Mentorship and professional growth for conservationists in primate-range countries.

Ways to support professional capacity of emerging conservation leadership in primate range countries.

Can we eliminate the primate pet trade in the United States?

International laws and conventions have gone a long way in reducing the number of wild primates entering the United States of America (US) for the pet trade. However, breeding primates for sale to private owners in the United States continues, and individual states present a bewildering array of laws and regulations on the holding of primates as pets. As primatologists we can act to decrease the demand for primate pets by (1) speaking out on the inappropriate use of primates in mass media and especially in social media; (2) not posing in photographs in close proximity to primates; (3) continuing to educate about why primates do not make good pets; and (4) contributing to the science that underlies state and federal legislation with the goal of eliminating captive breeding of primates for the pet trade. We encourage primatologists and others in related fields to be cognizant of the persistent commercialization of primates and be willing to take action to deter it.

Historical antecedents and recent innovations in pitheciid (titi, saki, and uakari) feeding ecology.

The modern pitheciids (titis, sakis, and uakaris) of northern South America represent one of the earliest radiations of platyrrhines and demonstrate morphological adaptations and ecological strategies for seed eating. While seeds can provide reliable resources for relatively long periods of time, they are often well protected by thick husks and hard seed coverings. Seeds also tend to be rich in lipids, but they may also be high in indigestible fiber. Even though seed eaters are found in each major primate radiation, only the pitheciids demonstrate primary adaptations for eating seeds. In this partly historical, partly contemporary review, I examine the ecological and anatomical correlates of seed eating. It is dedicated to two well-known field primatologists: ecologist and conservationist J. Márcio Ayres; and anatomist and ecologist Warren G. Kinzey. Using observations in Kinzey (1992, Am J Phys Anthropol, 88, pp. 499-514) as a framework, I provide context and analysis for the intervening three decades of pitheciid research to identify what we know about this understudied group of primates and propose directions for future work.

Reducing the primate pet trade: Actions for primatologists.

This commentary emerged from a panel presentation at the International Primatological Society Congress in Nairobi, Kenya, 2018. The goal was to provide regional updates on the status of primate removal from habitat countries, especially for the pet trade, and develop guidelines that could help primatologists address this critical problem. The trade in live primates includes those used as pets, in entertainment, and as subjects of biomedical experimentation, but here we focus on those primates destined for the pet trade. Such transactions are a hugely lucrative business, impacting hundreds of thousands of individuals annually and affecting the survival of wild populations. Being intimately familiar with primate social behavior, life history and biology, primatologists, whether they work with captive or wild primates, are in a unique position to understand the nature of the trade and attempt to counter its effects. In addition to updating the status of the primate pet trade, we provide recommendations that may help primatologists formulate a plan to deal, locally and regionally, with illegal trafficking in live primates. General guidelines include increasing awareness of local customs, policies and laws; developing collaborative research opportunities for local people; engaging in training/informational opportunities; and instructing on how to take action when encountering illegally-trafficked primates.

Commentaries on field-laboratory collaborations in primatology: Introduction to a special section of the American Journal of Primatology.

Finding better approaches to bridge field and laboratory primate research was identified as an important goal in a recent (2017) member survey of the American Society of Primatologists. Collaborative field-captive research was identified by >60% of respondents as somewhat or very underrepresented in the Society. In this introductory essay for a special section of American Journal of Primatology, I review commonalities and differences in the papers that were requested from field-captive primate collaborative teams. Each team approached important primate biology or welfare problems from different perspectives. The five commentaries in this section addressed how the collaborations began, scientific benefits that accrued, and insights or challenges that researchers faced in the collaboration. Despite the fact that the specific fields of inquiry were different (conservation genetics, chimpanzee captive welfare, environmental physiology, feeding biology, and reproductive physiology), the commentaries converged on the concept that an intentional, interdisciplinary approach, that included field observations and experiments informed by laboratory expertise, were essential to achieving innovative results.

Bearded saki feeding strategies on an island in Lago Guri, Venezuela.

Free-ranging bearded sakis (Chiropotes spp.) live in relatively large social groups (22-65+), inhabit very large home ranges (200-1,000 ha), and travel long distances (1.8 to >7 km) each day. While these characteristics would seem to reduce their ability to occupy habitat fragments, several studies suggest otherwise. The key to their success may lie in their dietary adaptations. Bearded sakis are strongly frugivorous, but are primarily seed eaters, and are able to ingest both young and mature fruit. We examined feeding activities of a group of bearded sakis over a 19-month period on a 180 ha island in Lago Guri, Venezuela. Given their feeding adaptations, we predicted that they would minimize peaks and troughs in plant species used for food, limit seasonal variation in the mechanical properties of foods ingested, and balance ingestion of energy-rich foods (e.g. lipids, nonstructural carbohydrates (TNC), and/or free simple sugars). We found that bearded sakis on Danto Manchado had a diverse (plant-based) diet, but two resources (Pradosia caracasana, Sapotaceae, and Oryctanthus alveolatus, Loranthaceae) provided a stable dietary base and were present in the diet almost every month. Second, we found little variation in the mechanical-resistance properties of fruits opened seasonally. Third, they alternated months ingesting foods with high TNC content and months of high lipid content. This may be an attempt to balance energy intake from available foods. Finally, their social propensity to split up into subgroups may predispose them to reduce group sizes to accommodate smaller available areas. We suggest that bearded sakis use both ecological and behavioral mechanisms to survive in smaller-than-typical areas. Longer-term studies (beyond a few generations) of bearded sakis in habitat fragments would allow us to estimate minimum survival area and identify critical resources or resource combinations.

Strategies for navigating large areas: a GIS spatial ecology analysis of the bearded saki monkey, Chiropotes sagulatus, in Suriname.

Animals with long day paths and large home ranges expend a considerable amount of energy on travel. Studies have shown that in the interest of reducing energy expenditure, animals selectively navigate the landscape using a variety of strategies. However, these studies have generally focused on terrestrial animals. Here we present data on an exceedingly mobile arboreal animal, bearded saki monkeys, in a topographically variable landscape in Suriname. Using ArcMap and Google Earth, we explore two potential navigation strategies: the nonrandom use of travel areas and the use of ridges in slope navigation. Over a year of data collection, bearded sakis were found to use relatively long travel paths daily, use some areas more intensely than others for travel, and when travel paths were converted to strings of points, 40.3% and 63.9% of the points were located on (50 m from the main ridgeline) or near (100 m from the main ridgeline) ridge tops, respectively. Thus in a habitat of high relief we found support for intensive use of ridge tops or slopes close to ridge tops by bearded sakis. Selective habitat use may be related to surveying tree crowns for fruit by large, fast moving groups of bearded sakis or monitoring the presence of potential predators.

Relative brain size, gut size, and evolution in New World monkeys.

The dynamics of brain evolution in New World monkeys are poorly understood. New data on brain weight and body weight from 162 necropsied adult individuals, and a second series on body weight and gut size from 59 individuals, are compared with previously published reports based on smaller samples as well as large databases derived from museum records. We confirm elevated brain sizes for Cebus and Saimiri and also report that Cacajao and Chiropotes have relatively large brains. From more limited data we show that gut size and brain mass have a strongly inverse relationship at the low end of the relative brain size scale but a more diffuse interaction at the upper end, where platyrrhines with relatively high encephalization quotients may have either relatively undifferentiated guts or similar within-gut proportions to low-EQ species. Three of the four main platyrrhine clades exhibit a wide range of relative brain sizes, suggesting each may have differentiated while brains were relatively small and a multiplicity of forces acting to maintain or drive encephalization. Alouatta is a likely candidate for de-encephalization, although its "starting point" is difficult to establish. Factors that may have compelled parallel evolution of relatively large brains in cebids, atelids and pitheciids may involve large social group sizes as well as complex foraging strategies, with both aspects exaggerated in the hyper-encephalized Cebus. With diet playing an important role selecting for digestive strategies among the seed-eating pitheciins, comparable in ways to folivores, Chiropotes evolved a relatively larger brain in conjunction with a moderately large and differentiated gut.

Physical properties of fruit and seeds ingested by primate seed predators with emphasis on sakis and bearded sakis.

Several primate radiations exhibit dental adaptations that enable them to gain access to seeds embedded in well-protected fruit. To a database drawn from published sources in which hardness of fruit and seeds were tested in the field, we added an additional 100+ species of plants used as resources by pitheciin primates (specifically, South American white-faced sakis (Pithecia pithecia) and bearded sakis (Chiropotes spp.). This sample allowed us to compare hardness of fruit and seeds and deduce the relative incisive and masticatory capability of several primate taxa (New World monkeys, Old World monkeys, prosimians and chimpanzees). Pitheciins have very well developed and highly modified anterior dentition that they use in gaining access to mechanically-protected fruit. In addition, their molars bear thin, but decussated enamel that protects the tooth enamel from crack proliferation. The ability of sakis (Chiropotes spp. and Pithecia pithecia) to open fruit orally was comparable to larger-bodied Old World seed predators-Lophocebus and Cercocebus. But, baboons and chimpanzees masticate seeds that are two to three orders of magnitude harder than sakis or mangabeys. In spite of their puncture abilities, ∼40% of foods ingested by pitheciins were in the range of a ripe fruit eater (Ateles paniscus). This raises the possibility that pitheciins exemplify Liem's paradox, that is, "that phenotypic specialization [is] not accompanied by ecological specialization" (Robinson and Wilson, 1998:224). Last, we examined the possibility that seeds may serve as fallback resources for primate seed predators. While pericarp hardness may vary seasonally for some seed predators (e.g., mangabeys), our data on bearded sakis and white-faced sakis suggest that seeds are their primary resources year round and pericarp hardness is unrelated to seasonal variation in rainfall. Pitheciins evolved specialized dentition that affords them access to relatively abundant and high-quality resources, a feeding strategy that results in minimal variation in resource availability seasonally.

Within-group social bonds in white-faced saki monkeys (Pithecia pithecia) display male-female pair preference.

White-faced saki monkeys (Pithecia pithecia) lack most of the behavioral and physical traits typical of primate monogamy [Fuentes, 1999]. In order to determine if social bonds in this species reflect patterns displayed by pair-bonded groups or larger multimale-multifemale groups, we draw on 17 months of data collected on wild white-faced sakis at Brownsberg Nature Park, Suriname. We analyzed within-group social bonds for three habituated groups (one two-adult and two multiadult groups) by measuring grooming, proximity, and approach/leave patterns between adult and subadult group members. We found that both two-adult and multiadult groups showed significantly stronger social bonds between a single male-female dyad within each group (deemed "primary dyads"). In all three groups, primary dyads were composed of the oldest adult male and a breeding female. These pairs had significantly higher levels of grooming than other within-group dyads and were also in close proximity (<1 m) more often than nonprimary dyads. Grooming in primary dyads was nonreciprocal, and consistently biased toward female investment. Grooming patterns in nonprimary dyads varied, but were often more reciprocal. Grooming and proximity of the primary dyad also changed in relation to infant development. Our results suggest that while white-faced sakis do not show behavioral and physical traits typical of monogamy or pair-bonding, social bonds are strongest between a single male-female pair. Pitheciine social systems range from small group monogamy in Callicebus to large multimale-multifemale groups in Chiropotes and Cacajao. As the middle taxon in this platyrrhine radiation, behavioral strategies of white-faced sakis provide a model for how social bonds and affiliation could be influenced by and affect the evolution of larger group size in primates.

Primates in 21st century ecosystems: does primate conservation promote ecosystem conservation?

Contributors to this issue of the American Journal of Primatology were among the participants in an invited symposium at the 2008 Association for Tropical Biology and Conservation meeting in Paramaribo, Suriname. They were asked to assess how essential primates are to tropical ecosystems and, given their research interests, discuss how primate research contributes to the broader understanding about how ecosystems function. This introduction to the issue is divided into three parts: a review of the roles that nonhuman primates play in tropical ecosystems; the implementation of large-scale landscape methods used to identify primate densities; and concerns about the increasingly porous boundaries between humans, nonhuman primates, and pathogens. Although 20th century primate research created a rich database on individual species, including both theoretical and descriptive approaches, the dual effects of high human population densities and widespread habitat destruction should warn us that creative, interdisciplinary and human-related research is needed to solve 21st century problems.

Optimal foraging on the roof of the world: Himalayan langurs and the classical prey model.

Optimal foraging theory has only been sporadically applied to nonhuman primates. The classical prey model, modified for patch choice, predicts a sliding "profitability threshold" for dropping patch types from the diet, preference for profitable foods, dietary niche breadth reduction as encounter rates increase, and that exploitation of a patch type is unrelated to its own abundance. We present results from a 1-year study testing these predictions with Himalayan langurs (Semnopithecus entellus) at Langtang National Park, Nepal. Behavioral data included continuous recording of feeding bouts and between-patch travel times. Encounter rates were estimated for 55 food types, which were analyzed for crude protein, lipid, free simple sugar, and fibers. Patch types were entered into the prey model algorithm for eight seasonal time periods and differing age-sex classes and nutritional currencies. Although the model consistently underestimated diet breadth, the majority of nonpredicted patch types represented rare foods. Profitability was positively related to annual/seasonal dietary contribution by organic matter estimates, whereas time estimates provided weaker relationships. Patch types utilized did not decrease with increasing encounter rates involving profitable foods, although low-ranking foods available year-round were taken predominantly when high-ranking foods were scarce. High-ranking foods were taken in close relation to encounter rates, while low-ranking foods were not. The utilization of an energetic currency generally resulted in closest conformation to model predictions, and it performed best when assumptions were most closely approximated. These results suggest that even simple models from foraging theory can provide a useful framework for the study of primate feeding behavior.

Digesta passage and fiber digestibility in captive white-faced sakis (Pithecia pithecia).

Wild white-faced sakis (Pithecia pithecia) ingest primarily seeds that provide a diet that is lipid-rich and moderately high in dietary fiber. Although little anatomical information is available on sakis, evidence from other vertebrate seed predators suggests that such a diet is correlated with adaptations in gut morphology or physiology. Milton [1984] reported a 20 hr transit time (TT=transit time or time of first appearance in feces) of a particulate marker for a single monk saki (Pithecia monachus). This suggests that TT for Pithecia sakis may be four to five times longer than what has been reported for soft-fruit-eating platyrrhines, such as Ateles and Cebus. During a captive study, we calculated an average TT of 14.7+/-0.4 hr (n=5 trials started in the evening) for a chromic oxide (Cr(2)O(3)) marker that follows liquid digesta and TTs of 14.5 hr (trial started the previous evening) and 23.0 hr (trial started the previous morning) for two trials using particulate markers. Mean retention time (MRT) for the liquid marker ranged from 15.3 hr to 37.7 hr in four trials that lasted longer than 90 hr. Marker recovery was incomplete for the particulate markers in these trials, and thus MRT could only be determined for the liquid phase marker. Three 5-day trials on a low-fiber, blended diet revealed high fiber fraction digestibilities (neutral detergent fiber (NDF)=77.4% and acid detergent fiber (ADF)=74.4%). Data collected for this study and nutritional data from wild sakis suggest that pitheciin seed predators may have a potential for fiber digestibility that is intermediate between ripe-pulp frugivores and folivores.

Challenge of neotropical frugivory: Travel patterns of spider monkeys and bearded sakis.

We compared travel patterns of two neotropical frugivores, Ateles paniscus (black spider monkeys) and Chiropotes satanas (bearded sakis), during a 6-month study at Raleighvallen-Voltzberg Nature Reserve in Surinam. Ateles were typically found in small foraging parties that changed in size and composition throughout the day. Chiropotes troops moved from one feeding area to the next, fragmenting "locally" when they entered an area with more than one feeding tree. Chiropotes moved through fewer half-hectare quadrats before encountering a feeding tree, and were more likely to locate multiple trees per quadrat than were Ateles. Several investigators have suggested that fission-fusion travel patterns (sensu Ateles and Pan) have the potential to reduce feeding competition among troop members. We suggest that even slight modifications in the size and composition of foraging parties, such as "local" temporary troop fragmentation, have the same effect, and may be common among frugivorous primates. © 1994 Wiley-Liss, Inc.

Predation by jaguar on howler monkeys (Alouatta seniculus) in Venezuela.

We document the loss of all but the youngest member of a troop of six howler monkeys due to probable jaguar predation during a 7-month period in 1988. The formation of Guri Lake resulted in forest fragmentation which forced monkeys into new and unfamiliar areas and altered the balance of predator and prey populations, and may thus have contributed indirectly to the success of the jaguar. The selection of defoliated (dead) trees for sleeping sites by the howlers may have directly increased the risk of predation. © 1992 Wiley-Liss, Inc.

Mechanisms promoting stability in mixed Saguinus mystax and S. fuscicollis troops.

Mixed-species troops composed of two species of tamarin monkeys, and rarely other ceboids, occur throughout much of western Amazonia and are notable for their long-term stability. This study identified several variables that appeared to promote mixed-species troop cohesion and yet maintained spatial segregation between species. Three variables enhanced in terspecific spatial segregation: differences in support use, vertical stratification, and interindividual spacing. In contrast, early morning vocalizations and well-coordinated movement patterns contribute to cohesion within a mixed-species troop. The combination of these variables may help explain how two congeneric species accommodate one another with little apparent interspecific aggression. The exact nature of benefits and costs to each individual in a mixed troop is still elusive; however, a comparison of population densities of sympatric and allopatric tamarins suggests that population growth of one partner (Saguinus fuscicollis) is enhanced in the presence of a congeneric species.