Primate Seed Dispersal and Forest Restoration: An African Perspective for a Brighter Future

Primate seed dispersal is a vital, but complex, ecological process that involves many interacting agents and plays important roles in the maintenance of old-growth forest, as well as in the development of regenerating forest. Focusing primarily on African examples, in this article we briefly review the ecological process of primate seed dispersal, highlighting understudied and contentious topics, and then we discuss how our knowledge on primate seed dispersal can promote both forest restoration and primate conservation. Though it is frequently claimed that primates are critically important for the maintenance of diverse tropical forest ecosystems, we believe that more empirical evidence is needed to support this claim. Confounding factors can often be difficult to rule out and long-term studies extending beyond the seedling or sapling stage are very rare. In addition, though primates are critical for initial seed dispersal of many tree species, spatial and temporal variation in post-deposition processes, such as secondary seed dispersal and predation by rodents, can dramatically alter the initial patterns generated by primates. However, given the need for immediate conservation action to prevent further primate extinctions, we advocate that the knowledge about primate seed dispersal be used in formulating informed conservation plans. One prominent area where this knowledge will prove extremely valuable is in forest restoration efforts. To aid in the development of such efforts, we pose five questions, the answers to which will help facilitate forest restoration becoming a useful tool in strategies designed to conserve primates.     

Low Primate Diversity and Abundance in Northern Amazonia and its Implications for Conservation

Large areas of the Rio Negro basin in Amazonia are covered by continuous tracts of tropical forest, but have few primate species. This is anomalous considering the general relationship between area and number of species. One possibility is that much of the forest is unsuitable habitat for most primates and the area of suitable habitat is much less than the forested area. This has important consequences for the design of reserves and predictions of the consequences of climate change, which tend to be based on broad categories based on satellite images, and not on information of species distributions within those broad categories. The study was conducted through diurnal and nocturnal line‐transect surveys in the Biodiversity Research Program 25‐km² permanent grid in Viruá National Park, which has vegetation associations typical of much of northern Amazonia. The highest primate diversity and abundances occurred in tall terra firme forests (58%), whereas inundated forests and scrublands, which cover 42 percent of the survey grid and 90.8 percent of the Viruá National Park, have virtually no primates. This suggests that parks and reserves in northwestern Amazonia will have to be very large to maintain viable populations of most primates and their ecological interactions, and that very broad habitat categories are not sufficient to make predictions about actual and future suitability of areas for primate conservation.     

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.     

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.     

Priority areas for conservation of primates in a threatened Amazonian savanna

Primates are globally recognized as an important component of biodiversity, however, more than half of primate species in the world are threatened and agriculture expansion is one of the main threats. Brazil has one of the largest networks of protected areas (PAs) in the world, but there are some conservation gaps, such as the Amazonian savannas. We aim to identify a network of priority areas to conserve a Brazilian Amazonian savanna highly threatened by agriculture expansion, by using seven primate species and four vegetation types as targets. We constructed species distribution models (SDMs) for the primates and used a Systematic Conservation Planning approach. We defined as a quantitative conservation target the proportion of the distribution of each primate species within the network according to traits related to their vulnerability to extinction. In addition, we set a target of including at least 30% of each savanna type within priority areas. We created a map of potential use of the land for agriculture and another of environmental risk, which were included as costs in the decision process, and together with the SDMs and vegetation types, identified the network of priority areas by using the software Marxan. We evaluated the feasibility of implementing conservation actions, such as establishing Conservation Units (e.g. reserves managed by the government), or implementing community-based conservation actions in each priority area. Additionally, we estimated the economic investment (US$/year) required to establish Conservation Units across the priority areas. Conservation targets for primates and vegetation types were met by protecting 3,240 km² of the Savannas of Amapá. An investment of approximately US$958,122/year over five years is required to turn these priority areas into Conservation Units, however, we propose other strategies such as conservation on community lands and public policies. All these strategies would allow for protecting forest cover and the heterogeneous environments that are suitable for primates and other biodiversity components.     

Vegetative predictors of primate abundance: utility and limitations of a fine-scale analysis

Determining ecological predictors of primate abundance is important for both theoretical and applied conservation management. For forest primates, research has focused on comparisons of primate abundance and vegetation in different forest blocks or forest compartments with different management histories. However, great variation in primate abundance often occurs within single forests, especially in mountainous areas or in areas with habitat mosaics due to past disturbance. Here we assess, for the first time, the usefulness and limitations of small-scale, within-transect analysis of vegetative parameters as predictors of primate abundance in a very heterogeneous forest habitat in the Udzungwa Mountains of Tanzania. Relative abundance of four species of diurnal primates was recorded over a period of 2.5 years by walking three census transects 48 times each. Tree size, density, species composition, and food plants were measured along the same census lines. The fine-scale relationship between primate abundance and vegetative variables was analyzed through generalized linear modeling applied to 58 segments of these three census lines. Each segment was 200 m in length. For all four primate species, we found significant associations between their abundance and selected vegetative variables. The abundance of the endemic and endangered Udzungwa red colobus Procolobus gordonorum was positively related to mean basal area of large trees (diameter at breast height greater than 20 cm) and to the species richness of their food plants. Considering the very great variation in primate abundance that was recorded among segments of the census lines, our approach proved useful in predicting the relationship between primate abundance and small-scale habitat differences. The main limitation of this study, however, was the relatively low-predictive power of the models for some species, especially the Angolan colobus Colobus angolensis. We discuss the potential reasons for this problem and suggest possible improvements for future studies.     

Comprehensive Conservation Profile of Tana Mangabeys

Forests along 60 kilometers of the lower Tana River, Kenya, provide habitat for one of the world’s top 25 most endangered primates, the Tana mangabey (Cercocebus galeritus). There is no current accurate estimate of the mangabey population, but a 1994 census estimated the population at 1,000–1,200. Their habitat has been severely degraded since then: visual estimates indicated that 30% of the forest area has been cleared and product use has increased in > 80% of forests surveyed. As the mean number of mangabey groups per forest is positively correlated with forest area and density of trees, this loss is damaging to the mangabey population. There has also been an increase in mangabey-human conflict, e.g., crop raiding, set traps, mangabeys chased by dogs. Mangabeys exhibit ecological flexibility, but behavioral data come from only a few mangabey groups. A new conservation approach is needed because past approaches, particularly the Tana River Primate National Reserve and a World Bank/Global Environment Facility Project, failed to protect the forests. The failure was mainly due to a disregard of the land-tenure issue within the Reserve, exclusion of local people from decision-making, and neglect of forests outside the reserve. Future actions must include community conservation programs and forest and corridor restoration. Research should focus on traditional management, status of primate groups in severely degraded forests, ecology of additional groups, and a population estimate to inform management as they implement more specific conservation strategies for the species.     

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.     

Distinguished primatologist address—moving from advocacy to activism: Changing views of primate field research and conservation over the past 40 years

Field studies of wild nonhuman primates have grown exponentially over the past 40 years and our knowledge of primate behavior, ecology, and social, and mating systems has expanded greatly. However, we are facing a major extinction crisis with some 60% of all primate species listed as threatened and more than 75% of species with declining populations. The primary factor driving primate population decline is human population increase, which over the past 50 years has resulted in the unsustainable conversion and degradation of natural landscapes for industrial agriculture, the production of nonagricultural commodities for international trade, pastureland for cattle, dam construction, fossil fuel exploration, mining, and the construction of road networks and infrastructure to support large urban centers. Recent ecological modeling predicts that by the end of the century, the four primate‐richest countries in the world will lose 32–78% of their existing primate habitat to agricultural expansion, and nine of the top 15 primate‐richest countries are expected to have 80–100% of their primate species extinct or threatened with extinction. If we are going to save the world's primates, the time to act is now! Not only should all primate field research include a strong conservation component, but in addition we must actively join with our professional societies, zoos and research facilities, universities, conservation organizations, concerned business leaders, global citizens, like‐minded political leaders, and grassroots organizations to inform, demand and direct governments, multinational corporations, and international organizations to engage in transformational change to protect biodiversity and seek environmental justice against those entities that actively destroy our planet. As the chief academic discipline dedicated to the study of primates, we must organize and collectively move from being advocates for primate conservation to becoming activists for primate conservation. This is a call to action.     

Taxonomy and conservation of Vietnam's primates: a review

Vietnam has the highest number of primate taxa overall (24-27) and the highest number of globally threatened primate taxa (minimum 20) in Mainland Southeast Asia. Conservation management of these species depends in part on resolving taxonomic uncertainties, which remain numerous among the Asian primates. Recent research on genetic, morphological, and acoustic diversity in Vietnam's primates has clarified some of these uncertainties, although a number of significant classification issues still remain. Herein, we summarize and compare the major current taxonomic classifications of Vietnam's primates, discuss recent advances in the context of these taxonomies, and suggest key areas for additional research to best inform conservation efforts in a region crucial to global primate diversity. Among the most important next steps for the conservation of Vietnam's primates is a new consensus list of Asian primates that resolves current differences between major taxonomies, incorporates recent research advances, and recognizes units of diversity at scales below the species-level, whether termed populations, morphs, or subspecies. Priority should be placed on recognizing distinct populations, regardless of the species concept in use, in order to foster the evolutionary processes necessary for primate populations to cope with inevitable environmental changes. The long-term conservation of Vietnam's primates depends not only on an accepted and accurate taxonomy but also on funding for on-the-ground conservation activities, including training, and the continued dedication and leadership of Vietnamese researchers and managers.     

我国灵长类的现状与保护

近些年来,国际上愈来愈认识到灵长类动物资源保护的重要性,在自然保护和拯救濒危物种方面作了种种努力。由于长期以来,人类对灵长类动物滥加捕杀和不合理的开发自然,特别是对于森林的毁坏,导致了栖息地的急剧改变,已使许多种类处于濒临灭绝的境地(Thorington,1974a,1974b,1978a,1978b)。国际自然与自然资源保护联盟编汇的红皮书（Red Data Book）录列了41种（亚种）属不同程度濒危种。濒危动植物种国际贸易公约（CITES）甚至已将全部灵长类分别列入国际间严禁或控制进出口贸易的名录之中。     

Primate frugivory in Kibale National Park, Uganda, and its implications for human use of forest resources

In an attempt to understand the practical and/or economic implications of primate seed dispersal, it was established which seed species are dispersed by frugivorous primates in Kibale National Park, Uganda, and which of this sort of species were used by Ugandan people. A list of fruit species consumed by Kibale primates was compiled using primary data and by reviewing all known published accounts of their fruit diet. Primates consume the fruit of 87 Kibale forest tree species; the seeds of 11% of these species are destroyed by the primates. The remaining 77 species are dispersed by either one, two, three or all four of the frugivorous Kibale primates. Of these 77 species, 42% have some utility to local Ugandan inhabitants, suggesting that maintaining populations of primates is important not only for natural forest regeneration, but also for human habitat use. This report illustrates the complexity of the seed dispersal process and suggests links not only between plants and their dispersers, but also between sets of plants/dispersers and the human populations that rely on forest resources.     

Use of Mangroves by Lemurs

Despite an increasing recognition of the ecosystem services provided by mangroves, we know little about their role in maintaining terrestrial biodiversity, including primates. Madagascar’s lemurs are a top global conservation priority, with 94 % of species threatened with extinction, but records of their occurrence in mangroves are scarce. I used a mixed-methods approach to collect published and unpublished observations of lemurs in mangroves: I carried out a systematic literature search and supplemented this with a targeted information request to 1243 researchers, conservation and tourism professionals, and others who may have visited mangroves in Madagascar. I found references to, or observations of, at least 23 species in 5 families using mangroves, representing >20% of lemur species and >50% of species whose distributions include mangrove areas. Lemurs used mangroves for foraging, sleeping, and traveling between terrestrial forest patches, and some were observed as much as 3 km from the nearest permanently dry land. However, most records were anecdotal and thus tell us little about lemur ecology in this habitat. Mangroves are more widely used by lemurs than has previously been recognized and merit greater attention from primate researchers and conservationists in Madagascar.     

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。     

Primate seed dispersal: Coevolution and conservation implications

Early studies of primates have demonstrated that many species rely heavily on fruit, and that primates constitute a large component of the frugivore biomass in tropical forests. Consequently, primates have long been thought to be important seed dispersers. It is only recently that studies have been conducted that have illustrated the complex nature of the interactions between fruit-eating primates and their food trees. Such studies have raised questions as to the causes and conse-quences of the intriguing differences between primate communities, the importance of other animals in the interactions (such as dung beetles and rodents that secon-darily disperse seeds), how primate-plant interactions evolve, and the significance of primates in forest regeneration and conservation. Since subsistence and com-mercial hunting of primates has heavily impacted frugivore communities, but left the physical structure of the forest relatively unaltered, studies of primate seed dispersal have important implications for the future of forests where seed dispersers have declined or disappeared.     

Ecological correlates of abundance in the Tana mangabey (Cercocebus galeritus)

I investigated the ecological correlates of abundance in the Tana mangabey (Cercocebus galeritus), one of the world's most endangered primates, with the goal of recommending management strategies. I systematically selected 31 forest fragments throughout the mangabey's 60-km distribution along the lower Tana River in southeastern Kenya. Within the 31 fragments, I measured vegetation structure, food abundance, and human forest product use in 107 belt transects, and conducted 370 mangabey surveys. I used a weighted multiple regression analysis to determine whether there was a dependence between the selected forest attributes and the mean number of mangabey groups per fragment. Fragment area and density of trees > or =10 cm diameter at breast height (DBH) were the only variables that significantly correlated with the variation in mangabey abundance. No additional variables were significant when the analysis was limited to forest fragments inside the Tana River Primate National Reserve (TRPNR) or to fragments outside the TRPNR. When I estimated the resources available before recent human forest product use by adding nonharvested and harvested variables, the total basal area of the top 15 food species became significant. This was only within the TRPNR, however. Management, therefore, should focus on increasing forest area, density of trees > or =10 cm DBH, and coverage of food trees throughout the mangabey's distribution. Solutions must be found for the problem of forest clearing, and forest product use must be better managed to protect the habitat of this critically endangered primate. The significance of food abundance only within the TRPNR suggests a need to collect dietary data from mangabey groups in fragments toward the southern limit of the mangabey's distribution, where plant species composition differs from that in fragments in which dietary data have been previously collected.     

A global assessment of primate responses to landscape structure

Land‐use change modifies the spatial structure of terrestrial landscapes, potentially shaping the distribution, abundance and diversity of remaining species assemblages. Non‐human primates can be particularly vulnerable to landscape disturbances, but our understanding of this topic is far from complete. Here we reviewed all available studies on primates' responses to landscape structure. We found 34 studies of 71 primate species (24 genera and 10 families) that used a landscape approach. Most studies (82%) were from Neotropical forests, with howler monkeys being the most frequently studied taxon (56% of studies). All studies but one used a site‐landscape or a patch‐landscape study design, and frequently (34% of studies) measured landscape variables within a given radius from the edge of focal patches. Altogether, the 34 studies reported 188 responses to 17 landscape‐scale metrics. However, the majority of the studies (62%) quantified landscape predictors within a single spatial scale, potentially missing significant primate–landscape responses. To assess such responses accurately, landscape metrics need to be measured at the optimal scale, i.e. the spatial extent at which the primate–landscape relationship is strongest (so‐called ‘scale of effect’). Only 21% of studies calculated the scale of effect through multiscale approaches. Interestingly, the vast majority of studies that do not assess the scale of effect mainly reported null effects of landscape structure on primates, while most of the studies based on optimal scales found significant responses. These significant responses were primarily to landscape composition variables rather than landscape configuration variables. In particular, primates generally show positive responses to increasing forest cover, landscape quality indices and matrix permeability. By contrast, primates show weak responses to landscape configuration. In addition, half of the studies showing significant responses to landscape configuration metrics did not control for the effect of forest cover. As configuration metrics are often correlated with forest cover, this means that documented configuration effects may simply be driven by landscape‐scale forest loss. Our findings suggest that forest loss (not fragmentation) is a major threat to primates, and thus, preventing deforestation (e.g. through creation of reserves) and increasing forest cover through restoration is critically needed to mitigate the impact of land‐use change on our closest relatives. Increasing matrix functionality can also be critical, for instance by promoting anthropogenic land covers that are similar to primates' habitat.     

Evaluating the suitability of planted forests for African forest monkeys: a case study from Kakamega forest, Kenya

As natural forest cover declines, planted forests have come to occupy an increasing percentage of the earth's surface, yet we know little about their suitability as alternative habitat for wildlife. Although some primate species use planted forests, few studies have compared primate populations in natural and nearby planted forests. From March 2006 to July 2010, we conducted line transect surveys and assessed group sizes and compositions in natural and nearby 60-70 year old mixed indigenous planted forest to determine the densities of diurnal primate species (Colobus guereza, Cercopithecus mitis, C. ascanius) in these two forest types at Isecheno, Kakamega Forest, Kenya. Line transect data were analyzed using the Encounter Rate, Whitesides, and Distance sampling methods, which all provided broadly consistent results. We found that all three diurnal primate species occupy both natural and planted forest at Isecheno. However, group densities of the two Cercopithecus species were 42-46% lower in planted than in natural forest. Colobus guereza achieved comparable group densities in the two forest types, although the species is found in smaller groups, and thus at lower (35%) individual density, in planted than in natural forest. Following a logging episode in the planted forest mid-way through our study, Cercopithecus ascanius group densities fell by 60% while C. mitis and Colobus guereza group densities remained stable over the next two years. Overall, our results suggest that while primate species vary in their response to habitat disturbance, planted forest has the potential to contribute to the conservation of some African monkey species. Even for the relatively flexible taxa in our study, however, 60-70 year old mixed indigenous planted forest failed to support densities comparable to those in nearby natural forest. From the perspective of Kakamega's primates, planted forests may supplement natural forest, but are not an adequate replacement for it.     

Distribution,population density and conservation of the critically endangered brown spider monkey (<Emphasis Type="Italic">Ateles hybridus</Emphasis>) and other primates of the inter-Andean forests of Colombia

The inter-Andean tropical rainforests and dry forests of the Magdalena river basin (Tumbes-Choco-Magdalena biodiversity hotspot) in northern Colombia have undergone significant forest loss and degradation in recent decades. Six primate species inhabit this region, five of which are currently threatened with extinction and one of which—the brown spider monkey, Ateles hybridus—is considered critically endangered. Accurate and recent information on the distribution and conservation status of these threatened primate populations is scarce or nonexistent, even though such data are needed to implement successful conservation actions and management plans. Between 2006 and 2016, we evaluated the status and distribution of primates across inter-Andean lowland forests in northern Colombia. We visited 30 sites to evaluate the presence/absence of brown spider monkeys and other primate taxa in the region. We also carried out surveys at 10 of these sites to obtain estimates of primate population densities and demographic information from forests with different levels of anthropogenic disturbance. Novel data on primate presence/absence were obtained for 27 sites, and 136 records were collected in total. Only 33% of the sites visited were large forest fragments (>?500 Ha). This study confirms that at least six primate species are still present in the Rio Magdalena region, which represents the highest platyrrhine diversity west of the Andes. This study also confirms the persistence of a wild population of Colombian woolly monkeys (Lagothrix lagotricha lugens) in the Serranía de San Lucas. Assigning formal protected status to this region is an urgent priority for the conservation of primates in the Rio Magdalena region.     

Social interaction in nonhuman primates: an underlying theme for primate research.

Social living is assumed to be a critical feature of nonhuman primate existence inasmuch as most primate species live in social groups in nature. Recent USDA legislation emphasizes the importance of social contact in promoting psychological well-being and recommends that laboratory primates be housed with companions when consistent with research protocols. Our goals were to examine the link between social housing and psychological well-being and to explore the idea that research may be compromised when primates are studied in environments that vary too greatly from their natural ecological setting (individual cage housing versus group housing). Three general points emerge from these examinations. First, providing companionship may be a very potent way in which to promote psychological well-being in nonhuman primates; however, social living is not synonymous with well-being. The extent to which social housing promotes psychological well-being can vary across species and among individual members of the same species (for example, high- and low-ranking monkeys). Secondly, housing conditions can affect research outcomes in that group-housed animals may differ from individually housed animals in response to some manipulation. Social interaction may be a significant variable in regulating the biobehavioral responses of nonhuman primates to experimental manipulations. Finally, a larger number of socially housed subjects than individually housed subjects may be necessary for some biomedical research projects to yield adequate data analysis. Thus, social living has significant benefits and some potential costs not only for the animals themselves, but for the research enterprise.