Human activity and climate change accelerate the extinction risk to non-human primates in China.

Human activity and climate change affect biodiversity and cause species range shifts, contractions, and expansions. Globally, human activities and climate change have emerged as persistent threats to biodiversity, leading to approximately 68% of the ~522 primate species being threatened with extinction. Here, we used habitat suitability models and integrated data on human population density, gross domestic product (GDP), road construction, the normalized difference vegetation index (NDVI), the location of protected areas (PAs), and climate change to predict potential changes in the distributional range and richness of 26 China's primate species. Our results indicate that both PAs and NDVI have a positive impact on primate distributions. With increasing anthropogenic pressure, species' ranges were restricted to areas of high vegetation cover and in PAs surrounded by buffer zones of 2.7-4.5 km and a core area of PAs at least 0.1-0.5 km from the closest edge of the PA. Areas with a GDP below the Chinese national average of 100,000 yuan were found to be ecologically vulnerable, and this had a negative impact on primate distributions. Changes in temperature and precipitation were also significant contributors to a reduction in the range of primate species. Under the expected influence of climate change over the next 30-50 years, we found that highly suitable habitat for primates will continue to decrease and species will be restricted to smaller and more peripheral parts of their current range. Areas of high primate diversity are expected to lose from 3 to 7 species. We recommend that immediate action be taken, including expanding China's National Park Program, the Ecological Conservation Redline Program, and the Natural Forest Protection Program, along with a stronger national policy promoting alternative/sustainable livelihoods for people in the local communities adjacent to primate ranges, to offset the detrimental effects of anthropogenic activities and climate change on primate survivorship.

Scientific activism to protect the world's primates and their environments from extinction: Introduction to the special issue.

Nonhuman primates and their habitats are facing an impending extinction crisis. Approximately 69% of primate species are listed by the International Union for Conservation of Nature as threatened and 93% have declining populations. Human population growth (expected to reach 10.9 billion by the year 2100), the unsustainable demands of a small number of consumer nations for forest-risk commodities, deforestation and habitat conversion, the expansion of roads and rail networks, cattle ranching, the hunting and trapping of wild primate populations, and the potential spread of infectious diseases are among the primary drivers of primate population decline. Climate change will only exacerbate the current situation. The time to act to protect primate populations is now! In this special issue of the American Journal of Primatology, we present a series of commentaries, formulated as "Action Letters." These are designed to educate and inform primatologists, conservation biologists, wildlife ecologists, political leaders, and global citizens about the conservation challenges faced by particular primate taxa and particular world regions, and present examples of specific actions that one can take, individually and collectively, to promote the persistence of wild primate populations and environmental justice for local human populations and impacted ecological communities. As scientists, researchers, and educators, primatologists are in a unique position to lead local, national, and international efforts to protect biodiversity. In this special issue, we focus on primates of the Brazilian Amazon, lemurs of northeast Madagascar, Temminck's red colobus monkey (Piliocolobus badius temminckii), night monkeys (Aotus spp.), long-tailed macaques (Macaca fascicularis), the primate pet trade, and professional capacity building to foster conservation awareness and action. We encourage primatologists, regardless of their research focus, to engage in both advocacy and activism to protect wild primate populations worldwide.

An urgent call-to-action to protect the nonhuman primates and Indigenous Peoples of the Brazilian Amazon.

Primates are facing an impending extinction crisis. Here, we examine the set of conservation challenges faced by the 100 primate species that inhabit the Brazilian Amazon, the largest remaining area of primary tropical rainforest in the world. The vast majority (86%) of Brazil's Amazonian primate species have declining populations. Primate population decline in Amazonia has been driven principally by deforestation related to the production of forest-risk commodities including soy and cattle ranching, the illegal logging and setting of fires, dam building, road and rail construction, hunting, mining, and the confiscation and conversion of Indigenous Peoples' traditional lands. In a spatial analysis of the Brazilian Amazon, we found that 75% of Indigenous Peoples' lands (IPLs) remained forested compared with 64% of Conservation Units (CUs) and 56% of other lands (OLs). In addition, primate species richness was significantly higher on IPLs than on CUs and OLs. Thus, safeguarding Indigenous Peoples' land rights, systems of knowledge, and human rights is one of the most effective ways to protect Amazonian primates and the conservation value of the ecosystems they inhabit. Intense public and political pressure is required and a global call-to-action is needed to encourage all Amazonian countries, especially Brazil, as well as citizens of consumer nations, to actively commit to changing business as usual, living more sustainably, and doing all they can to protect the Amazon. We end with a set of actions one can take to promote primate conservation in the Brazilian Amazon.

A simple assay for measuring tannin-protein precipitation capacity offers insights into the diet and food choice of black howler monkeys (Alouatta pigra).

Phenolics, like tannins, are plant-specialized metabolites that play a protective role against herbivory. Tannins can reduce palatability and bind with proteins to reduce digestibility, acting as deterrents to feeding and impacting nutrient extraction by herbivores. Some assays measure tannin and total phenolics content in plants but lack determination of their biological effects, hindering the interpretation of tannin function in herbivory and its impacts on animal behavior and ecology. In this study, we successfully applied the radial diffusion assay to assess tannin protein precipitation (PP) capacity and evaluate the anti-nutritional effects of tannins in food plants (n = 24) consumed by free-ranging black howler monkeys (Alouatta pigra) in Tabasco, Mexico. We found PP rings in five plant species consumed by the monkeys. The mature fruit of Inga edulis was the most consumed food plant, despite having a high tannin PP capacity (56.66 mg tannic acid equivalent/g dry matter). These findings highlight the presence of tannins in the black howler diet and provide insight into the primates' resilience and potential strategies for coping with anti-nutritional aspects of the diet.

Wild gibbons plan their travel pattern according to food types of breakfast.

Planning for the future is a complex skill that is often considered uniquely human. This cognitive ability has never been investigated in wild gibbons (Hylobatidae). Here we evaluated the movement patterns from sleeping trees to out-of-sight breakfast trees in two groups of endangered skywalker gibbons (Hoolock tianxing). These Asian apes inhabit a cold seasonal montane forest in southwestern China. After controlling for possible confounding variables including group size, sleeping pattern (sleep alone or huddle together), rainfall and temperature, we found that food type (fruits or leaves) of the breakfast tree was the most important factor affecting gibbon movement patterns. Fruit breakfast trees were more distant from sleeping trees compared with leaf trees. Gibbons left sleeping trees and arrived at breakfast trees earlier when they fed on fruits compared with leaves. They travelled fast when breakfast trees were located further away from the sleeping trees. Our study suggests that gibbons had foraging goals in mind and plan their departure times accordingly. This ability may reflect a capacity for route-planning, which would enable them to effectively exploit highly dispersed fruit resources in high-altitude montane forests.

Effects of food availability and climate on the activity budget of Shortridge's langur (Trachypithecus shortridgei) in the Drung Valley, Gaoligong Mountains, China.

Food availability and climate represent environmental factors that affect species' social behavior, ranging patterns, diet, and activity budget. From August 2012 to September 2013, we examined the effects of seasonal changes in food availability, temperature, and rainfall on the diet and behavioral ecology of Shortridge's langur (Trachypithecus shortridgei) an Endangered primate species inhabiting moist evergreen broadleaf forests in the Eastern Himalayas. Our field site represents the northernmost latitudinal distribution of this species. Data were collected using scan sampling at 10 min intervals, and analyzed based on generalized linear models. The results indicate that the langurs experienced two feeding peaks (9:00 and 17:00) and two traveling peaks (10:00 and 19:00) during each day. Periods of rest, mainly occurred between 10:00 and 13:00, and overnight. Feeding accounted for 38.5% of the daily activity budget, followed by resting (35%), traveling (24.5%), and socializing (2%). During periods when young leaves were most available, the langurs increased feeding time on young leaves (35% vs. 4%). During periods of maximum fruit availability, the langurs decreased total time spent feeding (36.6% vs. 40.4%), devoted more time to traveling (28.1% vs. 21%), and increased time spent consuming fruit (49.1% vs. 11.8%). During the winter, the langurs increased their consumption of mature leaves (44.5%) and reduced time spent traveling (20.2% vs. 25.4%). Overall, time spent resting was greatest in the spring (47.5%), time spent feeding was greatest during the summer (51.1%), and time spent in traveling was greatest in the autumn (33.2%). The frequency of social interactions remained relatively constant throughout the year. Foraging effort was greatest in the summer, when fruits dominated the diet. Like other species of temperate langurs, T. shortridgei devoted less time to resting, more time to feeding, and was characterized by a greater year-round foraging effort than tropical/subtropical langurs.

Effects of provisioning on the activity budget and foraging strategies of black-and-white snub-nosed monkeys (Rhinopithecus bieti) in the Baima Snow Mountain Nature Reserve, Yunnan, China.

Provisioning can significantly affect the ranging patterns, foraging strategies, and time budget of wild primates. In this study, we document for the first time, the effects of provisioning on the activity budget and foraging effort in an Asian colobine. Over 3-years, we used an instantaneous scanning method at 10-min intervals to collect data on the activity budget of a semiprovisioned breeding band (SPB) of black-and-white snub-nosed monkeys (Rhinopithecus bieti) (42-70 individuals) at Xiangguqing (Tacheng), Yunnan, China. We then compared the effects of provisioning in our study band with published data on a sympatric wild nonprovisioned breeding band (NPB) of R. bieti (ca. 360 monkeys) at the same field site. The SPB spent 25.6% of their daytime feeding, 17.1% traveling, 46.9% resting, and 10.3% socializing. In comparison, the NPB devoted more time to feeding (34.9%) and socializing (14.1%), less time to resting (31.3%), and was characterized by a greater foraging effort (1.74 versus 0.96, foraging effort = (feeding + traveling)/resting; see Methods). There was no difference between bands in the proportion of their activity budget devoted to traveling (15.7% vs. 17.1%). In addition, the SPB exhibited a more consistent activity budget and foraging effort across all seasons of the year compared to the NPB. These findings suggest that the distribution, availability, and productivity of naturally occurring feeding sites is a major determinant of the behavioral strategies and activity budget of R. bieti. Finally, a comparison of our results with data on six nonprovisioned R. bieti bands indicates that caution must be raised in meta-analyses or intraspecific comparisons of primate behavioral ecology that contain data generated from both provisioned and nonprovisioned groups.

The faecal metabolome of black howler monkeys (Alouatta pigra) varies in response to seasonal dietary changes.

Mammals rely on the metabolic functions of their gut microbiota to meet their energetic needs and digest potentially toxic components in their diet. The gut microbiome plastically responds to shifts in host diet and may buffer variation in energy and nutrient availability. However, it is unclear how seasonal differences in the gut microbiome influence microbial metabolism and nutrients available to hosts. In this study, we examine seasonal variation in the gut metabolome of black howler monkeys (Alouatta pigra) to determine whether those variations are associated with differences in gut microbiome composition and nutrient intake, and if plasticity in the gut microbiome buffers shortfalls in energy or nutrient intake. We integrated data on the metabolome of 81 faecal samples from 16 individuals collected across three distinct seasons with gut microbiome, nutrient intake and plant metabolite consumption data from the same period. Faecal metabolite profiles differed significantly between seasons and were strongly associated with changes in plant metabolite consumption. However, microbial community composition and faecal metabolite composition were not strongly associated. Additionally, the connectivity and stability of faecal metabolome networks varied seasonally, with network connectivity being highest during the dry, fruit-dominated season when black howler monkey diets were calorically and nutritionally constrained. Network stability was highest during the dry, leaf-dominated season when most nutrients were being consumed at intermediate rates. Our results suggest that the gut microbiome buffers seasonal variation in dietary intake, and that the buffering effect is most limited when host diet becomes calorically or nutritionally restricted.

Foraging networks and social tolerance in a cooperatively breeding primate (Callithrix jacchus).

Within-group competition over food resources can be a major cost of social living. In the wild, foragers are confronted with social (e.g. hierarchical rank) and ecological (e.g. food availability and distribution) challenges that affect their foraging decisions and feeding success. Exhibiting prosocial behaviours, such as tolerance at feeding sites, can benefit group members by developing affiliative social relationships, enhancing access to resources and maximizing fitness. We examined social tolerance at feeding sites in Callithrix jacchus, a cooperatively breeding primate species. We investigated the set of social (rank, age and sex) and ecological (food availability) factors that influence the structure and dynamics of within-group foraging association networks. We designed and conducted an experimental field study of four wild groups of common marmosets in which we controlled food distribution (concentrated or scattered) and productivity (high, medium or low food rewards). Then, we used social network analyses to assess the number and strength of foraging associations among group members, their effects on individual food consumption, and whether recent experiences with conspecifics during foraging affected subsequent associations. Overall, common marmoset foraging association networks were cohesive, as group members jointly occupied feeding sites. The number and strength of associations varied depending on the ecological context. Associations were stronger during conditions in which food was concentrated at a single site. Individuals obtained greater access to food resources when sharing a feeding site with conspecifics, but once a food item was obtained, the forager moved to a nearby tree and consumed it away from others. Additionally, the strength of previous foraging associations and subsequent levels of social tolerance at feeding sites were positively related, a relationship compatible with the ability of memorizing associations over time and recalling the information in future decision-making. In sum, marmosets adjusted their partner choices and the strength of foraging associations in response to food availability. They exhibited increased social tolerance at feeding sites during conditions in which opportunities for contest competition were expected to be greatest. These cooperative breeding primates appear to mutually benefit by maintaining cohesive and strong affiliative relationships, and by increasing opportunities for coordinated behaviour and offspring survival.

A competição por recursos alimentares dentro do grupo pode ser um grande custo da vida social. Na natureza, os forrageadores são confrontados com desafios sociais (e.g. posição hierárquica) e ecológicos (e.g. disponibilidade e distribuição de alimentos) que afetam suas decisões de forrageio e seu sucesso alimentar. Exibir comportamentos pró-sociais, como tolerância em sítios de alimentação, pode beneficiar os membros do grupo, desenvolvendo relações sociais afiliativas, melhorando o acesso aos recursos e maximizando sua aptidão evolutiva. Examinamos a tolerância social de um primata com reprodução cooperativa (Callithrix jacchus) em sítios de alimentação. Investigamos a influência de um conjunto de fatores sociais (hierarquia, idade, sexo) e ecológicos (disponibilidade de alimento) na estrutura e dinâmica das redes de associação de forrageio dentro do grupo social. Planejamos e conduzimos um experimento de campo com quatro grupos de saguis-comuns de vida livre, no qual controlamos a distribuição (concentrada e dispersa) e a produtividade de alimento (altas, médias ou baixas recompensas). Usamos análise de redes sociais para avaliar o número e a força das associações de forrageio entre os membros do grupo, seu efeito no consumo individual de alimento, e se experiências recentes de forrageio entre coespecíficos afetam associações subsequentes. Em geral, as redes de associação de forrageio dos saguis foram coesas e os membros de cada grupo ocuparam sítios de alimentação em conjunto. O número e a força das associações variaram dependendo do contexto ecológico. As associações foram mais fortes durante as condições em que o alimento se encontrava concentrado em um sítio. Os indivíduos obtiveram maior acesso aos recursos quando compartilharam o sítio de alimentação com coespecíficos, e uma vez que o item alimentar era obtido, o forrageador o consumia em uma árvore próxima, longe dos outros. Além disso, a força das associações recentes e os níveis subsequentes de tolerância social em sítios de alimentação foram positivamente relacionados, compatível com a capacidade de memorizar associações ao longo do tempo e relembrá-las em tomadas de decisão futuras. Em conclusão, os saguis ajustaram suas escolhas de parceiros e a força das associações de forrageio em resposta à disponibilidade de alimento. Eles exibiram uma maior tolerância social em sítios de alimentação durante as condições em que se esperava que as oportunidades de competição direta fossem maiores. Estes primatas com reprodução cooperativa parecem se beneficiar mutuamente ao manterem relações afiliativas coesas e fortes, as quais aumentam as oportunidades para comportamentos coordenados e a sobrevivência da prole.

Disassociation of social and sexual partner relationships in a gibbon population with stable one-male two-female groups.

Adult males living in a one-male multi-female social group are expected to try to monopolize copulations with resident females to increase reproductive fitness. Gibbons have traditionally been described as living in monogamous groups, with the sole resident adult male assumed to sire all of the group's offspring. Here, we used microsatellite analyses and behavioral observations to examine rates of extra-group paternity (EGP) over 16 years in a population of crested gibbons (Nomascus concolor) that form stable and long-term one-male two-female social units. Forty percent of offspring (N = 14) were sired by extra-group males. To understand this high level of EGP, we tested whether inbreeding avoidance was related to EGP. Females who engaged in EGP did not show larger pairwise relatedness with their resident male compared to females who did not engage in EGP. Nevertheless, the standardized heterozygosity of EGP offspring was significantly higher than for offspring sired by the group's resident male. These results provide partial support for the inbreeding avoidance hypothesis. It appears that resident male crested gibbons are unable to monopolize resident females' matings. Our results indicate that long-term social partners are often distinct from sexual partners in this population. Clearly, the breeding system of crested gibbons is more flexible than previously thought, indicating a need for integrating long-term behavioral data and genetic research to re-evaluate gibbon social and sexual relationships derived from concepts of monogamy and pair-bonding.

The 10th anniversary of the scientific description of the black snub-nosed monkey (Rhinopithecus strykeri): It is time to initiate a set of new management strategies to save this critically endangered primate from extinction.

Traditionally, the genus Rhinopithecus (Milne-Edwards, 1872, Primates, Colobinae) included four allopatric species, restricted in their distributions to China and Vietnam. In 2010, a fifth species, the black snub-nosed monkey (Rhinopithecus strykeri) was discovered in the Gaoligong Mountains located on the border between China and Myanmar. Despite the remoteness, complex mountainous terrain, dense fog, and armed conflict that characterizes this region, over this past decade Chinese and Myanmar scientists have begun to collect quantitative data on the ecology, behavior and conservation requirements of R. strykeri. In this article, we review the existing data and present new information on the life history, ecology, and population size of R. strykeri. We discuss these data in the context of past and current conservation challenges faced by R. strykeri, and propose a series of both short-term and long-term management actions to ensure the survival of this Critically Endangered primate species. Specifically, we recommend that the governments and stakeholders in China and Myanmar formulate a transboundary conservation agreement that includes a consensus on bilateral exchange mechanisms, scientific research and monitoring goals, local community development, cooperation to prevent the hunting of endangered species and cross-border forest fires. These actions will contribute to the long-term conservation and survival of this Critically Endangered species.

Identifying the environmental and anthropogenic causes, distribution, and intensity of human rhesus macaque conflict in Nepal.

Reducing conflict between humans and wildlife is considered a top conservation priority. However, increasingly human-induced disturbances across natural landscapes have escalated encounters between humans and wildlife. In Nepal, forests have been destroyed, fragmented, and developed for human settlements, agricultural production, and urban centers for decades. As a result, human-wildlife conflict, in the form of crop-raiding, livestock predation, and injuries to humans and wildlife, is common throughout the country. In particular, crop-raiding by macaques is an increasingly common form of human-wildlife conflict. Rhesus macaques (Macaca mulatta) have been identified as a top ten crop-raiding wildlife species in Nepal. In order to better understand the nationwide distribution and intensity of human-rhesus macaque conflict (HRMC), we conducted an extensive literature review of reported incidences of HRMC during the period 2000 to 2021 in Nepal. We also created an online survey to obtain nationwide data on the location and severity of HRMC, and modeled the set of ecological factors that affect habitat suitability for rhesus macaques. An ensemble of three different species distribution model (SDM) algorithms were used to analyze these data. We found that almost 44% of Nepal's land area contains suitable habitat for rhesus macaques, with less than 8% of all suitable habitat located in protected national parks. As humans continue to alter and fragment natural landscapes, HRMC in Nepal has intensified. At present, nearly 15% of the country's land area in which human settlements are permitted, is characterized by moderate or high rates of HRMC. We argue that prioritizing programs of forest restoration, strategic management plans designed to connect isolated forest fragments with high rhesus macaque population densities, creating government programs that compensate farmers for income lost due to crop-raiding, and educational outreach that informs local villagers of the importance of conservation and protecting biodiversity, offer the most effective solutions to reduce HRMC in Nepal.

Navigating in a challenging semiarid environment: the use of a route-based mental map by a small-bodied neotropical primate.

To increase efficiency in the search for resources, many animals rely on their spatial abilities. Specifically, primates have been reported to use mostly topological and rarely Euclidean maps when navigating in large-scale space. Here, we aimed to investigate if the navigation of wild common marmosets inhabiting a semiarid environment is consistent with a topological representation and how environmental factors affect navigation. We collected 497 h of direct behavioral and GPS information on a group of marmosets using a 2-min instantaneous focal animal sampling technique. We found that our study group reused not only long-route segments (mean of 1007 m) but entire daily routes, a pattern that is not commonly seen in primates. The most frequently reused route segments were the ones closer to feeding sites, distant to resting sites, and in areas sparse in tree vegetation. We also identified a total of 56 clustered direction change points indicating that the group modified their direction of travel. These changes in direction were influenced by their close proximity to resting and feeding sites. Despite our small sample size, the obtained results are important and consistent with the contention that common marmosets navigate using a topological map that seems to benefit these animals in response to the exploitation of clustered exudate trees. Based on our findings, we hypothesize that the Caatinga landscape imposes physical restrictions in our group's navigation such as gaps in vegetation, small trees and xerophytic plants. This study, based on preliminary evidence, raises the question of whether navigation patterns are an intrinsic characteristic of a species or are ecologically dependent and change according to the environment.

Social strategies used by dispersing males to integrate into a new group in Tibetan macaques (Macaca thibetana).

In group-living mammals, an individual's fitness depends, in part, on the quality of social relationships it has with others. Among species of nonhuman primates in which one sex is philopatric, individuals of that sex often develop strong social bonds and alliances with closely related kin. Less is known regarding the social processes used by dispersing adults to form stable bonds with nonkin in their new group. From May to December 2009, April to August 2010, September to December 2011, and February to May 2012, we collected data on grooming interactions in wild Tibetan macaques (Macaca thibetana), a female philopatric species, at Mt. Huangshan, China. Our goal was to compare social interactions and bond formation between resident males, recent immigrant males, and resident females. Our results indicate that recent immigrant males formed stable partner relationships with a small number of resident females and groomed these females more frequently or for longer than they received grooming. In contrast, resident males switched female grooming partners more frequently, received more grooming than they gave, and formed relationships with a greater number of female partners. We argue that the ability of recent immigrant male Tibetan macaques to maintain strong and persistent social bonds with a small set of resident adult females is a primary factor that enables them to establish residence in a new multimale-multifemale group. The present study provides new and important insights into the integrated social strategies used by dispersing males and resident females to maintain group stability.

Investment in science can mitigate the negative impacts of land use on declining primate populations.

Changes in land use and the conversion of natural forests to agricultural fields and cattle pastures are threatening the survival of many species of wild animals, including nonhuman primates. Given its almost 1.4 billion people, China faces a difficult challenge in balancing economic development, human well-being, environmental protection, and animal conservation. We examined the effects of poverty, anthropogenic land use (cropland and pasture/grazing), human population growth, government investment in science and public attention to primates during the period from the 1980s to 2015 on primate population persistence in China. We analyzed these data using generalized mixed-effects models, structural equation models (SEM) and random forests (a machine learning technique). We found that 16 of 21 (76%) primate species in China, for which data are available, have experienced a population decline over the past 35 years. Factors contributing most to primate population decline included human poverty and the conversion of natural habitat to cropland. In contrast, the five species of primates that were characterized by recent population increases were the subjects of substantial government research funding and their remaining distribution occurs principally in protected areas (PAs). We argue that increased funding for research, the establishment and expansion of PAs, a national policy focused on reducing poverty, and educational programs designed to inform and encourage local people to participate in scientific investigation and wildlife protection, can mitigate the negative impacts of historical patterns of land conversion on primate population survival in China.

Factors affecting the crop raiding behavior of wild rhesus macaques in Nepal: Implications for wildlife management.

In many areas of South Asia and Southeast Asia, macaques inhabiting agricultural landscapes are considered serious crop pests by local farmers. In Nepal, for example, the expansion of monocultures, increased forest fragmentation, the degradation of natural habitats, and changing agricultural practices have led to a significant increase in the frequency of human-macaque conflict. In order to more fully understand the set of factors that contribute to macaque crop raiding, and the set of preventive measures that can be put in place to avoid human-macaque conflict, we examined patterns of crop raiding by a group of 52 rhesus macaques (Macaca mulatta) in the Kavrepalanchok district, Nepal. We present data on macaque inflicted crop damage in 172 agricultural plots (each plot measuring 380 m2) from August to October 2019. Our results indicate that farmland invasions by macaques were principally affected by crop type (maize was preferred over rice), nearness of farmland to both the forest edge and the major travel route used by the macaques, and the mitigation efforts applied by farmers to discourage crop raiding. We found that as the proportion of maize farmland in the most direct path from the macaque's main travel route to nearby crop raiding sites increased, the amount of maize damage decreased. This is likely explained by the fact that macaques traveling across several adjacent maize fields encounter multiple farmers protecting their crops. We estimated that the financial cost to individual farmer households of macaque maize and rice raiding was on average US$ 14.9 or 4.2% of their annual income from cultivating those two crops. As human-macaque conflict is one of the most critical challenges faced by wildlife managers in South Asia and Southeast Asia, studies of macaque crop raiding behavior provide an important starting point for developing effective strategies to manage human-macaque conflict while promoting both primate conservation and the economic well-being of the local community.

Neonatal nipple preference and maternal cradling laterality in wild Taihangshan macaques (Macaca mulatta tcheliensis).

Lateralized behavior is considered an observable phenotype of cerebral functional asymmetry and has been documented in many mammalian species. In the present study, we examined evidence of lateralization in neonatal nipple contact, maternal cradling, and the relationship between these two behaviors during the first 12 weeks of life in wild Taihangshan macaques (Macaca mulatta tcheliensis). The results showed that across our sample of nine mother-infant dyads: (1) Seven of nine neonates exhibited a significant left-side nipple preference during the first 12 weeks of life, whereas eight of nine mothers displayed a significant right-side cradling preference; (2) at the population level, there was a significant preference for left nipple contact by neonatal Taihangshan macaques and a significant right-hand maternal cradling preference; (3) at the population level, there was a nonsignificant negative correlation between neonatal nipple preference and maternal cradling bias; and (4) the strength of individual neonatal nipple preference and maternal cradling laterality were not correlated. We conclude that asymmetry in nipple contact of Taihangshan macaques occurs early in behavioral development. Given that infant Taihangshan macaques are able to nurse and cling unassisted to their mothers within a few days after birth, it appears that the infant rather than its mother is responsible for determining a nipple-side preference. Our results indicating a left-side nipple bias in 78% of wild neonatal Taihangshan macaques are most consistent with the heartbeat hypothesis.

Cafeteria-style feeding trials provide new insights into the diet and nutritional strategies of the black snub-nosed monkey (Rhinopithecus strykeri): Implications for conservation.

Anthropogenic changes and fragmentation of natural habitats often exert a negative effect on resource availability and distribution, and the nutritional ecology and feeding behavior of nonhuman primates. The goals of this study are to examine food choice and to identify the nutritional profile of foods consumed by the Critically Endangered black snub-nosed monkey (Rhinopithecus strykeri). To accomplish our study goals, we presented cafeteria-style feeding trials of fresh food items collected in the home range of wild black snub-nosed monkeys to the only two captive R. strykeri, and compared the nutritional profiles of the leafy foods (buds, young, and mature leaves, 100 i23tems from 70 plant species) selected with those avoided (54 items from 48 plant species). Overall, the results indicate that captive R. strykeri selected foods that were higher in moisture (Mo; 77.7%), crude protein (CP; 21.2%), total nonstructural carbohydrates (TNC; 34.9%), and phosphorus (P; 0.37%) while tending to avoid foods with a neutral detergent fiber (NDF) content of greater than 46.8%. Leaves collected in autumn and selected by the monkeys were characterized by a slightly higher amount of metabolizable energy (ME) than those rejected (1,350 kJ/100 g vs. 1,268 kJ/100 g). In contrast, the protein content of foods collected and consumed during the spring was greater (22.9%) than in autumn (16.4%). Random Forests modeling, an ensemble learning method, indicated that the proportion of Mo, NDF, ME, CP, P, and TNC were among the most important factors in predicting which items were consumed by the captive R. strykeri during spring and autumn. On the basis of the nutritional profile of foods consumed across the two seasons, we identified 18 nutrient-rich native plant species that we recommend for use in ex- and in-situ conservation management and reforestation programs to provide long-term access to a nutritionally adequate diet.

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.

The gut microbiome and metabolome of saddleback tamarins (Leontocebus weddelli): Insights into the foraging ecology of a small-bodied primate.

Body mass is a strong predictor of diet and nutritional requirements across a wide range of mammalian taxa. In the case of small-bodied primates, because of their limited gut volume, rapid food passage rate, and high metabolic rate, they are hypothesized to maintain high digestive efficiency by exploiting foods rich in protein, fats, and readily available energy. However, our understanding of the dietary requirements of wild primates is limited because little is known concerning the contributions of their gut microbiome to the breakdown and assimilation of macronutrients and energy. To study how the gut microbiome contributes to the feeding ecology of a small-bodied primate, we analyzed the fecal microbiome composition and metabolome of 22 wild saddleback tamarins (adult body mass 360-390 g) in Northern Bolivia. Samples were analyzed using high-throughput Illumina sequencing of the 16 S rRNA gene V3-V5 regions, coupled with GC-MS metabolomic profiling. Our analysis revealed that the distal microbiome of Leontocebus weddelli is largely dominated by two main bacterial genera: Xylanibacter and Hallella (34.7 ± 14.7 and 22.6 ± 12.4%, respectively). A predictive analysis of functions likely carried out by bacteria in the tamarin gut demonstrated the dominance of membrane transport systems and carbohydrate metabolism as the predominant metabolic pathways. Moreover, given a fecal metabolome composed mainly of glucose, fructose, and lactic acid (21.7 ± 15.9%, 16.5 ± 10.7%, and 6.8 ± 5.5%, respectively), the processing of highly fermentable carbohydrates appears to play a central role in the nutritional ecology of these small-bodied primates. Finally, the results also show a potential influence of environmentally-derived bacteria in colonizing the tamarin gut. These results indicate high energetic turnover in the distal gut of Weddell's saddleback tamarin, likely influenced by dominant bacterial taxa that facilitate dietary dependence on highly digestible carbohydrates present in nectar, plant exudates, and ripe fruits.