two new taxa that correspond closely to N. hilleri and N. ornatus. The morphological traits that varied
signifi cantly and the external characteristic trends described in this study that contributed to these groupings might provide a baseline to classify Nycticebus taxa. This information is pertinent for appropriate captive management and specifi c designation of rescued individuals and for designing proper in-situ and ex-situ conservation strategies.
Nekaris K, 'Social lives of adult Mysore slender lorises (Loris lydekkerianus lydekkerianus)' American Journal of Primatology 68 (12) (2006) pp.1171-1182
Despite the persistent use of the word 'solitary' to describe nocturnal primate social behavior, increasing numbers of studies are revealing sophisticated levels of social interactions among nocturnal primates. This study explores the relationships among 11 adult Mysore slender lorises (Loris lydekkerianus lydekkerianus) studied over 101/2 months in Tamil Nadu, India. When all observations regarding dependent offspring are excluded, the animals spent on average 38% of their activity in various forms of neutral, affiliative, and agonistic behaviors. Affiliative behaviors were the most common type of social interaction, and males in general were more social than females. Low values for Cole's index (CI) of association emphasize that females rarely interacted with same-sex conspecifics, but commonly interacted with males. In turn, males also formed strong affiliative relationships with other adult males. This index also indicates that levels of affiliation are strongest among animals that share sleeping sites. The Hinde index (HI) suggests that males control proximity to females more than the reverse. A female's tolerance of multiple males in her home range and at a sleeping site may be related to high spatial variability of food resources. Such resources may constrain females with costly reproductive strategies (up to two sets of twins per annum) to a small home range. With their larger home ranges, males may be able to monopolize females by initiating social interactions, and also provide a benefit to females by contributing to parental care.
Few data are available on gibbon populations in peat-swamp forest. In order to assess the importance of this habitat for gibbon conservation, a population of Hylobates agilis albibarbis was surveyed in the Sabangau peat-swamp forest, Central Kalimantan, Indonesia. This is an area of about 5,500 km2 of selectively logged peat-swamp forest, which was formally gazetted as a national park during 2005. The study was conducted during June and July 2004 using auditory sampling methods. Five sample areas were selected and each was surveyed for four consecutive days by three teams of researchers at designated listening posts. Researchers recorded compass bearings of, and estimated distances to, singing groups. Nineteen groups were located. Population density is estimated to be 2.16 (±0.46) groups/km2. Sightings occurring either at the listening posts or that were obtained by tracking in on calling groups yielded a mean group size of 3.4 individuals, hence individual gibbon density is estimated to be 7.4 (±1.59) individuals/km2. The density estimates fall at the mid-range of those calculated for other gibbon populations, thus suggesting that peat-swamp forest is an important habitat for gibbon conservation in Borneo. A tentative extrapolation of results suggests a potential gibbon population size of 19,000 individuals within the mixed-swamp forest habitat sub-type in the Sabangau. This represents one of the largest remaining continuous populations of Bornean agile gibbons. The designation of the Sabangau forest as a national park will hopefully address the problem of illegal logging and hunting in the region. Further studies should note any difference in gibbon density post protection.
Members of the Order Primates are characterised by a wide overlap of visual fields or optic convergence. It has been proposed that exploitation of either insects or angiosperm products in the terminal branches of trees, and the corresponding complex, three-dimensional environment associated with these foraging strategies, account for visual convergence. Although slender lorises (Loris sp.) are the most visually convergent of all the primates, very little is known about their feeding ecology. This study, carried out over 10 ½ months in South India, examines the feeding behaviour of L. lydekkerianus lydekkerianus in relation to hypotheses regarding visual predation of insects. Of 1238 feeding observations, 96% were of animal prey. Lorises showed an equal and overwhelming preference for terminal and middle branch feeding, using the undergrowth and trunk rarely. The type of prey caught on terminal branches (Lepidoptera, Odonata, Homoptera) differed significantly from those caught on middle branches (Hymenoptera, Coleoptera). A two-handed catch accompanied by bipedal postures was used almost exclusively on terminal branches where mobile prey was caught, whereas the more common capture technique of one-handed grab was used more often on sturdy middle branches to obtain slow moving prey. Although prey was detected with senses other than vision, vision was the key sense used upon the final strike. This study strongly supports the notion that hunting for animal prey was a key ecological determinant in selecting for visual convergence early on in primate evolution. The extreme specialisations of slender lorises, however, suggest that early primates were not dedicated faunivores and lend further support to the emerging view that both insects and fruits were probably important components of the diet of basal primates, and that exploitation of fruits may account for other key primate traits.
In 2001 and 2002, surveys of slender lorises were carried out in Sri Lanka, providing the first recent information on four taxa (Loris lydekkerianus nordicus, L. l. grandis, L. tardigradus tardigradus, and L. t. nycticeboides) endemic to the island. Thirty-one sites across five ecological zones were surveyed. Approximately 766 km were covered in 17 areas where no lorises were found; 192 km were walked or motored in 14 sites yielding 185 sightings of Loris: L. l. nordicus (n=111), L. t. tardigradus (n=69), L. l. grandis (n=4), and L. t. nycticeboides (n=1). Density estimates, based on sightings of animals/km, were: L. t. tardigradus (0.86-13 animals/km) and L. l. nordicus (0.33-50 animals/km). Significantly fewer sightings occurred within protected areas than were made outside of them. Animal densities varied across habitat type with the highest density of lorises occurring in the dry zone in monsoon forests. Presence of Loris is positively associated with insect presence, and negatively associated with primary forest with little undergrowth; taxa differ in their ability to thrive on the edge of human habitations. Human-induced threats include habitat loss, electrocution on live wires, road accidents, the pet trade, and use in traditional medicine. Further behavioural and ecological studies are needed to estimate the habitat requirements for the different taxa of slender loris.
We studied the feeding ecology of the Mysore slender loris (Loris lydekkerianus lydekkerianus) for 10.5 mo in a dry scrub forest at Ayyalur Interface Forestry Division, Tamil Nadu, South India. We recorded and analyzed 1240 feeding incidents, which indicate that the lorises were almost exclusively faunivorous, with 96% of all feeding events representing animal prey. Of prey items that could be identified (n = 605), 62.9% were ants and termites. Lorises fed on ge9 orders and 17 families of insects, plus spiders, molluscs, and small vertebrates. Lorises infrequently fed on gums and a legume pod. They usually grabbed prey with one hand, while other appendages firmly held the substrate. Many of the identifiable prey items belong to insect taxa likely to contain toxic chemicals. Consumption of insects inferred to be toxic was accompanied by an elaborate behavioral repertoire of sneezing, slobbering and urine-washing. A high proportion of insects eaten by slender lorises (71%) occurred in patches or aggregations. The utilization of aggregated social insects may have implications for understanding the unusually high degree of gregarious behavior exhibited by the lorises.
Nekaris K, 'Observations of Mating, Birthing and Parental Behaviour in Three Subspecies of Slender Loris (Loris tardigradus and Loris lydekkerianus ) in India and Sri Lanka' Folia Primatologica 74 (2003) pp.312-336
Studies of the life history parameters of slender lorises in captivity have led to conflicting results regarding gestation length, birth seasonality, interspecies variation in litter size and the degree of parental care given to offspring. During the course of field studies of Loris lydekkerianus lydekkerianus, L. l. nordicus and L. tardigradus tardigradus, data were collected on these life history variables, as well as on behaviours relating to mating. All 3 taxa displayed courtship behaviour involving the pursuit of a female by multiple males. Mating corresponded closely with captive observations, with a period of prolonged single intromissions lasting 3-11 min. One gestation period of 163 days was calculated for L. l. lydekkerianus. Births for all 3 taxa were distributed throughout the year, and males were seenmating throughout the year. All 3 taxa gave birth to singletons and twins; no subspecific pattern in litter size was evident. Females carried infants for the first 4 weeks of life and were regularly attended by males, which groomed both the mother and her offspring. After infants had been parked, female L. l. lydekkerianus and L. l. nordicus rarely returned before dawn, though males visited and played with infants. Female L. t. tardigradus maintained proximity with their infants, whilst males were not observed in proximity to infants during the night. All 3 taxa slept in social groups. High-energy milk, in combination with male care, may aid in the potentially high reproductive output of 4 infants per year.
Loris lydekkerianus lydekkerianus has been shown to have a promiscuous copulatory pattern, to maintain social networks via frequent loud calls, to interact socially throughout the night with all age classes, and to sleep socially. Though these behaviors point towards a multimale social system, no study of their spacing system has yet been provided to support this view. From October 1997-August 1998, I conducted a study of the Mysore slender loris in Ayyalur, India. During 1,400 field hours, data were collected on range use of 3 adult females, 3 adult males, 1 subadult female, and 1 subadult male. Lorises slept in groups averaging 4 individuals, composed of an adult female, her offspring, and 1-2 adult and subadult males. Sleeping sites for three groups were located within 1.9 ha in the center of the study area. The minimum convex polygon in hectares encompassing each animal" s range was determined, as well as overlap among home ranges of individual lorises. Average home range sizes were: adult males, 3.6 ha 0.09; subadult/smaller males, 1.17 ha 0.26; and adult and subadult females, 1.59 ha 0.24. Male ranges overlapped with at least 2-3 other adult males (0.72 ha 0.23). Female ranges overlapped slightly with at least 2 other female ranges (0.22 ha 0.25). Male ranges overlapped those of at least 3 females (0.82 ha 0.51). Patterns of home range and sleeping site support previous suggestions of a multimale social system, similar to aye ayes and some galagos.
Both predator defense and feeding ecology models have been proposed to explain the relatively slow climbing locomotion of the Lorisinae. During a study of the socioecology of the Mysore slender loris (Loris tardigradus lydekkerianus) in Tamil Nadu, India, six categories of behavior and eleven different postures were recorded to estimate a general activity budget for the slender loris, and are examined here particularly in relation to slow climbing locomotor strategies. Reactions to potential predators are also described. The main study population was composed of 15 animals. Activity budgets were compiled in three ways: all instantaneous point samples collected over 1,173 h pooled (n = 13,717), the means of individual lorises (n = 15) and behavior at the moment of first contact (n = 357). No significant difference was found between these three data sets. Approximately 45% of the activity budget was spent in inactive behaviors including sitting vigilant, resting and sleeping. Foraging and traveling comprised nearly half the activity budget, with the rest of the time spent grooming. The most common postures assumed by lorises were sitting and quadrupedal walking. Individual lorises were relatively gregarious and spent up to half their activity budget with other animals. Unlike pottos and angwantibos, lorises did not freeze, head butt or drop from branches in reaction to potential predators, but either ignored them, fled or made loud calls. Cryptic and slow climbing locomotion were used before traveling on open ground between discontinuous substrates, thereby supporting hypotheses relating to predator pressure, and also before capturing fast moving insect prey, supporting hypotheses relating to diet. It is proposed that a divergence in foraging strategies between bushbabies and lorisines may be the best adaptive explanation for their behavioral and morphological differences, including predator defense mechanisms.
We integrate information from the fossil record, morphology, behavior and molecular studies to provide a current overview of lorisoid evolution. Several Eocene prosimians of the northern continents, including both omomyids and adapoids, have been suggested as possible lorisoid ancestors, but these cannot be substantiated as true strepsirhines. A small-bodied primate, Anchomomys, of the middle Eocene of Europe may be the best candidate among putative adapoids for status as a true strepsirhine. Recent finds of Eocene primates in Africa have revealed new prosimian taxa that are also viable contenders for strepsirhine status. Plesiopithecus teras is a Nycticebus-sized, nocturnal prosimian from the late Eocene, Fayum, Egypt, that shares cranial specializations with lorisoids, but it also retains primitive features (e.g. four premolars) and has unique specializations of the anterior teeth excluding it from direct lorisiform ancestry. Another unnamed Fayum primate resembles modern cheirogaleids in dental structure and body size. Two genera from Oman, Omanodon and Shizarodon, also reveal a mix of similarities to both cheirogaleids and anchomomyin adapoids. Resolving the phylogenetic position of these Africa primates of the early Tertiary will surely require more and better fossils. By the early to middle Miocene, lorisoids were well established in East Africa, and the debate about whether these represent lorisines or galagines is reviewed. Neontological data are used to address the controversial branching sequences among extant lorisid clades. Data from the skin and scent glands, when integrated with other lines of evidence, suggest that Asian and African lorisines share a common lorisine ancestry. The hypothesis of an African clade containing both pottos and galagos to the exclusion of Asian lorisines is less tenable. True galagines are found in the fossil record of Namibia, while true lorisines are known from the Miocene of Asia. The hypothetical branching sequences can be integrated with behavioral and morphological features to develop an adaptive model of lorisoid divergence. By specializing on two different foraging modes early in their radiation, lorisines and galagines subsequently underwent a chain of integrated evolutionary changes eventually having an impact on many components of locomotor behavior, anatomy, physiology, reproduction, life history, and social behavior. Ongoing evolutionary studies of extant galagines are illuminating population phenomena and processes of speciation in an ecological context.
Furry and wide-eyed, lorises and pottos are small, nocturnal primates inhabiting African, Asian and Southeast Asian tropical and subtropical forests. Their likeable appearance, combined with their unusual adaptations - from a marked reduction of the tail to their mostly slow, deliberate locomotion, powerful grasping and, in some species, a venomous bite - has led to a significant rise in research interest in the family Lorisidae over the last decade. Furthermore, lorises in particular have featured frequently in international media largely due to illegal trade, for example as pets. This is the first volume to present a full picture of the breadth of research being undertaken on lorisids to aid future studies as well as conservation efforts. Focusing on five key topics: evolutionary biology, ecomorphology, behavioural ecology, captive management and conservation, this book is a vital read for graduate students and researchers in primatology, biological anthropology, evolutionary biology, animal behaviour and conservation.
Building on the success of the first edition and bringing together contributions from a range of experts in the field, the second edition of this guide to research on wild primates covers the latest advances in the field, including new information on field experiments and measuring behaviour. It provides essential information and advice on the technical and practical aspects of both field and laboratory methods, covering topics such as ethnoprimatology; remote sensing; GPS and radio-tracking; trapping and handling; dietary ecology; and non-invasive genetics and endocrinology. This integrated approach opens up new opportunities to study the behavioural ecology of some of the most endangered primates and to collect information on previously studied populations. Chapters include methodological techniques; instructions on collecting, processing and preserving samples/data for later analysis; ethical considerations; comparative costs; and further reading, making this an invaluable tool for postgraduate students and researchers in primatology, behavioural ecology and zoology.
Nekaris K, Starr C, Collins R, Wilson A, 'Comparative Ecology of Exudate Feeding by Lorises (Nycticebus, Loris) and Pottos (Perodicticus, Arctocebus)' in The Evolution of Exudativory in Primates, Springer (2010)
The Evolution of Exudativory in Primates is the first edited volume to offer a comprehensive overview of this rare dietary niche in the primate order. Leading researchers in the field of primatology synthesize our current knowledge of the behavioral, socioecological, nutritional, morphological, and evolutionary aspects of exudate-feeding in primates. The Evolution of Exudativory in Primates covers exudate-feeding in callitrichines, callimicos, mouse lemurs, lorises, and galagos. Advances in our understanding of how these animals obtain their food and digest it, how this food resource affects social relationships, and how morphology is related to exudate-feeding are presented in subsequent essays. The final chapter synthesizes current data on what role exudate-feeding may have played in the earliest primates, the plesiadapiforms, and what exudate-feeding signals may be present in the fossil record. Ideal for upper-level undergraduate and graduate primatology courses, The Evolution of Exudativory in Primates can also be used for courses in biology, comparative mammalogy, and conservation. About the Editors: ANNE M. BURROWS is an Associate Professor in the Department of Physical Therapy at Duquesne University and a Research Associate Professor in the Department of Anthropology at the University of Pittsburgh. She has worked on the functional and evolutionary morphology of the primate craniofacial complex with a focus on strepsirrhines. LEANNE T. NASH is a Professor of Anthropology in the School of Human Evolution and Social Change at Arizona State University. She has worked extensively with a captive colony of Galago senegalensis held previously at ASU for 20 years. She has also done fieldwork in Africa and Madagascar on baboons, galagos, and sportive lemurs. Other collaborations have been on captive chimpanzee behavior with the Primate Foundation of Arizona.
Featuring forty-seven original essays by seventy leading researchers, Primates in Perspective, Second Edition, offers a comprehensive and contemporary overview of all major areas of primatology. Thoroughly revised and updated throughout, the second edition offers a diversity of theoretical positions on such topics as reproduction, ecology, and social behavior and intelligence. Primates in Perspective, Second Edition, is ideal for introductory primatology courses and can also be used in upper-division behavior and conservation courses. Additionally, it is an essential reference for primate researchers.
Nekaris K, Munds R, 'Using Facial Markings to Unmask Diversity: The Slow Lorises (Primates: Lorisidae: Nycticebus spp.) of Indonesia' in , Springer (2010) Abstract
The slow lorises (Nycticebus) are the only strepsirrhine primates found in Indonesia (Nekaris and Bearder 2007). In addition to features such as a toothcomb and moist nose, these small nocturnal primates were given their name based on their trademark steady, stealthy, and fluid locomotion. Morphologically incapable of leaping (Sellers 1996), slow lorises rather slither through the treetops, and if startled, they may freeze or even cover their face, resulting in one of their many Indonesian names, malu malu or -œthe shy one- (Supriatna and Wahyono 2000). Alternatively, they can fleetingly but silently escape, resulting in the name buah angin or -œwind monkey- in Acehnese (Nekaris and Nijman 2007a). One of two genera of nocturnal primates found in Indonesia (the other being Tarsius), slow lorises are a unique part of Indonesian primate communities, and are widely spread on at least 27 of Indonesia" s islands, including Borneo, Sumatra, and Java (Table 22.1) (Nijman and Nekaris in press). Despite this, studies of Indonesian slow lorises are in their infancy.
Since the 1960s, primatologists have recognized the impact of predation on the evolution of morphology, the social systems and cognitive behavior of monkeys and apes, but few studies considered its impact on the prosimians - lemurs, lorises, galagos and tarsiers. This comprehensive volume, written by experts in the field, narrows this gap by highlighting the effect of predation on the order Primates in general. Theoretical approaches to understanding how primates perceive predation threat, as well as proximate and ultimate causes to address threat and attack, are considered across the primate order. Although this volume concentrates on the least known group in this theoretical area - the prosimians - contributions by researchers on numerous primate taxa across four major geographical regions make this a novel and exciting contribution to students interested in primate evolution and ecology.
Nekaris K, Gursky S, 'Theoretical perspectives of primate anti-predator behaviour' in Primate Anti-Predator Strategies, Springer (2007)
Since the 1960s, primatologists have recognized the impact of predation on the evolution of morphology, the social systems and cognitive behavior of monkeys and apes, but few studies considered its impact on the prosimians - lemurs, lorises, galagos and tarsiers. This comprehensive volume, written by experts in the field, narrows this gap by highlighting the effect of predation on the order Primates in general. Theoretical approaches to understanding how primates perceive predation threat, as well as proximate and ultimate causes to address threat and attack, are considered across the primate order. Although this volume concentrates on the least known group in this theoretical area - the prosimians - contributions by researchers on numerous primate taxa across four major geographical regions make this a novel and exciting contribution to students interested in primate evolution and ecology.
Bearder S, Nekaris K, Buzzell C, 'Dangers in the Dark: are some noctural primates afraid of the dark?' in Eat or be Eaten: Predator Sensitive Foraging Among Primates, Cambridge University Press (2002)
This volume brings together primary data from a variety of primate species living in both natural habitats and experimental settings, and explores the variables that may play a role in primates' behavioral strategies. Taken together, these studies demonstrate that predator sensitive foraging is relevant to many primates, of various body sizes and group sizes and living in different environments. Eat or be Eaten encourages further discussion and investigation of the subject and will make fascinating reading for researchers and students in primatology, ecology, and animal behavior.
Nijman V, Nekaris KAI, 'Assessing Conflict Between Humans and Commensal Non-human Primates in Sri Lanka Following An Ethnoprimatological Approach', (2013)
Nekaris KAI, Pambudi JAA, Ahmad RD, Susanto D, Raharjo B, Nijman V, 'Densities, Distribution and Detectability of a Small Nocturnal Primate (javan Slow Loris Nycticebus Javanicus) in a Montane Rainforest', (2013)
Nijman V, Pambudi JA, Achmed D, Nekaris KA, 'Densities, Distribution and Detectability of a Small Nocturnal Primate (Javan Slow Loris Nycticebus Javanicus) in a Montane Rainforest', (2013) Abstract
Nocturnal mammals can be challenging to survey and, especially for many species
that live in dense forest habitats, limited information is available on densities and distributions. We surveyed the endemic Javan slow loris Nycticebus javanicus in the montane forests of Mount Gede Pangrango, West Java, Indonesia. Surveys were conducted on 23 transects (260 h covering some 93 km) walking at variable speeds between 200 and 800 m h−1. Densities on individual transects varied from 0 to 52 ind. km−2, with an overall density of 15.6 ind. km−2 (95% CI 9.7 to 25.2 ind. km−2). Encounter rates per kilometre were strongly influenced by the speed at which transects were walked, with fewer lorises detected at higher speeds. This effect was absent when considering encounter rates per hour. Detectability and behavior of Javan slow lorises were not affected by the amount of lunar light and, in contrast to studies of some of their congeners, we found no evidence of lunar phobia or lunar philia. Our study shows that slow lorises are not homogeneously distributed in their montane habitat and occur at intermediate densities. However, encounter rates did not differ between disturbed and primary forest. Analysis of data from multiple surveys of lorisforms, including this one, reveals no statistically significant relationship between survey effort or the speed at which transects are walked and estimated densities, but speed is positively correlated with encounter rates.
Lehtinen J, Nekaris KAL, Nijman V, Coudrat C, Wirdateti, 'Distribution of the Javan Slow Loris (Nycticebus Javanicus): Assessing the Presence in East Java, Indonesia', (2013)
Munds RA, Nekaris KAI, Nijman V, Goossens B, 'Living Together in the Night: Abundance and Habitat Use of Sympatric and Allopatric Populations of Slow Lorises and Tarsiers (Nycticebus and Tarsius).', (2013) Abstract
Throughout much of Asia slow lorises (Nycticebus) and tarsiers (Tarsius) live allopatrically but on several islands they occur in sympatry. As habitats dwindle, competition for resources may increase within the area of sympatry. An understanding of how they are coping with competition is necessary for conservation measures. To address this we gathered data on the abundances and vertical strata preferences of slow loris and tarsier species from the literature. We predict sympatric species will favour different heights from congeners. Allopatric species will have lower abundances compared to sympatric species. In addition, we studied tarsiers and lorises in sympatry in Sabah, Borneo. We estimated abundances of Bornean lorises (Nycticebus menagensis) and Western tarsiers (Tarsius bancanus borneanus) and investigated habitat use. Through the literature review we found lorises do not vary in densities, whether allopatric or sympatric. Abundances of sympatric and allopatric tarsiers were significant (sympatric: 3-27 individuals/km2, allopatric: 57-268 individuals/ km2). Vertical strata use of sympatric and allopatric tarsier populations was not significant, but was for sympatric and allopatric loris populations (p=0.036). On a small scale estimated densities of Bornean lorsies were 5.105 slow lorises/km² and 3.646 individuals/km² for Western tarsiers. Slow lorises favoured the upper and middle level of the forest (10-30 m) and tarsiers the lower levels (<5 m). In our analysis of vegetation plots we found that tree heights and diameter at breast height preferences differed between genera. Results indicate sympatric genera are able to share their nocturnal environment due to niche separation.
Nijman V, Nekaris KAI, Bickford DP, 'Asian Medicine: Small Species at Risk', (2012)
Nijman V, Nekaris KAI, 'Diurnal Eagles As Predators of Primates in Asia', (2012)
Svensson MS, Nijman V, Nekaris KAI, 'In Situ and Ex Situ Conservation of African Pottos and Angwantibos: Where Are We and Where Do We Need to Go?', (2012) Abstract
Despite a large geographic distribution, the African nocturnal perodicticines, pottos (Perodicticus) and angwantibos (Arctocebus ) remain amongst the least studied primate taxa. Only two one-year field studies have been conducted on pottos, with only circumstantial data onangwantibos, coming from field data on shot animals. Through a meta-analysis, based on published literature and unpublished reports, we here review recent skeletal and genetic evidence that point to five species, and indicate far more diversity: Perodicticus potto, P. Ibeanus, P. edwardsi, Arctocebus aureus, A. calabarensis. Pelage colour, dorsal markings and tail characteristics (for pottos) supplement the genetic data that suggest these comprise distinct taxa. Arctocebus ranges from Nigeria and Cameroon in the north to Gabon and Congo in the south, whilst Perodicticus is more widespread, having a combined distribution that encompasses a large portion of central and western Africa. Despite this large range, only nine surveys with any substantial effort have been published in the last twenty years from only five range countries; two re-ported new taxa (P. p. stockleyi and P. p. juju). Although not included in abundance counts,pottos frequently appear in bushmeat reports throughout their range, suggesting this is a realthreat to this cryptic, easy-to-catch primate. Despite an almost complete dearth of knowledgeabout these taxa, all perodicticine taxa are listed on the IUCN Red List of Threatened Species as Least Concern, with, contradictorily, only the reasonably studied P. p. stockleyi as Data Deficient. The situation of these primates is mirrored in zoos. No Arctocebus are kept in European zoos, with only 17 Perodicticus in ISIS institutions. Their taxonomy is uncertain, breeding rates are poor and infant mortality is high. Clearly the perodictines offer an open frontier for both in situ and ex situ studies. We certainly do not have the data to assess their conservation status yet.