Fifty+ years of primate research illustrates complex drivers of abundance and increasing primate numbers.

Many primate populations are threatened by human actions and a central tool used for their protection is establishing protected areas. However, even if populations in such areas are protected from hunting and deforestation, they still may be threatened by factors such as climate change and its cascading impacts on habitat quality and disease dynamics. Here we provide a long-term and geographically wide-spread population assessment of the five common diurnal primates of Kibale National Park, Uganda. Over 7 year-long or longer census efforts that spanned 52 years, our team walked 1466 km, and recorded 480 monkey groups. Populations were generally relatively stable with a few exceptions, for which no apparent causative factors could be identified. This stability is unexpected as many ecological changes documented over the last 34+ years (e.g., decreasing food abundance and quality) were predicted to have negative impacts. Populations of some species declined at some sites but increased at others. This highlights the need for large, protected areas so that declines in particular areas are countered by gains in others. Kibale has large areas of regenerating forest and this most recent survey revealed that after 20+ years, forest regeneration in many of these areas appears sufficient to sustain sizeable primate populations, except for blue monkeys that have not colonized these areas. Indeed, the average primate abundance in the regenerating forest was only 8.1% lower than in neighboring old-growth forest. Thus, park-wide primate abundance has likely increased, despite many pressures on the park having risen; however, some areas in the park remain to be assessed. Our study suggests that the restoration, patrolling, and community outreach efforts of the Uganda Wildlife Authority and their partners have contributed significantly to protecting the park and its animals.

Vertebrate environmental DNA from leaf swabs.

Terrestrial vertebrates are threatened by anthropogenic activities around the world. The rapid biodiversity loss that ensues is most intense in the tropics and affects ecosystem functions, such as seed dispersal, or may facilitate pathogen transmission1. Monitoring vertebrate distributions is essential for understanding changes in biodiversity and ecosystems and also for adaptive management strategies. Environmental DNA (eDNA) approaches have the potential to play a key role in such efforts. Here, we explore whether eDNA swabbed from terrestrial vegetation in a tropical biodiversity hotspot is a useful tool for vertebrate biomonitoring. By swabbing leaves, we collected eDNA from 24 swabs at three locations in Kibale National Park, Uganda and used two metabarcoding systems to catalog the vertebrate taxa in the samples. We detected 52 wild vertebrate genera, including 26 avian and 24 mammalian genera; 30 of these assignments could be refined to the species level. We detected an average of 7.6 genera per swab. This approach, with its inexpensive and simple collection and DNA extraction, opens the door for inexpensive large-scale vertebrate biomonitoring.

Can I afford to publish? A dilemma for African scholars.

With open-access publishing authors often pay an article processing charge and subsequently their article is freely available online. These charges are beyond the reach of most African academics. Thus, the trend towards open-access publishing will shift the business model from a pay-wall model, where access to literature is limited, to a pay-to-publish one, where African scholars cannot afford to publish. We explore the costs of publishing and the ability of African scholars to afford to publish via open access in top journals. Three-quarters of the 40 top ecology journals required payment for open-access publishing (average cost $3150). Paying such fees is a hardship for African scholars as grant funding is not available and it is not feasible to pay the fees themselves as salaries are low. We encourage funders and publishers to facilitate an equitable publishing model that allows African scholars to make their research available through open-access publishing.

The Movement of Pathogen Carrying Flies at the Human-Wildlife Interface.

Flies form high-density associations with human settlements and groups of nonhuman primates and are implicated in transmitting pathogens. We investigate the movement of nonhuman primate-associated flies across landscapes surrounding Kibale National Park, Uganda, using a mark-recapture experiment. Flies were marked in nine nonhuman primate groups at the forest edge ([Formula: see text] = 929 flies per group), and we then attempted to recapture them in more anthropized areas (50 m, 200 m and 500 m from where marked; 2-21 days after marking). Flies marked in nonhuman primate groups were recaptured in human areas (19/28,615 recaptured). Metabarcoding of the flies in nonhuman primate groups revealed the DNA of multiple eukaryotic primate parasites. Taken together, these results demonstrate the potential of flies to serve as vectors between nonhuman primates, livestock and humans at this biodiverse interface.

Long-term trends in a forest ungulate community: park establishment increases numbers, but poaching is a constant threat.

Deforestation represents one of the greatest threats to tropical forest mammals, and the situation is greatly exacerbated by bushmeat hunting. To construct informed conservation plans, information must be gathered about responses to habitat degradation, regeneration, and hunting over a sufficiently long period to allow demographic responses. We quantified changes in the abundance of three commonly occurring ungulate species (i.e., bushbuck, Tragelaphus scriptus; red duiker, Cephalophus sp.; blue duiker, Cephalophus monticola) at eight sites in Kibale National Park, Uganda (old growth=3; logged=3; regenerating=2) for 23 years. Changes in abundance (363 surveys totaling 1 450 km) were considered in regard to the park's management strategy, regional economic indicators, and estimates of illegal hunting. Bushbuck abundance increased in old-growth and logged forests from 1996 to 2009, and then oscillated around this level or declined. Duiker abundance demonstrated a similar pattern, but abundance in the old-growth forests showed a general increase from 1996 to present day. Duiker abundance in the logged forests exhibited an early increase, but subsequent oscillation. Poaching signs per patrol have remained stable over the last decade, despite increases in the size of the surrounding population, cost of living, and cost of schooling, thus reflecting successful efforts in conservation education and enforcement. Our study highlights the positive impact of park establishment, patrol, and conservation efforts on ungulate populations and shows the adaptability of forest mammal populations to different management schemes.

Discovery of Lanama Virus, a Distinct Member of Species Kunsagivirus C (Picornavirales: Picornaviridae), in Wild Vervet Monkeys (Chlorocebus pygerythrus).

We report the discovery and sequence-based molecular characterization of a novel virus, lanama virus (LNMV), in blood samples obtained from two wild vervet monkeys (Chlorocebus pygerythrus), sampled near Lake Nabugabo, Masaka District, Uganda. Sequencing of the complete viral genomes and subsequent phylogenetic analysis identified LNMV as a distinct member of species Kunsagivirus C, in the undercharacterized picornavirid genus Kunsagivirus.

Primates Can Be a Rallying Symbol to Promote Tropical Forest Restoration.

With 60% of all primate species now threatened with extinction and many species only persisting in small populations in forest fragments, conservation action is urgently needed. But what type of action? Here we argue that restoration of primate habitat will be an essential component of strategies aimed at conserving primates and preventing the extinctions that may occur before the end of the century and propose that primates can act as flagship species for restoration efforts. To do this we gathered a team of academics from around the world with experience in restoration so that we could provide examples of why primate restoration ecology is needed, outline how primates can act as flagship species for restoration efforts of tropical forest, review what little is known about how primate populations respond to restoration efforts, and make specific recommendations of the next steps needed to make restoration of primate populations successful. We set four priorities: (1) academics must effectively communicate both the value of primates and the need for restoration; (2) more research is needed on how primates contribute to forest restoration; (3) more effort must be put into Masters and PhD level training for tropical country nationals; and finally (4) more emphasis is needed to monitor the responses of regenerating forest and primate populations where restoration efforts are initiated. We are optimistic that populations of many threatened species can recover, and extinctions can be prevented, but only if concerted large-scale efforts are made soon and if these efforts include primate habitat restoration.

Genome-Wide Patterns of Gene Expression in a Wild Primate Indicate Species-Specific Mechanisms Associated with Tolerance to Natural Simian Immunodeficiency Virus Infection.

Over 40 species of nonhuman primates host simian immunodeficiency viruses (SIVs). In natural hosts, infection is generally assumed to be nonpathogenic due to a long coevolutionary history between host and virus, although pathogenicity is difficult to study in wild nonhuman primates. We used whole-blood RNA-seq and SIV prevalence from 29 wild Ugandan red colobus (Piliocolobus tephrosceles) to assess the effects of SIV infection on host gene expression in wild, naturally SIV-infected primates. We found no evidence for chronic immune activation in infected individuals, suggesting that SIV is not immunocompromising in this species, in contrast to human immunodeficiency virus in humans. Notably, an immunosuppressive gene, CD101, was upregulated in infected individuals. This gene has not been previously described in the context of nonpathogenic SIV infection. This expands the known variation associated with SIV infection in natural hosts and may suggest a novel mechanism for tolerance of SIV infection in the Ugandan red colobus.

The evolution of fruit colour: phylogeny, abiotic factors and the role of mutualists.

The adaptive significance of fruit colour has been investigated for over a century. While colour can fulfil various functions, the most commonly tested hypothesis is that it has evolved to increase fruit visual conspicuousness and thus promote detection and consumption by seed dispersing animals. However, fruit colour is a complex trait which is subjected to various constraints and selection pressures. As a result, the effect of animal selection on fruit colour are often difficult to identify, and several studies have failed to detect it. Here, we employ an integrative approach to examine what drives variation in fruit colour. We quantified the colour of ripe fruit and mature leaves of 97 tropical plant species from three study sites in Madagascar and Uganda. We used phylogenetically controlled models to estimate the roles of phylogeny, abiotic factors, and dispersal mode on fruit colour variation. Our results show that, independent of phylogeny and leaf coloration, mammal dispersed fruits are greener than bird dispersed fruits, while the latter are redder than the former. In addition, fruit colour does not correlate with leaf colour in the visible spectrum, but fruit reflection in the ultraviolet area of the spectrum is strongly correlated with leaf reflectance, emphasizing the role of abiotic factors in determining fruit colour. These results demonstrate that fruit colour is affected by both animal sensory ecology and abiotic factors and highlight the importance of an integrative approach which controls for the relevant confounding factors.

Cis-regulatory evolution in a wild primate: Infection-associated genetic variation drives differential expression of MHC-DQA1 in vitro.

Few studies have combined genetic association analyses with functional characterization of infection-associated SNPs in natural populations of nonhuman primates. Here, we investigate the relationship between host genetic variation, parasitism and natural selection in a population of red colobus (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. We collected parasitological, cellular and genomic data to test the following hypotheses: (i) MHC-DQA1 regulatory genetic variation is associated with control of whipworm (Trichuris) infection in a natural population of red colobus; (ii) infection-associated SNPs are functional in driving differential gene expression in vitro; and (iii) balancing selection has shaped patterns of variation in the MHC-DQA1 promoter. We identified two SNPs in the MHC-DQA1 promoter, both in transcription factor binding sites, and both of which are associated with decreased control of Trichuris infection. We characterized the function of both SNPs by testing differences in gene expression between the two alleles of each SNP in two mammalian cell lines. Alleles of one of the SNPs drove differential gene expression in both cell lines, while the other SNP drove differences in expression in one of the cell lines. Additionally, we found evidence of balancing selection acting on the MHC-DQA1 promoter, including extensive trans-species polymorphisms between red colobus and other primates, and an excess of intermediate-frequency alleles relative to genome-wide, coding and noncoding RADseq data. Our data suggest that balancing selection provides adaptive regulatory flexibility that outweighs the consequences of increased parasite infection intensity in heterozygotes.

Providing health care to improve community perceptions of protected areas.

Impoverished communities often turn to illegal extraction of resources from protected areas to alleviate economic pressures or to make monetary gains. Such practices can cause ecological damage and threaten animal populations. These communities also often face a high disease burden and typically do not have access to affordable health care. Here we argue that these two seemingly separate challenges may have a common solution. In particular, providing health care to communities adjacent to protected areas may be an efficient and effective way to reduce the disease burden while also improving local perceptions about protected areas, potentially reducing illegal extraction. We present a case study of a health centre on the edge of Kibale National Park, Uganda. The centre has provided care to c. 7,200 people since 2008 and its outreach programme extends to c. 4,500 schoolchildren each year. Contrasting the provision of health care to other means of improving community perceptions of protected areas suggests that health clinics have potential as a conservation tool in some situations and should be considered in future efforts to manage protected areas.

Genomic resources notes accepted 1 December 2014 - 31 January 2015.

This article documents the public availability of (i) transcriptome sequence data and assembly for the rostrum dace (Leuciscus burdigalensis) naturally infected by a copepod ectoparasite (Tracheliastes polycolpus) and (ii) SNPs identified and validated from RAD sequencing for the Ugandan red colobus (Procolobus rufomitratus tephrosceles) using RAD sequencing.

Hidden population structure and cross-species transmission of whipworms (Trichuris sp.) in humans and non-human primates in Uganda.

BACKGROUND: Whipworms (Trichuris sp.) are a globally distributed genus of parasitic helminths that infect a diversity of mammalian hosts. Molecular methods have successfully resolved porcine whipworm, Trichuris suis, from primate whipworm, T. trichiura. However, it remains unclear whether T. trichiura is a multi-host parasite capable of infecting a wide taxonomic breadth of primate hosts or a complex of host specific parasites that infect one or two closely related hosts. METHODS AND FINDINGS: We examined the phylogenetic structure of whipworms in a multi-species community of non-human primates and humans in Western Uganda, using both traditional microscopy and molecular methods. A newly developed nested polymerase chain reaction (PCR) method applied to non-invasively collected fecal samples detected Trichuris with 100% sensitivity and 97% specificity relative to microscopy. Infection rates varied significantly among host species, from 13.3% in chimpanzees (Pan troglodytes) to 88.9% in olive baboons (Papio anubis). Phylogenetic analyses based on nucleotide sequences of the Trichuris internal transcribed spacer regions 1 and 2 of ribosomal DNA revealed three co-circulating Trichuris groups. Notably, one group was detected only in humans, while another infected all screened host species, indicating that whipworms from this group are transmitted among wild primates and humans. CONCLUSIONS AND SIGNIFICANCE: Our results suggest that the host range of Trichuris varies by taxonomic group, with some groups showing host specificity, and others showing host generality. In particular, one Trichuris taxon should be considered a multi-host pathogen that is capable of infecting wild primates and humans. This challenges past assumptions about the host specificity of this and similar helminth parasites and raises concerns about animal and human health.

Nodule worm infection in humans and wild primates in Uganda: cryptic species in a newly identified region of human transmission.

INTRODUCTION: Soil-transmitted helminths (STHs) are a major health concern in tropical and sub-tropical countries. Oesophagostomum infection is considered endemic to West Africa but has also been identified in Uganda, East Africa, among primates (including humans). However, the taxonomy and ecology of Oesophagostomum in Uganda have not been studied, except for in chimpanzees (Pan troglodytes), which are infected by both O. bifurcum and O. stephanostomum. METHODS AND FINDINGS: We studied Oesophagostomum in Uganda in a community of non-human primates that live in close proximity to humans. Prevalence estimates based on microscopy were lower than those based on polymerase chain reaction (PCR), indicating greater sensitivity of PCR. Prevalence varied among host species, with humans and red colobus (Procolobus rufomitratus) infected at lowest prevalence (25% and 41% by PCR, respectively), and chimpanzees, olive baboons (Papio anubis), and l'hoest monkeys (Cercopithecus lhoesti) infected at highest prevalence (100% by PCR in all three species). Phylogenetic regression showed that primates travelling further and in smaller groups are at greatest risk of infection. Molecular phylogenetic analyses revealed three cryptic clades of Oesophagostomum that were not distinguishable based on morphological characteristics of their eggs. Of these, the clade with the greatest host range had not previously been described genetically. This novel clade infects humans, as well as five other species of primates. CONCLUSIONS: Multiple cryptic forms of Oesophagostomum circulate in the people and primates of western Uganda, and parasite clades differ in host range and cross-species transmission potential. Our results expand knowledge about human Oesophagostomum infection beyond the West African countries of Togo and Ghana, where the parasite is a known public health concern. Oesophagostomum infection in humans may be common throughout Sub-Saharan Africa, and the transmission of this neglected STH among primates, including zoonotic transmission, may vary among host communities depending on their location and ecology.

Deep sequencing identifies two genotypes and high viral genetic diversity of human pegivirus (GB virus C) in rural Ugandan patients.

Human pegivirus (HPgV), formerly 'GB virus C' or 'hepatitis G virus', is a member of the genus Flavivirus (Flaviviridae) that has garnered significant attention due to its inhibition of HIV, including slowing disease progression and prolonging survival in HIV-infected patients. Currently, there are six proposed HPgV genotypes that have roughly distinct geographical distributions. Genotypes 2 and 3 are the most comprehensively characterized, whereas those genotypes occurring on the African continent, where HPgV prevalence is highest, are less well studied. Using deep sequencing methods, we identified complete coding HPgV sequences in four of 28 patients (14.3%) in rural Uganda, east Africa. One of these sequences corresponds to genotype 1 and is the first complete genome of this genotype from east Africa. The remaining three sequences correspond to genotype 5, a genotype that was previously considered exclusively South African. All four positive samples were collected within a geographical area of less than 25 km(2), showing that multiple HPgV genotypes co-circulate in this area. Analysis of intra-host viral genetic diversity revealed that total single-nucleotide polymorphism frequency was approximately tenfold lower in HPgV than in hepatitis C virus. Finally, one patient was co-infected with HPgV and HIV, which, in combination with the high prevalence of HIV, suggests that this region would be a useful locale to study the interactions and co-evolution of these viruses.