Patrick A. Omeja

Are Primates Ecosystem Engineers

Animals can play important roles in structuring the plant communities in which they live. Some species are particularly influential in that they modify the physical environment by changing, maintaining, and/or creating new habitats; the term ecosystem engineer has been used to describe such species. We here assess the two major foraging strategies of primates, frugivory and folivory, in terms of the potential for primates to function as ecosystem engineers. We argue that whereas the role of primates as seed dispersers has received a great deal of attention, the potential role that folivorous primates play in structuring their environment through herbivory has received much less attention. Further, while quantifying if frugivorous primates are ecosystem engineers through their seed dispersal has proved very difficult, it is not as difficult to ascertain whether folivorous primates are ecosystem engineers. We document situations in which folivorous primates act as ecosystem engineers by 1) eating the leaves and/or bark of trees to the extent that they kill trees, 2) feeding on trees to the degree that they slow their growth relative to nonpreferred tree species, 3) eating the flowers of species to the extent that it does not set fruit, or 4) feeding on plants in such a way as to increase their productivity and abundance. Because evidence from the literature is very limited, where possible we present new evidence of these processes from the colobus monkeys at our long-term field site in Kibale National Park, Uganda. We conclude by discussing promising research programs that could be established to refine our understanding of the role primates play in shaping the structure of plant communities, especially tropical forests.

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.

Parks, people and pixels: evaluating landscape effects of an East African national park on its surroundings

Landscapes surrounding protected areas, while still containing considerable biodiversity, have rapidly growing human populations and associated agricultural development in most of the developing world that tend to isolate them, potentially reducing their conservation value. Using field studies and multi-temporal Landsat imagery, we examine a forest park, Kibale National Park in western Uganda, its changes over time, and related land cover change in the surrounding landscape. We find Kibale has successfully defended its borders and prevents within-park deforestation and other land incursions, and has maintained tree cover throughout the time period of the study. Outside the park there was a significant increase in tea plantations and continued forest fragmentation and wetland loss. The question of whether the park is a conservation success because of the network of forest fragments and wetlands or in spite of them remains unanswered.

What is the predictive power of the colobine protein-to-fiber model and its conservation value?

Predicting variation in animal abundance across time and space has proven very difficult; however, a model exists to predict the biomass of small folivorous primates that has considerable correlative support. This model suggests that the protein-to-fiber ratio of leaves in a habitat can predict folivore biomass. Here we present an experimental test of this protein-to-fiber model to assess if the number of infant monkeys per female and group size can be predicted based on the leaf chemistry of a habitat. We expected regenerating forest in Kibale National Park, Uganda to have leaves with higher concentrations of crude protein and lower concentrations of fiber than old-growth forest trees, and consequently, we expected a greater number of infants per female in the folivorous red colobus (Procolobus rufomitratus) with access to this area. As predicted, regenerating forests did have trees with leaves with high concentrations of protein and low concentrations of fiber, but there was no corresponding change in the demographic structure of red colobus groups. We also tested whether energy was a potential determinant of these parameters, but found no evidence for its importance. Our findings support recent studies that are critical of the protein-to-fiber model, which lead us to question the models generality, particularly for conservation and management.

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.

Fire control as a simple means of promoting tropical forest restoration

Tropical deforestation is occurring at an alarming rate. The loss of these forests contributes significantly to total global carbon dioxide emissions and accelerating rates of climate change; moreover, many deforested lands lose fertility and are abandoned. Demands to protect biodiversity and reverse climate change call for efforts to reforest such lands, and one method is through fire control, as fire suppresses tree regeneration. Unfortunately, the success of fire control is often not known for tropical regions because research efforts must span decades. We compared above ground biomass in two plots of regenerating forest that were protected from fire for 12 and 32 years in Kibale National Park, Uganda. Tree biomass of the plots was substantial, and while the biomass of the 12- and 32-year plots did not differ significantly, the 12-year plot had a higher biomass in the small diameter classes in comparison to the 32-year plot. Twenty-four tree species were growing in 12-year plot, while 46 grew in the 32-year plot. We conclude that fire exclusion is a promising approach for tropical forest restoration, and we demonstrate that it is cost-effective relative to programs that plant tree seedlings.

Park isolation in anthropogenic landscapes: land change and livelihoods at park boundaries in the African Albertine Rift

Landscapes are changing rapidly in regions where rural people live adjacent to protected parks and reserves. This is the case in highland East Africa, where many parks are increasingly isolated in a matrix of small farms and settlements. In this review, we synthesize published findings and extant data sources to assess the processes and outcomes of park isolation, with a regional focus on people’s livelihoods at park boundaries in the Ugandan Albertine Rift. The region maintains exceptionally high rural population density and growth and is classified as a global biodiversity hotspot. In addition to the impacts of increasing numbers of people, our synthesis highlights compounding factors—changing climate, increasing land value and variable tenure, and declining farm yields—that accelerate effects of population growth on park isolation and widespread landscape change. Unpacking these processes at the regional scale identifies outcomes of isolation in the unprotected landscape—high frequency of human-wildlife conflict, potential for zoonotic disease transmission, land and resource competition, and declining wildlife populations in forest fragments. We recommend a strategy for the management of isolated parks that includes augmenting outreach by park authorities and supporting community needs in the human landscape, for example through healthcare services, while also maintaining hard park boundaries through traditional protectionism. Even in cases where conservation refers to biodiversity in isolated parks, landscape strategies must include an understanding of the local livelihood context in order to ensure long-term sustainable biodiversity protection.

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.

Fruit defence syndromes: the independent evolution of mechanical and chemical defences

Plants are prone to attack by a great diversity of antagonists against which they deploy various defence mechanisms, of which the two principle ones are mechanical and chemical defences. These defences are hypothesized to be negatively correlated due to either functional redundancy or a trade-off, i.e., plants which rely on increased mechanical defence should downregulate their degree of chemical defence and vice versa. A competing hypothesis is that different defences perform distinct functions and draw from different pools of resources, which should result in their independent evolution. We examine these competing hypotheses using two independent datasets of fleshy fruits we collected from Madagascar and Uganda. We sampled mechanical defences, indexed by fruit puncture resistance, and defensive defences, indexed by defensive volatile organic compounds, and examined their associations using phylogenetically-controlled models. In both systems, we found no correlation between mechanical and chemical defences, thus supporting the independent evolution hypothesis. This implies that fruit defence mechanisms reflect a more complex array of selection pressures and constraints than previously perceived.

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 HIV 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.