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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.
Primates are traded yearly in the tens of thousands for reasons such as biomedical research, as trophies and pets, for consumption and to be used in traditional medicine. In many cases, this trade is illegal, unsustainable and considered a major impediment to primate conservation. Diurnal primates make up the vast majority of this trade, but recent studies have found that the trade in nocturnal primates is more common than previously thought, and among them are the galagos. There are currently 19 galagos recognized but there is still a dearth of research on these species and subspecies. The purpose of our study was to provide a more comprehensive picture of the trade in galagos within and across their African range countries, to help determine whether it is illegal or its sustainability needs to be assessed, and to provide baseline data and management recommendations to better regulate this trade, including strengthening policy, enforcement and conservation interventions. We gathered information on trade and use of galagos using an online questionnaire (May–August 2020), and on country-specific legislation relating to wildlife trade, hunting and legal protection of galagos, and looked at each range country’s Corruption Perception Index score to gain an understanding of the obstacles in the way of effective law enforcement. We received 140 responses to our online questionnaire, from 31 of the 39 galago range countries. Respondents from 16 of these countries reported on first-hand observations of galagos being traded or used. Out of these, 36% reported seeing galagos sold or used for consumption, 33% as pets and 25% had observed them sold or used for traditional practices (including medical and magical purposes and for witchcraft). Most reports came from West Africa followed by Central Africa, East Africa and Southern Africa. We found that the number of reports on galagos being traded was higher in countries with higher numbers of galago species. Countries with more restrictive legislation experienced a higher number of reports of trade. Galagos observed in the pet trade was more common in East Africa, whilst reports of them in the bushmeat trade were more common in Central and West Africa. Galagos observed in the trade for traditional practices was by far most common from West Africa. We found that all galago range countries have some level of legal protection for some or all of their native galago species. It is evident that use and trade of galagos occurs throughout their range, albeit localized to certain areas. We urge galago range countries to adequately protect all species and to ensure legal trade is effectively regulated. Range countries that prohibit the use and trade in galagos must ensure legislation is adequately enforced. Further research into the drivers behind the use and trade of galagos should be initiated in countries with high levels of use and trade to further inform conservation and policy actions and to catalyze enforcement actions against poaching and illegal trade.
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.
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.
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.
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.
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.
The switch from hunting wild meat for home consumption to supplying more lucrative city markets in Amazonia can adversely affect some game species. Despite this, information on the amounts of wild meat eaten in Amazonian cities is still limited. We estimated wild meat consumption rates in 5 cities in the State of Amazonas in Brazil through 1046 door‐to‐door household interviews conducted from 2004 to 2012. With these data, we modeled the relationship between wild meat use and a selection of socioeconomic indices. We then scaled up our model to determine the amounts of wild meat likely to be consumed annually in the 62 urban centers in central Amazonia. A total of 80.3% of all interviewees reported consuming wild meat during an average of 29.3 (CI 11.6) days per year. Most wild meat was reported as bought in local markets (80.1%) or hunted by a family member (14.9%). Twenty‐one taxa were cited as consumed, mostly mammals (71.6%), followed by reptiles (23.2%) and then birds (5.2%). The declared frequency of wild meat consumption was positively correlated with the proportion of rural population as well as with the per capita gross domestic product of the municipality (administrative divisions) where the cities were seated. We estimated that as much as 10,691 t of wild meat might be consumed annually in the 62 urban centers within central Amazonia, the equivalent of 6.49 kg per person per year. In monetary terms, this amounts to US$21.72 per person per year or US$35.1 million overall, the latter figure is comparable to fish and timber production in the region. Given this magnitude of wild meat trade in central Amazonia, it is fundamental to integrate this activity into the formal economy and actively develop policies that allow the trade of more resilient taxa and restrict trade in species sensitive to hunting.
Like other nocturnal primates, many species of galago (Galagidae) are phenotypically cryptic, making their taxonomic status difficult to resolve. Recent taxonomic work has disentangled some of the confusion. This has resulted in an increase in the number of recognised galago species. The most widespread galago species, and indeed the most widespread nocturnal primate, is the northern lesser galago (Galago senegalensis) whose geographic range stretches >7,000 km across Africa. Based on morphology, 4 subspecies are currently recognised: G. s. senegalensis, G. s. braccatus, G. s. sotikae and G. s. dunni. We explore geographic and subspecific acoustic variation in G. senegalensis, testing three hypotheses: isolation by distance, genetic basis, and isolation by barrier. There is statistical support for isolation by distance for 2 of 4 call parameters (fundamental frequency and unit length). Geographic distance explains a moderate amount of the acoustic variation. Discriminant function analysis provides some degree of separation of geographic regions and subspecies, but the percentage of misdesignation is high. Despite having (putative) parapatric geographic ranges, the most pronounced acoustic differences are between G. s. senegalensis and G. s. dunni. The findings suggest that the Eastern Rift Valley and Niger River are significant barriers for G. senegalensis. The acoustic structures of the loud calls of 121 individuals from 28 widespread sites are not significantly different. Although this makes it unlikely that additional unrecognised species occur within G. senegalensis at the sites sampled, vast areas of the geographic range remain unsampled. We show that wide-ranging species do not necessarily exhibit large amounts of variation in their vocal repertoire. This pattern may also be present in nocturnal primates with smaller geographic ranges.
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.
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.
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.
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.
We report on the illegal trade in ivory and elephant parts in the Special Development Zone of Mong La, Shan State, Myanmar, on the border with China. Mong La caters exclusively for the Chinese market and is best described as a Chinese enclave in Myanmar. We surveyed the morning market, shops and hotels in Feb 2006, Feb 2009 and Dec 2013-Jan 2014. Trade in body parts primarily concerned dried elephant skin (4 pieces in 2006, 278 in 2009 and 1,238 in 2013-2014), and to a lesser extent molars and bones. We found 3,494 pieces of carved ivory (none in 2006, 200 in 2009 and 3,294 in 2013-2014) and 49 whole tusks (all in 2013-2014) openly for sale, suggesting Mong La has recently emerged as a significant hub of the ivory trade. The origin of the ivory may constitute a combination of Asian elephant ivory from Myanmar and African ivory imported via China. According to local sources the carving was done by Chinese craftsmen, in Mong La as well as across the border in China, and was largely, if not exclusively, intended for the internal Chinese market. Based on asking prices of the most commonly offered items the retail value of the ivory on display in Mong La during the 2013-2014 survey totals an estimated US$1.2 million. Trade in elephant parts and elephant ivory is illegal in Myanmar and CITES I listing of elephants preclude international trade in them. Mong La is governed largely autonomously by an overlord and policed by an Eastern Shan State army. We urge both the Myanmar and Chinese governments to liaise with the Mong La rulers to curb the trade in ivory (and other high profile species), and recommend that the Myanmar and Chinese CITES authorities come together urgently as to resolve the illicit trade of ivory and elephant parts across their borders.
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.
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.
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.
Conserving a species depends on an understanding of its habitat requirements. Primatologists often characterize the habitat requirements of primates using macroscale population-based approaches relying on correlations between habitat attributes and population abundances between sites with varying levels of disturbance. This approach only works for species spread between several populations. The populations of some primates do not fulfill these criteria, forcing researchers to rely on individual-based (microscale) rather than population-based approaches for habitat characterization. We examined the reliability of using micro-scale habitat characterizations by studying the microhabitat preferences of a group of wild western hoolock gibbons (Hoolock hoolock) in order to compare our results to the habitat preferences of western hoolock gibbons identified during a macroscale study of populations across Bangladesh. We used stepwise discriminant analysis to differentiate between the areas of low, medium, and high usage based on microhabitat characteristics (tree species availability, altitude, canopy connection, distance from forest edge, and levels of human disturbance). The gibbons used interior forest habitat with low food tree availability most frequently for sleeping and socializing, and used edge habitat containing high food tree availability for medium periods for feeding. These results indicate that the gibbons prefer interior forest but are frequently forced to visit the forest edge to feed. Therefore, the optimal habitat would be interior forest away from human disturbance with high sleeping-tree and feeding-tree availability. These habitat preferences are consistent with the habitat attributes of Bangladesh's largest remaining western hoolock gibbon populations, which live in areas containing low agricultural encroachment and high food-tree availability. Microhabitat use studies can be used to characterize the habitat requirements of a species, but should include multiple scales of analysis wherever possible.
In our paper about the phylogeny of the open-habitat chat complex inadvertently the GenBank accession numbers of all newly generated sequences presented in Table 1 were left out. We here provide a corrected version of this Table. We would like to apologize for any inconvenience this may have caused to the readers of the journal.
Recently Dela (International Journal of Primatology, 28 (2007): 607–626; International Journal ofPrimatology, 33 (2012): 40–72) published her study from the mid-1980s on the diet of purple-faced langurs Trachypithecus (Semnopithecus) vetulus in village gardens and rubber plantations. Unlike studies from the 1970s that reported the species, like other colobines, to be largely folivorous with few ripe fruits eaten, Dela found them to be largely frugivorous. The frequent feeding on ripe fruits challenges the paradigm that colobine digestive adaptations restrict the use of ripe fleshy fruits. No reference was made to any other post-1970s study on the species. Here I provide a concise overview of more than a dozen studies conducted in the 1990s and 2000s that show that 1) other populations live in similar human-modified environments showing feeding adaptations as reported by Dela, 2) these populations rely largely on cultivated crops and feed heavily on fruits, 3) living in these situations introduces them to additional threats. Especially in western Sri Lanka little natural habitat remains and deforestation has led the langurs to exchange the forest jungle for the urban jungle, with power lines, fences, walls, and roofs being used instead of trees. The main fruits that provide a staple for langurs in these areas are jackfruit (Artocarpus heterophyllus), banana (Musaspp.), and mango (Mangifera indica); studies in undisturbed habitats and indeed Dela’s own study suggest the heavy use of human-edible fruits by langurs may not necessarily indicate preferential selection of these food sources. Living in human-modified environments makes the langurs more prone to infection with gastrointestinal parasites, and may lead to death by electrocution or being killed by guard dogs. The large degree of agreement between studies suggest that feeding on ripe fruits from cultivars is not unique to Dela’s two study groups and shows that some langur groups are able to survive for extended periods on uncolobine-like diets when they cannot access their preferred foods.
Open-habitat chats (genera Myrmecocichla, Cercomela, Oenanthe and relative) are a morphologically and ecologically cohesive group of genera with unclear phylogenetic relationships. They are distributed mostly in open, arid and/or rocky habitats of Africa and Eurasia. Here, we present the most comprehensive molecular phylogenetic analysis of this group to date, with a complete taxon sampling at the species level. The analysis, based on a multilocus dataset including three mitochondrial and three nuclear loci, allows us to elucidate the phylogenetic relationships and test the traditional generic limits. All genera are non-monophyletic, suggesting extensive convergence on similar plumage patterns in unrelated species. While the colour pattern appear to be a poor predictor of the phylogenetic relationships, some of the ecological and behavioural traits agree relatively well with the major clades. Following our results, we also propose a revised generic classification for the whole group.
Background International wildlife trade is one of the leading threats to biodiversity conservation. The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) is the most important initiative to monitor and regulate the international trade of wildlife but its credibility is dependent on the quality of the trade data. We report on the performance of CITES reporting by focussing on the commercial trade in non-native reptiles and amphibians into Thailand as to illustrate trends, species composition and numbers of wild-caught vs. captive-bred specimens. Methodology/Principal Findings Based on data in the WCMC-CITES trade database, we establish that a total of 75,594 individuals of 169 species of reptiles and amphibians (including 27 globally threatened species) were imported into Thailand in 1990-2007. The majority of individuals (59,895, 79%) were listed as captive-bred and a smaller number (15,699, 21%) as wild-caught. In the 1990s small numbers of individuals of a few species were imported into Thailand, but in 2003 both volumes and species diversity increased rapidly. The proportion of captive-bred animals differed greatly between years (from 0 to >80%). Wild-caught individuals were mainly sourced from African countries, and captive-bred individuals from Asian countries (including from non-CITES Parties). There were significant discrepancies between exports and imports. Thailand reports the import of >10,000 individuals (51 species) originating from Kazakhstan, but Kazakhstan reports no exports of these species. Similar discrepancies, involving smaller numbers (>100 individuals of 9 species), can be seen in the import of reptiles into Thailand via Macao. Conclusion/Significance While there has been an increase in imports of amphibian and reptiles into Thailand, erratic patterns in proportions of captive-bred specimens and volumes suggests either capricious markets or errors in reporting. Large discrepancies with respect to origin point to misreporting or possible violations of the rules and intentions of CITES.
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.
We report on the international trade in South American poison arrow frogs (Dendrobatidae) in the period 2004-2008, and focus on the role of Asian countries. All species of dendrobatid frogs are included in Appendix II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), regulating all commercial trade in these species. Based on data compiled in the WCMC CITES database, we establish that[63,000 dendrobatid frogs (of 32 species) were traded internationally. For 21 species the majority of individuals were reported as captive-bred. A quarter to a fifth of the commercial trade in dendrobatid frogs in terms of volume is destined for Asian markets (mainly Japan, Thailand and Taiwan, Province of China). Kazakhstan, the main supplier for the Thai market, is reported as a source country for 16 species, all captivebred. We found large discrepancies between the reported export of dendrobatid frogs from Kazakhstan-”none-”and imports reported by Thailand as coming from Kazakhstan ([2,500 individuals). A significant part of the trade flow goes via Lebanon, a non-CITES Party. We urge the CITES Management Authorities of the countries involved to investigate the trade in dendrobatid frogs to ensure it does not violate the rules and intentions of CITES.
International wildlife trade remains a leading threat to biodiversity conservation and is a common vector for infectious diseases and invasive species that also affect agriculture, livestock, and public health. With 175 member countries, the Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES) is the most important global initiative to monitor and regulate international trade of plants and animals. CITES regulates trade of nearly 34,000 species and has reduced threats associated with overharvest of imperiled species for international trade. Credible biological and trade data are core to informing decisions and garnering political will and consensus among CITES parties. This does not preclude party bargaining, as occurred during the March 2010 Conference of Parties (CoP) debate over bluefin tuna. Nevertheless, CITES decisions are also frequently hindered by a lack of basic data. We highlight CITES limitations and describe potential solutions related to systematic data collection, rigorous data analysis, flexible research methods, and peer review.
For comparative primatology proper recognition of basal taxa (i.e. species) is indispensable, and in this the choice of a suitable gene with high phylogenetic resolution is crucial. For the goals of species identification in animals, the cytochrome c oxidase subunit 1 (cox1) has been introduced as standard marker. Making use of the difference in intra- and interspecific genetic variation - the DNA barcoding gap - cox1 can be used as a fast and accurate marker for the identification of animal species. For the Order Primates we compare the performance of cox1 (166 sequences; 50 nominal species) in species-identification with that of two other mitochondrial markers, 16S ribosomal RNA (412 sequences, 92 species) and cytochrome b (cob: 547 sequences, 72 species). A wide gap exist between intra- and interspecific divergences for both cox1 and cob genes whereas this gap is less apparent for 16S, indicating that rRNAgenes are less suitable for species delimitation in DNA barcoding. For those species where multiple sequences are available there are significant differences in the intraspecific genetic distances between different mitochondrial markers, without, however, showing a consistent pattern. We conclude that cox1 allows accurate differentiation of species and as such DNA barcoding may have an important role to play in comparative primatology.
Background Bornean orangutans (Pongo pygmaeus) currently occur at low densities and seeing a wild one is a rare event. Compared to present low encounter rates of orangutans, it is striking how many orangutan each day historic collectors like Alfred Russel Wallace were able to shoot continuously over weeks or even months. Does that indicate that some 150 years ago encounter rates with orangutans, or their densities, were higher than now? Methodology/Principal Findings We test this hypothesis by quantifying encounter rates obtained from hunting accounts, museum collections, and recent field studies, and analysing whether there is a declining trend over time. Logistic regression analyses of our data support such a decline on Borneo between the mid-19th century and the present. Even when controlled for variation in the size of survey and hunting teams and the durations of expeditions, mean daily encounter rates appear to have declined about 6-fold in areas with little or no forest disturbance. Conclusions/Significance This finding has potential consequences for our understanding of orangutans, because it suggests that Bornean orangutans once occurred at higher densities. We explore potential explanations-”habitat loss and degradation, hunting, and disease-”and conclude that hunting fits the observed patterns best. This suggests that hunting has been underestimated as a key causal factor of orangutan density and distribution, and that species population declines have been more severe than previously estimated based on habitat loss only. Our findings may require us to rethink the biology of orangutans, with much of our ecological understanding possibly being based on field studies of animals living at lower densities than they did historically. Our approach of quantifying species encounter rates from historic data demonstrates that this method can yield valuable information about the ecology and population density of species in the past, providing new insight into species' conservation needs.
Aim: Asian elephants, Elephas maximus, are threatened throughout their range by a combination of logging, large scale forest conversion and conflict with humans. We investigate which environmental factors, both biotic and abiotic, constrain the current distribution of elephants. A spatially explicit habitat model is constructed to find core areas for conservation and to assess current threats. Location: Ulu Masen Ecosystem in the province of Nanggroe Aceh Darussalam on the island of Sumatra, Indonesia. Methods: A stratified survey was conducted at 12 sites (300 transects) to establish the presence of elephants. Presence records formed the basis to model potential habitat use. Ecological niche factor analysis (ENFA) is used to describe their niche and to identify key factors shaping elephant distribution. An initial niche model was constructed to describe elephant niche structure, and a second model focused on identifying core areas only. To assess the threat of habitat encroachment, overlap between the elephants' optimal niche and the occurrence of forest encroachment is computed. Results: Elephants were recorded throughout the study area from sea level to 1600 m a.s.l. The results show that the elephant niche and consequently habitat use markedly deviates from the available environment. Elephant presence was positively related to forest cover and vegetation productivity, and elephants were largely confined to valleys. A spatially explicit model showed that elephants mainly utilize forest edges. Forest encroachment occurs throughout the elephants range and was found within 80% of the elephants' ecological niche. Main conclusions: In contrast to general opinion, elephant distribution proved to be weakly constrained by altitude, possibly because of movement routes running through mountainous areas. Elephants were often found to occupy habitat patches in and near human-dominated areas. This pattern is believed to reflect the displacement of elephants from their former habitat.
Understanding the complex relationship between primates and their habitats is essential for effective conservation plans. Peat-swamp forest has recently been recognized as an important habitat for the Southern Bornean gibbon (Hylobates albibarbis), but information is scarce on the factors that link gibbon density to characteristics of this unique ecosystem. Our aims in this study were firstly to estimate gibbon density in different forest subtypes in a newly protected, secondary peat-swamp forest in the Sabangau Catchment, Indonesia, and secondly to identify which vegetation characteristics correlate with gibbon density. Data collection was conducted in a 37.1 km2 area, using auditory sampling methods and vegetation speed plotting. Gibbon densities varied between survey sites from 1.39 to 3.92 groups/km2. Canopy cover, tree height, density of large trees and food availability were significantly correlated with gibbon density, identifying the preservation of tall trees and good canopy cover as a conservation priority for the gibbon population in the Sabangau forest. This survey indicates that selective logging, which specifically targets large trees and disrupts canopy cover, is likely to have adverse effects on gibbon populations in peat-swamp forests, and calls for greater protection of these little studied ecosystems.
Tarsiers (Tarsius) and slow lorises (Nycticebus) are the only extant nocturnal primates occurring in Southeast Asia. Harcourt (1999) hypothesized that in insular Southeast Asia, slow lorises and tarsiers showed a checkerboard distribution on 12 small (<12,000 km2) islands, i.e., only one or the other occurs, and attributed this to extreme levels of competition between these 2 largely faunivorous primates. Further, he predicted slow lorises were able to persist on smaller islands than tarsiers. We re-evaluated these findings using an expanded dataset including 49 islands where tarsiers or slow lorises occur. Tarsiers and slow lorises live on islands of similar size (median size of ca. 300-900 km2), and both taxa inhabit an equal proportion of small, medium, and large islands. On small islands within their area of sympatry tarsiers occur on 1 island, slow lorises on 8, both genera on 3, and we can assume they have become extinct from 11 small islands since the Last Glacial Maximum. Sizes of islands where tarsiers or slow lorises have become extinct do not differ from islands where they are still extant. We show that slow lorises occur on more islands in insular Southeast Asia than perhaps previously assumed, but these islands are not smaller on average than islands where tarsiers occur. A checkerboard distribution between these taxa is not evident. More studies are needed at the macroecological level to assess the importance of biogeographic history in explaining their present-day distribution patterns.
We present data on ~600 gibbons in 22 zoos and 9 wildlife rescue centres and reintroduction centres in western Indonesia based on surveys conducted from 2003 to 2008. All gibbon species are protected by Indonesian law and cannot legally be kept as pets. Gibbons rarely breed successfully in Indonesian zoos, and the vast majority of animals present in these collections originate from the illegal wildlife trade, having been donated to the zoos by the public or brought in by Indonesian authorities after being confiscated from dealers or private owners. Gibbons in rescue and rehabilitation centres also derive largely from donations or confiscations. The surveys provide insight into the volume and species composition of gibbons in trade. All 7 species of gibbon that occur naturally in Indonesia were observed, with the highest numbers (130 ind.) being for the siamang Symphalangus syndactylus. About 100 ind. each for Bornean and Sumatran agile gibbons Hylobates albibarbis and H. agilis, Javan gibbon H. moloch and MÃ¼ller" s gibbon H. muelleri were present, but only a handful of white-handed H. lar and Kloss" gibbons H. klossi. No gibbons that do not occur in Indonesia were recorded. Numbers of the different species in trade appear to be positively related to their numbers in the wild. Trade in Sumatra and Borneo appears to be confined to species naturally occurring there, but all species are traded on Java. About twice as many gibbons were taken in by the respective institutions following confiscations by the Indonesian authorities compared to gibbons received as donations by the public. However, prosecution of offenders is rare, and given the large scale of the gibbon trade, we urge the Indonesian authorities to increase efforts to enforce wildlife protection laws.
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.
This study describes significant levels of trade in 2 or possibly 3 species of night monkeys (Aotus nancymaae, A. vociferans and A. nigriceps) from the Brazil-Colombia-Peru tri-border area. All 3 countries are Party to the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) and there is no documented trade in night monkeys among these 3 countries in the CITES trade database. However, interviews with 43 traders/collectors in 11 communities in the 3 countries suggest that for the period 2007-2008, ca. 4000 night monkeys were traded, representing a monetary value of over USD 100000 for the traders and intermediaries. The interviewees indicated that the animals were sold to a biomedical laboratory in the tri-border area on the Colombian side of the border. The international nature of the trade and the large volume of night monkeys being traded indicate a violation of, and a failure to adhere to, international trade regulations. In order to conserve these important species, we suggest cooperative action from environmental and conservation authorities and the respective CITES Management Authorities in Colombia, Peru and Brazil to curb the trade, and urge the Colombian authorities to investigate the illegal importation of night monkeys by a biomedical laboratory in the border area.
Increasingly identification of primate samples relies on molecular techniques. DNA barcoding, focussing on the mitochondrial cytochrome c oxidase subunit I, gains popularity as a universal species-identifier. Problems with conventional DNA barcoding include degradation in archival specimens and processed material (food products) and samples stored in DNA-unfriendly preservatives (formalin), preventing the recovery of PCR fragments >200 bp. Mini-barcodes may resolve these problems. We test the validity of mini-barcodes as a way of identifying (archaic) human and non-human primates, based on 540 sequences of 87 species deposited in GenBank. A 648 bp section was selected and a series of mini-barcodes (108 to 324 bp) were generated. Neighbour-joining trees were compiled for each mini-barcode, relying on bootstrap values to assess accuracy of species identification. The full sequence provided unambiguous support (bootstrap values ≥99%) for 68 (78.2%) species. Efficiency of mini-barcodes reached a maximum of 96.8% (mean 96±1.11%) for the 324 bp barcodes, 84.8% (mean 80.6±3.41%) for the 162 bp barcodes, and 78.8% (mean 67%±6.54%) for the 108 bp barcodes. Problem taxa, which did not provide unambiguous identification for any length of barcode, included those that frequently hybridise in nature, those close in evolutionary terms and those who have seen recent taxonomic change. The terminal 3’ end performed marginally better than the proximal 5’ end. We conclude that mini-barcodes in the order of 160-300 bp can be effective in identifying primates, especially when focussing on the terminal end. Mini-barcodes provide a feasible option for DNA barcode analysis of museum samples and applied diagnostics.
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.
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.