Matthew R. McLennan

Beleaguered Chimpanzees in the Agricultural District of Hoima, Western Uganda

Abstract: With approximately 5,000 chimpanzees, Uganda is important for the conservation of the eastern subspecies Pan troglodytes schweinfurthii. The population distribution is highly fragmented, however, and the prospects for the long-term viability of many populations will be greatly improved if dispersal opportunities are maintained between major forests via migratory corridors. Chimpanzees in unprotected human-dominated habitat outside the main forest blocks are often ignored by research and conservation efforts. This study assessed the status and distribution of chimpanzees in northern Hoima District, western Uganda. The survey region covered 400 km2 between 1°26′–1°37′N and 31°09′–31°32′E, and separates two major forest blocks, Bugoma and Budongo. Chimpanzees use small forest fragments along watercourses throughout this region, both on private or communal land and in small government reserves, and a number of distinct groups (‘communities’) are present. There has been no evidence to indicate that chimpanzee populations are isolated; on the contrary chimpanzees appear highly mobile in this forest-farm habitat, confirming the regions corridor potential. At one site in the region, chimpanzees occur at an estimated density of 0.66 individuals/km2 which, if extrapolated across the survey area, implies a larger population than previously thought. Recent and rapid habitat change resulting from unregulated timber extraction and clearance of fragments for agriculture—particularly for cash crops such as tobacco—has exposed the chimpanzees, causing increased negative interactions between apes and farming communities. The chimpanzees in northern Hoima are unlikely to survive without immediate intervention.

Apes in the Anthropocene: flexibility and survival

We are in a new epoch, the Anthropocene, and research into our closest living relatives, the great apes, must keep pace with the rate that our species is driving change. While a goal of many studies is to understand how great apes behave in natural contexts, the impact of human activities must increasingly be taken into account. This is both a challenge and an opportunity, which can importantly inform research in three diverse fields: cognition, human evolution, and conservation. No long-term great ape research site is wholly unaffected by human influence, but research at those that are especially affected by human activity is particularly important for ensuring that our great ape kin survive the Anthropocene.

Chimpanzee responses to researchers in a disturbed forest-farm mosaic at Bulindi, western Uganda.

We describe the behavior of a previously unstudied community of wild chimpanzees during opportunistic encounters with researchers in an unprotected forest–farm mosaic at Bulindi, Uganda. Data were collected during 115 encounters between May 2006 and January 2008. Individual responses were recorded during the first minute of visual contact. The most common responses were “ignore” for arboreal chimpanzees and “monitor” for terrestrial individuals. Chimpanzees rarely responded with “flight”. Adult males were seen disproportionately often relative to adult females, and accounted for 90% of individual responses recorded for terrestrial animals. Entire encounters were also categorized based on the predominant response of the chimpanzee party to researcher proximity. The most frequent encounter type was “ignore” (36%), followed by “monitor” (21%), “intimidation” (18%) and “stealthy retreat” (18%). “Intimidation” encounters occurred when chimpanzees were contacted in dense forest where visibility was low, provoking intense alarm and agitation. Adult males occasionally acted together to repel researchers through aggressive mobbing and pursuit. Chimpanzee behavior during encounters reflects the familiar yet frequently agonistic relationship between apes and local people at Bulindi. The chimpanzees are not hunted but experience high levels of harassment from villagers. Human‐directed aggression by chimpanzees may represent a strategy to accommodate regular disruptions to foraging effort arising from competitive encounters with people both in and outside forest. Average encounter duration and proportion of encounters categorized as “ignore” increased over time, whereas “intimidation” encounters decreased, indicating some habituation occurred during the study. Ecotourism aimed at promoting tolerance of wildlife through local revenue generation is one possible strategy for conserving great apes on public or private land. However, the data imply that habituating chimpanzees for viewing‐based ecotourism in heavily human‐dominated landscapes, such as Bulindi, is ill‐advised since a loss of fear of humans could lead to increased negative interactions with local people. Am. J. Primatol. Am. J. Primatol. 72:907–918, 2010.

Wild chimpanzees show group differences in selection of agricultural crops

The ability of wild animals to respond flexibly to anthropogenic environmental changes, including agriculture, is critical to survival in human-impacted habitats. Understanding use of human foods by wildlife can shed light on the acquisition of novel feeding habits and how animals respond to human-driven land-use changes. Little attention has focused on within-species variation in use of human foods or its causes. We examined crop-feeding in two groups of wild chimpanzees – a specialist frugivore – with differing histories of exposure to agriculture. Both groups exploited a variety of crops, with more accessible crops consumed most frequently. However, crop selection by chimpanzees with long-term exposure to agriculture was more omnivorous (i.e., less fruit-biased) compared to those with more recent exposure, which ignored most non-fruit crops. Our results suggest chimpanzees show increased foraging adaptations to cultivated landscapes over time; however, local feeding traditions may also contribute to group differences in crop-feeding in this species. Understanding the dynamic responses of wildlife to agriculture can help predict current and future adaptability of species to fast-changing anthropogenic landscapes.

Protected Apes, Unprotected Forest: Composition, Structure and Diversity of Riverine Forest Fragments and Their Conservation Value in Uganda

Small forest fragments are common in anthropogenic landscapes in the tropics. These have conservation value if they provide habitat for threatened wildlife and maintain connectivity between larger habitats. Riverine forests have particular ‘corridor’ potential due to their linear shape, but are under-studied in many regions. We surveyed trees in riverine fragments in Bulindi, an anthropogenic landscape 25 km south of the Budongo Forest in western Uganda, to determine their condition and assess their value for wildlife, particularly endangered chimpanzees Pan troglodytes. We assessed tree composition, structure and diversity and compared results with a previous survey made in Budongo, the nearest main forest block. Riverine fragments were considerably less species-dense and species-rich than Budongo. Community composition differed markedly between sites and there was virtually no overlap in common species. Common trees in fragments were characteristic of East African swamp and groundwater forests (e.g. the palm Phoenix reclinata) and the dominant tree family was the Moraceae, members of which produce fleshy fruits attractive to frugivores (e.g. figs). Important fruit foods for chimpanzees differed between habitats. While basal area of important fruit trees was comparable, overall density was greater in fragments. Our data suggest the riverine fragments offer a relatively food-dense habitat for chimpanzees and other frugivores. Small riverine forests have little or no protection regionally and are being extensively logged and cleared for agriculture. Species logged for timber in Bulindi included important chimpanzee fruit trees. Unless conservation projects successfully reverse current trends, the value of the riverine corridors for maintaining connectivity between main forest blocks is limited.

Chimpanzees in mantraps: lethal crop protection and conservation in Uganda

A 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 chimpanzees Pan troglodytes schweinfurthii . Farmers sometimes use large metal mantraps to guard their fields against crop-raiding wildlife, particularly baboons Papio anubis and wild pigs Potamochoerus sp.. 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 Ugandas 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.

High frequency of leaf swallowing and its relationship to intestinal parasite expulsion in "village" chimpanzees at Bulindi, Uganda.

Self‐medication by great apes to control intestinal parasite infections has been documented at sites across Africa. Chimpanzees (Pan troglodytes) swallow the leaves of certain plant species whole, without chewing. Previous studies demonstrated a relationship between chimpanzee leaf swallowing and expulsion of nematode worms (Oesophagostomum sp.) and tapeworms (Bertiella sp.) in dung. We investigated the relationship between leaf swallowing and parasite expulsion in chimpanzees inhabiting a fragmented forest–farm mosaic at Bulindi, Uganda. During 13 months whole undigested leaves occurred in chimpanzee dung at a considerably higher frequency (10.4% of dungs) than at other sites (0.4–4.0%). Leaf swallowing occurred year‐round and showed no pronounced seasonality. Chimpanzees egested adults of multiple species of Oesophagostomum (including O. stephanostomum) and proglottids of two tapeworms—Bertiella sp. and probably Raillietina sp. The latter may not be a true infection, but the byproduct of predation on domestic fowl. Compared to previous studies, the co‐occurrence of whole leaves and parasites in chimpanzee dung was low. Whereas the presence of leaves in dung increased the probability of adult nematode expulsion, no association between leaf swallowing and the shedding of tapeworm proglottids was apparent. Anthropogenic habitat changes have been linked to alterations in host–parasite interactions. At Bulindi, deforestation for agriculture has increased contact between apes and people. Elevated levels of leaf swallowing could indicate these chimpanzees are especially vulnerable to parasite infections, possibly due to environmental changes and/or increased stress levels arising from a high frequency of contact with humans. Frequent self‐medication by chimpanzees in a high‐risk environment could be a generalized adaptation to multiple parasite infections that respond differently to the behavior. Future parasitological surveys of apes and humans at Bulindi are needed for chimpanzee health monitoring and management, and to investigate the potential for disease transmission among apes, people, and domestic animals. Am. J. Primatol. 74:642–650, 2012.

Tool-use to obtain honey by chimpanzees at Bulindi: new record from Uganda

Honey-gathering from bee nests has been recorded at chimpanzee (Pan troglodytes) study sites across tropical Africa. Different populations employ different strategies, ranging from simple ‘smash-and grab’ raids to use of sophisticated tool-sets, i.e., two or more types of tool used sequentially in a single task. In this paper I present evidence of tool-use, and the probable use of a tool-set, for honey-gathering by unhabituated chimpanzees at Bulindi, a forest–farm mosaic south of the Budongo Forest in Uganda. Between June and December 2007, 44 stick tools were found in association with 16 holes dug in the ground, corresponding to the period when stingless bees (Meliponula sp.) appeared in chimpanzee dung. In 11 cases the confirmed target was a Meliponula ground nest. Two potential tool types were distinguished: digging sticks encrusted with soil, and more slender and/or flexible sticks largely devoid of soil that may have functioned to probe the bees’ narrow entry tubes. Reports of chimpanzees using tools to dig for honey have been largely confined to Central Africa. Honey-digging has not previously been reported for Ugandan chimpanzees. Similarly, use of a tool-set to obtain honey has thus far been described for wild chimpanzee populations only in Central Africa. Evidence strongly suggests that Bulindi chimpanzees also use sticks in predation on carpenter bee (Xylocopa sp.) nests, perhaps as probes to locate honey or to disable adult bees. These preliminary findings from Bulindi add to our understanding of chimpanzee technological and cultural variation. However, unprotected forests at Bulindi and elsewhere in the region are currently severely threatened by commercial logging and clearance for farming. Populations with potentially unique behavioral and technological repertoires are being lost.

Managing Humans, Managing Macaques: Human–Macaque Conflict in Asia and Africa

Conflict between humans and wild animals is one of the greatest challenges to biodiversity conservation globally. Of all primates, macaques are particularly successful at exploiting human-modified environments, both rural and urban, and in some contexts develop commensal relationships with humans. However, this frequent association with people inevitably leads to conflicts. In this chapter we review the human–macaque conflict situation in Asia and North Africa and, using specific case studies, explore three main areas of interaction that can lead to conflict: rural crop-damage, tourism sites and urban contexts. With ever-expanding human populations, changing socio-economic conditions and shifting cultural attitudes, the future of human–macaque relationships is likely to be an uneasy one. The rise in human–macaque conflicts throughout the range of Macaca calls for effective mitigation strategies to facilitate coexistence. We discuss conflict management approaches that (1) aim to alter the behaviour of macaques and/or people; and (2) seek to control the size, demography or distribution of macaque populations. Macaque conservation requires a multiple management strategy approach, depending on the specific context. Conservation strategies should focus on promotion of tolerant cultural attitudes in addition to reduction of negative interactions in order to ensure long-term survival of macaque populations.

The Implications of Primate Behavioral Flexibility for Sustainable Human–Primate Coexistence in Anthropogenic Habitats

People are an inescapable aspect of most environments inhabited by nonhuman primates today. Consequently, interest has grown in how primates adjust their behavior to live in anthropogenic habitats. However, our understanding of primate behavioral flexibility and the degree to which it will enable primates to survive alongside people in the long term remains limited. This Special Issue brings together a collection of papers that extend our knowledge of this subject. In this introduction, we first review the literature to identify past and present trends in research and then introduce the contributions to this Special Issue. Our literature review confirms that publications on primate behavior in anthropogenic habitats, including interactions with people, increased markedly since the 2000s. Publications concern a diversity of primates but include only 17% of currently recognized species, with certain primates overrepresented in studies, e.g., chimpanzees and macaques. Primates exhibit behavioral flexibility in anthropogenic habitats in various ways, most commonly documented as dietary adjustments, i.e., incorporation of human foods including agricultural crops and provisioned items, and as differences in activity, ranging, grouping patterns, and social organization, associated with changing anthropogenic factors. Publications are more likely to include information on negative rather than positive or neutral interactions between humans and primates. The contributions to this Special Issue include both empirical research and reviews that examine various aspects of the human–primate interface. Collectively, they show that primate behavior in shared landscapes does not always conflict with human interests, and demonstrate the value of examining behavior from a cost–benefit perspective without making prior assumptions concerning the nature of interactions. Careful interdisciplinary research has the potential to greatly improve our understanding of the complexities of human–primate interactions, and is crucial for identifying appropriate mechanisms to enable sustainable human–primate coexistence in the 21st century and beyond.