Noninvasive Assessment of Gastrointestinal Parasite Infections in Free-Ranging Primates

Recent evidence of emerging human diseases with origins or likely transmission to humans, or both, that involve primates and a greater recognition of the risk of human pathogen transmission to free-ranging primates have raised awareness of the potential impact of zoonotic pathogen transmission on primate conservation and nonhuman primate and human health. As human population density continues to increase exponentially, speeding the reduction and fragmentation of primate habitats, greater human-primate contact is inevitable and even higher rates of pathogen transmission are likely. Thus interest has grown in collecting baseline data on patterns of parasitic infections in wild primate populations to provide an index of population health and to begin to assess and, to manage disease risks. Primatologists traditionally have been involved with such surveys through noninvasive assessment of gastrointestinal parasites. Unfortunately, previous studies have tended toward divergent methodologies, compromising the potential for longitudinal and comparative work. Here, I provide practical guidelines and standardized methodologies for the noninvasive assessment of gastrointestinal parasites of primates.

Epidemiological study of zoonoses derived from humans in captive chimpanzees

Emerging infectious diseases (EIDs) in wildlife are major threats both to human health and to biodiversity conservation. An estimated 71.8 % of zoonotic EID events are caused by pathogens in wildlife and the incidence of such diseases is increasing significantly in humans. In addition, human diseases are starting to infect wildlife, especially non-human primates. The chimpanzee is an endangered species that is threatened by human activity such as deforestation, poaching, and human disease transmission. Recently, several respiratory disease outbreaks that are suspected of having been transmitted by humans have been reported in wild chimpanzees. Therefore, we need to study zoonotic pathogens that can threaten captive chimpanzees in primate research institutes. Serological surveillance is one of several methods used to reveal infection history. We examined serum from 14 captive chimpanzees in Japanese primate research institutes for antibodies against 62 human pathogens and 1 chimpanzee-borne infectious disease. Antibodies tested positive against 29 pathogens at high or low prevalence in the chimpanzees. These results suggest that the proportions of human-borne infections may reflect the chimpanzee’s history, management system in the institute, or regional epidemics. Furthermore, captive chimpanzees are highly susceptible to human pathogens, and their induced antibodies reveal not only their history of infection, but also the possibility of protection against human pathogens.     

Patterns of Infection with Cryptosporidium sp. and Giardia sp. in Three Species of Free-Ranging Primates in the Peruvian Amazon

Recent evidence of pathogen transmission to humans from wild primates and a greater recognition of the risk of human pathogen transmission to free-ranging primates have raised awareness of the potential impact of zoonotic pathogen transmission on primate conservation and nonhuman primate and human health. Cryptosporidium and Giardia are zoonotic protozoan parasites transmitted via fecal–oral contamination or water that can cause gastritis or enteritis in human and nonhuman primates. From June 2002 to September 2003, we collected fecal samples noninvasively from two species of tamarins (Saguinus mystax and S. nigrifrons) and one species of titi monkeys (Callicebus cupreus) at the Estación Biológica Quebrada Blanco in the Peruvian Amazon to determine the distribution and prevalence of these potential pathogens. We screened 140 fecal samples representing known individuals of each species for Cryptosporidium and Giardia using the Merifluor immunoflourescence assay to determine the prevalence and intensity of infection with these organisms. With the exception of two samples we collected during the same week from a juvenile male Saguinus mystax, all samples were negative for Cryptosporidium. None of the fecal samples were positive for Giardia. The low prevalence of infection we observed limited our ability to examine the effects of demographic and environmental variables on patterns of infection; however, the exceptionally low prevalence of Cryptosporidium suggests that it is not a current health threat to these primate populations. Although the origin of infection with Cryptosporidium in the juvenile male Saguinus mystax cannot be determined, its presence alerts us to the potential for cross-species transmission and highlights the need for more detailed research to improve our understanding of the distribution and diversity of potentially pathogenic protozoa in Neotropical primate populations.     

Is 2020 the year when primatologists should cancel fieldwork? A reply

The aim of this article is to explore the impact of coronavirus disease (COVID-19) pandemic on primate-related conservation work. The withdrawal of primatologists and conservation staff from field research can lead to a number of detrimental effects not just on conservation but also on local communities in low- and middle-income countries. Inequalities in access to health and financial insecurities may be drivers for the illegal wildlife trade and the lack of tourism and research activity may allow poachers to work with greater ease. The paper also looks at how conservation organizations and research bodies should modify their field protocols by developing robust occupational health policies that will not only make field work safer but also support local staff as they are likely to face the greatest threats to their physical health, psychological health, and economic loss from COVID-19. By adopting a One Health approach that considers the complex interactions between human and primate health, researchers will be able to find new ways of working not only to protect primates but understand how they adapt to the COVID-19 pandemic.     

Disease risk analysis: A paradigm for using health-based data to inform primate conservation and public health

Risk analysis is a multidisciplinary process used to evaluate existing knowledge in order to prioritize risks associated with the spread of disease. A principle aim of risk analysis is to facilitate the development of cost-effective management strategies. Risk analysis calls for a multidisciplinary approach to piece together and integrate the numerous factors that influence disease transmission. The seven papers included in this volume of AJP present current primatological research as viewed through the prism of risk analysis. Issues such as interspecies disease transmission, public health, and conservation of endangered species are addressed, and risk analysis is put forward as a possible paradigm to promote understanding of infectious disease and its impact on nonhuman primate and human populations.     

Interactions between Social Structure,Demography, and Transmission Determine Disease Persistence in Primates

Catastrophic declines in African great ape populations due to disease outbreaks have been reported in recent years, yet we rarely hear of similar disease impacts for the more solitary Asian great apes, or for smaller primates. We used an age-structured model of different primate social systems to illustrate that interactions between social structure and demography create ‘dynamic constraints’ on the pathogens that can establish and persist in primate host species with different social systems. We showed that this varies by disease transmission mode. Sexually transmitted infections (STIs) require high rates of transmissibility to persist within a primate population. In particular, for a unimale social system, STIs require extremely high rates of transmissibility for persistence, and remain at extremely low prevalence in small primates, but this is less constrained in longer-lived, larger-bodied primates. In contrast, aerosol transmitted infections (ATIs) spread and persist at high prevalence in medium and large primates with moderate transmissibility;, establishment and persistence in small-bodied primates require higher relative rates of transmissibility. Intragroup contact structure – the social network - creates different constraints for different transmission modes, and our model underscores the importance of intragroup contacts on infection prior to intergroup movement in a structured population. When alpha males dominate sexual encounters, the resulting disease transmission dynamics differ from when social interactions are dominated by mother-infant grooming events, for example. This has important repercussions for pathogen spread across populations. Our framework reveals essential social and demographic characteristics of primates that predispose them to different disease risks that will be important for disease management and conservation planning for protected primate populations.     

Identification of 13 Human Microsatellite Markers via Cross-species Amplification of Fecal Samples from Rhinopithecus bieti

Yunnan snub-nosed monkeys (Rhinopithecus bieti) are 1 of 3 snub-nosed monkey species endemic to China. Only ca. 1500 individuals remain in high-altitude forests 3000–4500 m above sea level on the Tibetan Plateau, making them the nonhuman primate living at the highest known elevation. It is one of the most endangered 25 primate species in the world. Proper knowledge of the population genetics and social system of Rhinopithecus bieti will contribute to more appropriate conservation management decisions. Cross-species amplification of human microsatellite loci has facilitated analysis of the population genetics and reproductive strategies of various primate species. We screened 72 human-derived markers to assess their utility in Yunnan snub-nosed monkeys. Thirteen of them produced reliable results and exhibited moderate levels of polymorphism.     

A global gap analysis of infectious agents in wild primates

A number of infectious diseases have emerged as threats to humans and wildlife. Despite the growing importance of georeferenced data for mitigating disease risk, information on parasite threat is patchily distributed at a global scale. In this paper, we explore the utility of gap analysis techniques to investigate the global geographical distribution of parasite sampling in non-human primates. Specifically, we identify geographical areas that are undersampled for parasites in relation to primate geographical distributions, primate taxonomic sampling, primate threat status, and parasite taxonomy. Our results reveal that East Asia (particularly China), South-East Asia, and the South American Amazon are the most deficient in sampling effort with respect to all criteria. We also identify sampling gaps based on several criteria in West and Central Africa. Future research aimed at filling these gaps is needed for both human health and primate conservation purposes.     

Long-term dynamics of wild primate populations across forests with contrasting protection in Tanzania

Anthropogenic activities driving tropical forests' loss imperil global biodiversity and provision of ecosystem services. In this context, systematic monitoring programs evaluating wildlife trends are essential. Non-human primates are relevant conservation targets since they represent vital components of tropical forests by serving as pollinators and seed dispersers. Here, we present primate group counts data collected over 19 years in a primate hotspot in Tanzania. We analyzed data with a hierarchical dynamic model accounting for imperfect detection that estimates local group abundance and temporal rates of change, to assess whether habitat protection explained trends of the arboreal and diurnal Peters' Angola colobus (Colobus angolensis palliatus), Udzungwa red colobus (Piliocolobus gordonorum), and Tanzania Sykes' monkey (Cercopithecus mitis subsp. moloneyi). We targeted populations occurring in two forest blocks with contrasting protection regimes, with one block impacted by targeted poaching of the two Colobus species. We found that these latter species were much less abundant in the more human impacted forest, underwent a rapid decline, and subsequently remained at low abundance and without signs of recovery once this forest was granted greater protection. Instead, Sykes' abundance did not differ between forests, and improved protection was associated with a slight increase in abundance. Age class composition for social groups of both Colobus species differed between forests, indicating altered births and survivorship rates in the impacted forest. Results suggest that targeted hunting can prevent recovery for several years and even after increased habitat protection. Our approach appears valuable to monitor population dynamics over the long term, highlighting species-specific variations in both vulnerability to anthropogenic disturbance and recovery patterns in primate populations.     

Primates and parasites: A case for a multidisciplinary approach

Examinations of primate parasitic infections can inform both primatologists and parasitologists about evolutionary and ecological relationships. Interspecific, intraspecific, and interindividual variation in parasitic infections may correlate with environmental, demographic, behavioral, and human variables. Understanding these relationships is particularly important for conservation management issues for endangered species. We describe techniques for the noninvasive collection and preservation of fecal samples from wild primates and the salvaging of parasitological information from primate hosts in the field.     

Monkey Abundance and Social Structure in Two High-Elevation Forest Reserves in the Udzungwa Mountains of Tanzania

The effects of human activity on population and social structure are a pantropical concern for primate conservation. We compare census data and social group counts from two forests in the Udzungwa Mountains, Tanzania. The main aim is to relate differences within and between the forests to current theory on the effect of human disturbance on primate abundance and group size. The survey reveals the presence of the restricted-range red colobus, Procolobus gordonorum, in New Dabaga/Ulangambi Forest Reserve (NDUFR). The primate community of NDUFR is impoverished compared to that in Ndundulu forest. Red colobus and black-and-white colobus (Colobus angolensis palliatus) abundance and group size are lowest in NDUFR. Fission-fusion of red colobus social groups may be occurring in previously logged areas of both forests. Our observations are consistent with current theory on the effect of habitat degradation and hunting on primates, but the relative effects of the 2 factors could not be differentiated. We pooled the results with previous data to show that abundance of red colobus in the Udzungwa Mountains is lowest at high elevations. Low red colobus group sizes appear to be related to human activity rather than elevation. Black-and-white colobus and Sykes monkeys (Cercopithecus mitis) show no relationship with elevation. Future studies will require more detailed information on vegetation, diet and ranging patterns to interpret fully intraspecific variation in population demography and social structure in the Udzungwa Mountains.     

Preliminary Report on the Distribution of <Emphasis Type="Italic">Callicebus oenanthe</Emphasis> on the Eastern Feet of the Andes

In 2007 we conducted a field study of almost 6 mo to determine the distribution of Callicebus oenanthe, formerly known as the Andean titi monkey. There previously has been no extensive study on the distribution and status by other fieldworkers. We visited a total of 96 localities within or around the presumed distribution of this rare primate species to determine the distribution of Callicebus oenanthe. We collected additional information on group size and threats to the species. Our expeditions revealed that the species is not endemic to the Alto Mayo Valley, as earlier authors suggested, but that its distribution extends into the Bajo Mayo and Huallaga Central. The study area is heavily deforested, and to date only one area was found where a viable population might live, although further research is needed to confirm this. The species lives in the southern part of its distribution in sympatry with another, undescribed species of Callicebus. We will continue the study to determine more precisely the distribution and conservation status of the Callicebus oenanthe, to determine if conservation measures are necessary for this species. This is the first activity of a long-term project for the conservation of Callicebus oenanthe initiated by La Vallée des Singes Primate park.     

Evolution of human Y-chromosome DNA

We have used human male-specific 3.4 kb Hae III restriction endonuclease fragments to explore the evolutionary history of man's Y-chromosome. We have identified four sets of reiterated, sequences on the basis of their relative sequence homology with autosomal DNA. The sequences account for approximately 40% of the human Y-chromosome, are interspersed within the same 3.4 kb Hae III fragments, are heterogeneous and contain all reiterated DNA previously demonstrated to be specific for the Y-chromosome (it-Y DNA). Y-specific 3.4 kb Hae III sequences do not reassociate with either human female or ape DNA at standard reassociation criteria. However, approximately half of it-Y DNA (cross reacting it-Y) reassociates with both human female and ape DNA at reduced reassociation criteria. The remaining half (Y-specific it-Y) retains its specificity for the human Y-chromosome. These two sets of it-Y DNA have distinct reiteration frequencies and thermal stabilities with their Y-chromosome homologs. Non-Y-specific 3.4 kb Hae III sequences reassociate with both human female and ape DNA at standard reassociation criteria. The abundance of these non-Y-specific sequences decreases as a function of their evolutionary distance from man. One subset of non-Y-specific 3.4 kb Hae III sequences forms stable duplexes with human Y-chromosome DNA and with human and ape autosomal DNA. No detectable base-mismatch occurs among these homologs suggesting complete conservation of these sequences during primate evolution. The second subset of Non-Y-specific Hae III sequences form stable duplexes with human Y-chromosome DNA but highly mismatched duplexes with human and ape autosomal DNA.The finding that homologs of 3.4 kb Hae III sequences are not found within the Y-chromosome of apes but are only present in autosomes suggests that 3.4 kb Hae III sequences are largely autosomal in origin. Since autosomal homologs of most 3.4 kb Hae III-sequences exhibit a greater degree of divergence than those localized to the Y-chromosome, their evolutionary history seems to be chromosome-dependent.Our findings are not easily correlated with the comparative morphology of primate Y-chromosomes and suggest that sequence rearrangement has been a major event in the evolution of the human Y-chromosome. The significance of the specific interspersion of four sets of reiterated sequences, with distinct evolutionary histories, within a repeating unit specific to the human Y-chromosome is not clear. The apparent conservation of at least some of these reiterated sequences suggests they may be of functional importance.     

Phylogenetic diversity and the conservation biogeography of African primates

Aim Phylogenetics has an important role in conservation biogeography. However, there are few data on the phylogenetic diversity of African primates. The phylogenetic diversity (PD) of a species is a measure of its taxonomic distinctness and can be estimated by looking at the phylogenetic relationships among taxa. Species‐specific metrics on PD can then be used to determine conservation priorities at various biogeographical scales. We used PD metrics to rank 55 African primate species according to their conservation priorities at the country level and within six African biogeographical regions. We also addressed the following question: are there differences in conservation rankings between the IUCN Red List and our PD metrics? Location Africa. Methods We created a consensus phylogeny for all African primate clades based on genetic studies. Analyses of species distributions were determined using presence/absence scores at two levels: country and biogeographical region. A node‐based method that standardizes for widespread taxa and endemicity was used to calculate PD indices. Hierarchical cluster analysis was used to convert one of the standardized, phylogenetic indices into three clusters that could be ranked and compared with the main IUCN conservation rankings of endangered, vulnerable, and lower risk. Results At the country and region levels, the top‐priority species in terms of PD are Pan paniscus, Macaca sylvanus, Arctocebus calabarensis, Gorilla beringei, Arctocebus aureus, Allenopithecus nigroviridis, Gorilla gorilla, Procolobus verus, Cercopithecus solatus, Cercocebus galeritus, Colobus angolensis, Theropithecus gelada, Galagoides zanzibaricus, Galagoides granti, and Procolobus (Piliocolobus) badius. Geographic rankings were highest for the Democratic Republic of the Congo (country level) and Central Africa (region level). Although there were no overall differences between IUCN conservation ranks and the PD rankings, there were significant differences between the two systems for vulnerable and endangered primate taxa. Main conclusions There are few ecological and behavioural data on populations of some of the African primates that represent the highest levels of phylogenetic diversity. Studies of primate taxa with high PD rankings should focus on identifying sites suitable for intensive studies of population densities, feeding ecology, and reproductive behaviour. We suggest that PD metrics can serve as an important, complementary data set in the IUCN ranking system for primates.     

The monkey puzzle: a systematic review of studies of stress, social hierarchies, and heart disease in monkeys

Background

It is often suggested that psychosocial factors, such as stress, or one''s social position, may play an important role in producing social gradients in human disease. Evidence in favour of this model of health inequalities has relied, in part, on studies of the health effects of the natural social hierarchies found among non-human primates. This study aimed to assess the strength of this evidence.

Methodology/Principal Findings

A systematic review was carried out to identify all studies of psychosocial factors and coronary artery disease (CAD) in non-human primates. We searched databases (MEDLINE, PsycInfo, EMBASE, and Primatelit from inception to November 2010) to identify experimental and observational studies of the impact of social reorganisation, social instability, and disruption of dominance hierarchies on primate CAD outcomes. We also handsearched bibliographies and examined the citations to those studies in public health articles. Fourteen studies were found which presented evidence on CAD and social status and/or psychosocial stress. These suggested that the association between social status and disease may be sex-specific: in female monkeys dominant status may be protective, with subordinate females having a greater extent of atherosclerosis. In male monkeys the reverse may be the case.

Conclusions/Significance

Overall, non-human primate studies present only limited evidence for an association between social status and CAD, Despite this, there is selective citation of individual non-human primate studies in reviews and commentaries relating to human disease aetiology. Such generalisation of data from monkey studies to human societies does not appear warranted.     

Thirty Years of Research in Kibale National Park,Uganda, Reveals a Complex Picture for Conservation

Kibale National Park, Uganda, has a rich and abundant primate community and a complicated history of anthropogenic disturbance. Moreover, it has been the focus of over 30 yr of research and has received considerable attention from nongovernmental and governmental conservation organizations. As a result, Kibale serves as a valuable case study with which to evaluate the factors that regulate primate population density and the challenges of deriving generalizations for conservation. We review the impact of logging and forest fragmentation on primate population density and trace the efficacy of various conservation strategies. A 28-yr comparison of primate abundance in logged and unlogged forests and a 10-yr study of forest dynamics showed that primate recovery in logged areas is generally slow or not occurring at all for some species, which is likely driven by the fact that the forest is not recovering as expected. No primate species characteristic predicted their ability to live in forest fragments around Kibale. While a nutritional model was useful to predict the abundance of colobus in forest fragments outside of Kibale, a 5-yr study revealed that human land-use practices are more fundamentally shaping population dynamics. We evaluate data on primate abundance in light of Milton’s protein/fiber model to predict colobine biomass. We demonstrate that while the model can predict colobus biomass in pristine habitats, the 2 colobus species respond differently to disturbance. We offer suggestions for future conservation research and consider strategies to conserve forested national parks based on experiences gained over 30 yr.     

Comparative Sequence Analysis of the VHL Tumor Suppressor Gene

Comparative genome analysis may provide novel insights into gene evolution and function. To investigate the von Hippel–Lindau (VHL) disease tumor suppressor gene, we sequenced the VHL gene in seven primate species. Comparative analysis was performed for human, primate, and rodent VHL genes and for a putative Caenorhabditis elegans VHL homologue identified by database analysis. The VHL gene has two translation initiation sites (at codons 1 and 54); however, the relative importance of the full-length translation product (pVHL₃₀) and that translated from the second internal translation initiation site (pVHL₁₉) is unclear. The N-terminal sequence of pVHL₃₀ contains eight copies of a GXEEX acidic repeat motif in human and higher primates, but only three copies were present in the marmoset, and only one copy was present in rodent VHL genes. Evolutionary analysis suggested that the N-terminal repetitive sequence in pVHL₃₀ was of less functional importance than those regions present in both pVHL₃₀ and pVHL₁₉. The VHL gene product is reported to form complexes with various proteins including elongin B, elongin C, VBP-1, fibronectin, Sp1, CUL2, and HIF-1. Although most of the regions in pVHL that had been implicated in binding specific proteins demonstrated evolutionary conservation, the carboxy-terminal putative VBP-1 binding site was less well conserved, suggesting that VBP-1 binding may have less functional significance. Although an amino acid substitution (K171T) close to the pVHL elongin binding region was found in baboon, analysis of the structure of human pVHL suggested that this substitution would not interfere with pVHL/elongin C interaction. In general, there was a good correlation between the pVHL domains that demonstrated most evolutionary conservation and those that were most frequently mutated in tumors. Analysis of human/C. elegans conservation and human germline and somatic mutation patterns identified a highly conserved mutation cluster region between codons 74 and 90. However, this region is likely to be important for the structural integrity of pVHL rather than representing an additional protein binding domain.     

Group Size Dynamics over 15+ Years in an African Forest Primate Community

Group size affects many aspects of the ecology and social organization of animals. We investigated group size stability for five primate species in Kibale National Park, Uganda from 1996 to 2011 at three nested spatial scales. Survey data indicated that group sizes did not change for most species, with the exception of red colobus monkeys (Procolobus rufomitratus), in which group size increased at all spatial scales. Mangabey (Lophocebus albigena) group size increased in old‐growth forest, but the sample size and increase were small. To augment this survey data, we collected several years of demographic data on three habituated groups of redtail monkeys (Cercopithecus ascanius), eight groups of black‐and‐white colobus (Colobus guereza), and one red colobus group. The red colobus group increased from 59 to 104 individuals, while redtail monkey and black‐and‐white colobus group sizes were stable, mirroring our survey results. To understand mechanisms behind group size changes in red colobus versus stability in other primates, we monitored forest dynamics at two spatial scales between 1990 and 2013, considered changes in predator population, and explored evidence of disease dynamics. The cumulative size of all trees and red colobus food trees increased over 24 yr, suggesting that changing food availability was driving group size changes for red colobus, while predation and disease played lesser roles. Overall, our results and evidence of changing primate densities suggest that the Kibale primate community is in a non‐equilibrium state. We suggest future conservation and management efforts take this into consideration.