The costs and benefits of coexistence: What determines people's willingness to live near nonhuman primates?

Living near primate species has positive and negative outcomes for human communities. While most studies focus on understanding people's perceptions regarding the adverse consequences of interacting with primates, less is known about people's willingness to coexist with primates or reasons that may promote human-primate coexistence. We surveyed 794 people co-living with four different primate species-rhesus macaque Macaca mulatta, bonnet macaque Macaca radiata, lion-tailed macaque Macaca silenus, and Hanuman langur Semnopithecus dussumieri-in southern and western India to understand how people perceived the costs and benefits of coexistence. The results of our semi-structured interview study revealed that although tangible costs (i.e., financial losses from primate depredation) primarily drive people's stated tolerance for primate presence, intangible benefits from primates (i.e., their ecological, existence, sentience, and religious values) also critically affect attitudes towards coexistence. Amongst the four species, people associated rhesus macaques with the greatest costs and fewest benefits, lion-tailed macaques with the lowest costs, and bonnet macaques with the highest benefits. People preferred lion-tailed macaques and Hanuman langurs more than bonnet and rhesus macaques, and affection for a species shaped how people viewed costs accruing from the species. People's preferences for species were influenced by their existence, ecological, and sentience values more than their religious value. We suggest that intangible benefits influence people's fondness for a primate species and this, in turn, shapes how people perceive costs resulting from the species. Hence strengthening people's perceptions of the intangible benefits they receive from primate species will improve human tolerance for living near primates. We argue that there is a need to understand the context of human-primate conflicts beyond the cost aspects and focus on the benefits to improve human-primate coexistence.

Selecting between iron-rich and clay-rich soils: a geophagy field experiment with black-and-white colobus monkeys in the Budongo Forest Reserve, Uganda.

Geophagy, the intentional consumption of soil, has been observed in humans and numerous other animal species. Geophagy has been posited to be adaptive, i.e., consumed soil protects against gastrointestinal distress and/or supplements micronutrients. We conducted a field experiment in the Budongo Forest, Uganda, to investigate geophagic behaviors, including soil preference, the quantity of soil eaten, and competition for access to preferred soils. We placed pairs of artificial tree stumps at two existing geophagy sites. One stump contained soil from the surrounding area, Sonso, that could supplement bioavailable iron. The other stump contained soil from a neighboring community, Waibira, that was richer in clay minerals, which could provide protection from plant secondary compounds. We monitored activity and engagement with the stumps for 10 days using camera traps. After 5 days, we reversed the type of soil that was in the stumps at both sites (i.e., a crossover design). Only Colobus guereza (black-and-white colobus monkeys) interacted with the stumps. These monkeys used visual and olfactory cues to select between the two soils and exclusively ate the clay-rich soil, consuming 9.67 kg of soil over 4.33 h. Our findings lend the greatest plausibility to the protection hypothesis. Additionally, monkeys competed for access to the stumps, and 13% of the videos captured aggression, including pushing, excluding, and chasing other individuals from the experimental stumps. Nine episodes of vigilance and flight behavior were also observed. Given that intentionally ingested soil is a valuable resource that may confer health benefits, geophagy sites should be conserved and protected.

Correction to: Review of GPS collar deployments and performance on nonhuman primates.

In the original publication of the article, figure 1 was wrongly published as a duplication.

Review of GPS collar deployments and performance on nonhuman primates.

Over the past 20 years, GPS collars have emerged as powerful tools for the study of nonhuman primate (hereafter, "primate") movement ecology. As the size and cost of GPS collars have decreased and performance has improved, it is timely to review the use and success of GPS collar deployments on primates to date. Here we compile data on deployments and performance of GPS collars by brand and examine how these relate to characteristics of the primate species and field contexts in which they were deployed. The compiled results of 179 GPS collar deployments across 17 species by 16 research teams show these technologies can provide advantages, particularly in adding to the quality, quantity, and temporal span of data collection. However, aspects of this technology still require substantial improvement in order to make deployment on many primate species pragmatic economically. In particular, current limitations regarding battery lifespan relative to collar weight, the efficacy of remote drop-off mechanisms, and the ability to remotely retrieve data need to be addressed before the technology is likely to be widely adopted. Moreover, despite the increasing utility of GPS collars in the field, they remain substantially more expensive than VHF collars and tracking via handheld GPS units, and cost considerations of GPS collars may limit sample sizes and thereby the strength of inferences. Still, the overall high quality and quantity of data obtained, combined with the reduced need for on-the-ground tracking by field personnel, may help defray the high equipment cost. We argue that primatologists armed with the information in this review have much to gain from the recent, substantial improvements in GPS collar technology.

Geophagy among East African Chimpanzees: consumed soils provide protection from plant secondary compounds and bioavailable iron.

Geophagy, the intentional consumption of earth materials, has been recorded in humans and other animals. It has been hypothesized that geophagy is an adaptive behavior, and that clay minerals commonly found in eaten soil can provide protection from toxins and/or supplement micronutrients. To test these hypotheses, we monitored chimpanzee geophagy using camera traps in four permanent sites at the Budongo Forest Reserve, Uganda, from October 2015-October 2016. We also collected plants, and soil chimpanzees were observed eating. We analyzed 10 plant and 45 soil samples to characterize geophagic behavior and geophagic soil and determine (1) whether micronutrients are available from the soil under physiological conditions and if iron is bioavailable, (2) the concentration of phenolic compounds in plants, and (3) if consumed soils are able to adsorb these phenolics. Chimpanzees ate soil and drank clay-infused water containing 1:1 and 2:1 clay minerals and > 30% sand. Under physiological conditions, the soils released calcium, iron, and magnesium. In vitro Caco-2 experiments found that five times more iron was bioavailable from three of four soil samples found at the base of trees. Plant samples contained approximately 60 µg/mg gallic acid equivalent. Soil from one site contained 10 times more 2:1 clay minerals, which were better at removing phenolics present in their diet. We suggest that geophagy may provide bioavailable iron and protection from phenolics, which have increased in plants over the last 20 years. In summary, geophagy within the Sonso community is multifunctional and may be an important self-medicative behavior.

Geophagy among nonhuman primates: A systematic review of current knowledge and suggestions for future directions.

OBJECTIVES: Geophagy, the intentional consumption of earth, is widely practiced among humans and other mammals, but its causes are not well understood. Given the growing number of reports of geophagy among nonhuman primates (NHP), we sought to (1) advance and codify our understanding of the patterns and functional and evolutionary significance of geophagy among NHP and (2) provide a research agenda for a more unified approach to its study. METHODS: We systematically reviewed all available literature on NHP geophagy, extracted available data on taxa, geography, climate, diet, sex, age-class, reproductive status, and the characteristics of the earth. We used these data to evaluate three major hypotheses about geophagy, that it is protective, provides mineral supplementation, and is nonadaptive. RESULTS: We identified 287 accounts of geophagy among 136 species, adding 79 new primate species to the list of those considered in prior reviews. Nineteen percent of species were in the suborder Strepsirrhini, while 81% were in the suborder Haplorrhini. There were reports of geophagy from 9 of the 17 families and 39 of the 76 genera currently recognized by the International Union for Conservation of Nature. DISCUSSION: The limited evidence suggests that geophagy is adaptive, and provides protection and mineral supplementation. We specify the behavioral, dietary, and soil data required to more rigorously investigate these hypotheses across representative species of all taxonomic groups, geographical regions, and dietary classification. Given the plausibility of geophagy for maintaining the health of both wild and captive populations, we urge further study and conservation of geophagy sites.

Soil eaten by chacma baboons adsorbs polar plant secondary metabolites representative of those found in their diet.

Geophagy, the deliberate consumption of earth materials, is common among humans and animals. However, its etiology and function(s) remain poorly understood. The major hypotheses about its adaptive functions are the supplementation of essential elements and the protection against temporary and chronic gastrointestinal (GI) distress. Because much less work has been done on the protection hypothesis, we investigated whether soil eaten by baboons protected their GI tract from plant secondary metabolites (PSMs) and described best laboratory practices for doing so. We tested a soil that baboons eat/preferred, a soil that baboons never eat/non-preferred, and two clay minerals, montmorillonite a 2:1 clay and kaolinite a 1:1 clay. These were processed using a technique that simulated physiological digestion. The phytochemical concentration of 10 compounds representative of three biosynthetic classes of compounds found in the baboon diet was then assessed with and without earth materials using high-performance liquid chromatography with diode-array detection (HPLC-DAD). The preferred soil was white, contained 1% halite, 45% illite/mica, 14% kaolinite, and 0.8% sand; the non-preferred soil was pink, contained 1% goethite and 1% hematite but no halite, 40% illite/mica, 19% kaolinite, and 3% sand. Polar phenolics and alkaloids were generally adsorbed at levels 10× higher than less polar terpenes. In terms of PSM adsorption, the montmorillonite was more effective than the kaolinite, which was more effective than the non-preferred soil, which was more effective than the preferred soil. Our findings suggest that HPLC-DAD is best practice for the assessment of PSM adsorption of earth materials due to its reproducibility and accuracy. Further, soil selection was not based on adsorption of PSMs, but on other criteria such as color, mouth feel, and taste. However, the consumption of earth containing clay minerals could be an effective strategy for protecting the GI tract from PSMs.

Molecular identification of Oesophagostomum spp. from 'village' chimpanzees in Uganda and their phylogenetic relationship with those of other primates.

Oesophagostomum spp. are parasitic nematodes of mammals, including humans and other primates. To identify species and determine phylogeny, we analysed DNA sequences of adult and larval Oesophagostomum from wild chimpanzees in Bulindi, Uganda, which inhabit degraded forest fragments amid villages. Oesophagostome larvae and/or eggs from baboons in Tanzania and South Africa and from a Japanese macaque were also sequenced. Based on the internal transcribed spacer 2 (ITS2) of nuclear ribosomal DNA and partial cytochrome c oxidase subunit 1 gene (Cox1) of mtDNA, O. stephanostomum and O. bifurcum were identified from chimpanzees. Bulindi is the second locality where molecular detection of O. bifurcum in wild chimpanzees has been made. While most O. stephanostomum had ITS2 genotypes recorded previously, three new genotypes were detected. Among four ITS2 genotypes of O. bifurcum from chimpanzees, one was identical to that from various monkey species in Kibale, Uganda, and baboons from Tanzania and South Africa; another was shared by a baboon from Tanzania. No genotype was identical with that of the cryptic species reported from humans and monkeys in Kibale. Phylogeny based on Cox1 sequences of O. stephanostomum showed locality-dependent clades, whereas those of O. bifurcum formed clades composed of worms from different hosts and localities.

Soil consumed by chacma baboons is low in bioavailable iron and high in clay.

Despite widespread consumption of soil among animals, the role of geophagy in health maintenance remains an enigma. It has been hypothesized that animals consume soil for supplementation of minerals and protection against toxins. Most studies determine only the total elemental composition of soil, which may not reflect the amount of minerals available to the consumer. Our aim was to test these hypotheses by evaluating the bioavailability of iron in soil consumed by chacma baboons, using a technique that simulates digestion and adsorption. Our results indicate that, despite variation in absolute iron concentration of soil samples, actual iron bioavailability was low while clay content was quite high. This suggests that iron supplementation is unlikely to be the primary motivation for geophagy in this population, and that detoxification is a plausible explanation. This study demonstrates that more research on bioavailability and clay composition is needed to determine the role geophagy plays in health maintenance.

Parasite transmission risk from geophagic and foraging behavior in chacma baboons.

Numerous behavioral and ecological factors are associated with parasite transmission. One factor explored in human research, but absent from nonhuman primate research, is parasite transmission from soil ingestion. Human studies suggest geophagy, the regular and deliberate consumption of soil, increases risk of soil-transmitted helminth (STH) infection. Geophagy, which is prevalent in nonhuman primates, has several positive associations: gastrointestinal distress alleviation, possible mineral supplementation, and bacterial infection prevention. Our objective was to determine whether STH transmission was possible from deliberate or accidental soil ingestion, in a troop of chacma baboons (Papio hamadryas ursinus) that engaged in geophagy, foraged on the terrestrial substrata, and had a Trichuris sp. sample prevalence of 100%. We collected and analyzed 80 soil samples from geophagy and ground foraging sites on and around Wildcliff Nature Reserve, South Africa. Forty soil samples were collected from sites where soil was consumed, and 40 were collected from sites where soil was not consumed. At geophagy sites, the number of Trichuris sp. eggs recovered varied significantly between areas used and unused by the baboons, suggesting behavior is an important factor. In contrast, at foraging sites, there was only a tendency to recover more eggs at used than unused areas, and we propose egg recovery was influenced by fecal contamination that occurred throughout foraging stands. The difference in egg recovery between used areas at geophagy sites and used areas at foraging sites was not significant. These preliminary findings suggest both geophagy and foraging sites are a potential source of STH infection for this troop. Whether geophagy benefits outweigh the potential cost of parasite reinfection for this baboon troop is unknown, so we encourage future research on the influence that host foraging behavior may have on parasite reinfection.

Evaluating home range techniques: use of Global Positioning System (GPS) collar data from chacma baboons.

Global Positioning System (GPS) collars have revolutionized the field of spatial ecology, but to date, few primate studies have used them. We fitted a free-ranging, semi-habituated, juvenile male chacma baboon (Papio hamadryas ursinus) with an automatic self-releasing GPS collar and tracked his movements for 359 days. The collar captured 4254 fixes out of 5719 programmed opportunities, a 74.4 % acquisition rate, suggesting that the collar effectively tracked this baboon in a variety of habitat types. Of the data points captured, 73.7 % were three-dimensional fixes, and of these fixes, 66.9 % were highly accurate, having a dilution of precision of less than four. We calculated home range using three protocols with three estimation methods: minimum convex polygon, fixed kernel-density estimation (KDE), and fixed r local convex hull. Using all data points and the 95 % contour, these methods created home range estimations ranging from 10.8 to 23.1 km(2) for this baboon troop. Our results indicate that the KDE output using all data locations most accurately represented our data set, as it created a continuous home range boundary that excluded unused areas and outlying, potentially exploratory data points while including all seven sleeping sites and a movement corridor. However, home range estimations generated from KDE varied from 15.4 to 18.8 km(2) depending on the smoothing parameter used. Our results demonstrated that the ad hoc smoothing parameter selection technique was a better method for our data set than either the least squares cross-validation or biased cross-validation techniques. Our results demonstrate the need for primatologists to develop a standardized reporting method which documents the tool, screening protocol, and smoothing parameter used in the creation of home range estimations in order to make comparisons that are meaningful.

Geophagy in chacma baboons: patterns of soil consumption by age class, sex, and reproductive state.

Despite baboons' widespread distribution across Africa, geophagy among all subspecies has been poorly documented. We used video camera traps and soil analyses to investigate geophagy in chacma baboons (Papio cynocephalus ursinus) inhabiting the Western Cape of South Africa. During an 18-month study, from August 2009 to January 2011, we continually monitored the largest and most frequently visited geophagy sites with camera traps for 545 days and captured soil consumption at one or more sites on 266 of those days (49%). In 3,500 baboon visits to geophagy sites, video camera traps captured 58.6 hr of geophagy. From these data, we evaluated site preference based on time spent consuming soil among these four geophagy sites. One hundred and seventy days of soil consumption data from the most frequently visited geophagy site allowed us to look for demographic trends in geophagy. Selected consumed soils from geophagy sites were analyzed for mineral, physical, and chemical properties. The baboons spent more time consuming white alkaline soils with high percentages of clay and fine silt, which contained higher concentrations of sodium than non-white acidic soils that contained higher concentrations of iron. Our data indicate that pregnant chacma baboons spent more time consuming soil at monitored geophagy sites than baboons of any other age class, sex, or reproductive state. Based on analytical results, the soils consumed would be effective at alleviating gastrointestinal distress and possibly supplementing minerals for all age/sex classes, but potentially for different age/sex requirements.