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Abstract Conservation funding is currently limited; cost‐effective conservation solutions are essential. We suggest that the thousands of field stations worldwide can play key roles at the frontline of biodiversity conservation and have high intrinsic value. We assessed field stations’ conservation return on investment and explored the impact of COVID‐19. We surveyed leaders of field stations across tropical regions that host primate research; 157 field stations in 56 countries responded. Respondents reported improved habitat quality and reduced hunting rates at over 80% of field stations and lower operational costs per km2 than protected areas, yet half of those surveyed have less funding now than in 2019. Spatial analyses support field station presence as reducing deforestation. These “earth observatories” provide a high return on investment; we advocate for increased support of field station programs and for governments to support their vital conservation efforts by investing accordingly.

Chimpanzees are known to suffer from malaria parasitism. Here, the prevalence and epidemiology of several malaria parasites is examined in a wild chimpanzee population.

The primary purpose of the Man and the Biosphere Program is the sustainable development of both the economy and nature conservation activities. Although the effectiveness of eco-tourism to reach this goal has been proposed, due to the lack of long-term monitoring data and a model species, there has been no obvious mechanism to evaluate the effectiveness of this policy. This study explored the effectiveness of the sustainable development policy of HMBR based on 30 years data of monitoring the Tibetan macaque, local human population, visitors, and annual ecotourism income in Huangshan by estimating species habitat suitability and the impact of ecotourism. The results showed increases in the income for the local human population, the number of visitors, and annual eco-tourism. Simultaneously, the reserve’s Tibetan macaque population size and suitable habitat areas increased. The macaques expanded their habitat to the low-altitude buffer zone (400–800 m), an area with lower eco-tourism disturbance. Scenic spots had a significant negative impact on habitat suitability (the substantially increased contributions of scenic spots from 0.71% to 32.88%). Our results and methods provide a suitable evaluation framework for monitoring the sustainable development and effectiveness of eco-tourism and wildlife conservation in Man and the Biosphere reserves.

Crop-foraging by primates is a rapidly growing concern. Effective mitigation strategies are urgently required to resolve this issue. In the Garhwal Himalayas, local people’s high dependency on forest resources is a major cause of habitat loss, which paves the way for human-primate interactions in this area. To investigate the socioeconomic factors that might explain langur crop-foraging, we conducted structured interviews among 215 households in the Garhwal Himalayas in India. We also examined langur resource use by monitoring their feeding and sleeping site activity. Less agricultural land, less agricultural production, and possession of large numbers of livestock significantly predicted villagers reporting crop-foraging events, although economic status of the correspondents did not have any effect. Perception of the villagers about reduction in forest resource was significantly affected by the amount of livestock possessed by the villagers. Our observations suggested that Banj oak Quercus leucotrichophora was the dominant species (59.2%, N = 306) in the pool of sleeping trees used by the langurs. Langurs also showed a preference in their use of sleeping sites and feeding sites, which were different from that expected by chance. Sleeping sites with high density of oak were re-used most frequently. Similarly, dense oak patches were also the preferred feeding patches. Thus, we suggest replanting of oak trees and conservation of intact oak patches, environmental education outreach, and empowerment of women in the community as potential mitigating factors to lessen the interaction between humans and langurs.

Pygmy slow lorises (Nycticebus pygmaeus) are threatened with extinction in the wild. Their nocturnal lifestyle and small size make them difficult to study in their natural habitat, but increasing evidence suggests that they are more social than previously thought. Our study was designed to assess the sociability of pygmy slow lorises by transferring six adult females from solo cages into environmentally enriched group home cages at the Japan Monkey Centre’s Slow Loris Conservation Centre. Two females were paired to create one group, while the other four were placed together in a second group. We compared their social interactions, activity budgets, and postural behaviors before and after social housing was initiated. We found that all-female slow loris groups had a high degree of sociality, preferred to stay close to each other, nested together every night, and spent less time in locomotion and more time grooming than when living alone. These results suggest that female pygmy slow lorises actively seek companions when available. The captive housing of all-female groups of lorises could lead to better husbandry practices and improved animal welfare by allowing them to have conspecific companions. We conclude that isosexual groups of pygmy slow lorises should be preferred over single housing when possible.

Stone handling (SH), has been identified in four closely related primate species of the Macaca genus. We provide the first ethogram of SH in long-tailed macaques (Macaca fascicularis), a primate species known to use stones for extractive foraging. A total of 62.7 hrs of video recorded data were scored from a population of Balinese long-tailed macaques living in Ubud, Bali, Indonesia, and a total of 36 stone handling patterns were identified. Behavior discovery curves were generated and showed that the minimum threshold of completeness was exceeded for the SH repertoire in this group. A “foraging substitute” hypothesis for the expression of SH was proposed, suggesting that SH consists of performing foraging-like actions on non-edible objects. We used a “behavior systems” framework to test this prediction, finding that all 36 stone handling patterns could be reliably categorized in a foraging behavior system, supporting the hypothesis that stone handling can be considered pseudo-foraging behavior. Our “behavior systems” approach will serve as a foundation for the future testing of the motivational basis of stone handling. Additionally, a comparison of 39 stone handling patterns performed by three macaque species (M. fascicularis, M. fuscata and M. mulatta) showed overlapping behavioral propensities to manipulate stones; however, the differences suggest that long-tailed macaques might be more prone to use stones as percussive tools in a foraging context. This work could offer insights into the development and evolution of complex activities such as percussive stone tool use in early humans.

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.

Wild chimpanzees consume a variety of plants to meet their dietary needs and maintain wellbeing. While some plants have obvious value, others are nutritionally poor and/or contain bioactive toxins which make ingestion costly. In some cases, these nutrient-poor resources are speculated to be medicinal, thought to help individuals combat illness. In this study, we observed two habituated chimpanzee communities living in the Budongo Forest, Uganda, and collected 17 botanical samples associated with putative self-medication behaviors (e.g., bark feeding, dead wood eating, and pith-stripping) or events (e.g., when consumer had elevated parasite load, abnormal urinalysis, or injury). In total, we selected plant parts from 13 species (nine trees and four herbaceous plants). Three extracts of different polarities were produced from each sample using n-hexane, ethyl acetate, and methanol/water (9/1, v/v) and introduced to antibacterial and anti-inflammatory in vitro models. Extracts were evaluated for growth inhibition against a panel of multidrug-resistant clinical isolates of bacteria, including ESKAPE strains and cyclooxygenase-2 (COX-2) inhibition activity. Pharmacological results suggest that Budongo chimpanzees consume several species with potent medicinal properties. In the antibacterial library screen, 45 out of 53 extracts (88%) exhibited ≥40% inhibition at a concentration of 256 μg/mL. Of these active extracts, 41 (91%) showed activity at ≤256μg/mL in subsequent dose-response antibacterial experiments. The strongest antibacterial activity was achieved by the n-hexane extract of Alstonia boonei dead wood against Staphylococcus aureus (IC50: 16 μg/mL; MIC: 32 μg/mL) and Enterococcus faecium (IC50: 16 μg/mL; MIC: >256 μg/mL) and by the methanol-water extract of Khaya anthotheca bark and resin against E. faecium (IC50: 16 μg/mL; MIC: 32 μg/mL) and pathogenic Escherichia coli (IC50: 16 μg/mL; MIC: 256 μg/mL). We observed ingestion of both these species by highly parasitized individuals. K. anthotheca bark and resin were also targeted by individuals with indicators of infection and injuries. All plant species negatively affected growth of E. coli. In the anti-inflammatory COX-2 inhibition library screen, 17 out of 51 tested extracts (33%) showed ≥50% COX-2 inhibition at a concentration of 5 μg/mL. Several extracts also exhibited anti-inflammatory effects in COX-2 dose-response experiments. The K. anthotheca bark and resin methanol-water extract showed the most potent effects (IC50: 0.55 μg/mL), followed by the fern Christella parasitica methanol-water extract (IC50: 0.81 μg/mL). This fern species was consumed by an injured individual, a feeding behavior documented only once before in this population. These results, integrated with associated observations from eight months of behavioral data, provide further evidence for the presence of self-medicative resources in wild chimpanzee diets. This study addresses the challenge of distinguishing preventative medicinal food consumption from therapeutic self-medication by integrating pharmacological, observational, and health monitoring data-an essential interdisciplinary approach for advancing the field of zoopharmacognosy.

The Spix’s Saddleback Tamarin, Leontocebus fuscicollis is widely distributed across the Amazon region, but is endangered. This species is serving an important role in biomedical research in captivity. However, reference values for hematological and biochemical parameters are required for the proper characterization of the species. It was therefore the objective of our research to establish these parameters taking into consideration sex and body mass differences in healthy adult Spix’s saddleback tamarins. Collecting 2 mL of blood from each individual, 20 animals were examined (7 males, 13 females), and hematological and biochemical parameters were determined using commercial kits. Of the sixteen variables measured, only red blood cell (RBC), hemoglobin (Hb) and hematocrit (Ht) values were significantly higher in males (7.12 ± 0.98 106/mm, 14.98 ± 1.25 g/dL and 48.71 ± 4.91%, respectively), while red cell distribution width (RDW) was higher in females (14.58 ± 1.89%). Of the biochemical parameters measured, only gamma-glutamyl transferase (GGT) enzyme showed higher activity in females (8.08 ± 4.87 U/L), and a high glucose concentration range was observed (102.0 to 521.0 mg/dL) for both sexes. These parameters established with reference ranges for healthy adults provide a reliable reference source for the interpretation of laboratory housed saddleback tamarin.

Monitoring health in wild great apes is integral to their conservation and is especially important where they share habitats with humans, given the potential for zoonotic pathogen exchange. We studied the intestinal parasites of wild chimpanzees (Pan troglodytes schweinfurthii) inhabiting degraded forest fragments amid farmland and villages in Bulindi, Uganda. We first identified protozoan and helminth parasites infecting this population. Sixteen taxa were demonstrated microscopically (9 protozoa, 5 nematodes, 1 cestode, and 1 trematode). DNA sequence analysis enabled more precise identification of larval nematodes (e.g. Oesophagostomum stephanostomum, O. bifurcum, Strongyloides fuelleborni, Necator sp. Type II) and tapeworm proglottids (genus Bertiella). To better understand the ecology of infections, we used multidimensional scaling analysis to reveal general patterns of association among parasites, climate, and whole leaf swallowing-a prevalent self-medicative behaviour at Bulindi linked to control of nodular worms (Oesophagostomum spp.). Prevalence of parasites varied with climate in diverse ways. For example, Oesophagostomum sp. was detected in faeces at higher frequencies with increasing rainfall but was most clearly associated with periods of low temperature. Certain parasites occurred together within chimpanzee hosts more or less frequently than expected by chance. For example, the commensal ciliate Troglodytella abrassarti was negatively associated with Balantidium coli and Oesophagostomum sp., possibly because the latter taxa make the large intestine less suitable for T. abrassarti. Whole leaves in faeces showed independent associations with the prevalence of Oesophagostomum sp., Strongyloides sp., and hookworm by microscopic examination, and with egestion of adult O. stephanostomum by macroscopic inspection. All parasites identified to species or genus have been reported in wild chimpanzees inhabiting less-disturbed environments than Bulindi. Nevertheless, several disease-causing taxa infecting these chimpanzees are potentially transmissible between apes and humans (e.g. rhabditoid and strongyle nematodes), underscoring the importance of identifying and reducing risks of pathogen exchange in shared landscapes.

Our research interests are focused on the evolution of mating systems in primates and we aim at providing a better understanding of the adaptive signification of reproductive processes in female primates, using a comparative approach. Our Franco-Japanese collaboration (2006 - present) allowed us to study sociality and reproduction in a Catarrhine species, the Japanese macaque (Macaca fuscata), and on different but complementary topics (reproductive energetics, reproductive strategies, sexual signaling). We first investigated the links between energetics (i.e. nutritional status, body composition) and reproductive outcomes and our studies in captive Japanese macaques showed that, even in captivity with relaxed energetic constraints (e.g. constant food availability), seasonal breeding entails relatively high energy costs and females with higher energy status could invest more in reproductive activities and could afford to reproduce more rapidly. We also investigated the information that male Japanese macaques received from females that might enable them to discern periods with higher probabilities of conception and we developed a research program on the extent to which Japanese macaques, in common with people, have evolved a system of multimodal sexual signaling. We focused on the cues and signals available to males to make their mating decisions, and we provided information on the potential role of female behavior, female skin color, odours and vocalizations as sexual signals. We suggested, in particular, that females advertized their pregnancy through changes in behavioral, visual, and potentially auditory signals, and that males use these signals to adjust their mating behaviors and avoid wasting energy on non-reproductive copulations. This holistic study, combining fieldwork and laboratory experiments, and using a multidisciplinary approach (behavioral observations (sexual interactions), digital photography (visual scoring of female sexual skin color), hormonal (fecal ovarian steroids) and chemical data (components of female vaginal secretions)) allowed us to assess how different signals may combine to influence patterns of primate mate choices.

In the wild, primate foraging behaviors are related to the diversity and nutritional properties of food, which are affected by seasonal variation. The goal of environmental enrichment is to stimulate captive animals to exhibit similar foraging behavior of their wild counterparts, e.g. to extend foraging time. We conducted a 12-month study on the foraging behavior of Japanese macaques in a semi-naturally forested enclosure to understand how they use both provisioned foods and naturally available plant foods and what are the nutritional criteria of their consumption of natural plants. We recorded time spent feeding on provisioned and natural plant foods and collected the plant parts ingested of their major plant food species monthly, when available. We conducted nutritional analysis (crude protein, crude lipid, neutral detergent fiber-‘NDF’, ash) and calculated total non-structural carbohydrate – ‘TNC’ and total energy of those food items. Monkeys spent 47% of their feeding time foraging on natural plant species. The consumption of plant parts varied significantly across seasons. We found that leaf items were consumed in months when crude protein, crude protein-to-NDF ratio, TNC and total energy were significantly higher and NDF was significantly lower, fruit/nut items in months when crude protein and TNC were significantly higher and crude lipid content was significantly lower, and bark items in months when TNC and total energy were higher and crude lipid content was lower. This preliminary investigation showed that the forested enclosure allowed troop members to more fully express their species typical flexible behavior by challenging them to adjust their foraging behavior to seasonal changes of plant item diversity and nutritional content, also providing the possibility for individuals to nutritionally enhance their diet [Current Zoology 56 (2): 198–208, 2010].

In wildlife populations, group-living is thought to increase the probability of parasite transmission because contact rates increase at high host densities. Physical contact, such as social grooming, is an important component of group structure, but it can also increase the risk of exposure to infection for individuals because it provides a mechanism for transmission of potentially pathogenic organisms. Living in groups can also create variation in susceptibility to infection among individuals because circulating levels of immunosuppressive hormones like glucocorticoids often depend on an individual's position within the group's social structure. Yet, little is known about the relative roles of socially mediated exposure versus susceptibility in parasite transmission among free-living animal groups. To address this issue, we investigate the relationship between host dominance hierarchy and nematode parasite transmission among females in a wild group of Japanese macaques (Macaca fuscata yakui). We use social network analysis to describe each individual female's position within the grooming network in relation to dominance rank and relative levels of infection. Our results suggest that the number of directly-transmitted parasite species infecting each female, and the relative amount of transmission stages that one of these species sheds in faeces, both increase with dominance rank. Female centrality within the network, which shows positive associations with dominance hierarchy, is also positively associated with infection by certain parasite species, suggesting that the measured rank-bias in transmission may reflect variation in exposure rather than susceptibility. This is supported by the lack of a clear relationship between rank and faecal cortisol, as an indicator of stress, in a subset of these females. Thus, socially mediated exposure appears to be important for direct transmission of nematode parasites, lending support to the idea that a classical fitness trade-off inherent to living in groups can exist.

Identifying microbial pathogens with zoonotic potential in wild-living primates can be important to human health, as evidenced by human immunodeficiency viruses types 1 and 2 (HIV-1 and HIV-2) and Ebola virus. Simian foamy viruses (SFVs) are ancient retroviruses that infect Old and New World monkeys and apes. Although not known to cause disease, these viruses are of public health interest because they have the potential to infect humans and thus provide a more general indication of zoonotic exposure risks. Surprisingly, no information exists concerning the prevalence, geographic distribution, and genetic diversity of SFVs in wild-living monkeys and apes. Here, we report the first comprehensive survey of SFVcpz infection in free-ranging chimpanzees (Pan troglodytes) using newly developed, fecal-based assays. Chimpanzee fecal samples (n = 724) were collected at 25 field sites throughout equatorial Africa and tested for SFVcpz-specific antibodies (n = 706) or viral nucleic acids (n = 392). SFVcpz infection was documented at all field sites, with prevalence rates ranging from 44% to 100%. In two habituated communities, adult chimpanzees had significantly higher SFVcpz infection rates than infants and juveniles, indicating predominantly horizontal rather than vertical transmission routes. Some chimpanzees were co-infected with simian immunodeficiency virus (SIVcpz); however, there was no evidence that SFVcpz and SIVcpz were epidemiologically linked. SFVcpz nucleic acids were recovered from 177 fecal samples, all of which contained SFVcpz RNA and not DNA. Phylogenetic analysis of partial gag (616 bp), pol-RT (717 bp), and pol-IN (425 bp) sequences identified a diverse group of viruses, which could be subdivided into four distinct SFVcpz lineages according to their chimpanzee subspecies of origin. Within these lineages, there was evidence of frequent superinfection and viral recombination. One chimpanzee was infected by a foamy virus from a Cercopithecus monkey species, indicating cross-species transmission of SFVs in the wild. These data indicate that SFVcpz (i) is widely distributed among all chimpanzee subspecies; (ii) is shed in fecal samples as viral RNA; (iii) is transmitted predominantly by horizontal routes; (iv) is prone to superinfection and recombination; (v) has co-evolved with its natural host; and (vi) represents a sensitive marker of population structure that may be useful for chimpanzee taxonomy and conservation strategies.