Project

Primate Conservation

Goal: We are a group of researchers, students, and alumni interested in primate conservation and that are linked to the MSc in Primate Conservation at Oxford Brookes University in the UK.
As a network we aim to improve our knowledge of primates, their conservation needs, and to assess and implement actions and policies that will benefit primates, their habitats, and the people that live side-by-side with primates.

Methods: Genetics, Conservation, Evolution, Natural Resource Management, MAXENT, Behavioral Observation, Convention on International Trade in Endangered Species of Wild Fauna and Flora

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Sam Pottie
added a research item
Many primate species have been observed descending to the forest floor to intentionally consume soil (geophagy) at licks. The practice of geophagy is assumed to provide health benefits, such as mineral supplementation and/or gastrointestinal tract protection. We collected data on geophagy events through the use of camera traps at Tambopata National Reserve in southeastern Peru. Two geophagy sites were monitored for 42 months, during which time we observed repeated geophagy events by a group of large-headed capuchin monkeys (Sapajus apella macrocephalus). To the best of our knowledge, this is the first report of its kind for the species. Geophagy was rare, with only 13 events recorded over the study period. All but one event took place during the dry season, and 85% of events took place in the late afternoon between 1600 and 1800 hours. The monkeys were observed consuming soil both in situ and ex situ, and displayed heightened vigilance behavior during geophagy events. Although the small sample size makes it difficult to draw clear conclusions as to the drivers of this behavior, the seasonal timing of the events and the high percentage of clay in the consumed soils suggest that these events are linked to the detoxification of secondary plant compounds in the monkeys' diet.
Brooke Aldrich
added a research item
The cryptic nature of the titi monkey is referred to repeatedly throughout the literature on Callicebus, and is often fingered as the reason for exaggeratedly low density estimates. Genus Callicebus is, however, highly vocal, engaging daily in ritualized bouts of song that function to define and reinforce the boundaries of strictly maintained territories. This high audibility could be used as a conservation tool, for surveying and monitoring populations that are difficult to locate visually. The Andean titi monkey, Callicebus oenanthe, is endemic to a tiny region of Northern Peru which is facing high rates of human colonization and attendant deforestation. I conducted a song-based survey of the population of C. oenanthe at Tarangue, a 74 ha private reserve near Moyobamba. Triangulation of song was used to map groups of titi monkeys on and around the reserve, and resulted in a estimated population density of 1.4 individuals per ha-a much higher estimate than that resulting from a visually-based survey conducted three years earlier. Loud calls and bouts of song were recorded and a brief investigation into the vocal repertoire of the species was conducted. Many of the call types of Callicebus cupreus appear to have homologous call types in C. oenanthe at Tarangue. Several additional call types were tentatively identified. More recordings and research are necessary to describe the vocal repertoire of C. oenanthe in further detail. Several different colourations and unexpected social groupings are described for the individuals sighted at the reserve. Approximately 20% of observed groups consisted of between six and eight individuals, which is unusually Callicebus oenanthe at Tarangue iii large for Callicebus. It may be that the incessant destruction of habitat occurring in the area surrounding Tarangue has caused the reserve to become a refuge for displaced individuals, and that opportunities for dispersal and establishment of new territories are few or non-existent. Immediate measures to prevent further destruction or fragmentation within the Andean titi monkey's small geographic range is essential, soon, in order to allow the species to persist. Such measures could include increased financial and logistical support of organizations like Ikamaperou, who own and protect Tarangue. Additionally, larger tracts of habitat could be purchased, protected and managed by large, influential international conservation organizations.
Chris R Shepherd
added a research item
The Black Crested Macaque Macaca nigra (Desmarest) is a Critically Endangered species endemic to Indonesia. Populations are in decline due to habitat loss and hunting for the wild meat and exotic pet trade. International trade data involving this species is lacking, though anecdotal information suggests it is being smuggled to the Philippines. To verify this, we conducted online and physical market surveys of publicly accessible wildlife facilities in the Philippines and analysed seizure data for M. nigra in Indonesia and the Philippines from 2010 to 2019. This study reveals insights into illegal trade in M. nigra, which is enabled by laundering illegally sourced animals through zoos and wildlife breeding facilities. Surveys of publicly accessible wildlife facilities in the Philippines confirmed the presence of at least 36 individuals in the country, and an additional 12 were exported from the Philippines to China in 2014-2015. The acquisition of this species by wildlife facilities such as zoos in the Philippines is a concern, as there are no records of legal export to the Philippines. We also documented evidence of smuggling of at least 30 M. nigra individuals to the Philippines through seizure analysis. These findings warrant further research and investigation by authorities to determine the origins of M. nigra in captive wildlife facilities to assess whether they were legally acquired and to prevent the laundering of illegally acquired wildlife.
Sam Pottie
added a research item
Howler monkeys Alouatta are almost exclusively arboreal. They will, however, occasionally descend to the forest floor to conduct geophagy at clay licks if these are present within their home range. They do this to incorporate certain minerals into their diet and/or for detoxification purposes. Clay licks are risky areas however, especially for arboreal mammals, as visiting them requires the monkeys to leave the safety of the trees. This has been confirmed by observed predation attempts on howler monkeys by large felines at clay licks. We report an additional risk for howler monkeys descending to the forest floor that has not previously been considered, namely potential attacks by collared peccaries Dicotyles tajacu. Camera traps were placed at three different clay licks in the Taricaya Ecological Reserve, located in the southeastern Peruvian Amazon, to monitor the fauna within the reserve. On 4 June 2017, the camera traps registered a lethal attack on a howler monkey by a group of collared peccaries at one of the clay licks.
Elena Račevska
added a research item
Tropical forests support a diversity of plants. Many of them are threatened, emphasising that their shared use by people and wildlife may benefit their conservation. Litt forests of southeast Madagascar, home to seven threatened lemur species, provide the Antanosy people with natural resources. In the early 2000s, protected areas were established in two regions that historically incurred different levels of anthropogenic pressures: Sainte Luce and Mandena. We explored the local use of plants as medicine, construction materials and firewood, and examined the overlap of plants used by people and the red-collared brown lemur (Eulemur collaris), the largest lemur in this ecosystem and an important seed disperser. Between July and October 2018, 60 adults (30 women, 30 men) participated in semi-structured interviews. Our findings show 122 plants are locally used as medicines, 60 as construction materials, and 71 as firewood. Of all utilitarian plants, 52 were confirmed in this lemur’s diet. Sainte Luce participants reported they used a higher diversity of species in all three categories. Western medicines were available and preferred to medicinal plants, but the choice also often depended on the health condition being addressed. Firewood was preferred to charcoal for cooking. Resource restrictions of the protected areas has negatively affected the local people. Local ethnobotanical knowledge reflects the importance of plants, while differences in plant use of the two communities reflect differences in biodiversity and socio-economic circumstances. Emphasising this interdependence, especially in forest restoration, could be a path towards conservation of plants, lemurs, and people, as well as traditional livelihoods.
Denise Spaan
added 3 research items
Commercial, off-the-shelf, multirotor drones are increasingly employed to survey wildlife due to their relative ease of use and ability to cover areas quicker than traditional methods. Such drones fitted with high-resolution visual spectrum (RGB) cameras are an appealing tool for wildlife biologists. However, evaluations of the application of drones with RGB cameras for monitoring large-bodied arboreal mammals are largely lacking. We aimed to assess whether Geoffroy’s spider monkeys (Ateles geoffroyi) could be detected in RGB videos collected by drones in tropical forests. We performed 77 pre-programmed grid flights with a DJI Mavic 2 Pro drone at a height of 10 m above the maximum canopy height covering 45% of a 1-hectare polygon per flight. We flew the drone directly over spider monkeys who had just been sighted from the ground, detecting monkeys in 85% of 20 detection test flights. Monkeys were detected in 17% of 18 trial flights over areas of known high relative abundance. We never detected monkeys in 39 trial flights over areas of known low relative abundance. Proportion of spider monkey detections during drone flights was lower than other commonly employed survey methods. Agreement between video-coders was high. Overall, our results suggest that with some changes in our research design, multirotor drones with RGB cameras might be a viable survey method to determine spider monkey presence in closed-canopy forest, although its applicability for rapid assessments of arboreal mammal species′ distributions seems currently unfeasible. We provide recommendations to improve survey design using drones to monitor arboreal mammal populations.
Forest loss due to anthropogenic activities is one of the main causes of plant and animal species decline. Studying the species’ population status (i.e., density, abundance, and geographic distribution) on a regular basis is one of the main tools to assess the effect of anthropogenic activities on wildlife, to monitor population dynamics and to intervene with effective conservation strategies when the population of an endangered species declines. On Sulawesi Island, Indonesia, anthropogenic activities, such as agriculture, are decreasing the remaining natural habitats available for several endemic and endangered species. The effect of this forest loss on the threatened moor macaques ( Macaca maura ) in South Sulawesi is unknown, and data on the population status of this species are needed to design effective conservation strategies. To assess the population status of the moor macaques, we walked linear transects (N = 29, survey effort = 114 km) at six sites between November 2019 and March 2020 to estimate macaque population density and encounter rate. We tested the effect of anthropogenic activities on macaque encounter rate. Our global density estimate (24 individuals/km ² ) was lower than the overall estimate from the most detailed survey conducted on this species, which covered its whole geographic distribution (36.1 individuals/km ² ). However, these results should be interpreted with caution because the previous density estimate falls within the confidence intervals of our estimate. Furthermore, we found regional declines in moor macaque encounter rates in at least two sites compared with previous studies. We found a high presence of anthropogenic activity in the forests inhabited by macaques. Moor macaques were less abundant in open areas with no forest (i.e., clear cuttings) than in forested areas, and in the presence of nonspecies-specific hunting traps (i.e., wire-loop traps). Moreover, moor macaques were more abundant in areas with a higher presence of humans and domestic animals. Overall, our data suggest that the population of this species may be declining in certain regions but further surveys are needed to corroborate whether this is occurring across the entire geographic distribution.
Deforestation impacts canopy connectivity when landscapes are fragmented due to roads and other types of linear infrastructure. Natural canopy bridges become vital to arboreal animals, especially for animals that are reluctant to use the ground. When canopy regrowth cannot occur, artificial canopy bridges have been implemented to mitigate the consequences of linear infrastructure. The aim of our study was to evaluate the evidence for the use of artificial canopy bridges by spider monkeys (Ateles spp.) to cross linear infrastructure that interrupts canopy connectivity. We report details of five cases in which the absence of evidence for spider monkeys using artificial canopy bridges to cross linear infrastructure was based on systematic monitoring. We examined the factors that may constrain spider monkeys to use artificial faunal overpasses and made recommendations for effective artificial faunal overpasses for spider monkeys.
Carter Payne
added a research item
One of the main threats to wild primates is habitat alteration, fragmentation and destruction. Therefore it is crucial to understand the ability of those species to adapt to human-induced habitat changes to prevent extirpation. Key to this is a species diet plasticity. In Paraguay over 91% of the Upper Paraná Atlantic Forest has been destroyed to expand agricultural land. We determined the diet composition of three Sapajus cay groups in degraded and near-pristine Atlantic Forest in eastern Paraguay to assess whether the diet composition of this species changes with habitat degradation. We accounted for diet variability associated with demographic traits and forest characteristics using multinomial linear models. Once the effect of age, sex, and season were accounted for, we found that the diet of capuchins was plastic and shifted to adapt to studied degraded forest conditions. The results showed that (as expected) the capuchins have a generalist and flexible diet, including opportunistically taking advantage of crop plants, particularly Slash Pine plantations, when the risks were lower. The capuchins ability to adjust their diet in different habitat fragments demonstrates that small islands of Paraguayan Atlantic Forest are valuable for their persistence. This insight can be used to create applied conservation strategies, such as using the existing Payment for Ecosystem Services (PES) legislation to provide an opportunity to begin reconnecting fragments using native trees bordered by Slash Pine plantations. Using the capuchins as an umbrella species would increase public support of the program, while compensation through the PES scheme and profiting from the timber would encourage landowner participation.
Matthew R McLennan
added a research item
Large animal species are most likely to survive human-induced rapid environmental change if they display high levels of behavioural flexibility. Examining social responses in species that form closely bonded social groups and display high fission–fusion dynamics, such as chimpanzees, Pan troglodytes, will help determine their resilience to dynamic human activities and the potential for sustainable human–wildlife interactions. Coinciding with the seasonal availability of cultivated jackfruit, Artocarpus heterophyllus, a dominant food available in croplands and village gardens, we examined the social adjustments of wild chimpanzees to risks presented by a human-modified landscape at Bulindi, Uganda. Absolute party size decreased when chimpanzees moved from low-risk ‘natural’ habitat (forest fragments) to high-risk ‘anthropogenic’ habitat (croplands and other village areas), driven mainly by parties containing fewer females. Using social network analysis, we found that chimpanzee social structure showed partial flexibility in response to anthropogenic risk. The strength of social ties in a 5 m proximity network stayed similar and individual centrality measures were correlated between low- and high-risk habitats. Nevertheless, in high-risk habitat males were more central than females and exclusively dominated the core of the network's core–periphery structure. However, sex differences were not apparent when we corrected for party membership, indicating that differences were driven by changes to party membership between habitat types rather than changes in social proximity within parties. We suggest that perception of anthropogenic risk can drive continual adjustments to grouping dynamics in response to changing conditions that modify social lives of male and female chimpanzees in different ways. Consequently, changes in grouping patterns induced by continuing anthropogenic change could impact ecological and evolutionary processes influenced by social structure, including cultural evolution and the spread of infectious disease.
Claire Cardinal
added a research item
Primatological research is often associated with understanding animals and their habitats, yet practical conservation depends entirely on human actions. This encompasses the activities of Indigenous and local people, conservationists, and NGOs working on the ground, as well as more remote funders and policymakers. In this paper we explore what it means to be a conservationist in the 2020s. While many primatologists accept the benefits of more socially inclusive dimensions of research and conservation practice, in reality there remain many challenges. We discuss the role primatologists can play to enhance interdisciplinary working and their relationships with communities living in and around their study sites, and examine how increased reflexivity and consideration of one’s positionality can improve primatological practice. Emphasis on education and stakeholder consultation may still echo colonial, top-down dialogues, and the need for greater emphasis on genuine knowledge-sharing among all stakeholders should be recognised. If we are sincere about this approach, we might need to redefine how we see, consider, and define conservation success. We may also have to embrace more compromises. By evaluating success in conservation we explore how reflexive engagements with our positionality and equitable knowledge-sharing contribute to fostering intrinsic motivation and building resilience.
Vincent Nijman
added 27 research items
Population viability analysis is a predictive procedure that uses a combination of different modelling approaches to estimate species vulnerability to extinction. Javan gibbons (Hylobates moloch) are vulnerable to local extinction primarily due to loss of habitat and hunting for the illegal pet trade. Using the modelling software VORTEX, we assessed the status of Javan gibbons in 3 areas (Ujung Kulon National Park, Halimun-Salak National Park, and Dieng Mountains) which hold over half of the remaining estimated number of gibbons on Java. Ujung Kulon and Halimun-Salak are long-time protected areas, whereas Dieng Mountains remain unprotected. For each area, we calculated the probability of extinction over a 100-year time period by testing different area-specific scenarios (e.g., hunting, deforestation, and increase in carrying capacity). Our modelling suggests each of the populations has a high chance of becoming extinct within the next 100 years if hunting and deforestation persist. If these threats are eliminated, the model shows each of the populations are large enough to persist in the long term whilst maintaining high levels of current genetic diversity. We conclude that specific actions should be implemented to develop more inclusive conservation management practices, especially improving awareness regarding the illegal wildlife trade and increased protection of wild populations and their habitats.
Nonhuman 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. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats— mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture , large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world's primates and the costs of their loss to ecosystem health and human society is imperative.
In a world increasingly dominated by human demand for agricultural prod- ucts, 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 impor- tance 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.
Timothy M. Eppley
added a research item
Given the current rate of habitat degradation and loss in the tropics, data on primate population densities and habitat use are indispensable for assessing conservation status and designing feasible management plans for primates. The Omo River guereza (Colobus guereza guereza) is a subspecies of the eastern black-and-white colobus monkey endemic to the western Rift Valley forests of Ethiopia. Their restricted distribution along with habitat loss and hunting within their range render them vulnerable to local extirpation and extinction. Furthermore, there are no published data available on the population status and habitat use patterns of the Omo River guereza. We therefore aimed to assess the population size of Omo River guerezas in diferent habitats (Erica-Juniperus mixed forest, mixed plantation forest, undisturbed natural forest, disturbed natural forest) using transect surveys at Wof-Washa Natural State Forest (WWNSF) in central Ethiopia. Our surveys covered a cumulative distance of 88.5 km in four diferent habitats, during which we recorded a total of 140 Omo River guereza groups. The average group density was 14.3 groups/km 2 , average individual density was 94.4 individuals/km , and we estimated the total population size within WWNSF to be 2549 individuals. The sex ratio of the population was split evenly between males and females, though the age classes skewed strongly towards adults. Of the habitats surveyed, the highest group encounter rate (1.83 groups/km) occurred in the disturbed natural forest. However, the highest individual density (110.1 individuals/ km 2 ) was recorded in undisturbed natural forest. Still, sizable densities (group and individual) were recorded in three of the disturbed habitats (disturbed natural forest, mixed plantation forest, and to a lesser extent Erica-Juniperus mixed forest). Our study ofers the irst baseline information with which to compare future population density estimates and habitat use in the range of Omo River guerezas.
Jordi Salmona
added a research item
Mouse lemurs (Microcebus) are a radiation of morphologically cryptic primates distributed throughout Madagascar for which the number of recognized species has exploded in the past two decades. This taxonomic revision has prompted understandable concern that there has been substantial oversplitting in the mouse lemur clade. Here, we investigate mouse lemur diversity in a region in northeastern Madagascar with high levels of microendemism and predicted habitat loss. We analyzed RADseq data with multispecies coalescent (MSC) species delimitation methods for two pairs of sister lineages that include three named species and an undescribed lineage previously identified to have divergent mtDNA. Marked differences in effective population sizes, levels of gene flow, patterns of isolation-by-distance, and species delimitation results were found among the two pairs of lineages. Whereas all tests support the recognition of the presently undescribed lineage as a separate species, the species-level distinction of two previously described species, M. mittermeieri and M. lehilahytsara is not supported - a result that is particularly striking when using the genealogical discordance index (gdi). Non-sister lineages occur sympatrically in two of the localities sampled for this study, despite an estimated divergence time of less than 1 Ma. This suggests rapid evolution of reproductive isolation in the focal lineages, and in the mouse lemur clade generally. The divergence time estimates reported here are based on the MSC calibrated with pedigree-based mutation rates and are considerably more recent than previously published fossil-calibrated relaxed-clock estimates. We discuss the possible explanations for this discrepancy, noting that there are theoretical justifications for preferring the MSC estimates in this case.
Jordi Salmona
added 4 research items
The geographic distribution of a species can provide insights into its population size, ecology, evolution, and how it responded to past (and may respond to future) environmental change. Improving our knowledge of the distribution of threatened species thus is a high priority in assessing their conservation status. However, there are few data available for many recently described yet understudied and potentially threatened primate taxa, making their conservation difficult. Here, we investigated the distribution of the Montagne d’Ambre fork-marked lemur, Phaner electromontis, a threatened nocturnal primate endemic to northern Madagascar and classified as Endangered by the IUCN. Because fork-marked lemurs are highly vocal, we used acoustic surveys to assess the species’ presence-absence and relative population density within 66 distinct forest survey sites in northern Madagascar. Further, we compared data among five forest types within the study area and investigated the relationship between relative population density and climate variables. We report the presence of P. electromontis in 22 study sites; several of these populations were unknown previously. Although we found P. electromontis most frequently in dry-transitional forests, our results suggest that geography (spatial autocorrelation) rather than environmental variables explains the species’ distribution. We hypothesize that environmental unpredictability and gummivory, combined with the presence of several distinct Phaner species in the studied area, could explain the observed distribution.
Delimitation of cryptic species is increasingly based on genetic analyses but the integration of distributional, morphological, behavioral, and ecological data offers unique complementary insights into species diversification. We surveyed communities of nocturnal mouse lemurs (Microcebus spp.) in five different sites of northeastern Madagascar, measuring a variety of morphological parameters and assessing reproductive states for 123 individuals belonging to five different lineages. We documented two different non‐sister lineages occurring in sympatry in two areas. In both cases, sympatric species pairs consisted of a locally restricted (M. macarthurii or M . sp. #3) and a more widespread lineage (M. mittermeieri or M. lehilahytsara ). Estimated Extents of Occurrence (EOO) of these lineages differed remarkably with 560 and 1,500 km² versus 9,250 and 50,700 km², respectively. Morphometric analyses distinguished unambiguously between sympatric species and detected more subtle but significant differences among sister lineages. Tail length and body size were most informative in this regard. Reproductive schedules were highly variable among lineages, most likely impacted by phylogenetic relatedness and environmental variables. While sympatric species pairs differed in their reproductive timing (M . sp. #3/M. lehilahytsara and M. macarthurii/M. mittermeieri ), warmer lowland rainforests were associated with a less seasonal reproductive schedule for M. mittermeieri and M. lehilahytsara compared with populations occurring in montane forests. Distributional, morphological, and ecological data gathered in this study support the results of genomic species delimitation analyses conducted in a companion study, which identified one lineage, M . sp. #3, as meriting formal description as a new species. Consequently, a formal species description is included. Worryingly, our data also show that geographically restricted populations of M . sp. #3 and its sister species (M. macarthurii ) are at high risk of local and perhaps permanent extinction from both deforestation and habitat fragmentation. Highlights • Two pairs of Microcebus species occur in partial sympatry. • Morphological distinctiveness supports genomic species delimitation in cryptic lemurs. • High plasticity in reproductive schedules in a lineage of habitat generalists detected.
Quaternary climatic changes have been invoked as important drivers of species diversification worldwide. However, the impact of such changes on vegetation and animal population dynamics in tropical regions remains debated. To overcome this uncertainty, we integrated high-resolution paleoenvironmental reconstructions from a sedimentary record covering the past 25,000 years with demographic inferences of a forest-dwelling primate species ( Microcebus arnholdi ), in northern Madagascar. Result comparisons suggest that climate changes through the African Humid Period (15.2 – 5.5 kyr) strongly affected the demographic dynamics of M. arnholdi . We further inferred a population decline in the last millennium which was likely shaped by the combination of climatic and anthropogenic impacts. Our findings demonstrate that population fluctuations in Malagasy wildlife were substantial prior to a significant human impact. This provides a critical knowledge of climatically driven, environmental and ecological changes in the past, which is essential to better understand the dynamics and resilience of current biodiversity.
Magdalena S Svensson
added a research item
In January 2021, the International Union for the Conservation of Nature's Primate Specialist Group Section for Human Primate Interactions (IUCN PSG SHPI) published best practice guidelines on the use of non-human primate imagery online. This paper explores the contribution of professional primate keepers to the detrimental online sharing of images involving humans and primates, and their knowledge and opinions towards this subject. A total of 421 primate keepers responded to an online questionnaire shared in March 2021, providing information about their use of primate imagery on social media platforms and sharing their understanding of scientific studies on this topic. Over half (56%) of primate keepers admitted to sharing images online of themselves and primates, that could be considered irresponsible. A complementary review of posts shared on Instagram™ under the hashtag #primatekeeper revealed that 64% of 128 images surveyed depicted primates in situations which prior research has shown to have negative consequences for primate conservation, in addition to affecting the way the public perceives the conservation status of species in such imagery. Of the respondents, 53% had not heard of the IUCN PSG SHPI, and 67% of primate keepers were unaware of the new guidelines published by the group. It is recommended that the best practice guidelines are disseminated to zookeepers directly through appropriate forums to ensure primate keepers are acting in line with the recommendations in the best practice guidelines, and that further research is conducted regarding human-primate two-shot images to better guide decisions made by primatologists and others working both in and ex situ with primates.
Denise Spaan
added a research item
Land-use change transforms natural ecosystems, threatening species persistence worldwide. There is increasing evidence that forest loss negatively affects forest-dependent species and matrix quality can favor species maintenance, whereas forest fragmentation has mainly null or positive effects on species. However, the effects of these landscape attributes may depend on the level of regional deforestation. Here, we assess the effects of forest cover, matrix quality, and forest fragmentation (forest patch density) on primate species richness in 92 landscapes in Brazil. We grouped landscapes by their regional deforestation level into low, intermediate, high, and severe deforestation. The effects of landscape attributes varied depending on the level of regional deforestation. Forest loss decreased the proportion of primate species in the four regional deforestation levels, but this association was more important in the low, intermediate and high regional deforestation levels. Matrix quality was positively related to the proportion of primate species in three regional deforestation levels and this association was more important in the high regional deforestation level. Yet, matrix quality decreased the proportion of primate species in the severe regional deforestation level. Forest fragmentation had no clear effects across all deforestation levels. Therefore, different conservation strategies should be prioritized under distinct scenarios. Preventing forest loss is needed in all regions. Increasing matrix quality has positive effects on species richness, especially in highly deforested regions (30–15% remaining forest cover). Finally, as fragmentation had no clear effects on the proportion of primate species, landscape composition should be prioritized in conservation planning over landscape configuration.
Chris R Shepherd
added a research item
Despite being protected throughout their range, the illegal trade in slow lorises is a clear impediment to their con- servation. Little is known about this trade from Myanmar. We report on three visits to the town of Mong La, Myanmar, on the border with China, where Bengal slow lorises Nycticebus bengalensis are traded illegally. Combined with survey data from other researchers, it is clear that slow lorises are ubiquitously present at Mong La’s animal market. They are traded either as parts— carcasses, skins, and hands and feet (average of 26 items/survey)—or alive (average of 5 individuals/survey). Live animals typi- cally arrive at the market in the morning; they are slaughtered, and the carcass at least is sold the same day. Estimating from live animals, our data suggest that over a thousand Bengal slow lorises may be traded annually from this one market alone. Trade in Mong La may be local or may be geared towards the Chinese market, and thus the trade in Mong La is not only contra to Myan- mar’s law but also clearly violates the rules and intentions of CITES. We hope that by documenting the trade in slow lorises we will raise awareness amongst conservationists and primatologists about the realities of the unsustainable hunting of slow lorises and that it will be an incentive for the Myanmar and Chinese authorities to take appropriate action to curb this illegal trade.
Elena Bersacola
added a research item
In this thesis I explore how humans and nonhuman primates, including chimpanzees, share the space in a coastal forest-agriculture-village landscape mosaic at Cantanhez National Park (NP), southern Guinea-Bissau (West Africa). I integrate data from arboreal and terrestrial camera traps with habitat surveys, remote sensing and interviews with local people. For the first part of this thesis I use arboreal and terrestrial camera trap occupancy modelling across the landscape to investigate patterns of occurrence of seven primate species. Based on the landscape of fear concept, in Part 2 I combine camera trap based-Bayesian spatiotemporal models with interview data to investigate chimpanzee-human interactions at one focal site within the park (Caiquene–Cadique). Some primates showed high sensitivity to anthropogenic influences particularly king colobus (Colobus polykomos) and Guinea baboon (Papio papio). King colobus was the rarest primate and showed a strong avoidance of villages. Baboons largely relied on forest, and in the rainy season their distribution was severely constrained to areas away from human land uses. The highly restricted spatial occurrence of king colobus and baboons is likely the result of intensive hunting pressures particularly in the recent past. In constrast, at the landscape scale chimpanzees showed a tendency to occur nearer villages in both dry and rainy seasons, suggesting that chimpanzees are able to find opportunities for feeding and nesting in areas highly frequented by people. When looking at the fine scale, chimpanzees in Caiquene–Cadique visited the villages but intensified the use of areas further away from them, showing some levels of risk avoidance. Chimpanzees also displayed a tendency to minimise the use of cultivated areas but used areas near roads more frequently. Chimpanzee home range use was also positively influenced by the spatiotemporal availability of ripe oil palm fruit, thus taking advantage of a dominant resource across both forest and the heterogeneous matrix. During the period of wild food scarcity, chimpanzees increased visits within the villages when orange, lime and papaya were available. Thus, when forest foods were scarce, risk avoidance was temporally overruled in favour of optimal foraging. Interview data with local people corroborated biological data and provided additional information on chimpanzee behaviour within villages. Based on local narratives, when foraging at the villages chimpanzees used different social groupings depending on the targeted resource, and behaved more boldly towards women and children during close interactions. My data emphasise the importance of using different spatial scale approaches and further highlight chimpanzee resilience and flexibility in human-dominated landscapes where people remain willing to share the space with them.
Sam Pottie
added a research item
Establishing reintroduced primates in a suitable predetermined area has proven to be a challenge. Establishment is the first major step that has to be taken in the long process of reintroduction. When this first goal is not achieved, the chances of success decline drastically. Understanding the main determinants of establishment is therefore crucial for reintroduction success. This study examined the influence of three independent factors on the establishment success of reintroduced spider monkeys. We analysed data from the releases of eight groups of black-faced spider monkeys (Ateles chamek), which are part of the official reintroduction program of spider monkeys in the South Eastern Peruvian Amazon. Establishment success was measured by the proportion of individuals within groups that were found in the target area 6 months after release. The hours research assistants and volunteers spent with the group within the first 3 months after release—in the context of post-release monitoring—was shown to have a positive effect on the establishment success of the released group in the target area. The presence of an already established group in the area was also found to have a significant positive effect on establishment success. The influence of the days of post-release food provisioning had no effect. Our findings emphasize the importance of long-term monitoring programs to help increase the efficiency of primate reintroductions.
Yvonne A. de Jong
added a research item
The "Critically Endangered" southern patas monkey Erythrocebus baumstarki, thought to be endemic to Tanzania, has been resurrected to species level based on its geographic isolation, and on the coloration and pattern of its pelage. This study presents the first evidence for E. baumstarki in Kenya and reviews its historic and current geographic distributions based on the literature, museum specimens, online platforms, responses to requests for site records, and our own fieldwork. The distribution of E. baumstarki in the early 20th century was roughly 66,000 km2 . This has declined about 85% to around 9700 km2 at present (post-2009). The current "Extent of Occurrence" is only about 2150 km2 . This species was extirpated from Kenya in about 2015 and from the Kilimanjaro Region in Tanzania in about 2011. At present, E. baumstarki appears to be restricted to the protected areas of the western Serengeti, with the western Serengeti National Park being the stronghold. The number of individuals remaining is probably between 100 and 200, including between 50 and 100 mature individuals. The ultimate threat to E. baumstarki is the very rapidly increasing human population, while the main proximate threats are the degradation, loss, and fragmentation of natural habitats, and the related competition with people and livestock for habitat and water, particularly during droughts. Other problems are hunting by poachers and domestic dogs, and probably loss of genetic variation and climate change. This article provides recommendations for reducing the threats and promoting the recovery of E. baumstarki. We hope this article heightens awareness of the dire conservation status of E. baumstarki and encourages an increase in research and conservation action for this monkey.
Matthew R McLennan
added a research item
Chimpanzees (Pan troglodytes) build nests at night for sleeping and occasionally during daytime for resting. Over the course of seven years, forest fragments in Bulindi, Uganda, were reduced in size by about 80% when landowners converted forest to agricultural land. However, unlike other studies on nesting behavior in response to habitat disturbance, chimpanzees at Bulindi had no opportunity to retreat into nearby undisturbed forest. To understand behavioral adaptations to forest clearance, we compared Bulindi chimpanzees' nesting characteristics before and after this period of major deforestation. After deforestation, chimpanzees built nests at lower heights in shorter trees, and reused a larger proportion of their nests. Additionally, average nest group size increased after deforestation, even though community size declined by approximately 20% over the same period. The substantial decrease in available forest habitat may have caused the chimpanzees to aggregate for nesting. However, more cohesive nesting may also have been influenced by dietary shifts (increased reliance on agricultural crops) and a need for enhanced safety with increased human encroachment. Conversely, the chimpanzees selected similar tree species for nesting after deforestation, apparently reflecting a strong preference for particular species, nested less often in exotic species, and built integrated nests (constructed using multiple trees) at a similar frequency as before fragment clearance. Chimpanzees living in unprotected habitat in Uganda, as at Bulindi, face mounting anthropogenic pressures that threaten their survival. Nevertheless, our study shows that chimpanzees can adjust their nesting behavior flexibly in response to rapid, extensive habitat change. While behavioral flexibility may enable them to cope with deforestation, at least to a certain point, the long-term survival of chimpanzees in fast-changing human-modified landscapes requires intensive conservation efforts.
Matthew R McLennan
added a research item
Zoonotic pathogen transmission is considered a leading threat to the survival of non-human primates and public health in shared landscapes. Giardia spp., Cryptosporidium spp. and Microsporidia are unicellular parasites spread by the fecal-oral route by environmentally resistant stages and can infect humans, livestock, and wildlife including non-human primates. Using immunoassay diagnostic kits and amplification/sequencing of the region of the triosephosphate isomerase, small ribosomal subunit rRNA and the internal transcribed spacer genes, we investigated Giardia, Cryptosporidium, and microsporidia infections, respectively, among humans, domesticated animals (livestock, poultry, and dogs), and wild nonhuman primates (eastern chimpanzees and black and white colobus monkeys) in Bulindi, Uganda, an area of remarkably high human–animal contact and spatial overlap. We analyzed 137 fecal samples and revealed the presence of G. intestinalis assemblage B in two human isolates, G. intestinalis assemblage E in one cow isolate, and Encephalitozoon cuniculi genotype II in two humans and one goat isolate. None of the chimpanzee and colobus monkey samples were positive for any of the screened parasites. Regular distribution of antiparasitic treatment in both humans and domestic animals in Bulindi could have reduced the occurrence of the screened parasites and decreased potential circulation of these pathogens among host species.
Magdalena S Svensson
added a research item
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.
Magdalena S Svensson
added a research item
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,
Brooke Aldrich
added a research item
In this article, we attempt to characterize the widespread trade in pet macaques in Vietnam. Data on confiscations as well as surrenders, releases, and individuals housed at rescue centers across Vietnam for 2015–2019 were opportunistically recorded. Data comparisons between Education for Nature Vietnam and three government-run wildlife rescue centers show that at least 1254 cases of macaque keeping occurred during the study period, including a minimum of 32 Assamese macaques (Macaca assamensis), 158 long-tailed macaques (Macaca fascicularis), 291 Northern pig-tailed macaques (Macaca leonina), 65 rhesus macaques (Macaca mulatta), and 110 stump-tailed macaques (Macaca arctoides). A minimum of 423 individuals were confiscated, and at least 490 individual macaques were released. Three semi-structured interviews were conducted with two key Animals Asia (a non-governmental organization) colleagues and their insights are presented. Although we recognize that the data included are limited and can serve only as a baseline for the scale of the macaque pet trade in Vietnam, we believe that they support our concern that the problem is significant and must be addressed. We stress the need for organizations and authorities to work together to better understand the issue. The keeping of macaques as pets is the cause of serious welfare and conservation issues in Vietnam.
Matthew R McLennan
added a research item
Endangered wildlife increasingly inhabits human-dominated landscapes outside protected areas. Large-bodied mammals require large spaces, and their ranging may be especially impacted by landscape modifications including farming, road development and urbanisation. We studied the Wagaisa community of chimpanzees (Pan troglodytes) in Uganda, which inhabit a landscape characterised by high human population density, widespread deforestation, and rapid agricultural and infrastructural development. We aimed to assess whether this dynamic, fragmented environment constrains the chimpanzees’ ranging, and to identify critical habitat patches to aid their conservation. During March–May 2018, we assessed range use from locations of direct observations and indirect signs, corroborated by longer-term behavioural monitoring of the chimpanzees (June 2018–December 2019). No evidence of limited ranging was found. The Wagaisa chimpanzees used an area measuring ≥ 43 km² (100% MCP) and ranged extensively in the anthropogenic matrix. Most frequently used parts of the range (‘core habitat areas’) centred around small (5–20 acres), widely dispersed remnant forest patches and exotic eucalyptus plantations. Forty per cent of chimpanzee nests were constructed in eucalyptus trees, suggesting a behavioural adjustment to landscape changes. Actions to facilitate conservation of these ‘village chimpanzees’ and others surviving in transformed human-dominated habitat need not conflict with the sustainable development of the region. © 2020 The Authors. African Journal of Ecology published by John Wiley & Sons Ltd
Elena Račevska
added a research item
The biologically rich littoral forests of Sainte Luce support an isolated sub-population of Endangered red-collared brown lemur (Eulemur collaris). The area encompasses 17 disconnected forest fragments, separated by a matrix of eri-caceous heath, grasslands, swamps and watercourses. Since the earliest faunal studies in the late 1980s, this species has only been recorded within four forest patches. We detail this lemur's recent re-colonisation of a protected fragment and consider its broader implications for future conservation initiatives. This observation highlights the value of small, seemingly unimportant patches of forest and the importance of maintaining functional habitat connectivity. Our observations also provide insight into the conditions that likely led to the current distribution of this species in Sainte Luce.
Jennifer A. Rey-Goyeneche
added a research item
Se estudiaron el patrón de actividad y requerimientos de espacio de una tropa de Alouatta seniculus, entre febrero-julio/2010, antes y durante la entresaca de culmos, en un guadual bajo aprovechamiento persistente tipo II, en Quindío. Los datos fueron colectados con combinación de barridos lentos y muestreos instantáneos de localización de la tropa, cada quince minutos, doce horas/día, cinco días/mes. La tropa invirtió descansando 60.7% del tiempo, alimentándose 21.4%, desplazándose 14.9% e interacciones sociales 3%. No se presentaron variaciones durante la entresaca para alimentación, desplazamiento e interacciones sociales; pero los monos incrementaron el descanso. Este incremento podría estar más relacionado con su estrategia de ahorro energético, por su dieta principalmente folívora durante los meses de abril a julio, que con la entresaca como tal. El área de actividad fue de 13.75-ha y el área usada cada mes (7.3±1.1ha) no varió durante la entresaca. El porcentaje de uso del área entresacada disminuyó durante el aprovechamiento (antes: 66.9%, durante: 38.8%), a diferencia del área no entresacada (antes: 33.1%, durante: 61.2%); esta variación estuvo relacionada también con la oferta de recursos alimenticios. El promedio de distancias diarias recorridas fue mayor antes (1017±378.1m) que durante el aprovechamiento (759±230.2m). Se evidenció durante la entresaca una alteración temporal en las rutinas de los monos (cambio de rutas y dirección de desplazamientos), posiblemente para evitar trabajadores y por reducción de la continuidad del dosel. El cambio temporal en la estructura del bosque causado por la entresaca parece no tener efecto negativo significativo en los aulladores (temporal, pues la guadua recupera altura y densidad de culmos aproximadamente seis meses después de talada), posiblemente porque el aprovechamiento es restringido sólo a la guadua, se extrae un porcentaje específico de culmos, manteniendo un mínimo de conectividad de dosel, y se dejó un área no entresacada que funcionaría como posible refugio.
Amanda Webber
added a research item
The recognition that much biodiversity exists outside protected areas is driving research to understand how animals survive in anthropogenic landscapes. In Madagascar, cacao (Theobroma cacao) is grown under a mix of native and exotic shade trees, and this study sought to understand whether lemurs were present in these agroecosystems. Between November 2016 and March 2017, discussions with farmers, nocturnal reconnaissance surveys and camera traps were used to confirm the presence of lemurs in the Cokafa and Mangabe plantations near Ambanja, north-west Madagascar. Four species of lemur were encountered in nocturnal surveys: Mirza zaza, Phaner parienti, Microcebussp. and Cheirogaleussp. with encounter rates of 1.2, 0.4, 0.4 and 0.3 individuals/km, respectively. The presence of Lepilemur dorsalis was confirmed by camera trap. This is the first time lemurs have been studied in cacao plantations, and understanding how these threatened animals use anthropogenic landscapes is vital for their conservation.
Matthew R McLennan
added 3 research items
Behavioral flexibility, including an ability to modify feeding behavior, is a key trait enabling primates to survive in forest fragments. In human‐dominated landscapes, unprotected forest fragments can become progressively degraded, and may be cleared entirely, challenging the capacity of primates to adjust to the changes. We examined responses of wild chimpanzees (Pan troglodytes schweinfurthii) to major habitat change: that is, clearance of forest fragments for agriculture. Over 7 years, fragments in Bulindi, Uganda, were reduced in size by 80%. We compared the chimpanzees’ diet at the start and end of this period of rapid deforestation, using data derived mainly from fecal analysis. Similar to other long‐term study populations, chimpanzees in Bulindi have a diverse diet comprising over 169 plant foods. However, extensive deforestation seemed to impact their feeding ecology. Dietary changes after fragment clearance included reduced overall frugivory, reduced intake of figs (Ficus spp.; formerly a dietary “staple” for these chimpanzees), and reduced variety of fruits in fecal samples. Nevertheless, the magnitude of most changes was remarkably minor given the extent of forest loss. Agricultural fruits increased in dietary importance, with crops accounting for a greater proportion of fruits in fecal samples after deforestation. In particular, cultivated jackfruit (Artocarpus heterophyllus) became a “staple” food for the chimpanzees but was scarcely eaten before fragment clearance. Crops offer some nutritional benefits for primates, being high in carbohydrate energy and low in hard‐to‐digest fiber. Thus, crop feeding may have offset foraging costs associated with loss of wild foods and reduced overall frugivory for the chimpanzees. The adaptability of many primates offers hope for their conservation in fragmented, rural landscapes. However, long‐term data are needed to establish whether potential benefits (i.e. energetic, reproductive) of foraging in agricultural matrix habitats outweigh fitness costs from anthropogenic mortality risk for chimpanzees and other adaptable primates. Two adult males of the Bulindi chimpanzee community sharing a large cultivated jackfruit (Artocarpus heterophyllus) (Photo by Jacqueline Rohen). Chimpanzees in Bulindi experienced 80% forest loss in 7 years Chimpanzees adapted to fragment clearance by eating more agricultural crops, especially jackfruit Long‐term data are needed to establish if crop foraging benefits in matrix habitats outweigh costs (i.e., anthropogenic mortality risk) Chimpanzees in Bulindi experienced 80% forest loss in 7 years Chimpanzees adapted to fragment clearance by eating more agricultural crops, especially jackfruit Long‐term data are needed to establish if crop foraging benefits in matrix habitats outweigh costs (i.e., anthropogenic mortality risk)
The papers included in this special issue examine interspecific responses to habitat fragmentation by primate populations We identify intra and interspecific variables that can help predict primate population viability and potential persistence in fragmented landscapes The papers included in this special issue examine interspecific responses to habitat fragmentation by primate populations We identify intra and interspecific variables that can help predict primate population viability and potential persistence in fragmented landscapes
Social rank is positively correlated with reproductive success in numerous species, albeit demographic factors often influence those patterns. In multimale primate species, reproductive skew tends to decrease with increasing numbers of males and sexually receptive females. Alpha male chimpanzees (Pan troglodytes) often sire a disproportionate, though somewhat variable, percentage of offspring compared to other males. In a small community of eastern chimpanzees inhabiting a human-dominated landscape in Bulindi, Uganda, we found extraordinarily high levels of alpha male reproductive success over a 5-year period (7/8 offspring = 88%), despite the presence of multiple subordinate males. The skew exceeds that reported in other studies of chimpanzees as well as closely related bonobos (Pan paniscus). Our findings underscore the role of demographic and social factors in male reproductive success and also suggest that conclusions about species differences may be premature. The interaction of small community size, dispersal limitations, and male reproductive strategies like those found here may decrease genetic diversity and increase the risk of concomitant inbreeding in chimpanzee communities under strong anthropogenic pressure.
Jordi Salmona
added a research item
The geographic distribution of a species can provide insights into its population size, ecology, evolution, and how it responded to past (and may respond to future) environmental change. Improving our knowledge of the distribution of threatened species thus is a high priority in assessing their conservation status. However, there are few data available for many recently described yet understudied and potentially threatened primate taxa, making their conservation difficult. Here, we investigated the distribution of the Montagne d'Ambre fork-marked lemur, Phaner electromontis, a threatened nocturnal primate endemic to northern Madagascar and classified as Endangered by the IUCN. Because fork-marked lemurs are highly vocal, we used acoustic surveys to assess the species' presence-absence and relative population density within 66 distinct forest survey sites in northern Madagascar. Further, we compared data among five forest types within the study area and investigated the relationship between relative population density and climate variables. We report the presence of P. electromontis in 22 study sites; several of these populations were unknown previously. Although we found P. electromontis most frequently in dry-transitional forests, our results suggest that geography (spatial autocorrelation) rather than environmental variables explains the species' distribution. We hypothesize that environmental unpredictability and gummivory, combined with the presence of several distinct Phaner species in the studied area, could explain the observed distribution.
Yvonne A. de Jong
added a research item
The complex taxonomy and biogeography of the highly polytypic and widespread gentle monkey Cercopithecus mitis continue to be debated. Tanzania and Kenya, together, support eight of the currently recognized 17 subspecies of C. mitis. This paper reviews the taxonomy of the eight subspecies of C. mitis recognized for Kenya and Tanzania and presents an overview of their geographic distribution and pelage coloration and pattern. This paper also describes a new, endemic, subspecies of C. mitis for Tanzania, offers two hypotheses for its origin and phylogenetic affinities, and assesses its conservation status and conservation needs. Cercopithecus mitis in the Lake Manyara-Ngorongoro Region of central north Tanzania (i.e., the "Manyara Population") has often been referred to as "C. m. stuhlmanni × C. m. albogularis hybrids" and as representative of a "hybrid swarm." To better understand the taxonomic and conservation status of this population, four field surveys totaling 25 days were undertaken in southwest Kenya and central north Tanzania. The aim was to determine the geographic distribution of this population and to obtain detailed descriptions and photographs of as many individuals as possible. In addition, the literature was searched, and 88 C. mitis specimen skins were directly examined at four museums. We found no evidence to support the contention that C. mitis of the Lake Manyara-Ngorongoro Region are hybrids or represent a hybrid swarm. The Manyara C. mitis is geographically isolated from other C. mitis by >90 km of semi-arid habitat, is phenotypically distinct from other C. mitis, and presents little intra-population variation. As such, the diagnosable phenotypic characters of this population appear to be fixed, genetic, and heritable.
Kathleen Danielle Reinhardt
added a research item
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.
Timothy M. Eppley
added a research item
Primates worldwide are faced with increasing threats making them more vulnerable to extinction. Anthropogenic disturbances, such as habitat degradation and fragmentation , are among the main concerns, and in Madagascar, these issues have become widespread. As this situation continues to worsen, we sought to understand how fragmentation affects primate distribution throughout the island. Further, because species may exhibit different sensitivity to fragmentation, we also aimed to estimate the role of functional traits in mitigating their response. We collated data from 32 large-bodied lemur species ranges, consisting of species from the families Lemuridae (five genera) and Indriidae (two genera). We fitted Generalized Linear Models to determine the role of habitat fragmentation characteristics, for example, forest cover, patch size, edge density, and landscape configuration, as well as the protected area (PA) network, on the species relative probability of presence. We then assessed how the influence of functional traits (dietary guild, home range size) mitigate the response of species to these habitat metrics. Habitat area had a strong positive effect for many species, and there were significantly negative effects of fragmentation on the distribution of many lemur species. In addition, there was a positive influence of PAs on many lemur species' distribution. Functional trait classifications showed that lemurs of all dietary guilds are negatively affected by fragmentation; however, folivore-frugivores show greater flexibility/variability in terms of habitat area and landscape complexity compared to nearly exclusive foli-vores and frugivores. Furthermore, species of all home range sizes showed a negative response to fragmentation, while habitat area had an increasingly positive effect as home range increased in size. Overall, the general trends for the majority of lemur species are dire and point to the need for immediate actions on a multitude of fronts, most importantly landscape-level reforestation efforts.
Ellesse Janda
added a research item
Whilst primates were assumed to be either diurnal or nocturnal, many lemuriforms exhibit activity throughout the 24-hour cycle, known as cathemerality. The number of species showing this activity pattern and its evolution in primates are still uncertain. Recent studies exploring the temporal niche of woolly lemurs (genus Avahi) provide evidence of diurnal activity within in this nocturnal group, suggesting some degree of cathemerality. In this study, we investigated the degree of diurnality in the southern woolly lemur, A. meridionalis, and explore the link between activity bouts and sleeping site selection. From May to July 2018 we conducted systematic surveys in the lowland rainforest of Tsitongambarika in Southeastern Madagascar within the home ranges of three pairs of A. meridionalis to locate day-time sleeping trees. At the sleeping trees, we conducted continuous behavioural observations from dawn to dusk until the animals left the tree for their nocturnal activity. We measured the characteristics of the sleeping trees to identify the driving factors of sleeping site selection, and to investigate whether the micro-habitat architecture influences diurnal activity. Our results show that the nocturnal A. meridionalis exhibited opportunistic diurnal activity: being active for 28% of their time within or around the sleeping site. While active individuals displayed vigilance, grooming and feeding behaviours. The study animals demonstrated a selection for tree-height within pristine areas as opposed to vegetation density in edge areas. Similarly, our behavioural analysis revealed that A. meridionalis exhibited more diurnal activity in disturbed edge habitats. We suggest that an anti-predatory strategy may be a driving factor in both sleeping site selection and diurnal activity. Our results confirm that the secondary nocturnal genus Avahi exhibits cathemerality and add support to the idea that activity patterns in lemurs are more diversified than traditionally thought.
Rebecca Sweet
added 2 research items
: Gorillas are complex and intelligent primates, with the western-lowland subspecies being a familiar favourite in zoo collections across the world. Blackpool Zoo is one such place which currently houses a breeding family of six gorillas. Captive living can raise some issues for animals, particularly for gorillas which, in the wild, live in large family groups and travel fair distances to maintain territory and in search for food. In captivity, these elements are not always replicable and so smaller housing conditions are often alleviated by utilising vertical spaces. This project studies two important elements of this group’s life: social associations and enclosure use. The gorillas were observed using interval focal sampling over a six-hour period for two months, with a different individual being observed daily. Behavioural data were collected with reference to an ethogram and utilised in both studies. Chi-squared tests of independence were conducted initially on the three behavioural categories (locomotion, independent & social) which gave results that suggested gorillas spent much of their time performing independent behaviours. Category specific behaviours were then analysed further to determine which behaviours were more common across individuals. Inactive behaviours were most common across everyone with adult gorillas displaying increased levels of sitting and lying in comparison with younger individuals. Using the same statistical method, enclosure and substrate use were analysed and it was determined gorillas most frequently used ground level and used grass and straw most commonly out of all other substrate types. Juvenile individuals used moveable objects such as rope more. Additionally, the focal animal’s nearest neighbour and how far away they were from each other was recorded and these data were analysed using the same statistical test, and by creating a cluster analysis diagram. The results presented that there were clear individual preferences for social associations, with younger individuals associating closely with their mothers, and a mother and infant associating closely with the silverback. A subadult female was less associated with anyone which could suggest her readiness to transfer. 9 This study emphasises the influence that both environment and hierarchy have on gorilla behaviour, and how animals with the same routine and diet can perform unique and individual behaviours.
Gorillas are complex and intelligent primates, with the western-lowland sub-species being a familiar favourite in zoo collections across the world. Blackpool Zoo currently houses a breeding troop of six individuals. Captive living can raise some issues for gorillas which, in the wild, live in large family groups and travel fair distances to maintain territory and in search for food. In captivity, these elements are not always replicable and so smaller housing conditions are often alleviated by utilising vertical spaces. This project studies two important elements of this group's life: social associations and enclosure use. The gorillas were observed using interval focal sampling over a six-hour period for two months, with a different individual being observed daily. Inactive behaviours were most common across everyone with adult gorillas displaying increased levels of sitting and lying in comparison with younger individuals. It was determined gorillas most frequently used ground level and used grass and straw most commonly out of all other substrate types. Juvenile individuals used moveable objects such as rope more. Additionally, the focal animal's nearest neighbour and how far away they were from each other was recorded and these data were analysed, and by creating a cluster analysis diagram. The results presented that there were clear individual preferences for social associations, with younger individuals associating closely with their mothers, and a mother and infant associating closely with the silverback. A sub-adult female was less associated with anyone which could suggest her readiness to transfer. This study emphasizes the influence that both environment and hierarchy have on gorilla behaviour, and how animals with the same routine and diet can perform unique and individual behaviours. Methodology Data were collected for two month period (40 days or 320 hours) by one researcher. Non-data collection days were staggered to avoid bias (and influence of visitor levels) individuals were also studied on different days to further remove bias. One individual was studied each day-this was done due to the variability of locations of individuals (making it challenging to accurately record behaviour or more than one gorilla at a time). Behavioural data were collected with reference to an in depth ethogram and utilised in both studies. Social data was collected included recording nearest neighbour to individual and how far away the individual was. These distances were then categorised in to distance 'levels': 0, 1-5, 6-10 and 10+. Additionally, information on enclosure use was also collected. This included the level of enclosure use: Ground-level 6. It also included subsrtate use or fixture being used, e.g. level 3, straw and rope. This information was then compiled into a spreadsheet and analysed using the statistical methods discussed below. Statistical analysis was conducted in SPSS v.24 (IBM Corporation, Armonk, NY). Contingency tables (r x c) were created. Frequency counts for enclosure substrate use per individual were compared against each other using chi-squared test for independence or association. Additionally, this was done for enclosure height per individual. Behaviours were divided into three categories: social, locomotion and independent behaviours. The most common individual behaviours were also analysed with the same statistical method. To further analyse results a post hoc test (Cramer's V) was done to test the expected residual from observed by analysing data cell-by-cell to determine how far the observed were from the expected.
Jordi Salmona
added a research item
Tropical forests harbor extremely high levels of biological diversity and are quickly disappearing. Despite the increasingly recognized high rate of habitat loss, it is expected that new species will be discovered as more effort is put to document tropical biodiversity. Exploring under-studied regions is particularly urgent if we consider the rapid changes in habitat due to anthropogenic activities. Madagascar is known for its extraordinary biological diversity and endemicity. It is also threatened by habitat loss and fragmentation. It holds more than 100 endemic primate species (lemurs). Among these, Microcebus (mouse lemurs) is one of the more diverse genera. We sampled mouse lemurs from several sites across northern Madagascar, including forests never sampled before. We obtained morphological data from 99 Microcebus individuals; we extracted DNA from tissue samples of 42 individuals and amplified two mitochondrial loci (cytb and cox2) commonly used for species identification. Our findings update the distribution of three species (Microcebus tavaratra, Microcebus arnholdi, and Microcebus mamiratra), including a major increase in the distribution area of M. arnholdi. We also report the discovery of a new Microcebus lineage genetically related to M. arnholdi. Several complementary approaches suggest that the newly identified Microcebus lineage might correspond to a new putative species, to be confirmed or rejected with additional data. In addition, morphological analyses showed (a) clear phenotypic differences between M. tavaratra and M. arnholdi, but no clear differences between the new Microcebus lineage and the sister species M. arnholdi; and (b) a significant correlation between climatic variables and morphology, suggesting a possible relationship between species identity, morphology, and environment. By integrating morphological, climatic, genetic, and spatial data of two northern Microcebus species, we show that the spatial distribution of forest-dwelling species may be used as a proxy to reconstruct the past spatial changes in forest cover and vegetation type.
Jordi Salmona
added a research item
A bstract Mouse lemurs ( Microcebus ) are a radiation of morphologically cryptic primates distributed throughout Madagascar for which the number of recognized species has exploded in the past two decades. This taxonomic explosion has prompted understandable concern that there has been substantial oversplitting in the mouse lemur clade. Here, we take an integrative approach to investigate species diversity in two pairs of sister lineages that occur in a region in northeastern Madagascar with high levels of microendemism and predicted habitat loss. We analyzed RADseq data with multispecies coalescent (MSC) species delimitation methods for three named species and an undescribed lineage previously identified to have divergent mtDNA. Marked differences in effective population sizes, levels of gene flow, patterns of isolation-by-distance, and species delimitation results were found among them. Whereas all tests support the recognition of the presently undescribed lineage as a separate species, the species-level distinction of two previously described species, M. mittermeieri and M. lehilahytsara is not supported – a result that is particularly striking when using the genealogical discordance index ( gdi ). Non-sister lineages occur sympatrically in two of the localities sampled for this study, despite an estimated divergence time of less than 1 Ma. This suggests rapid evolution of reproductive isolation in the focal lineages, and in the mouse lemur clade generally. The divergence time estimates reported here are based on the MSC and calibrated with pedigree-based mutation rates and are considerably more recent than previously published fossil-calibrated concatenated likelihood estimates, however. We discuss the possible explanations for this discrepancy, noting that there are theoretical justifications for preferring the MSC estimates in this case.
Magdalena S Svensson
added a research item
Like other nocturnal primates, many species of galago (Galagidae) are phenotypi-cally 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 (fundamen-tal 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
Matthew R McLennan
added a research item
Rural, human-dominated landscapes present substantial risks to chimpanzees and other primates. In western Uganda, some farmers guard against crop losses to wildlife by placing large steel leg-hold traps ('mantraps') near their agricultural fields. Chimpanzees (Pan troglodytes schweinfurthii) can step in these illegal devices, resulting in severe injury or death. Here, we report a case of trapping and subsequent death of a wild chimpanzee from the Bulindi community (Hoima District). The elderly female chimpanzee died 13 days after being injured by a mantrap. Her injury could have contributed to the cause of death by impacting her balance in low trees above a stream; her body was subsequently found in the water. Behavioural observations prior to death and evidence from physical inspection of her injured hand suggest she may have otherwise recovered from her injury. Together with previous reports of chimpanzee trappings regionally, this case underlines the urgent need for a dedicated conservation program to reduce risks of inhabiting unprotected agricultural areas for chimpanzees. We propose an integrated strategy including (1) increased presence of wildlife authorities outside protected areas, (2) strengthening of existing legislation prohibiting use of mantraps, (3) targeted education programs and media campaigns, (4) and increased engagement of local people in chimpanzee conservation.
Denise Spaan
added a research item
Accurate and precise population estimates form the basis of conservation action but are lacking for many arboreal species due to the high costs and difficulty in surveying these species. Recently, researchers have started to use drones to obtain data on animal distribution and density. In this study, we compared ground and drone counts for spider monkeys (Ateles geoffroyi) at their sleeping sites using a custom-built drone fitted with a thermal infrared (TIR) camera. We demonstrated that a drone with a TIR camera can be successfully employed to determine the presence and count the number of spider monkeys in a forested area. Using a concordance analysis, we found high agreement between ground and drone counts for small monkey subgroups (<10 individuals), indicating that the methods do not differ when surveying small subgroups. However, we found low agreement between methods for larger subgroups (>10 individuals), with drone counts being higher than the corresponding ground counts in 83% of surveys. We could identify additional individuals from TIR drone footage due to a greater area covered compared to ground surveys. We recommend using TIR drones for surveys of spider monkey sleeping sites and discuss current challenges to implementation.
Denise Spaan
added an update
Our new research is open-access in the journal Drones
 
Catherine M Hill
added 2 research items
Representations of animals are diverse and can portray local understandings of nature conservation, information that is often missing from conservation debates. In Cantanhez National Park (southern Guinea-Bissau), chimpanzees ( Pan troglodytes verus ) are recognized as animals that share certain features with humans but live independently of them in the forest. However, chimpanzees are also integral to socially mediated, deep-rooted local narratives about sorcery and nature conservation. We use results from ethnographic research to explore local interpretations of chimpanzee attacks on people. Attacks by ‘bush’ chimpanzees occur when an animal is provoked by someone's actions towards it. Unprovoked attacks, however, are either interpreted as the act of a shape-shifted chimpanzee (i.e. a sorcerer) or as the responsibility of conservation stakeholders. In the case of unprovoked attacks, chimpanzee aggression is linked to a perceived abuse of power and to greed, with implications for nature conservation locally. Close analysis of local representations of animals contributes to a broader consideration of conservation priorities and practice.
Crop foraging or crop raiding concerns wildlife foraging and farmers' reactions and responses to it. To understand crop foraging and its value to wildlife or its implications for humans requires a cross-disciplinary approach that considers the behavior and ecology of wild animals engaging in this behavior; the types and levels of competition for resources between people and wildlife; people's perceptions of and attitudes toward wildlife, including animals that forage on crops; and discourse about animals and their behaviors and how these discourses can be used for expressing dissent and distress about other social conflicts. So, to understand and respond to conflicts about crop damage, we need to look beyond what people lose, i.e., crop loss and economic equivalence, and focusmore on what people say about wildlife and why they say it.
Matthew R McLennan
added a research item
Sharing environments with humans is linked to heightened stress responses in many wildlife species. In Uganda, deforestation for agriculture has increased competitive interactions between chimpanzees and villagers. To investigate whether this situation is 'stressful' for chimpanzees we compared faecal glucocorticoid metabolite (FGCM) concentrations in chimpanzees within an unprotected agricultural landscape and in a nearby protected forest with minimal disturbance. We further examined if changes in diet quality, including crop consumption (a proxy for chimpanzee-villager interactions) and sexually receptive females influenced glucocorticoid output in the 'village chimpanzee' population. Similar to findings from other species, FGCMs levels in the village chimpanzees were substantially higher than in chimpanzees in minimally-disturbed habitat. Within the village chimpanzees, overall fruit intake and number of sexually receptive females had a combined effect on elevating FGCM concentrations, probably through increasing social stress. However, crop consumption correlated negatively with FGCM levels, indicating crop feeding per se did not elevate glucocorticoid secretions (associated with increased interactions with humans), as suggested for some other mammals. Eating nutritionally-dense crops might instead buffer chimpanzees against energetic stress, enabling them to cope with consistent high exposure to anthropogenic stressors through moderating negative effects of glucocorticoids on the immune system. Our findings should nevertheless alert wildlife managers to potential detrimental impacts of human-induced stress on endangered mammals interacting frequently with rural farming communities. Initiatives offering villagers viable livelihood alternatives to deforestation, which increase their capacity to accommodate large mammals like great apes, alongside targeted education outreach, would help promote more peaceful, less 'stressful' coexistence.
Laura Ginn
added a research item
With continued expansion of anthropogenically modified landscapes, the proximity between humans and wildlife is continuing to increase, frequently resulting in species decline. Occasionally however, species are able to persist and there is an increased interest in understanding such positive outliers and underlying mechanisms. Eventually, such insights can inform the design of effective conservation interventions by mimicking aspects of the social-ecological conditions found in areas of species persistence. Recently, frameworks have been developed to study the heterogeneity of species persistence across populations with a focus on positive outliers. Applications are still rare, and to our knowledge this is one of the first studies using this approach for terrestrial species conservation. We applied the positive deviance concept to the western chimpanzee, which occurs in a variety of social-ecological landscapes. It is now categorized as Critically Endangered due to hunting and habitat loss and resulting excessive decline of most of its populations. Here we are interested in understanding why some of the populations did not decline. We compiled a dataset of 17,109 chimpanzee survey transects (10,929 km) across nine countries and linked them to a range of social and ecological variables. We found that chimpanzees seemed to persist within three social-ecological configurations: first, rainforest habitats with a low degree of human impact, second, steep areas, and third, areas with high prevalence of hunting taboos and low degree of human impact. The largest chimpanzee populations are nowadays found under the third social-ecological configuration, even though most of these areas are not officially protected. Most commonly chimpanzee conservation has been based on exclusion of threats by creation of protected areas and law enforcement. Our findings suggest, however, that this approach should be complemented by an additional focus on threat reduction, i.e., interventions that directly target individual human behavior that is most threatening to chimpanzees, which is hunting. Although changing human behavior is difficult, stakeholder co-designed behavioral change approaches developed in the social sciences have been used successfully to promote pro-environmental behavior. With only a fraction of chimpanzees and primates living inside protected areas, such new approaches might be a way forward to improve primate conservation.
Denise Spaan
added a research item
Population estimates are critical for making informed conservation decisions. However, methods for data collection and analysis of population estimates from wildlife surveys vary, often preventing comparisons between sites or years. In this study we compared population density estimates of spider monkeys, Ateles geoffroyi, derived from four commonly used methods to the actual density estimate based on known individual monkeys and home-range size and corroborated these results with surveys done on unhabituated monkeys in the same area. We recorded perpendicular distances of individual monkeys in the Otoch Ma’ax yetel Kooh Protected Area during two surveys: within the home range of an individually-recognized spider monkey group (survey one) and largely outside of the home range (survey two). We sighted 278 and 76 spider monkeys for a total effort of 93.74 and 42.78 km in surveys one and two, respectively. The actual density estimate was 65.4 individuals/km² (survey one). This value lies closer to the population density estimate obtained using the Kelker method (58.2 individuals/km²) than conventional distance sampling (CDS; 92.9–93.8 individuals/km²). Density estimates obtained with King and maximum perpendicular distance methods deviated substantially from the actual density. Population density estimates using the Kelker method and CDS differed less in survey two. Population density estimates differed little whether transects were walked slow or fast. We recommend using the Kelker method and CDS to estimate population density with a correction for distance estimation errors. We demonstrate how studies on populations of known size can improve the methods to survey populations of unknown size.
Denise Spaan
added an update
" Standardizing methods to estimate population density: an example based on habituated and unhabituated spider monkeys" has been published in Biodiversity and Conservation.
Use the link to read the full text.
 
Jennifer A. Rey-Goyeneche
added a research item
Animals’ space use patterns present dynamic responses to the availability of the main food resources that vary on different temporal and spatial scales. Although it is recognized that the interplay between main food resources shapes movement patterns in primates, few studies have simultaneously assessed the impact of fruit and arthropod supply on the ranging patterns of a frugivorous-insectivorous primate. Here, we studied the influence of ripe fruit and arthropod supply on six different ranging behavioral responses—daily distance traveled, home range size, backtracking, turning angles, travel speed, and arthropod-foraging speed—by a group of wild tufted-capuchin monkeys (Sapajus apella) in the Colombian amazon forest, during 1 year. Two approaches were considered: first, we compared the ranging patterns between periods in which ripe fruits and arthropods were abundant with periods of scarcity of both resources; second, we built models to test if predictor variables related to fruit and arthropod availability could explain each one of the ranging behavior variables. Group ranging patterns were larger or tended to be larger during periods of both food resources scarcity, suggesting that capuchins expand their movements throughout their home range in search for food as a response to the combined low food availability. Fruit supply was an influential factor for the daily path length and, marginally, for travel speed, with shorter distances related to a high density of fruiting trees and the capuchins’ tendency to travel to the nearest food source. Arthropod-capture success rate determined the turning angles and the arthropod-foraging speed, with tortuous and faster travels during low prey availability, related to a meticulous and fine-scaled search. There were not conclusive results for backtracking and home range size. Our results showed that the study group modified its ranging behavior according to the supply of their two main food resources, fruits and arthropods; in general, variation in large-scale travels throughout its home range reflected a frugivorous diet, while variation in small-scale movements revealed an insectivorous one.
Simon Knoop
added a research item
The Amazon basin is one of the most important ecosystems for the sustenance of biodiversity on the planet. This biodiversity is threatened by large-scale deforestation and hunting. Effective planning, monitoring, and management of protected areas are needed to effectively preserve species on the long-term. This requires a detailed understanding about local biodiversity and how it is influenced by humans as well as about the significance of wildlife for local people. The present study was conducted along the lower Abacaxis, Urariá and Marimari rivers in the Brazilian state of Amazonas, Central Amazon. Semi-structured interviews and display of primate pictures were used to access local and traditional ecological knowledge (LEK and TEK) of the indigenous Maraguá people about primate diversity and their use of primates, the role of wildlife for people’s sustenance and threats to biodiversity in the study area. The study confirms the presence of 13 species of primates in the study region, three of which are Endangered (Ateles chamek, Lagothrix cana and Chiropotes albinasus). It furthermore reveals the influence of food taboos associated with Adventist religion on hunting. Adventists focused on different target species than non-Adventists. Maraguá livelihoods were found to depend mainly on fishing, agriculture and hunting. Commercial hunting was identified as the most important threat to local biodiversity. The study sites are situated within the area proposed as indigenous Maraguá land. The legal demarcation process is pending. In the light of the results, the conservation potential of the study area as indigenous land is discussed.
Sarah Banet-Eugene
added a research item
Biodiversity conservation in South East Asia is under international pressure, from illegal wildlife trade, agroforestry industry, mining and logging. In Bangladesh, North East India, China and Myanmar, among a hotspot of biodiversity live the hoolock gibbons, a genus gathering three species, all threaten by anthropogenic pressure and all classified on the IUCN Red List. The Eastern Hoolock gibbon (Hoolock leuconedys) listed as Vulnerable, the Western Hoolock gibbon (Hoolock hoolock), listed as Endangered and was among the 25 Most Endangered Primates in the world in 2005 and 2008, and Skywalker Hoolock gibbon (Hoolock tianxing) listed as Critically Endangered and was among the 25 Most Endangered Primates in the world in 2017. Hunting pressure and the habitat degradation is considered as the lead actor for those species’ population decline. Their habitat is currently highly fragmented, often population of hoolock gibbons are found to be one or two groups into small patches of forests, unsuitable for establishing a viable population. The deterioration and destruction of those evergreen forests are results from the collection of firewood, timber extraction, plantations, crop cultivation, road construction and urbanization. Additionally, the illegal trade of gibbons is still expanding, and they are regularly hunted, for food and trade as a common livelihood. Reintroduction and translocation for conservation reinforcement is currently described as the main conservation process to develop to conserve this genus. It has for aim to reinforce current wild population living in protected areas with reintroduction from either captive population to wild population or wild to wild population. Nevertheless, conservation measures for saving these species are limited, only one rescue, rehabilitation centre is counted for the whole genera. This study describes the current conservation status of all three species, and why for those species, reintroduction and translocation following IUCN guidelines should be the main conservation tool to use.
Magdalena S Svensson
added a research item
The mountain gorilla, Gorilla beringei beringei, is listed by the International Union for Conservation of Nature (IUCN) as Endangered. About 1000 individuals remain in the wild, and the loss of even a single animal has implications for the viability of their two populations. Poaching, political instability and risk of anthropozoonotic disease transmission are potential threats to this species' recovery. Consequently, reducing the risk of infectious disease transmission by humans to the approximately 400 mountain gorillas of Bwindi Impenetrable National Park, Uganda, must be a priority for conservationists, tourists and the Uganda Wildlife Authority (UWA). Tourist revenue from gorilla trekking is significant and vital to the local communities and the UWA, and for the total gross revenue of Uganda. Data collected through a questionnaire survey (N = 136) and semi-structured interviews (N = 25) were used to (i) document tourists' self-reported health status, (ii) explore risk of disease transmission to gorillas, and (iii) assess tourists' reported willingness to wear disposable face masks during gorilla trekking. Results show that tourists pose a health risk to gorillas-contact and proximity to gorillas while trekking has increased compared to previous studies, and most respondents reported an average viewing distance of 5 m or less. Twenty-five percent of respondents indicated they might trek if sick, especially when symptoms were not severe and even when aware of regulations forbidding they do so. However, tourists are willing to adapt to new protocols, especially the use of face masks (51%). The introduction of face masks for tourists and guides during gorilla trekking is unlikely to reduce tourism revenue by reducing tourist numbers or reducing their willingness to pay. There is a need for improved access to information regarding potential risks of tourist-gorilla disease transmission in order to encourage responsible health-related behavior in tourists.
Jordi Salmona
added a research item
Forest loss, fragmentation, and anthropization threaten the survival of forest species all over the world. Shifting agriculture is one of these threatening processes in Madagascar. However, when its cycle is halted and the land is left to regenerate, the resulting growth of secondary forest may provide a viable habitat for folivorous and omnivorous lemur species. We aimed to identify the response of nocturnal lemurs to different successional stages of regenerating secondary, degraded mature, and mature forest across a mosaic-type landscape. We surveyed four nocturnal lemur species (Avahi laniger, Microcebus cf. simmonsi, Allocebus trichotis, and Daubentonia madagascariensis) in four forest types of varying habitat disturbance in northeastern Madagascar. We estimated densities in mature and regenerating secondary forest for the eastern woolly lemur (Avahi laniger) and mouse lemur (Microcebus cf. simmonsi), two sympatric species with folivorous and omnivorous diets respectively. We did not estimate densities of Allocebus trichotis and Daubentonia madagascariensis owing to small sample size; however, we observed both species exclusively in mature forest. We found higher population densities of A. laniger and M. cf. simmonsi in secondary than in mature forest, showing the potential of regenerating secondary forest for lemur conservation. Several environmental factors influenced the detectability of the two lemur species. While observer and habitat type influenced detection of the eastern woolly lemur, canopy height and vine density influenced detection of mouse lemurs. Understanding how different species with different diets interact with anthropogenically impacted habitat will aid future management decisions for the conservation of primate species.
Magdalena S Svensson
added a research item
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.
Yvonne A. de Jong
added a research item
Jordi Salmona
added a research item
Despite the fact that lemurs are the most threatened group of mammals and live in one of the world's richest biodiversity hotspots, there are still lemur lineages and regions of Madagascar that suffer from a lack of naturalistic data. This is particularly striking for the genus Phaner as well as for many unprotected forests of Northeastern Madagascar. We detected the presence of Phaner in the isolated lowland dry forest of Analafiana, located south of the Manambato River and close to the city of Vohémar. Little is known about the presence of Phaner in this region. The only record of Phaner in the area around Analafiana comes from museum specimens (Groves and Tattersall, 1991) geographically assigned to Vohémar and identified as belonging to a "doubtful subspecies". Here we provide morphological and genetic (mitochondrial DNA) data for a single juvenile individual captured in Analafiana. We compare our sequence data to the only four Phaner sequences publicly available: two P. electromontis individuals sampled in Montagne d'Ambre and Ankarana, and two other from P. pallescens and P. parienti species. We find that the new mtDNA sequence is divergent from the two P. electromontis sequences, but closer to these than other Phaner sequences. We also note that the Analafiana Phaner individual is morphologically more similar to P. electromontis than to the other species. Altogether, this data suggests this unique and isolated population of Phaner survives in the unprotected Analafiana forest in northeastern Madagascar. It is urgent to carry out more genetic, behavioral, acoustic, and demographic research in this region and on this population, whose exact taxonomic status should be urgently clarified. Our results strongly suggest that Analafiana's Phaner population likely holds the memory of a unique evolutionary history.
Elena Bersacola
added a research item
Background West African landscapes are largely characterised by complex agroforest mosaics. Although the West African forests are considered a nonhuman primate hotspot, knowledge on the distribution of many species is often lacking and out-of-date. Considering the fast-changing nature of the landscapes in this region, up-to-date information on primate occurrence is urgently needed, particularly of taxa such as colobines, which may be more sensitive to habitat modification than others. Understanding wildlife occurrence and mechanisms of persistence in these human-dominated landscapes is fundamental for developing effective conservation strategies. Methods In this paper, we aim to review current knowledge on the distribution of three threatened primates in Guinea-Bissau and neighbouring regions, highlighting research gaps and identifying priority research and conservation action. We conducted a systematic literature review of primate studies from 1976 to 2016 in Guinea-Bissau, southern Senegal and western Guinea (Boké Region). We mapped historical observation records of chimpanzee ( Pan troglodytes verus ), Temminck’s red colobus ( Pilicolobus badius temminckii ) and king colobus ( Colobus polykomos ), including our preliminary survey data from Dulombi, a newly established National Park (NP) in Guinea-Bissau. Results We found 151 documents, including 87 journal articles, that contained field data on primates in this region. In Guinea-Bissau, nearly all studies focussed south of the Corubal River, including mainly Cantanhez, Cufada, and Boé NP’s. In Senegal, most of the data came from Fongoli and Niokolo-Koba NP. In Boké (Guinea) studies are few, with the most recent data coming from Sangarédi. In Dulombi NP we recorded eight primate species, including chimpanzees, red colobus and king colobus . Across the selected region, chimpanzees, red colobus and king colobus were reported in eleven, twelve and seven protected areas, respectively. Discussion Our study demonstrates large geographical research gaps particularly for the two colobines. For the first time after more than two decades, we confirm the presence of red colobus and king colobus north of the Corubal River in Guinea-Bissau. The little information available from large parts of the red colobus range raises questions regarding levels of population fragmentation in this species, particularly in Casamance and across northern Guinea-Bissau. There are still no records demonstrating the occurrence of king colobus in Senegal, and the presence of a viable population in north-eastern Guinea-Bissau remains uncertain. While the occurrence of chimpanzees in Guinea-Bissau and Senegal is well documented, data from Boké (Guinea) are sparse and out-of-date. Our approach—the mapping of data gathered from a systematic literature review—allows us to provide recommendations for selecting future geographical survey locations and planning further research and conservation strategies in this region.