Primate Conservation: Unmet Challenges and the Role of the International Primatological Society

In the last 40 years, threats to the survival of wild primate populations have greatly increased. Primatologists have long been aware of these threats, and since 1978 have formulated plans to safeguard threatened species. Yet an increasing number of primate species face a high to extremely high risk of extinction. I asked 14 experienced field primatologists for their views on the most serious challenges to more effective primate conservation. They listed habitat loss and hunting as the major direct threats to primate survival, and noted that these activities are driven predominantly by the growth of human populations and the tendency of people to consume resources beyond their immediate survival needs. Two factors identified as most hindering effective action were a lack of political will and insufficient funding, while the main actions recommended to mitigate threats were to undertake more awareness-raising and make protected areas more effective. Such actions have long been recommended, so why have they not worked better? Perhaps the pressures on the natural world are too great to be countered, but I suggest also that too many of the various actors involved in conservation are overly driven by materialism and self-interest. I recommend more attention to the common good and a greater emphasis on the ethical and spiritual reasons for conservation. The International Primatological Society itself could have more vigorous debates on conservation policy at its congresses, and should consider the creation of regional chapters with the aim of promoting primatology in habitat countries.     

The primate extinction crisis in China: immediate challenges and a way forward

China is facing an unprecedented set of challenges in balancing the effects of economic development and global climate change with environmental protection and maintaining biodiversity. Although positive steps have been undertaken to remedy this situation, currently 80% of China’s 25 extant primate species are threatened, 15–18 species have population sizes of less than 3000 individuals, and two species of gibbons and one species of langur have been extirpated over the past few decades. Today, virtually all species of primates in China inhabit fragmented landscapes and are distributed in small isolated subpopulations with limited opportunities to exchange individuals or genetic information. Here we present a historical framework examining how human-induced environmental changes, particularly since the second half of the 20th century, accelerated primate population decline in China. In addition, we modeled the expected spatial conflict between agricultural expansion and primate distributions over the next 25–75 years and assessed the current overlap between protected areas and primate distributions. Depending on the assumptions of the spatial conflict model, primate distributions are expected to decline by an additional 51–87% by the year 2100. Thus, unless large-scale conservation policies are implemented immediately the current trend of primate population decline, local extirpation, and species extinctions will accelerate. To mitigate against such extinction scenarios, we advocate the creation of a Chinese national agency and repository of environmental information focused on public awareness and education, the implementation of targeted programs of habitat restoration designed to return impacted forests to a more natural state especially within and at the boundaries of nature reserves, the establishment of additional protect areas, and the construction of a latticework of corridors connecting isolated primate subpopulations. This comprehensive approach offers the most effective way to protect China’s animal and plant biodiversity, including its endangered primate populations.     

Significance of Riparian Forests for the Conservation of Central African Primates

We compared the structure of 12 Central African primate communities, 6 in riparian forests and 6 in adjacent terra firma forests and discussed the implications for primate conservation. The communities in riparian forests included on average 1.5 times more primate species than those in terra firma forests due to the fact that riparian forests shelter 4 specialist species and 6–7 generalist species. The results differ from findings in Amazonia where riparian forests consistently have fewer primate species than terra firma forests accommodate. This may be partly explained by the water level amplitude in Amazonian riparian forests, which deterred the radiation of semiterrestrial species. In Africa, most riparian-specialist primates are terrestrially-adapted and have access to an enlarged food niche. In terms of African primate conservation, we recommend protecting riparian forests and adjacent terra firma forests so that most of the lowland forest diversity is captured. The linear shape of riparian forests (which allows gene flow over long distance) and their persistence in anthropic landscape (because they represent lands of lesser value for agriculture and logging than mainland forests) predispose them to act as biodiversity sanctuaries.     

Responses of Primates to Landscape Change in Amazonian Land‐bridge islands—a Multi‐scale Analysis

Large hydroelectric dams are one of the current drivers of habitat loss across Amazonian forests. We investigated how the primate community at a hydroelectric dam in Brazilian Amazonia responded to changes in the landscape and local habitat structure of land‐bridge islands after 21 yr of post‐isolation history. The Balbina Dam, constructed in 1986, inundated 3129 km² of primary forests and created more than 3500 variable‐sized islands. We conducted primate and habitat structure surveys on 20 islands from 5 to 1815 ha, and extracted forest patch and landscape metrics for each island. The number of primate species per island varied between 0 and 7 species. Primate composition varied substantially according to both island area and forest cover remaining within the landscape, whereas island area alone was the most significant predictor of richness. Locally, tree density and vertical stratification were the most significant explanatory variables of primate composition and richness. A model containing area effects had the most explanatory power regarding site occupancy for most species. Individually, each species responded differently, with howler and brown capuchin monkeys showing greater tolerance to cope with habitat changes. Body size was also an important predictor of primate occupancy. We recommend protecting large fragments and enhancing the suitability of surrounding habitats to ensure primate conservation in most Neotropical fragmented landscapes. Given the flat topography of hydroelectric reservoirs, which mainly favors the formation of small islands, and the escalating hydropower development plans in Amazonia, our findings provide evidence for pervasive detrimental impacts of dams on primate communities.     

Primates as pets in Mexico City: an assessment of the species involved, source of origin, and general aspects of treatment

The large human populations in cities are an important source of demand for wildlife pets, including primates, and not much is known about the primate species involved in terms of their general origin, the length of time they are kept as pets, and some of the maintenance problems encountered with their use as pets. We report the results of a survey conducted in Mexico City among primate pet owners, which was aimed at providing some of the above information. We used an ethnographic approach, and pet owners were treated as informants to gain their trust so that we could enter their homes and learn about the life of their primate pets. We surveyed 179 owners of primate pets, which included 12 primate species. Of these, three were native species (Ateles geoffroyi, Alouatta pigra, and A. palliata). The rest were other neotropical primate species not native to Mexico, and some paleotropical species. Spider monkeys and two species of howler monkeys native to Mexico accounted for 67% and 15%, respectively, of the primate cases investigated. The most expensive primate pets were those imported from abroad, while the least expensive were the Mexican species. About 45% of the native primate pets were obtained by their owners in a large market in Mexico City, and the rest were obtained in southern Mexico. Although they can provide companionship for children and adults, primate pets are subject to a number of hazards, some of which put their lives at risk. The demand by city dwellers for primate pets, along with habitat destruction and fragmentation, exerts a significant pressure on wild populations in southern Mexico.     

Human-modified landscapes driving the global primate extinction crisis

The world's primates have been severely impacted in diverse and profound ways by anthropogenic pressures. Here, we evaluate the impact of various infrastructures and human-modified landscapes on spatial patterns of primate species richness, at both global and regional scales. We overlaid the International Union for the Conservation of Nature (IUCN) range maps of 520 primate species and applied a global 100 km² grid. We used structural equation modeling and simultaneous autoregressive models to evaluate direct and indirect effects of six human-altered landscapes variables (i.e., human footprint [HFP], croplands [CROP], road density [ROAD], pasture lands [PAST], protected areas [PAs], and Indigenous Peoples' lands [IPLs]) on global primate species richness, threatened and non-threatened species, as well as on species with decreasing and non-decreasing populations. Two-thirds of all primate species are classified as threatened (i.e., Critically Endangered, Endangered, and Vulnerable), with ~86% experiencing population declines, and ~84% impacted by domestic or international trade. We found that the expansion of PAST, HFP, CROP, and road infrastructure had the most direct negative effects on primate richness. In contrast, forested habitat within IPLs and PAs was positively associated in safeguarding primate species diversity globally, with an even stronger effect at the regional level. Our results show that IPLs and PAs play a critical role in primate species conservation, helping to prevent their extinction; in contrast, HFP growth and expansion has a dramatically negative effect on primate species worldwide. Our findings support predictions that the continued negative impact of anthropogenic pressures on natural habitats may lead to a significant decline in global primate species richness, and likely, species extirpations. We advocate for stronger national and international policy frameworks promoting alternative/sustainable livelihoods and reducing persistent anthropogenic pressures to help mitigate the extinction risk of the world's primate species.     

非人灵长类种群数量调查方法综述

监测估算野生动物的种群数量是保护的核心工作。由于气候变化和人类活动的影响,野生动物种群常处于不稳定的状态。非人灵长类是动物界的高等类群,具有复杂的社会行为、丰富的物种多样性,全球有701种 (含亚种),生活在多种类型的栖息地中,包括热带雨林、沼泽森林、红树林、次生林、落叶林、季雨林、山地森林,和包含孤存林、长廊森林、热带旱生林、山地草甸、地中海灌木林的稀树草原和干草原,以及荒漠、干旱的山地,甚至是雪地。绝大多数非人灵长类处于濒危的状态,长期有效的监测对于灵长类的保护十分重要。物种多样性和栖息地类型的多样性使得灵长类种群数量的调查方法多种多样。本文归纳总结了目前常用的非人灵长类种群数量调查方法的类型、基本原理、适用场景和局限性,并以研究实例加以分析;介绍了无人机、热成像、计算机学习系统等新技术应用在调查方法中的进展,希望为今后的非人灵长类野外数量调查、种群监测提供参考和启发。     

Recalculating route: dispersal constraints will drive the redistribution of Amazon primates in the Anthropocene

Climate change will redistribute the global biodiversity in the Anthropocene. As climates change, species might move from one place to another, due to local extinctions and colonization of new environments. However, the existence of permeable migratory routes precedes faunal migrations in fragmented landscapes. Here, we investigate how dispersal will affect the outcome of climate change on the distribution of Amazon's primate species. We modeled the distribution of 80 Amazon primate species, using ecological niche models, and projected their potential distribution on scenarios of climate change. Then, we imposed landscape restrictions to primate dispersal, derived from a natural biogeographical barrier to primates (the main tributaries of the Amazon river) and an anthropogenic constraint to the migration of many canopy‐dependent animals (deforested areas). We also highlighted potential conflict zones, i.e. regions of high migration potential but predicted to be deforested. Species response to climate change varied across dispersal limitation scenarios. If species could occupy all newly suitable climate, almost 70% of species could expand ranges. Including dispersal barriers (natural and anthropogenic), however, led to range expansion in only less than 20% of the studied species. When species were not allowed to migrate, all of them lost an average of 90% of the suitable area, suggesting that climate may become unsuitable within their present distributions. All Amazon primate species may need to move as climate changes to avoid deleterious effects of exposure to non‐analog climates. The effect of climate change on the distribution of Amazon primates will ultimately depend on whether landscape permeability will allow climate‐driven faunal migrations. The network of protected areas in the Amazon could work as ‘stepping stones’ but most are outside important migratory routes. Therefore, protecting important dispersal corridors is foremost to allow effective migrations of the Amazon fauna in face of climate change and deforestation.     

Techniques for determining protein sequence evolution applied to primates

Each amino acid in a protein is considered to be an individual, mutable characteristic of the species from which the protein is extracted. For a branching tree representing the evolutionary history of the known sequences in different species, our computer programs use majority logic and parsimony of mutations to determine the most likely ancestral amino acid for each position of the protein at each node of the tree. The number of mutations necessary between the ancestral and present species is summed for each branch and the entire tree. The programs then move branches to make many different configurations, from which we select the one with the minimum number of mutations as the most likely evolutionary history. We used this method to elucidate primate phylogeny from sequences of fibrinopeptides, carbonic anhydrase, and the hemoglobin beta, delta and alpha chains. All available sequences indicate that the early Pongidae had diverged into two lines before the divergence of an ancestor for the human line alone. We have constructed some probable ancestral sequences at major points during primate evolution and have developed tentative trees showing the order of divergences and evolutionary distances among primate groups. Further questions on primate evolution could be answered in the future by the detemination of the appropriate sequences.     

Primate population dynamics: variation in abundance over space and time

The rapid disappearance of tropical forests, the potential impacts of climate change, and the increasing threats of bushmeat hunting to wildlife, makes it imperative that we understand wildlife population dynamics. With long-lived animals this requires extensive, long-term data, but such data is often lacking. Here we present longitudinal data documenting changes in primate abundance over 45 years at eight sites in Kibale National Park, Uganda. Complex patterns of change in primate abundance were dependent on site, sampling year, and species, but all species, except blue monkeys, colonized regenerating forest, indicating that park-wide populations are increasing. At two paired sites, we found that while the primate populations in the regenerating forests had increased from nothing to a substantial size, there was little evidence of a decline in the source populations in old-growth forest, with the possible exception of mangabeys at one of the paired sites. Censuses conducted in logged forest since 1970 demonstrated that for all species, except black-and-white colobus, the encounter rate was higher in the old-growth and lightly-logged forest than in heavily-logged forest. Black-and-white colobus generally showed the opposite trend and were most common in the heavily-logged forest in all but the first year of monitoring after logging, when they were most common in the lightly-logged forest. Overall, except for blue monkey populations which are declining, primate populations in Kibale National Park are growing; in fact the endangered red colobus populations have an annual growth rate of 3%. These finding present a positive conservation message and indicate that the Uganda Wildlife Authority is being effective in managing its biodiversity; however, with constant poaching pressure and changes such as the exponential growth of elephant populations that could cause forest degradation, continued monitoring and modification of conservation plans are needed.     

Primate Populations and Their Interactions with Changing Habitats

Given that 90% of nonhuman primates depend on tropical forests, the most effective way to conserve them must emphasize the conservation of tropical forest habitats. To achieve this effectively, we need to address root causes of forest disturbance in developing nations: poverty, high population growth rates, crippling foreign debts, and the overdependence on tree and land resources. Moreover, it is now generally accepted that most primate populations will in future live in modified forest habitats. Studies of how primate populations respond to forest habitat modifications are therefore critical to future primate conservation. Currently most studies of primate responses to forest habitat alterations are difficult to interpret owing to differences in research methods and lack of information on the past histories of the modified forests. We review potential factors that may have to be considered while evaluating primate responses to forest habitat changes such as degradation and fragmentation.     

Spatial Patterns of Primate Electrocutions in Diani,Kenya

Electrocution from power infrastructure threatens many primate species, yet knowledge of effective evidence-based mitigation strategies is limited. Mitigation planning requires an understanding of the spatial distribution of electrocutions to prioritize high-risk areas. In Diani, a coastal Kenyan town, electrocution is an important cause of death for five primate species. In this study we aim to describe the spatial patterns of electrocutions and electric shock incidents (collectively referred to as electrocutions hereafter) and identify electrocution hotspots to guide an effective primate conservation approach in Diani. Colobus Conservation, a not-for-profit organization, has recorded electrocutions and annual primate census data since 1998. We georeferenced 329 electrocution data points and analyzed them using QGIS. We identified and compared hotspots across species, seasons, and time using kernel density estimation and Getis-Ord-Gi*. We employed spatial regression models to test whether primate population density and power line density predicted the location of electrocution hotspots. Electrocutions occurred in hotspots that showed little variation in location between species and seasons. The limited variation in hotspot location over time likely occurred as a result of new building development in Diani and variability in primate detection rates by community members. Primate density and power line density were significant predictors of electrocution density for Angolan black-and-white colobus (Colobus angolensis palliatus) and Sykes monkeys (Cercopithecus mitis albogularis), but the relationship was weak, suggesting the presence of additional risk factors. This study provides a framework for systematic spatial prioritization of power lines that can be used to reduce primate electrocutions in Diani, and can be adopted in other areas of the world where primates are at risk from electrocution.     

A SINE-based dichotomous key for primate identification

For DNA samples or ‘divorced’ tissues, identifying the organism from which they were taken generally requires some type of analytical method. The ideal approach would be robust even in the hands of a novice, requiring minimal equipment, time, and effort. Genotyping SINEs (Short INterspersed Elements) is such an approach as it requires only PCR-related equipment, and the analysis consists solely of interpreting fragment sizes in agarose gels. Modern primate genomes are known to contain lineage-specific insertions of Alu elements (a primate-specific SINE); thus, to demonstrate the utility of this approach, we used members of the Alu family to identify DNA samples from evolutionarily divergent primate species. For each node of a combined phylogenetic tree (56 species; n = 8 [Hominids]; 11 [New World monkeys]; 21 [Old World monkeys]; 2 [Tarsiformes]; and, 14 [Strepsirrhines]), we tested loci (> 400 in total) from prior phylogenetic studies as well as newly identified elements for their ability to amplify in all 56 species. Ultimately, 195 loci were selected for inclusion in this Alu-based key for primate identification. This dichotomous SINE-based key is best used through hierarchical amplification, with the starting point determined by the level of initial uncertainty regarding sample origin. With newly emerging genome databases, finding informative retrotransposon insertions is becoming much more rapid; thus, the general principle of using SINEs to identify organisms is broadly applicable.     

The Narrow Niche hypothesis: gray squirrels shed new light on primate origins

Current hypotheses for primate origins propose that nails and primate-like grasping hands and feet were important early adaptations for feeding in fine branches. Comparative research in this area has focused on instances of convergence in extant animals, showing that species with primate-like morphology feed predominantly from terminal branches. Little has been done to test whether animals without primate-like morphology engage in similar behavior. We tested the fine-branch niche hypothesis for primate origins by observing branch use in Eastern gray squirrels, Sciurus carolinensis, a species lacking primate grasping adaptations that has been understudied in the context of primate origins. We hypothesized that because gray squirrels lack primate-like grasping adaptations, they would avoid feeding and foraging in terminal branches. Instantaneous focal animal sampling was used to examine the locomotor and postural behaviors used while feeding and foraging. Our results demonstrate habitual and effective usage of terminal branches by gray squirrels while feeding and foraging, primarily on tree seeds (e.g., oak, maple, and elm). Discriminant function analysis indicates that gray squirrels feed and forage like primates, unlike some other tree squirrel species. Given the absence of primate-like features in gray squirrels, we suggest that although selection for fine-branch foraging may be a necessary condition for primate origins, it is not sufficient. We propose an alternative model of primate origins. The Narrow Niche hypothesis suggests that the primate morphological suite evolved not only from selection pressure for fine branch use, but also from a lack of engagement in other activities.     

Primate assemblage structure in Amazonian flooded and unflooded forests

There is considerable variation in primate species richness across neotropical forest sites, and the richest assemblages are found in western Amazonia. Forest type is an important determinant of the patterns of platyrrhine primate diversity, abundance, and biomass. Here we present data on the assemblage structure of primates in adjacent unflooded (terra firme) and seasonally inundated (várzea and igapó) forests in the lower Purús region of central-western Brazilian Amazonia. A line-transect census of 2,026 km in terra firme, 2,309 km in várzea, and 277 km in igapó was conducted. Twelve primate species were recorded from 2,059 primate group sightings. Although terra firme was found to be consistently more species-rich than várzea, the aggregate primate density in terra firme forest was considerably lower than that in the species-poor várzea. Consequently, the total biomass estimate was much higher in várzea compared to either terra firme or igapó forest. Brown capuchin monkeys (Cebus apella) were the most abundant species in terra firme, but were outnumbered by squirrel monkeys (Saimiri cf. ustus) in the várzea. The results suggest that floodplain forest is a crucial complement to terra firme in terms of primate conservation in Amazonian forests.     

A major shift in diversification rate helps explain macroevolutionary patterns in primate species diversity

Primates represent one of the most species rich, wide ranging, and ecologically diverse clades of mammals. What major macroevolutionary factors have driven their diversification and contributed to the modern distribution of primate species remains widely debated. We employed phylogenetic comparative methods to examine the role of clade age and evolutionary rate heterogeneity in the modern distribution of species diversity of Primates. Primate diversification has accelerated since its origin, with decreased extinction leading to a shift to even higher evolutionary rates in the most species rich family (Cercopithecidae). Older primate clades tended to be more diverse, however a shift in evolutionary rate was necessary to adequately explain the imbalance in species diversity. Species richness was also poorly explained by geographic distribution, especially once clade age and evolutionary rate shifts were accounted for, and may relate instead to other ecological factors. The global distribution of primate species diversity appears to have been strongly impacted by heterogeneity in evolutionary rates.     

Habitat preference of the Preuss's guenon<Emphasis Type="Italic">(Cercopithecus preussi), on Bioko island,Equatorial Guinea</Emphasis>

The Press's guenon (Cercopithecus preussi) is considered to be one of the most threatened African primates. There is little information on the ecology and status of this primate on Bioko island, where it is found in the form of an endemic subspecies. The Press's, guenon shows preference for theSchefflera forest and the mountain habitat on Bioko island. As on the mainland they also have semitterrestrial habits and are found usually at the understorey of the forest. Competitive exclusion between this guenon and other guenon species could be an explanation of these ecological preferences. Habitat use and vertical stratification of the activity in the forest canopy seem to reduce competition with other sympatric primate species that inhabit on the island. Habitat destruction, and isolation in a reduced habitat, show to be the major threats for the survival of this primate on Bioko island.     

A Global-Scale Evaluation of Primate Exposure and Vulnerability to Climate Change

Human-induced climate change poses many potential threats to nonhuman primate species, many of which are already threatened by human activities such as deforestation, hunting, and the exotic pet trade. Here, we assessed the exposure and potential vulnerability of all nonhuman primate species to projected future temperature and precipitation changes. We found that overall, nonhuman primates will experience 10 % more warming than the global mean, with some primate species experiencing >1.5 °C for every °C of global warming. Precipitation changes are likely to be quite varied across primate ranges (from >7.5 % increases per °C of global warming to >7.5 % decreases). We also identified individual endangered species with existing vulnerabilities (owing to their small range areas, specialized diet, or restricted habitat use) that are expected to experience the largest climate changes. Finally, we defined hotspots of primate vulnerability to climate changes as areas with many primate species, high concentrations of endangered species, and large expected climate changes. Although all primate species will experience substantial changes from current climatic conditions, our hotspot analysis suggests that species in Central America, the Amazon, and southeastern Brazil, as well as portions of East and Southeast Asia, may be the most vulnerable to the anticipated impacts of global warming. It is essential that impacts of human-induced climate change be a priority for research and conservation planning in primatology, particularly for species that are already threatened by other human pressures. The vulnerable species and regional hotspots that we identify here represent critical priorities for conservation efforts, as existing challenges are expected to become increasingly compounded by the impacts of global warming.     

Asian Primate Classification

In the foreseeable future there is little likelihood of achieving consensus on the number of Asian primate genera and species, and their subspecific composition. There is a more realistic hope of reaching agreement on the number of recognizable subspecies. The latter objective is more urgent because in order to reliably assess generic and specific numbers, it is essential that effective conservation measures are implemented for as many subspecies as possible. This cannot be comprehensively accomplished until their validity is assessed and they are satisfactorily established and defined. The Asian primate classification that we present is the outcome of electronic communication among the co-authors after a workshop, which was especially convened to attempt to determine the number of recognizable primate subspecies and to identify potentially recognizable subspecies. The generic and specific arrangement is a compromise that does not necessarily reflect the individual views of the co-authors: 183 subspecies in 77 species in 16 genera. The 31 subspecies allotted a low credibility rating are almost balanced by the 22 scientifically unnamed populations that may warrant subspecific status.