Nikki Tagg

Origin of the HIV-1 group O epidemic in western lowland gorillas

Significance Understanding emerging disease origins is important to gauge future human infection risks. This is particularly true for the various forms of the AIDS virus, HIV-1, which were transmitted to humans on four independent occasions. Previous studies identified chimpanzees in southern Cameroon as the source of the pandemic M group, as well as the geographically more restricted N group. Here, we show that the remaining two groups also emerged in southern Cameroon but had their origins in western lowland gorillas. Although group P has only been detected in two individuals, group O has spread extensively throughout west central Africa. Thus, both chimpanzees and gorillas harbor viruses that are capable of crossing the species barrier to humans and causing major disease outbreaks. HIV-1, the cause of AIDS, is composed of four phylogenetic lineages, groups M, N, O, and P, each of which resulted from an independent cross-species transmission event of simian immunodeficiency viruses (SIVs) infecting African apes. Although groups M and N have been traced to geographically distinct chimpanzee communities in southern Cameroon, the reservoirs of groups O and P remain unknown. Here, we screened fecal samples from western lowland (n = 2,611), eastern lowland (n = 103), and mountain (n = 218) gorillas for gorilla SIV (SIVgor) antibodies and nucleic acids. Despite testing wild troops throughout southern Cameroon (n = 14), northern Gabon (n = 16), the Democratic Republic of Congo (n = 2), and Uganda (n = 1), SIVgor was identified at only four sites in southern Cameroon, with prevalences ranging from 0.8–22%. Amplification of partial and full-length SIVgor sequences revealed extensive genetic diversity, but all SIVgor strains were derived from a single lineage within the chimpanzee SIV (SIVcpz) radiation. Two fully sequenced gorilla viruses from southwestern Cameroon were very closely related to, and likely represent the source population of, HIV-1 group P. Most of the genome of a third SIVgor strain, from central Cameroon, was very closely related to HIV-1 group O, again pointing to gorillas as the immediate source. Functional analyses identified the cytidine deaminase APOBEC3G as a barrier for chimpanzee-to-gorilla, but not gorilla-to-human, virus transmission. These data indicate that HIV-1 group O, which spreads epidemically in west central Africa and is estimated to have infected around 100,000 people, originated by cross-species transmission from western lowland gorillas.

Fatal chimpanzee attack in Loango National Park, Gabon

In some populations, chimpanzees engage in lethal aggression within and between social units. We report a fatal attack on an adult male chimpanzee at a new research site in Loango National Park, Gabon. We found a fresh corpse of an adult male chimpanzee only a few hundred meters from the research camp, after noting numerous vocalizations and chimpanzee movements the previous evening. Previous contacts with chimpanzees and fresh tracks in the area around the corpse suggest that 2 communities of chimpanzees range where the attack occurred and that members of the neighboring community killed the chimpanzee. To support the conclusion, we conducted genetic analysis for 13 Y-chromosome loci and 9 microsatellite loci of fecal samples from the dead individual, 5 possible attackers, and 2 members of the other community Though we cannot exclude the possibility of an intracommunity killing, the combined observational and genetic evidence suggest an intercommunity attack. The case study adds to the growing evidence that intercommunity killings are a rare but widespread phenomenon among chimpanzees and not an artifact of human provisioning or habituation.

Chimpanzee accumulative stone throwing

The study of the archaeological remains of fossil hominins must rely on reconstructions to elucidate the behaviour that may have resulted in particular stone tools and their accumulation. Comparatively, stone tool use among living primates has illuminated behaviours that are also amenable to archaeological examination, permitting direct observations of the behaviour leading to artefacts and their assemblages to be incorporated. Here, we describe newly discovered stone tool-use behaviour and stone accumulation sites in wild chimpanzees reminiscent of human cairns. In addition to data from 17 mid- to long-term chimpanzee research sites, we sampled a further 34 Pan troglodytes communities. We found four populations in West Africa where chimpanzees habitually bang and throw rocks against trees, or toss them into tree cavities, resulting in conspicuous stone accumulations at these sites. This represents the first record of repeated observations of individual chimpanzees exhibiting stone tool use for a purpose other than extractive foraging at what appear to be targeted trees. The ritualized behavioural display and collection of artefacts at particular locations observed in chimpanzee accumulative stone throwing may have implications for the inferences that can be drawn from archaeological stone assemblages and the origins of ritual sites.

Phenological patterns in a natural population of a tropical timber tree species, Milicia excelsa (Moraceae): evidence of Isolation By Time and its interaction with feeding strategies of dispersers

PREMISE OF THE STUDY Population genetic structuring over limited timescales is commonly viewed as a consequence of spatial constraints. Indirect approaches have recently revealed reproductive isolation resulting from flowering time (so-called isolation by time, IBT). Since phenological processes can be subject to selection, the persistence of flowering asynchrony may be due to opposing selective pressures during mating, dispersal, and regeneration phases. Our study aimed to investigate phenology, fruit handling by animals, and their interaction in a timber tree species, Milicia excelsa. METHODS We analyzed phenological data collected over 6 years on 69 genotyped trees in a Cameroonian natural rainforest complemented by data from germination trials and field observations of dispersers. KEY RESULTS Initiation of flowering was correlated with variation in temperature and relative humidity, but was also affected by genetic factors: pairwise differences in flowering time between nearby individuals correlated with kinship coefficient, and earliness of flowering remained stable over time. A decrease in mean seed production per fruit with increasing flowering time suggests selection against late bloomers. However, germination rate was not affected by seed collection date, and the main seed disperser, the bat Eidolon helvum, seemed to increase in abundance at the end of the reproductive season and preferred trees in open habitats where early and late bloomers are expected. CONCLUSIONS The pairwise approach performs well in detecting IBT. The persistence of different mating pools in such a case may result from a trade off between selective forces during the mating and seed dispersal processes.

Ground night nesting in chimpanzees: new insights from central chimpanzees (Pan troglodytes troglodytes) in South-East Cameroon.

Some chimpanzee populations exhibit ground night nesting, which occurs in different habitat types, is driven by a variety of interconnected factors, and may reflect cultural or social differences. This has important implications for ape conservation management, given that accurate nest builder identification is required to estimate density, crucial in monitoring, and allows inferences about environmental and social factors that may have contributed to the transition from tree to ground sleeping in early hominins. We conducted a 24-month marked nest count survey in La Belgique, Cameroon, and recorded the occurrence of chimpanzee tree and ground night nests, temperature and rainfall, predator and large mammal abundance, human activities, nesting tree species, and Uapaca spp. consumption. Ground night nesting occurred at a rate of 3.47% (n = 1,008), with more in swamps, in the dry season and with increasing human activities. We found no influence of leopard/elephant presence, but a possible influence of lack of nesting trees. We suggest chimpanzees visit swamps in the dry season (low water levels) for relief from hunting pressure and to consume Uapaca spp. fruits. Ground nesting may be enabled due to high abundance of terrestrial herbaceous vegetation, and may be favoured for inconspicuousness and safety from gun hunters.

The role of great apes in seed dispersal of the tropical forest tree species Dacryodes normandii (Burseraceae) in Gabon

The identification of seed dispersers and predators is essential to understand the effect of anthropogenic disturbances, and the associated defaunation process, on tropical forest dynamics in Central Africa. In this study, the animals involved in seed predation and dispersal of Dacryodes normandii (Burseraceae), an endozoochorously dispersed tree species endemic to Gabonese forests, were identified in a site in south-east Gabon using two complementary methods: direct observation and camera-trap monitoring of fruit piles. The combined sampling effort (172 h of direct observations and 796 d of camera trapping) led to the identification of six disperser and eight predator species of D. normandii seeds. With high frequency of consumption (88% and 57% of their visits, respectively) and long visit duration (83 and 23 min, respectively), the western lowland gorilla and central chimpanzee were identified as the main dispersers of this species. Seeds passed through the gorilla gut exhibited high germination success (68%). Rodents were identified as predators of D. normandii seeds, potentially displaying rare secondary dispersal through scatter-hoarding. The results of this study highlight the importance of great apes in the seed dispersal of this tree species.

The Cross River Gorillas (Gorilla gorilla diehli) at Mawambi Hills, South-West Cameroon: Habitat Suitability and Vulnerability to Anthropogenic Disturbance

Only about 300 individuals of the Cross River gorilla (CRG; Gorilla gorilla diehli) survive today. The subspecies is endemic to approximately 12–14 sites at the Cameroon-Nigeria border, and is critically endangered. To understand survival prospects of the CRG at Mawambi Hills, Cameroon, a maximum entropy (MaxEnt) distribution model was used to predict the distribution of gorillas. Overall, 24% of the study area was predicted to be suitable for gorillas. The most important predictors of gorilla distribution were elevation as a surrogate for accessibility (52.4%), distance to nearby villages which represents proximity to anthropogenic disturbance (22.7%), and slope steepness as a proxy for security (19.4%). Gorillas mainly occupied slopes of steep hills and avoided areas of human disturbance. To evaluate the spatial relationship between gorilla distribution and human activities, the predicted habitat suitability map was overlaid with a kernel density map of human activities. A positive correlation was found between locations of human activity and suitable habitat for gorillas (r = 0.5). This suggests that anthropogenic pressures in previously unused forest areas are increasing as a result of resource depletion at lower altitudes, consequently putting the gorillas at greater risk. Conservation management plans that seek to reduce human encroachment into habitats preferred by gorillas such as steep hills will probably contribute to gorilla survival.

Nocturnal activity in wild chimpanzees (Pan troglodytes): Evidence for flexible sleeping patterns and insights into human evolution

OBJECTIVES We investigated occurrences and patterns of terrestrial nocturnal activity in wild chimpanzees (Pan troglodytes) and modelled the influence of various ecological predictors on nocturnal activity. METHODS Data were extracted from terrestrial camera-trap footage and ecological surveys from 22 chimpanzee study sites participating in the Pan African Programme: The Cultured Chimpanzee. We described videos demonstrating nocturnal activity, and we tested the effects of the percentage of forest, abundance of predators (lions, leopards and hyenas), abundance of large mammals (buffalos and elephants), average daily temperature, rainfall, human activity, and percent illumination on the probability of nocturnal activity. RESULTS We found terrestrial nocturnal activity to occur at 18 of the 22 study sites, at an overall average proportion of 1.80% of total chimpanzee activity, and to occur during all hours of the night, but more frequently during twilight hours. We found a higher probability of nocturnal activity with lower levels of human activity, higher average daily temperature, and at sites with a larger percentage of forest. We found no effect of the abundance of predators and large mammals, rainfall, or moon illumination. DISCUSSION Chimpanzee terrestrial nocturnal activity appears widespread yet infrequent, which suggests a consolidated sleeping pattern. Nocturnal activity may be driven by the stress of high daily temperatures and may be enabled at low levels of human activity. Human activity may exert a relatively greater influence on chimpanzee nocturnal behavior than predator presence. We suggest that chimpanzee nocturnal activity is flexible, enabling them to respond to changing environmental factors.

Feeding Ecology of Cross River Gorillas (Gorilla gorilla diehli) at Mawambi Hills: The Influence of Resource Seasonality

Determining the composition of primate diet and identifying factors that affect food choice are important in understanding habitat requirements of primates and designing conservation plans. We studied the diet of Cross River gorillas (Gorilla gorilla diehli) in relation to availability of food resources, in a semideciduous lowland forest site (Mawambi Hills) in Cameroon, from November 2009 to September 2011. Based on 109 d of feeding trail data, 203 fecal samples, and 22 mo of phenological monitoring, we determined that gorillas consumed a total of 242 food items, including 240 plant items from 186 species and 55 taxonomic families. Mawambi gorillas diversified fruit consumption when fruit availability increased, and consumed more fibrous foods (pith, leaf, bark) during times of fruit scarcity, consistent with results of other gorilla studies. However, fruit availability was not related to rainfall, and the period of fruit scarcity was more pronounced at Mawambi than at other gorilla study sites, due to a single long dry season and extreme rainfall at the end of the rainy season that delayed fruit production and ripening. We found no relationship between the daily path length of the gorillas and fruit consumption. We found feeding habits of Mawambi gorillas to be notably similar to those of a population of Cross River gorillas at Afi Mountain, Nigeria, although subtle differences existed, possibly due to site-specific differences in forest composition and altitude. At both sites the liana Landolphia spp. was the single most important food species: the leaves are a staple and the fruits are consumed during periods of fruit scarcity. Snails and maggots were consumed but we observed no further faunivory. We suggest that tree leaves and lianas are important fallback food sources in the gorilla diet in seasonally dry forests.

An unexpected diversity of trypanosomatids in fecal samples of great apes

Charismatic great apes have been used widely and effectively as flagship species in conservation campaigns for decades. These iconic representatives of their ecosystems could also play a role as reservoirs of several zoonotic diseases. Recently it was demonstrated that African great apes can host Leishmania parasites (Kinetoplastea: Trypanosomatidae). Given that this finding raised a strong negative reaction from leishmania experts and the subsequent discussion did not lead to a clear resolution, we decided to analyze wild gorilla (Gorilla gorilla gorilla) and chimpanzee (Pan troglodytes troglodytes) fecal samples collected from the same area in Cameroon as in the original study. Fecal samples, used to circumvent the difficulties and ethics involved in obtaining blood samples from endangered wild apes, were screened by three different PCR assays for detection of Leishmania DNA. We did not detect any leishmania parasites in analyzed feces; however, sequencing of SSU rRNA revealed an unexpected diversity of free-living bodonids (Kinetoplastea: Bodonidae) and parasitic trypanosomatids (Kinetoplastea: Trypanosomatidae) other than Leishmania. A single detected Phytomonas species, found in chimpanzee feces, most likely originated from animal plant food. On the other hand, the presence of four free-living bodonid species and four parasitic insect monoxenous trypanosomatid, including two possible new species of the genus Herpetomonas, could be explained as ex post contamination of feces either from the environment or from flies (Diptera: Brachycera).