Budongo Forest Research Articles

An intentional vocalization draws others' attention: a playback experiment with wild chimpanzees.

A vital step in the evolution of language is likely to have been when signalers explicitly intended to direct recipients' attention to external objects with the use of referential signals. Although animal signals can direct the attention of others to external events, such as in monkey predator alarm calls, there is little evidence that this is the result of an intention to inform the recipient. Two recent studies, however, indicate that the production of chimpanzee quiet alarm calls, given to snakes, complies with some standard behavioral markers of intentional signaling, such as gaze alternation. But it is currently unknown whether the calls alone direct receivers' attention to the threat. To address this, we carried out a playback experiment with free-ranging chimpanzees in Budongo Forest, Uganda, using a within-subjects design. From a hidden speaker, we broadcast either quiet alarm 'hoos' ('alert hoos') or acoustically distinguishable hoos produced while resting ('rest hoos') and found a significant increase in search behavior after 'alert' compared with 'rest' hoos, with subjects monitoring either the call provider or the area near the call provider. In sum, chimpanzee 'alert hoos' represent a plausible case of an intentionally produced animal vocalization (other studies) that refers recipients to signalers and/or to an external event (this study).

Social, contextual, and individual factors affecting the occurrence and acoustic structure of drumming bouts in wild chimpanzees (Pan troglodytes).

The production of structured and repetitive sounds by striking objects is a behavior found not only in humans, but also in a variety of animal species, including chimpanzees (Pan troglodytes). In this study we examined individual and social factors that may influence the frequency with which individuals engage in drumming behavior when producing long distance pant hoot vocalizations, and analyzed the temporal structure of those drumming bouts. Male chimpanzees from Budongo Forest, Uganda, drummed significantly more frequently during travel than feeding or resting and older individuals were significantly more likely to produce drumming bouts than younger ones. In contrast, we found no evidence that the presence of estrus females, high ranking males and preferred social partners in the caller's vicinty had an effect on the frequency with which an individual accompanied their pant hoot vocalization with drumming. Through acoustic analyses, we demonstrated that drumming sequences produced with pant hoots may have contained information on individual identity and that qualitatively, there was individual variation in the complexity of the temporal patterns produced. We conclude that drumming patterns may act as individually distinctive long-distance signals that, together with pant hoot vocalizations, function to coordinate the movement and spacing of dispersed individuals within a community, rather than as signals to group members in the immediate audience.

Social network analysis shows direct evidence for social transmission of tool use in wild chimpanzees.

Author SummaryChimpanzees are widely considered as the most “cultural” of all animals, despite the lack of direct evidence for the spread of novel behaviors through social learning in the wild. Here, we present a novel, dynamic network-based diffusion analysis to describe the acquisition patterns of novel tool-use behavior in the Sonso chimpanzee community of Budongo Forest, Uganda. We find strong evidence for social transmission of “moss-sponging” (the production of a sponge consisting of moss) along the innovators' social network, demonstrating that wild chimpanzees learn novel tool-use behaviors from each other and supporting the more general claim that some of the observed behavioral diversity in wild chimpanzees should be interpreted as “cultural.” Our model also estimated that, for each new observation, naïve individuals enhanced their chances of developing moss-sponging by a factor of 15. We conclude that group-specific behavioral variants can be socially learned in wild chimpanzees, addressing an important critique of the claim of culture in our closest relatives.

Using participatory risk mapping (PRM) to identify and understand people's perceptions of crop loss to animals in Uganda.

Considering how people perceive risks to their livelihoods from local wildlife is central to (i) understanding the impact of crop damage by animals on local people and (ii) recognising how this influences their interactions with, and attitudes towards, wildlife. Participatory risk mapping (PRM) is a simple, analytical tool that can be used to identify and classify risk within communities. Here we use it to explore local people's perceptions of crop damage by wildlife and the animal species involved. Interviews (n = 93, n = 76) and seven focus groups were conducted in four villages around Budongo Forest Reserve, Uganda during 2004 and 2005. Farms (N = 129) were simultaneously monitored for crop loss. Farmers identified damage by wildlife as the most significant risk to their crops; risk maps highlighted its anomalous status compared to other anticipated challenges to agricultural production. PRM was further used to explore farmers' perceptions of animal species causing crop damage and the results of this analysis compared with measured crop losses. Baboons (Papio anubis) were considered the most problematic species locally but measurements of loss indicate this perceived severity was disproportionately high. In contrast goats (Capra hircus) were considered only a moderate risk, yet risk of damage by this species was significant. Surprisingly, for wild pigs (Potamochoerus sp), perceptions of severity were not as high as damage incurred might have predicted, although perceived incidence was greater than recorded frequency of damage events. PRM can assist researchers and practitioners to identify and explore perceptions of the risk of crop damage by wildlife. As this study highlights, simply quantifying crop loss does not determine issues that are important to local people nor the complex relationships between perceived risk factors. Furthermore, as PRM is easily transferable it may contribute to the identification and development of standardised approaches of mitigation across sites of negative human-wildlife interaction.

<Note> Encountering Crocodiles while Chasing Chimpanzees

Associate Editors: Christophe Boesch, Max-Planck Institute, Germany Jane Goodall, Jane Goodall Institute, USA Tetsuro Matsuzawa, Kyoto University, Japan William C. McGrew, University of Cambridge, UK John C. Mitani, University of Michigan, USA Vernon Reynolds, Budongo Forest Project, UK Yukimaru Sugiyama, Kyoto University, Japan Richard W. Wrangham, Harvard University, USA Takeshi Furuichi, Kyoto University, Japan

The risk of disease to great apes: simulating disease spread in orang-utan (Pongo pygmaeus wurmbii) and chimpanzee (Pan troglodytes schweinfurthii) association networks.

All great ape species are endangered, and infectious diseases are thought to pose a particular threat to their survival. As great ape species vary substantially in social organisation and gregariousness, there are likely to be differences in susceptibility to disease types and spread. Understanding the relation between social variables and disease is therefore crucial for implementing effective conservation measures. Here, we simulate the transmission of a range of diseases in a population of orang-utans in Sabangau Forest (Central Kalimantan) and a community of chimpanzees in Budongo Forest (Uganda), by systematically varying transmission likelihood and probability of subsequent recovery. Both species have fission-fusion social systems, but differ considerably in their level of gregariousness. We used long-term behavioural data to create networks of association patterns on which the spread of different diseases was simulated. We found that chimpanzees were generally far more susceptible to the spread of diseases than orang-utans. When simulating different diseases that varied widely in their probability of transmission and recovery, it was found that the chimpanzee community was widely and strongly affected, while in orang-utans even highly infectious diseases had limited spread. Furthermore, when comparing the observed association network with a mean-field network (equal contact probability between group members), we found no major difference in simulated disease spread, suggesting that patterns of social bonding in orang-utans are not an important determinant of susceptibility to disease. In chimpanzees, the predicted size of the epidemic was smaller on the actual association network than on the mean-field network, indicating that patterns of social bonding have important effects on susceptibility to disease. We conclude that social networks are a potentially powerful tool to model the risk of disease transmission in great apes, and that chimpanzees are particularly threatened by infectious disease outbreaks as a result of their social structure.

Chimpanzee insectivory in the northern half of Uganda’s Rift Valley: do Bulindi chimpanzees conform to a regional pattern?

Insects are a nutritious food source for many primates. In chimpanzees, insectivory is most prevalent among communities that manufacture tools to harvest social insects, particularly ants and termites. In contrast to other long-term study sites, chimpanzees (Pan troglodytes schweinfurthii) in Budongo Forest and Kibale National Park, Uganda, rarely eat insects and have small foraging tool kits, supporting speculation that infrequent insectivory--technically aided or otherwise--characterises chimpanzees in this part of Uganda's Rift Valley. To expand the dataset for this region, insect foraging was investigated at Bulindi (25 km from Budongo) over 19 months during two studies in 2007-2008 and 2012-2013. Systematic faecal analysis demonstrated that insectivory is a habitual foraging activity at this site. Overall levels of insect consumption varied considerably across months but were not predicted by monthly changes in rainfall or fruit intake. Unlike their Budongo and Kibale counterparts, Bulindi chimpanzees often consume ants (principally weaver ants, Oecophylla longinoda) and use sticks to dig out stingless bee (Meliponini) ground nests. In other respects, however, insectivory at Bulindi conforms to the pattern observed elsewhere in this region: they do not manufacture 'fishing' or 'dipping' tools to harvest termites and aggressive or hard-to-access ants (e.g., army ants, Dorylus spp.), despite availability of suitable prey. The Bulindi data lend support to the supposition that chimpanzees in this part of the Rift Valley rarely exploit termites and Dorylus ants, apparently lacking the 'cultural knowledge' that would enable them to do so most efficiently (i.e., tool use). The study's findings contribute to current debates about the relative influence of genetics, environment and culture in shaping regional and local variability in Pan foraging ecology.

Socially learned habituation to human observers in wild chimpanzees

Habituation to human observers is an essential tool in animal behaviour research. Habituation occurs when repeated and inconsequential exposure to a human observer gradually reduces an animal's natural aversive response. Despite the importance of habituation, little is known about the psychological mechanisms facilitating it in wild animals. Although animal learning theory offers some account, the patterns are more complex in natural than in laboratory settings, especially in large social groups in which individual experiences vary and individuals influence each other. Here, we investigate the role of social learning during the habituation process of a wild chimpanzee group, the Waibira community of Budongo Forest, Uganda. Through post hoc hypothesis testing, we found that the immigration of two well-habituated, young females from the neighbouring Sonso community had a significant effect on the behaviour of non-habituated Waibira individuals towards human observers, suggesting that habituation is partially acquired via social learning.

Genetic analyses suggest no immigration of adult females and their offspring into the Sonso community of chimpanzees in the Budongo Forest Reserve, Uganda

Chimpanzees are frequently used to illustrate the relationship between sex differences in dispersal and sex differences in cooperation in primates and other group-living mammals. Male chimpanzees are highly philopatric, typically remaining in their natal communities for their entire lives to cooperate with related males in competition against less related males from other groups, whereas females typically disperse once at adolescence and cooperate with each other less frequently. However, there have been a few reports of dependent male offspring joining groups when their mothers transferred between communities as adults. Although such events are difficult to document, determining how often they actually occur is important for elucidating the links between philopatry, kinship, and cooperation in both chimpanzees and group-living animals more generally. Here we use genetic analyses to investigate a previous report of a large-scale transfer of many females and their offspring into the Sonso community of chimpanzees in the Budongo Forest Reserve, Uganda. Using autosomal microsatellite genotypes, we assigned a Sonso father to ten of the fourteen putative immigrants, and found that the four putative immigrants for whom we could not assign a Sonso father (perhaps due to incomplete sampling of all Sonso candidate fathers) nevertheless had Y-chromosome microsatellite haplotypes that were common in Sonso males but absent in males from four other chimpanzee communities at Budongo. These results suggest that these putative immigrant females and their offspring were probably actually long-term residents of Sonso whose identifications were delayed by their peripheral or unhabituated status. These results are consistent with other genetic and behavioral evidence showing that male between-community gene flow is exceedingly rare in east African chimpanzees.

Hypothèses historiques à propos du comportement d’utilisation d’outils par les chimpanzés en relation avec les changements naturels et anthropiques d’une forêt tropicale d’Afrique de l'Est

Chimpanzees and humans have co-existed in Africa for millennia. The forests inhabited by chimpanzees have experienced numerous changes in recent time, most notably during the last 12,000 years, as the current interglacial age started. In this article, I will study the case of Western Ugandan forests to describe the different factors, natural and human-induced, which affect a tropical forest, and draw hypotheses on the influence of these changes on chimpanzee cultural behaviour. Before colonial times, the Budongo Forest was shaped by elephant migrations and fires lit by the pastoralists who settled in the area. Later on, the British colonial power organized the exploitation of the forest through work plans aimed at insuring sustainable extraction of valuable timber. The human activity resulted in unexpected consequences in the forest. Interestingly, the resident chimpanzees are nowadays remarkable in the small size of their tool use repertoire. Ecological analysis and tool use observations in Uganda only support partly the opportunity and necessity hypotheses that are currently proposed to explain the influence of ecological factors on tool-using behaviour. Rather, the data I present here suggest that the temporal dimension of ecological changes in the forest must be taken into account to explain tool use behaviour variation in Ugandan forests. I propose a dynamic model connecting the necessity and opportunity factors influenced by ecological changes over time, most salient in Ugandan forests through the variability in food diversity. Finally, I conclude on the ever-changing ecological situation in Budongo Forest.

Impact of Collaborative Forest Management on Forest Status and Local Perceptions of Contribution to Livelihoods in Uganda

This study assessed the impacts of Collaborative Forest Management (CFM) initiatives on forest status of Budongo Forest reserve in Uganda and perceptions of the participating communities on the contribution of CFM towards their livelihood. Impact on conservation was assessed by applying a Participatory community based Forest Resource Assessment (PFRA) method to examine population structure, dynamics, and incidences of human disturbance across two forest compartments under CFM and comparing these with the status in two compartments without CFM, but otherwise similar to the former in terms of forest type, history of resource use-patterns, silvicultural management practices and location (in the production zone of the forest and close proximity to local communities). Impact on local livelihoods was examined through a survey that involved ten focus group discussions and semi-structured interviews among 140 randomly selected forest neighbours. With the exception of tree regeneration, CFM improved forest status in terms of more live stems of timber, pole tree species, trees with harvestable logs, merchantable volume, and lowered incidences of human disturbances. However, local people do not perceive CFM to have contributed to their livelihoods because whereas CFM created opportunities for income generation particularly through bee keeping, the in-forest activities it halted were superior sources of livelihood. As a result, nearly 50% of the respondents explicitly reported dissatisfaction with the CFM arrangements. Other reasons for dissatisfaction included the inability of CFM to deliver benefits as promised in the signed agreements, local people were frequently not consulted or involved in making key management decisions, and inequality in sharing CFM benefits amongst members of the local community. CFM at Budongo forest reserve has thus contributed to improving forest status, but is perceived to have had limited benefits to local livelihoods.

Crop-raiding deterrents around Budongo Forest Reserve: an evaluation through farmer actions and perceptions

AbstractCrop-raiding by primates and bushpigsPotamochoerus porcusis a major cause of human–wildlife conflict around Budongo Forest Reserve, Uganda. In 2006–2007 a project was initiated, with farmer participation, to investigate the efficacy of on-farm techniques to reduce crop-raiding, including guarding and early-warning techniques, fences, plant barriers, trenches, lights and nets. Here, farmers' perceptions of the effectiveness and sustainability of these deterrents were evaluated using semi-structured interviews and direct observations. Factors important to farmers in effective, sustainable and locally appropriate crop-raiding mitigation are that deterrents be cost-effective, easily manipulated, improve guarding efficiency and require minimal labour inputs. Farmers reported paid guards, guard dogs, wire fences, lights and bells/alarms as most effective. This differs from observations that farmers independently maintained certain deterrents that they presumably considered valuable, namely wire fences, guard dogs, bells/alarms, trenches, lights and nets. This evaluation demonstrates the importance of farmers' participation and perceptions in the viability and uptake of crop-raiding deterrents, and the importance of assessing conflict mitigation trials over the long term.

A method for automated individual, species and call type recognition in free-ranging animals

The ability to identify individuals reliably is often a key prerequisite for animal behaviour studies in the wild. In primates, recognition of other group members can be based on individual differences in the voice, but these cues are typically too subtle for human observers. We applied a combined mechanism consisting of a call feature extraction (mel frequency cepstral coefficients) and pattern recognition algorithm (artificial neural networks) to investigate whether automated caller identification is possible in free-ranging primates. The mechanism was tested for its accuracy in recognizing species, call type and caller identity in a large population of free-ranging blue monkeys, Cercopithecus mitis stuhlmanni, in Budongo Forest, Uganda. Classification was highly accurate with 96% at the species, 98% at the call type and 73% at the caller level. It also outperformed conventional discriminant function analysis in the individual recognition task. We conclude that software based on this method will make a powerful tool for future animal behaviour research, as it allows for automatic, fast and objective classifications in different animal species.

Avian frugivore assemblages on Celtis gomphophylla, Baker, in Budongo Forest Reserve, Uganda

AbstractThe relationship between selective logging and avian frugivores feeding on Celtis gomphophylla was examined in Budongo Forest Reserve, from June to July 2005, using scan sampling. Abundance and species richness of avian frugivores were compared between two compartments (N3 and W22 last logged in 1952 and 1997 respectively). Two 1‐ha plots were established in each compartment from which two C. gomphophylla trees selected for observation. A total of 203 avian frugivores comprising 17 species, visited the eight C. gomphophylla trees. Avian frugivore abundance and richness were significantly higher in N3 than W22 (χ2 = 5.83, χ2 = 0.03, P < 0.05). Fischer's alpha diversity index also indicated a higher avian frugivore (frugivory?) in N3 than that in W22. The Sorensen's similarity index showed that species composition between the two compartments was moderately similar. The diversity of forest specialists and generalists was not significantly different in the two compartments (F = 0.3451, P = 0.082 and F = 0.368, P = 0.553). Our results stress the significance of logging intensity on avian feeding guilds and confirm that forests which have had enough recovery time are better habitats for avian frugivore assemblages.

Laterality in the gestural communication of wild chimpanzees

We examined hand preference in the intentional gestural communication of wild chimpanzees in the Budongo forest, Uganda. Individuals showed some tendency to be lateralized, although less than has been reported for begging and pointing gestures in captivity; on average, their absolute bias was around 0.25 (where 1.0 represents complete right- or left-hand use and 0.0 represents no bias). Lateralization was incomplete even in individuals with major manual disabilities. Where individuals had a stronger preference, this was more often toward the right hand; moreover, as age increased, the direction (but not the extent) of hand preference shifted toward the right. While the gestural repertoire as a whole was largely employed ambilateraly, object-manipulation gestures showed a strong right-hand bias.

Chimpanzees in mantraps: lethal crop protection and conservation in Uganda

AbstractA main concern of farmers worldwide is how to reduce crop losses to wildlife. Some potentially lethal crop protection methods are non-selective. It is important to understand the impact of such methods on species of conservation concern. Uganda has important populations of Endangered eastern chimpanzeesPan troglodytes schweinfurthii. Farmers sometimes use large metal mantraps to guard their fields against crop-raiding wildlife, particularly baboonsPapio anubisand wild pigsPotamochoerussp.. Chimpanzees that range onto farmland also step in these illegal devices and without rapid veterinary invention face severe injury or eventual death. Unlike inadvertent snaring of great apes in African forests, the problem of mantraps in forest–farm ecotones has received little attention. We report 10 cases of entrapped chimpanzees in the cultivated landscape surrounding Uganda's Budongo Forest during 2007–2011, undoubtedly only a portion of the actual number of cases. Mantraps currently present a substantial threat to ape populations in this important conservation landscape. Our data underscore the need for conservation programmes to consider the techniques used by rural farmers to protect their livelihoods from wild animals.

Communicative intentions in wild chimpanzees: persistence and elaboration in gestural signalling

We examine evidence for communicative intent during conspecific interactions in wild chimpanzees (Budongo Forest, Uganda), focusing on persistence in gestural communication. Previous research indicates that great apes have large gestural repertoires and produce gestural communication in a flexible and intentional manner, including the production of gesture sequences. Although there is a lack of consensus on the form and function of sequences, there is some evidence that sequences are produced when signallers fail to receive any response from a recipient. Here, we provide first systematic evidence for communicative persistence in wild chimpanzees. Rather than examining only the presence or absence of a response, we used the most commonly observed response to assign meanings to gestures and examined sequence production in relation to response congruency. Chimpanzees ceased communication if successful, but persevered when unsuccessful. Chimpanzees repeated gestures when a response partially matched their goal but substituted the original gesture when a response was incongruent. Persistence was also mediated by recipient intent to respond, with more sequences produced within competitive than affiliative contexts. Gestures within sequences were homogenous in semantic meaning and signallers continued until the response matched the assigned meaning of the initial gesture. Gestural sequence production was not primarily affective; gesture intensity (in terms of modality) did not increase within sequences. Chimpanzee gestural sequences emerged to achieve specific outcomes; given variability in recipient behaviour following initial gestures, signallers were flexible in their persistence towards these goals.

Impact of human activities on chimpanzee ground use and parasitism (Pan troglodytes)

AbstractThe potential of human activities, including research, to alter parasite transmission ecology in wildlife is unknown. We examined gastrointestinal parasitism in chimpanzees (Pan troglodytes schweinfurthii) in Budongo Forest, Uganda. Trail use and time spent on the ground was recorded during 10 months of observations in four sites with differing human disturbance. Disturbance was quantified using transect plots (n = 320). Fecal (n = 435) samples were examined for helminth eggs, larvae, and for protozoan cysts. Individuals that spent more time on the ground had more infections and higher intensity infections. Prevalence of 13 parasite species was similar across sites, but percentage of multiple infections and infection intensity differed, as did ground use. Chimpanzees at the long‐term research site spent more time on the ground or on human trails. We hypothesize that researcher presence and trail creation may influence ground use, and thereby parasite burden, by altering trade‐offs between foraging and predation risk.

Qualitative impacts of Senna spectabilis on distribution of welfare: A household survey of dependent communities in Budongo Forest Reserve, Uganda

AbstractThis paper presents the results of a household survey designed to qualitatively evaluate the impacts of the invasive alien species Senna spectabilis on the distribution of welfare across dependent communities in the Budongo Forest Reserve (BFR) in Uganda. The BFR is the largest forest reserve in Uganda, with globally significant conservation values. The study establishes that households in the BFR have high levels of knowledge as to its conservation values; they are aware of the invasiveness of S. spectabilis and its potential to compromise the conservation values of the BFR, and that S. spectabilis confers tangible benefits to dependent households, whose levels significantly vary with proximity to the reserve. The study concludes by evaluating strategies that are designed to manage the spread of S. spectabilis in the BFR and which consider its demonstrated socio‐economic impacts.

Crop protection and conflict mitigation: reducing the costs of living alongside non-human primates

Conflict between farmers and primates increasingly impacts conservation efforts in Africa and Asia. Field crops provide a reliable and readily-accessible source of food for primates coping with habitat loss. However, crop-raiding undermines food security and tolerance of wildlife within neighbouring human communities. Many primates consume crops regularly yet there are few accounts of systematic evaluation of techniques to deter them. Working in partnership with farmers, this study was conducted over two growing seasons within four villages adjacent to the Budongo Forest Reserve, Uganda. Using systematic observational sampling, semi-structured interviews, and focus groups, we (i) monitored primate crop-raiding behaviour prior to and after installing locally-appropriate deterrents, developed with local farmers, and (ii) explored farmers’ initial responses to the methods trialled. Deterrent efficacy was assessed by comparing the frequency and characteristics of raiding events across seasons. Primates were the predominant diurnal crop-raiders; six species were observed raiding. Deterrents implemented included barriers, alarms, repellents, and systematic guarding. Incidence of raiding and crop loss decreased in almost all cases, often by shifting raiding to unprotected fields or adjacent farms. Farmers identified benefits and shortcomings for each deterrent, and considered most to be effective and valuable. Insights from the research directly inform intervention strategies to address crop-raiding issues and extend options to mitigate human–wildlife conflict.