Josephine Head

Complex tool sets for honey extraction among chimpanzees in Loango National Park, Gabon

Homo faber was once proposed as a label for humans specifically to highlight their unique propensity for tool use. However, new observations on complex tool use by the chimpanzees of Loango National Park, Gabon, expand our knowledge about tool-using abilities in Pan troglodytes. Chimpanzees in Loango, when using tools to extract honey from three types of bee nests, were observed to regularly use three- to five-element tool sets. In other words, different types of tools were used sequentially to access a single food source. Such tool sets included multi-function tools that present typical wear for two distinct uses. In addition, chimpanzees exploited underground bee nests and used ground-perforating tools to locate nest chambers that were not visible from the ground surface. These new observations concur with others from Central African chimpanzees to highlight the importance of honey extraction in arguments favoring the emergence of complex tool use in hominoids, including different tool types, expanded tool sets, multifunction tools, and the exploitation of underground resources. This last technique requires sophisticated cognitive abilities concerning unseen objects. A sequential analysis reveals a higher level of complexity in honey extraction than previously proposed for nut cracking or hunting tools, and compares with some technologies attributed to early hominins from the Early and Middle Stone Age. A better understanding of similarities in human and chimpanzee tool use will allow for a greater understanding of tool-using skills that are uniquely human.

Novel Adenoviruses in Wild Primates: a High Level of Genetic Diversity and Evidence of Zoonotic Transmissions

ABSTRACT Adenoviruses (AdVs) broadly infect vertebrate hosts, including a variety of nonhuman primates (NHPs). In the present study, we identified AdVs in NHPs living in their natural habitats, and through the combination of phylogenetic analyses and information on the habitats and epidemiological settings, we detected possible horizontal transmission events between NHPs and humans. Wild NHPs were analyzed with a pan-primate AdV-specific PCR using a degenerate nested primer set that targets the highly conserved adenovirus DNA polymerase gene. A plethora of novel AdV sequences were identified, representing at least 45 distinct AdVs. From the AdV-positive individuals, 29 nearly complete hexon genes were amplified and, based on phylogenetic analysis, tentatively allocated to all known human AdV species (Human adenovirus A to Human adenovirus G [HAdV-A to -G]) as well as to the only simian AdV species (Simian adenovirus A [SAdV-A]). Interestingly, five of the AdVs detected in great apes grouped into the HAdV-A, HAdV-D, HAdV-F, or SAdV-A clade. Furthermore, we report the first detection of AdVs in New World monkeys, clustering at the base of the primate AdV evolutionary tree. Most notably, six chimpanzee AdVs of species HAdV-A to HAdV-F revealed a remarkably close relationship to human AdVs, possibly indicating recent interspecies transmission events.

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.

Remote video-camera traps measure habitat use and competitive exclusion among sympatric chimpanzee, gorilla and elephant in Loango National Park, Gabon

Speciescommonlyexistinsympatry,yetecologicalstudiesareoftenbasedonasinglespeciesapproachwhile ignoring the impact of sympatric competitors. Over 13 mo we used 24 remote video-camera traps to monitor habitat use of sympatric chimpanzee, gorilla and elephant in four different habitat types in Loango National Park, Gabon. Habitat use by each species was predicted to vary according to seasonal changes in food availability and precipitation. Increased interspecific competition between the three species was expected at times of reduced resource availability, leading to exclusion of the inferior competitor. Supporting the predictions, species abundance per habitat showed seasonal variation: all three species responded positively to increased fruit availability in all habitats, but the response was only significant for gorilla in mature forest and elephant in coastal forest. Responses to rainfall varied, with the chimpanzee responding negatively to rainfall in swamp forest, the gorilla responding positively to rainfall in coastal andsecondaryforest,andtheelephantrespondingpositivelytorainfallinmatureforest.Elephantpresenceresultedin competitive exclusion of the apes under certain conditions: the chimpanzee was excluded by the elephant where fruit availability was low, whereas the gorilla was excluded by the elephant in areas of low herb density despite high fruit availability. Our results emphasize the value of applying a multi-species, longer-term approach to studying variation in habitat use among sympatric species and highlight the impact competitors can exert on one anothers distribution.

A novel adenovirus of Western lowland gorillas (Gorilla gorilla gorilla)

Adenoviruses (AdV) broadly infect vertebrate hosts including a variety of primates. We identified a novel AdV in the feces of captive gorillas by isolation in cell culture, electron microscopy and PCR. From the supernatants of infected cultures we amplified DNA polymerase (DPOL), preterminal protein (pTP) and hexon gene sequences with generic pan primate AdV PCR assays. The sequences in-between were amplified by long-distance PCRs of 2 - 10 kb length, resulting in a final sequence of 15.6 kb. Phylogenetic analysis placed the novel gorilla AdV into a cluster of primate AdVs belonging to the species Human adenovirus B (HAdV-B). Depending on the analyzed gene, its position within the cluster was variable. To further elucidate its origin, feces samples of wild gorillas were analyzed. AdV hexon sequences were detected which are indicative for three distinct and novel gorilla HAdV-B viruses, among them a virus nearly identical to the novel AdV isolated from captive gorillas. This shows that the discovered virus is a member of a group of HAdV-B viruses that naturally infect gorillas. The mixed phylogenetic clusters of gorilla, chimpanzee, bonobo and human AdVs within the HAdV-B species indicate that host switches may have been a component of the evolution of human and non-human primate HAdV-B viruses.

Distribution and Numbers of Pygmies in Central African Forests

Pygmy populations occupy a vast territory extending west-to-east along the central African belt from the Congo Basin to Lake Victoria. However, their numbers and actual distribution is not known precisely. Here, we undertake this task by using locational data and population sizes for an unprecedented number of known Pygmy camps and settlements (n = 654) in five of the nine countries where currently distributed. With these data we develop spatial distribution models based on the favourability function, which distinguish areas with favourable environmental conditions from those less suitable for Pygmy presence. Highly favourable areas were significantly explained by presence of tropical forests, and by lower human pressure variables. For documented Pygmy settlements, we use the relationship between observed population sizes and predicted favourability values to estimate the total Pygmy population throughout Central Africa. We estimate that around 920,000 Pygmies (over 60% in DRC) is possible within favourable forest areas in Central Africa. We argue that fragmentation of the existing Pygmy populations, alongside pressure from extractive industries and sometimes conflict with conservation areas, endanger their future. There is an urgent need to inform policies that can mitigate against future external threats to these indigenous peoples’ culture and lifestyles.

Protected Areas in Tropical Africa: Assessing Threats and Conservation Activities

Numerous protected areas (PAs) have been created in Africa to safeguard wildlife and other natural resources. However, significant threats from anthropogenic activities and decline of wildlife populations persist, while conservation efforts in most PAs are still minimal. We assessed the impact level of the most common threats to wildlife within PAs in tropical Africa and the relationship of conservation activities with threat impact level. We collated data on 98 PAs with tropical forest cover from 15 countries across West, Central and East Africa. For this, we assembled information about local threats as well as conservation activities from published and unpublished literature, and questionnaires sent to long-term field workers. We constructed general linear models to test the significance of specific conservation activities in relation to the threat impact level. Subsistence and commercial hunting were identified as the most common direct threats to wildlife and found to be most prevalent in West and Central Africa. Agriculture and logging represented the most common indirect threats, and were most prevalent in West Africa. We found that the long-term presence of conservation activities (such as law enforcement, research and tourism) was associated with lower threat impact levels. Our results highlight deficiencies in the management effectiveness of several PAs across tropical Africa, and conclude that PA management should invest more into conservation activities with long-term duration.

Spatio-temporal complexity of chimpanzee food: how cognitive adaptations can counteract the ephemeral nature of ripe fruit

Ecological complexity has been proposed to play a crucial role in primate brain‐size evolution. However, detailed quantification of ecological complexity is still limited. Here we assess the spatio‐temporal distribution of tropical fruits and young leaves, two primary chimpanzee (Pan troglodytes) foods, focusing on the predictability of their availability in individual trees. Using up to 20 years of information on monthly availability of young leaf, unripe and ripe fruit in plant species consumed by chimpanzees from tropical forests in East, Central, and West Africa, we estimated: (1) the forest‐wide frequency of occurrence of each food type and (2) the predictability of finding ripe fruit‐bearing trees, focusing on the timing, frequency, and amount of ripe fruit present. In all three forests, at least half of all encountered trees belonged to species that chimpanzees were known to feed on. However, the proportion of these trees bearing young leaves and fruit fluctuated widely between months. Ripe fruit was the most ephemeral food source, and trees that had more than half of their crown filled were at least nine times scarcer than other trees. In old growth forests only one large ripe fruit crop was on average encountered per 10 km. High levels of inter‐individual variation in the number of months that fruit was present existed, and in some extreme cases individuals bore ripe fruit more than seven times as often as conspecifics. Some species showed substantially less variation in such ripe fruit production frequencies and fruit quantity than others. We hypothesize that chimpanzees employ a suite of cognitive mechanisms, including abilities to: (1) generalize or classify food trees; (2) remember the relative metrics of quantity and frequency of fruit production across years; and (3) flexibly plan return times to feeding trees to optimize high‐energy food consumption in individual trees, and efficient travel between them. Am. J. Primatol. 78:626–645, 2016.

The spatio-temporal complexity of chimpanzee food: How cognitive adaptations can counteract the ephemeral nature of ripe fruit (advance online)

Ecological complexity has been proposed to play a crucial role in primate brain‐size evolution. However, detailed quantification of ecological complexity is still limited. Here we assess the spatio‐temporal distribution of tropical fruits and young leaves, two primary chimpanzee (Pan troglodytes) foods, focusing on the predictability of their availability in individual trees. Using up to 20 years of information on monthly availability of young leaf, unripe and ripe fruit in plant species consumed by chimpanzees from tropical forests in East, Central, and West Africa, we estimated: (1) the forest‐wide frequency of occurrence of each food type and (2) the predictability of finding ripe fruit‐bearing trees, focusing on the timing, frequency, and amount of ripe fruit present. In all three forests, at least half of all encountered trees belonged to species that chimpanzees were known to feed on. However, the proportion of these trees bearing young leaves and fruit fluctuated widely between months. Ripe fruit was the most ephemeral food source, and trees that had more than half of their crown filled were at least nine times scarcer than other trees. In old growth forests only one large ripe fruit crop was on average encountered per 10 km. High levels of inter‐individual variation in the number of months that fruit was present existed, and in some extreme cases individuals bore ripe fruit more than seven times as often as conspecifics. Some species showed substantially less variation in such ripe fruit production frequencies and fruit quantity than others. We hypothesize that chimpanzees employ a suite of cognitive mechanisms, including abilities to: (1) generalize or classify food trees; (2) remember the relative metrics of quantity and frequency of fruit production across years; and (3) flexibly plan return times to feeding trees to optimize high‐energy food consumption in individual trees, and efficient travel between them. Am. J. Primatol. 78:626–645, 2016.

Comparative isotope ecology of African great apes

The isotope ecology of great apes is a useful reference for palaeodietary reconstructions in fossil hominins. As extant apes live in C3-dominated habitats, variation in isotope signatures is assumed to be low compared to hominoids exploiting C4-plant resources. However, isotopic differences between sites and between and within individuals are poorly understood due to the lack of vegetation baseline data. In this comparative study, we included all species of free-ranging African great apes (Pan troglodytes, Pan paniscus, Gorilla sp.). First, we explore differences in isotope baselines across different habitats and whether isotopic signatures in apes can be related to feeding niches (faunivory and folivory). Secondly, we illustrate how stable isotopic variations within African ape populations compare to other extant and extinct primates and discuss possible implications for dietary flexibility. Using 701 carbon and nitrogen isotope data points resulting from 148 sectioned hair samples and an additional collection of 189 fruit samples, we compare six different great ape sites. We investigate the relationship between vegetation baselines and climatic variables, and subsequently correct great ape isotope data to a standardized plant baseline from the respective sites. We obtained temporal isotopic profiles of individual animals by sectioning hair along its growth trajectory. Isotopic signatures of great apes differed between sites, mainly as vegetation isotope baselines were correlated with site-specific climatic conditions. We show that controlling for plant isotopic characteristics at a given site is essential for faunal data interpretation. While accounting for plant baseline effects, we found distinct isotopic profiles for each great ape population. Based on evidence from habituated groups and sympatric great ape species, these differences could possibly be related to faunivory and folivory. Dietary flexibility in apes varied, but temporal variation was overall lower than in fossil hominins and extant baboons, shifting from C3 to C4-resources, providing new perspectives on comparisons between extinct and extant primates.