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.

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.

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.

Current and future trends in socio-economic, demographic and governance factors affecting global primate conservation.

Currently, ~65% of extant primate species (ca 512 species) distributed in 91 countries in the Neotropics, mainland Africa, Madagascar, South Asia and Southeast Asia are threatened with extinction and 75% have declining populations as a result of deforestation and habitat loss resulting from increasing global market demands, and land conversion for industrial agriculture, cattle production and natural resource extraction. Other pressures that negatively impact primates are unsustainable bushmeat hunting, the illegal trade of primates as pets and as body parts, expanding road networks in previously isolated areas, zoonotic disease transmission and climate change. Here we examine current and future trends in several socio-economic factors directly or indirectly affecting primates to further our understanding of the interdependent relationship between human well-being, sustainable development, and primate population persistence. We found that between 2001 and 2018 ca 191 Mha of tropical forest (30% canopy cover) were lost as a result of human activities in the five primate range regions. Forty-six percent of this loss was in the Neotropics (Mexico, Central and South America), 30% in Southeast Asia, 21% in mainland Africa, 2% in Madagascar and 1% in South Asia. Countries with the greatest losses (ca 57% of total tree cover loss) were Brazil, Indonesia, DRC, China, and Malaysia. Together these countries harbor almost 50% of all extant primate species. In 2018, the world human population was estimated at ca 8bn people, ca 60% of which were found in primate range countries. Projections to 2050 and to 2100 indicate continued rapid growth of the human populations in these five primate range regions, with Africa surpassing all the other regions and totaling ca 4bn people by the year 2100. Socioeconomic indicators show that, compared to developed nations, most primate range countries are characterized by high levels of poverty and income inequality, low human development, low food security, high levels of corruption and weak governance. Models of Shared Socioeconomic Pathway scenarios (SSPs) projected to 2050 and 2100 showed that whereas practices of increasing inequality (SSP4) or unconstrained growth in economic output and energy use (SSP5) are projected to have dire consequences for human well-being and primate survivorship, practices of sustainability-focused growth and equality (SSP1) are expected to have a positive effect on maintaining biodiversity, protecting environments, and improving the human condition. These results stress that improving the well-being, health, and security of the current and future human populations in primate range countries are of paramount importance if we are to move forward with effective policies to protect the world's primate species and promote biodiversity conservation.

Bachelor groups in primate multilevel society facilitate gene flow across fragmented habitats.

In the face of ongoing habitat fragmentation, many primate species have experienced reduced gene flow resulting in a reduction of genetic diversity, population bottlenecks, and inbreeding depression, including golden snub-nosed monkeys Rhinopithecus roxellana. Golden snub-nosed monkeys live in a multilevel society composed of several 1 male harem units that aggregate to form a cohesive breeding band, which is followed by one or more bachelor groups composed of juvenile, subadult, and adult male members. In this research, we examine the continuous landscape resistance surface, the genetic diversity and patterns of gene flow among 4 isolated breeding bands and 1 all-male band in the Qinling Mountains, China. Landscape surface modeling suggested that human activities and ecological factors severely limit the movement of individuals among breeding bands. Although these conditions are expected to result in reduced gene flow, reduced genetic diversity, and an increased opportunity for a genetic bottleneck, based on population genetic analyses of 13 microsatellite loci from 188 individuals inhabiting 4 isolated breeding bands and 1 all-male band, we found high levels of genetic diversity but low levels of genetic divergence, as well as high rates of gene flow between males residing in the all-male band and each of the 4 breeding bands. Our results indicate that the movement of bachelor males across the landscape, along with their association with several different breeding bands, appears to provide a mechanism for promoting gene flows and maintaining genetic diversity that may counteract the otherwise isolating effects of habitat fragmentation.

Primates in peril: the significance of Brazil, Madagascar, Indonesia and the Democratic Republic of the Congo for global primate conservation.

Primates occur in 90 countries, but four-Brazil, Madagascar, Indonesia, and the Democratic Republic of the Congo (DRC)-harbor 65% of the world's primate species (439) and 60% of these primates are Threatened, Endangered, or Critically Endangered (IUCN Red List of Threatened Species 2017-3). Considering their importance for global primate conservation, we examine the anthropogenic pressures each country is facing that place their primate populations at risk. Habitat loss and fragmentation are main threats to primates in Brazil, Madagascar, and Indonesia. However, in DRC hunting for the commercial bushmeat trade is the primary threat. Encroachment on primate habitats driven by local and global market demands for food and non-food commodities hunting, illegal trade, the proliferation of invasive species, and human and domestic-animal borne infectious diseases cause habitat loss, population declines, and extirpation. Modeling agricultural expansion in the 21st century for the four countries under a worst-case-scenario, showed a primate range contraction of 78% for Brazil, 72% for Indonesia, 62% for Madagascar, and 32% for DRC. These pressures unfold in the context of expanding human populations with low levels of development. Weak governance across these four countries may limit effective primate conservation planning. We examine landscape and local approaches to effective primate conservation policies and assess the distribution of protected areas and primates in each country. Primates in Brazil and Madagascar have 38% of their range inside protected areas, 17% in Indonesia and 14% in DRC, suggesting that the great majority of primate populations remain vulnerable. We list the key challenges faced by the four countries to avert primate extinctions now and in the future. In the short term, effective law enforcement to stop illegal hunting and illegal forest destruction is absolutely key. Long-term success can only be achieved by focusing local and global public awareness, and actively engaging with international organizations, multinational businesses and consumer nations to reduce unsustainable demands on the environment. Finally, the four primate range countries need to ensure that integrated, sustainable land-use planning for economic development includes the maintenance of biodiversity and intact, functional natural ecosystems.

A new conservation strategy for China-A model starting with primates.

Although the evolutionary history of primates in China dates to the Eocene, and includes major radiations of lorisids, hominoids, cercopithecines, and colobines during the Miocene, Pliocene, and Pleistocene, extensive human-induced habitat change and deforestation over the past few centuries has resulted in 22 of 25 extant species listed as threatened or endangered, and two species of gibbons extirpated in the last few years. This commentary briefly reviews factors that have contributed to the decline of primates in China over the past 400 years, and in particular how major social events and economic development in modern China have resulted in unsustainable environmental change. In response, we describe our efforts to develop a strategic scientific, educational and conservation partnership in China, focusing on primates, in which GIS technology will be used to integrate geographical profiles, climatic information, and changes in land use patterns and human and nonhuman primate distributions to highlight issues of immediate concern and to develop priority-based conservation solutions. Our goal is to evaluate how human-induced environmental change has impacted primates over time and to predict the likelihood of primate population extinctions in the near future. This model represents an early warning system that will be widely available to the Chinese government, public, educational institutions, researchers, and NGOs through social media and educational videos in order to arouse public awareness and promote wildlife conservation. We encourage colleagues across a broad range of academic disciplines, political ideologies, and the public to help move this strategy into reality, the sooner the better. Am. J. Primatol. 78:1137-1148, 2016. © 2016 Wiley Periodicals, Inc.

Determinants of daily path length in black and gold howler monkeys (Alouatta caraya) in northeastern Argentina.

Models used to explain the social organization of primates suggest that variation in daily path length (DPL) is a response to variation in resource distribution and the intensity of intragroup feeding competition. However, daily path length may be affected by a number of other factors including the availability and distribution of nutritionally complementary food items, temperature which can influence activity budget, patterns of subgrouping, and the frequency and function of intergroup encounters. In this 6-month study (total 495 hr of quantitative data), we examined daily path lengths in two neighboring groups of black and gold howler monkeys (Alouatta caraya) inhabiting a semi-deciduous gallery forest in San Cayetano (27° 30'S, 58° 41'W), in the northwest province of Corrientes, Argentina. Both study groups were of similar size and composition. We identified relationships across groups between time spent feeding on fruits, leaves, and flowers, the number of trees visited, group spread, frequency of intergroup encounters, mean daily temperature, and DPL. Our results suggest that variation in food availability had a significant impact on howler ranging behavior by increasing DPL under conditions of high immature and mature fruit availability, and by decreasing DPL with increased availability and increased time invested in feeding on mature leaves. These results do not support the contention that a reduction in food availability or an increase in within-group feeding competition increased DPL in black and gold howler monkeys. DPL in black and gold howlers is influenced by several interrelated factors. In this regard we suggest that models of socio-ecology and ecological constraints need to reconsider how factors such as individual nutritional requirements, social tolerance and group cohesion, and the spatial and temporal availability of preferred and nearby food resources influence primate ranging behavior. Am. J. Primatol. 78:825-837, 2016. © 2016 Wiley Periodicals, Inc.

Optimized spatial priorities for biodiversity conservation in China: a systematic conservation planning perspective.

By addressing several key features overlooked in previous studies, i.e. human disturbance, integration of ecosystem- and species-level conservation features, and principles of complementarity and representativeness, we present the first national-scale systematic conservation planning for China to determine the optimized spatial priorities for biodiversity conservation. We compiled a spatial database on the distributions of ecosystem- and species-level conservation features, and modeled a human disturbance index (HDI) by aggregating information using several socioeconomic proxies. We ran Marxan with two scenarios (HDI-ignored and HDI-considered) to investigate the effects of human disturbance, and explored the geographic patterns of the optimized spatial conservation priorities. Compared to when HDI was ignored, the HDI-considered scenario resulted in (1) a marked reduction (∼9%) in the total HDI score and a slight increase (∼7%) in the total area of the portfolio of priority units, (2) a significant increase (∼43%) in the total irreplaceable area and (3) more irreplaceable units being identified in almost all environmental zones and highly-disturbed provinces. Thus the inclusion of human disturbance is essential for cost-effective priority-setting. Attention should be targeted to the areas that are characterized as moderately-disturbed, <2,000 m in altitude, and/or intermediately- to extremely-rugged in terrain to identify potentially important regions for implementing cost-effective conservation. We delineated 23 primary large-scale priority areas that are significant for conserving China's biodiversity, but those isolated priority units in disturbed regions are in more urgent need of conservation actions so as to prevent immediate and severe biodiversity loss. This study presents a spatially optimized national-scale portfolio of conservation priorities--effectively representing the overall biodiversity of China while minimizing conflicts with economic development. Our results offer critical insights for current conservation and strategic land-use planning in China. The approach is transferable and easy to implement by end-users, and applicable for national- and local-scale systematic conservation prioritization practices.

Supply and demand determine the market value of access to infants in the golden snub-nosed monkey (Rhinopithecus roxellana).

According to a biological market paradigm, trading decisions between partners will be influenced by the current 'exchange rate' of commodities (good and services), which is affected by supply and demand, and the trader's ability to outbid competitors. In several species of nonhuman primates, newborn infants are attractive to female group members and may become a desired commodity that can be traded for grooming within a biological market place. We investigated whether grooming was interchanged for infant handling in female golden snub-nosed monkeys (Rhinopithecus roxellana) inhabiting the Qinling Mountains of central China. R. roxellana exhibit a multilevel social organization characterized by over 100 troop members organized into 6-11 one-male units each composed one adult male and several adult females and their offspring. Behavioral data were collected over the course of 28 months on grooming patterns between mothers with infants less than 6 months old (N = 36) and other adult female troop members. Our results provide strong evidence for the interchange of grooming for access to infants. Grooming for infant access was more likely to be initiated by potential handlers (nonmothers) and less likely reciprocated by mothers. Moreover, grooming bout duration was inversely related to the number of infants per female present in each one-male unit indicating the possibility of a supply and demand market effect. The rank difference between mothers and handlers was negatively correlated with grooming duration. With increasing infant age, the duration of grooming provided by handlers was shorter suggesting that the 'value' of older infants had decreased. Finally, frequent grooming partners were allowed to handle and maintain access to infants longer than infrequent groomers. These results support the contention that grooming and infant handling may be traded in R. roxellana and that the price individuals paid for access to infants fluctuated with supply and demand.

Evidence of allomaternal nursing across one-male units in the Yunnan snub-nosed monkey (Rhinopithecus Bieti).

BACKGROUND: Allomaternal nursing, common in several species of social mammals, also has been reported in nonhuman primates. However, the function of this behavior in enhancing infant survivorship remains poorly understood. METHODOLOGY AND PRINCIPAL FINDINGS: The study was conducted on a free-ranging group of the Yunnan snub-nosed monkey (Rhinopithecus bieti) in the Baimaxueshan Natural Reserve. Direct observation and ad libitum sampling were used to record allocare behavior during a 20 month field study. R. bieti exhibits a multilevel social organization in which a large single troop, consisting of over 100 individuals, is divided into many one-male units (OMUs: 6∼41). These OMUs coordinate their daily activities, and feed, forage, travel, and rest together. Here we report on one case of infant temporary adoption in which an adult female from one OMU engaged in allomaternal nursing and cared for an infant from a different OMU of the same troop. This event began when the mother and her five-month-old infant were found to became separated accidentally. The victim infant was observed staying in another OMU. Over the next several days we observed a lactating female in the new OMU to care for and nurse both her infant and the immigrant infant, who also was tolerated by and cared for by the harem male. CONCLUSIONS AND SIGNIFICANCE: Our findings suggest that lactating primate females are primed to care for young infants and, that the misdirected parental care hypothesis may offer the strongest explanation for allomaternal nursing in R. bieti.

Experimental field study of the relative costs and benefits to wild tamarins (Saguinus imperator and S. fuscicollis) of exploiting contestable food patches as single- and mixed-species troops.

Several species of tamarins form stable mixed-species troops in which groups of each species feed, forage, rest, and travel together during much of the year. Although the precise set of factors that facilitate this ecological relationship remains unclear, predator detection and foraging benefits are presumed to play a critical role in maintaining troop stability. In this work we present data from an experimental field study designed to examine how factors such as social dominance and within-patch foraging decisions affect the costs and benefits to tamarins of visiting feeding sites as single- and mixed-species troops. Our data indicate that when they exploited contestable food patches (sets of eight feeding platforms, two of which contained a 100-g banana), each tamarin species experienced foraging costs when they arrived as part of a mixed-species troop. These costs were found to be less severe for emperor tamarins because they were socially dominant to saddle-back tamarins and could displace them at feeding sites. We conclude that the foraging benefits to tamarins residing in mixed-species troops are asymmetrical, and that at feeding sites in which the amount of food in a patch is insufficient to satiate all troop members, even minor differences in the timing of return to food patches and changes in troop cohesion have a measurable effect on the costs and benefits to participating tamarin species.

Social and reproductive patterns in neotropical primates: Relation to ecology, body size, and infant care.

The papers in this issue stem from a symposium presented at the 1992 International Primatological Congress in Strasbourg, France. Due to the paucity of information on social organization, reproduction, and the relation of these to ecology in neotropical primates, we organized this symposium, which included researchers conducting comparative studies and those examining aspects of socioecology in single platyrrhine species. The papers in the symposium are organized around three issues: (1) the relation between body size, ecology, and reproduction (papers by Dietz et al., Tardif, and Williams et al.); (2) ranging and dispersal patterns as determinants of social structure (papers by Boinski and Mitchell, Norconk and Kinzey, and Kinzey and Cunningham); (3) phylogenetic and comparative analyses of behavioral and anatomical traits (Ford and Garber). Within these areas, the papers provide new information and new syntheses of existing information on platyrrhine socioecology. In addition, many detail innovative methodological approaches which could fruitfully be applied to other primates.