Sarah A. Boyle

Impending extinction crisis of the world's primates: why primates matter

Impending extinction of the world’s primates due to human activities; immediate global attention is needed to reverse the trend. 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.

Home Range Estimates Vary with Sample Size and Methods

Accurate estimates of a primate’s home range are important, yet methods vary greatly. This paper examines the accuracy of minimum convex polygon (MCP), adaptive kernel (AK) and fixed kernel (FK) estimators by comparing home range estimates of northern bearded saki monkeys (Chiropotes satanas chiropotes) living in forest fragments and continuous forest in the Brazilian Amazon area. MCP was more accurate than AK and FK in calculating home and day range when sample size was small, and AK overestimated range most frequently. It is important to consider the various home range methods, as the appropriate method may depend on sample size and the species’ behavioral ecology.

High-Resolution Satellite Imagery Is an Important yet Underutilized Resource in Conservation Biology

Technological advances and increasing availability of high-resolution satellite imagery offer the potential for more accurate land cover classifications and pattern analyses, which could greatly improve the detection and quantification of land cover change for conservation. Such remotely-sensed products, however, are often expensive and difficult to acquire, which prohibits or reduces their use. We tested whether imagery of high spatial resolution (≤5 m) differs from lower-resolution imagery (≥30 m) in performance and extent of use for conservation applications. To assess performance, we classified land cover in a heterogeneous region of Interior Atlantic Forest in Paraguay, which has undergone recent and dramatic human-induced habitat loss and fragmentation. We used 4 m multispectral IKONOS and 30 m multispectral Landsat imagery and determined the extent to which resolution influenced the delineation of land cover classes and patch-level metrics. Higher-resolution imagery more accurately delineated cover classes, identified smaller patches, retained patch shape, and detected narrower, linear patches. To assess extent of use, we surveyed three conservation journals (Biological Conservation, Biotropica, Conservation Biology) and found limited application of high-resolution imagery in research, with only 26.8% of land cover studies analyzing satellite imagery, and of these studies only 10.4% used imagery ≤5 m resolution. Our results suggest that high-resolution imagery is warranted yet under-utilized in conservation research, but is needed to adequately monitor and evaluate forest loss and conversion, and to delineate potentially important stepping-stone fragments that may serve as corridors in a human-modified landscape. Greater access to low-cost, multiband, high-resolution satellite imagery would therefore greatly facilitate conservation management and decision-making.

Implications of habitat fragmentation on the diet of bearded saki monkeys in central Amazonian forest

Abstract Forest fragmentation demonstrably alters plant species composition, distribution, and diversity, and, in turn, may affect the availability of food resources for primary consumers. We investigated to what extent fragmentation affected the diets of 6 groups of bearded saki monkeys (Chiropotes chiropotes) living in two 10-ha fragments, two 100-ha “fragments” that were no longer fully isolated, and 2 areas of continuous forest in central Amazonia. When changes occurred we tested whether differences in diet were due to plant species availability by comparing the prevalence of consumed items against their relative abundance at the 6 sites. In total, the monkeys consumed fruits, seeds, flowers, and leaves of 244 plant species, of which less than 2% were shared among all 6 groups. Although there was a positive correlation between relative abundance of diet species and consumption frequency, monkeys did not eat all available potential resources, and groups inhabiting the 10-ha fragments consumed items that were ignored in larger forested areas. Our findings suggest that bearded sakis living in small forest fragments are limited in their dietary choices as a consequence of the reduced number of plant species present, and therefore consume species that monkeys inhabiting continuous forests typically can ignore. We conclude that the ability to consume a diverse diet that includes seeds and unripe fruit helps this species survive in forest fragments, but it appears that these conditions are unviable unless connectivity increases among the forest fragments and continuous forest in the landscape. RESUMEN Comprovadamente a fragmentação florestal altera a composição das espécies de plantas, sua distribuição e diversidade, afetando por sua vez a disponibilidade de recursos para consumidores primários. Neste contexto, investigamos se a fragmentação florestal afetou as dietas de 6 grupos de macaco-cuxiú (Chiropotes chiropotes) presentes em 2 fragmentos florestais de 10 ha isolados, 2 de 100 ha parcialmente isolados, e em 2 áreas de mata contínua na Amazônia Central. Quando mudanças foram detectadas, nós testamos se as diferenças nas dietas foram relacionadas à disponibilidade de recursos, comparando a prevalência de itens consumidos em relação à sua abundância relativa nos 6 sítios amostrados. No total, os macacos consumiram frutos, sementes e flores de 244 espécies vegetais, das quais menos de 2% foram consumidas por todos os 6 grupos. Embora houve uma correlação positiva entre abundância relativa de espécies utilizadas na dieta e frequência de consumo, os macacos não utilizaram todas as espécies de plantas disponíveis no ambiente, e grupos habitantes de fragmentos de 10 ha consumiram recursos que foram ignorados pelos demais em ambientes florestais de maior porte. Nossos resultados sugerem que cuxiús que habitam pequenos fragmentos florestais são limitados em suas escolhas alimentares em consequência do número reduzido de espécies vegetais presentes e, como consequência, consomem espécies de plantas que são ignoradas pelos que habitam floresta contínua. Nós concluímos que a capacidade de utilizar uma dieta diversa, como sementes e frutos imaturos, contribui para que este primata sobreviva em fragmentos florestais. No entanto, esta condição nos parece viável somente se houver maior conectividade entre os fragmentos e florestas contínuas dentro da paisagem.

Primary seed dispersal by three Neotropical seed-predating primates ( Cacajao melanocephalus ouakary , Chiropotes chiropotes and Chiropotes albinasus )

The Neotropics house two guilds of large arboreal vertebrate seed predators: parrots and the pitheciin primates. Both have diets dominated by immature fruits. The possibility of members of the Pitheciinae (genera Cacajao, Chiropotes and Pithecia) acting as occasional seed dispersers has been mooted, but not experimentally shown. We combined primate behavioural data and seed germination data from three separate field studies in the Brazilian states of Amazonas and Para to analyse patterns of post-consumption seed survivorship for seeds discarded by three pitheciin species (Cacajao melanocephalus ouakary, Chiropotes chiropotes and Chiropotes albinasus). We then calculated the frequency of dispersal events for four species eaten by C. m. ouakary. All three primate species dropped intact seeds while feeding, and 30.7% of 674 dropped seeds germinated ex situ. Undamaged seeds from unripe and ripe samples germinated (29.3% and 42.7%. respectively), and all three primate species carried some fruits up to 20 m from the parent tree before consuming them. Potential seed-dispersal events varied from 1 (Macrolobium acaciifolium) per fruiting cycle to more than 6500 (Duroia velutina), suggesting that there are differences in dispersal potential. In summary, although they are highly specialized seed predators, these primates may also act as important dispersers for some plant species, and effective dispersal is not restricted to ripe fruits, as immature fruits removed from a tree may continue to mature and the seeds later germinate, a much-neglected aspect of dispersal ecology. The possibility that similar events occur in parrots should be experimentally investigated.

Terrestrial Activity in Pitheciins (Cacajao, Chiropotes, and Pithecia)

Neotropical monkeys of the genera Cacajao, Chiropotes, and Pithecia (Pitheciidae) are considered to be highly arboreal, spending most of their time feeding and traveling in the upper canopy. Until now, the use of terrestrial substrates has not been analyzed in detail in this group. Here, we review the frequency of terrestrial use among pitheciin taxa to determine the ecological and social conditions that might lead to such behavior. We collated published and unpublished data from 14 taxa in the three genera. Data were gleaned from 53 published studies (including five on multiple pitheciin genera) and personal communications of unpublished data distributed across 31 localities. Terrestrial activity was reported in 61% of Pithecia field studies (11 of 18), in 34% of Chiropotes studies (10 of 29), and 36% of Cacajao studies (4 of 11). Within Pithecia, terrestrial behavior was more frequently reported in smaller species (e.g. P. pithecia) that are vertical clingers and leapers and make extensive use of the understory than in in the larger bodied canopy dwellers of the western Amazon (e.g. P. irrorata). Terrestrial behavior in Pithecia also occurred more frequently and lasted longer than in Cacajao or Chiropotes. An apparent association was found between flooded habitats and terrestrial activity and there is evidence of the development of a “local pattern” of terrestrial use in some populations. Seasonal fruit availability also may stimulate terrestrial behavior. Individuals also descended to the ground when visiting mineral licks, escaping predators, and responding to accidents such as a dropped infant. Overall, the results of this review emphasize that terrestrial use is rare among the pitheciins in general and is usually associated with the exploitation of specific resources or habitat types. Am. J. Primatol. 74:1106‐1127, 2012.

Human impacts on primate conservation in central Amazonia

Deforestation in the Amazon is a serious environmental, economic, and social concern. This article examines how a colonization plan to bring 180 families to an area north of Manaus, Brazil, would negatively impact the conservation of the six primate species residing in the area. The colonization sites would be located within the Biological Dynamics Forest Fragments Project (BDFFP) study area, the longest-running study of forest fragmentation. An increase in human density in the area would likely increase deforestation and hunting pressure on the fauna, thereby threatening those species that have not fared well in forest fragments. Furthermore, the colonization plan threatens future research at BDFFP and other research sites, as well as the Central Amazonian Conservation Corridor. This would be a great scientific and conservation loss.

Primates of the Biological Dynamics of Forest Fragments Project: A History

The Biological Dynamics of Forest Fragments Project (BDFFP), located approximately 80 km north of Manaus, Brazil, is the longest-running study of forest fragmentation in the world. The BDFFP was created in 1979 and the first primate census occurred in 1980. Six primate species inhabit the study area: red howler (Alouatta macconnelli), black spider (Ateles paniscus), brown capuchin (Sapajus apella), northern bearded saki (Chiropotes satanas chiropotes), golden-faced saki (Pithecia chrysocephala), and golden-handed tamarin (Saguinus midas). The distribution of these six species throughout the forest fragments has varied during the past three decades with some species (i.e., howler monkeys) being more prevalent than others (i.e., spider monkeys), particularly in the smaller fragments. Researchers did not find primates in some of the 1-ha forest fragments prior to 2007. Here we present a history of primate research at the BDFFP, including findings from three decades of primate censuses and behavioral and ecological studies of several species in the forest fragments, the surrounding matrix, and the continuous forest. These primate studies have provided information on seed dispersal in forest fragments, parasite infections, use of the matrix, and changes in group size, activity budget, and diet of groups in the forest fragments. Many of the once-cleared pastures surrounded by continuous primary forest are now dominated by various stages of secondary growth. Unfortunately, deforestation continues in many areas of the continuous forest north of Manaus. We discuss the implications of these land-cover changes on the primate community and suggest avenues for future primate research at the BDFFP.

Geographic comparison of plant genera used in frugivory among the pitheciids Cacajao, Callicebus, Chiropotes, and Pithecia.

Pitheciids are known for their frugivorous diets, but there has been no broad‐scale comparison of fruit genera used by these primates that range across five geographic regions in South America. We compiled 31 fruit lists from data collected from 18 species (three Cacajao, six Callicebus, five Chiropotes, and four Pithecia) at 26 study sites in six countries. Together, these lists contained 455 plant genera from 96 families. We predicted that 1) closely related Chiropotes and Cacajao would demonstrate the greatest similarity in fruit lists; 2) pitheciids living in closer geographic proximity would have greater similarities in fruit lists; and 3) fruit genus richness would be lower in lists from forest fragments than continuous forests. Fruit genus richness was greatest for the composite Chiropotes list, even though Pithecia had the greatest overall sampling effort. We also found that the Callicebus composite fruit list had lower similarity scores in comparison with the composite food lists of the other three genera (both within and between geographic areas). Chiropotes and Pithecia showed strongest similarities in fruit lists, followed by sister taxa Chiropotes and Cacajao. Overall, pitheciids in closer proximity had more similarities in their fruit list, and this pattern was evident in the fruit lists for both Callicebus and Chiropotes. There was no difference in the number of fruit genera used by pitheciids in habitat fragments and continuous forest. Our findings demonstrate that pitheciids use a variety of fruit genera, but phylogenetic and geographic patterns in fruit use are not consistent across all pitheciid genera. This study represents the most extensive examination of pitheciid fruit consumption to date, but future research is needed to investigate the extent to which the trends in fruit genus richness noted here are attributable to habitat differences among study sites, differences in feeding ecology, or a combination of both. Am. J. Primatol. 78:493–506, 2016.

Run, hide, or fight: anti-predation strategies in endangered red-nosed cuxiú (Chiropotes albinasus, Pitheciidae) in southeastern Amazonia

Although primate predation is rarely observed, a series of primate anti-predation strategies have been described. Energetic costs of such strategies can vary from high-cost mobbing, via less costly alarm calling, to low-cost furtive concealment. Here we report the anti-predation strategies of red-nosed cuxiú, Chiropotes albinasus, based on direct observations from four study sites in southeastern Brazilian Amazonia. Over a collective period of 1255 fieldwork hours, we observed nine direct interactions between raptors (all potential predators) and red-nosed cuxiús. Of these, one (11%) resulted in predation. Raptors involved were: Harpia harpyja (four events), Leucopternis sp. (two events), Spizaëtus tyrannus (one event), and unidentified large raptors (two events). Predation attempts occurred in flooded-forest and terra firme rainforest, were directed at both adult and non-adult cuxiús, and involved both adult and juvenile raptors. Anti-predation strategies adopted by the cuxiús included: (1) group defence and mobbing behaviour (two occasions), (2) dropping into dense sub-canopy (seven occasions), (3) alarm calling (eight occasions), and (4) fleeing to, and hiding in, dense vegetation (eight occasions). During each encounter at least two of these behaviours were recorded. These are the first published records of predation, predation attempts, and anti-predator behaviour involving red-nosed cuxiú.