As a contribution to the existing knowledge of grooming in primates five and a half years of grooming data were examined from a group of free-living chimpanzees (Pan troglodytes) in the Budongo Forest, Uganda, to investigate various functional significances of grooming behaviour within the context of social reinforcement. The fission–fusion social structure of chimpanzees results in group members not moving around as a single unit, but forming temporary units as the need arises. This reduces opportunities for individuals to groom others and therefore, based on time and association constraints alone, grooming was as expected found to be unevenly distributed among group members. Grooming patterns found among this group of chimpanzees were comparable to those observed in other free-living populations with variations possibly being attributed to resource base, population numbers and differences in age-sex class composition. One of the suggested social benefits of grooming is that it is used to enhance reproductive success, either by allowing males to enhance their proximity to oestrous females, or by influencing female choice through the development of affiliative relationships with males. Grooming was found to increase between males and females, whilst females displayed sexual receptivity through the presence of anogenital swellings and grooming may be a strategy used by males to increase their access to copulation opportunities, whereas females may use grooming to increase protection from harassment by less preferred males during swollen periods and also increase the likelihood of copulation with preferred partners. Based on the availability of oestrous females, copulations between males and adult females occurred significantly less frequently than expected, whereas copulations between males and subadult females occurred significantly more frequently than expected. Overall a positive correlation was found between grooming of females by males and frequency of copulations. Due to concerns regarding the validity of different sampling methods, scan-focal and ad libitum sampling methods were compared to establish if results from different sampling methods were similar. Results from the scan-focal and ad libitum sampling methods had very few discrepancies, and it is suggested that ad libitum sampling methods which record behaviour types whenever they occur, may be more beneficial for species which don’t move around as a single unit and live in environments where visibility is reduced, therefore increasing the possibility of recording individuals or behaviours that are observed infrequently. Scan-focal sampling may be more beneficial in studying species which move around together in habitats which are conducive to greater visibility, therefore allowing all or most group members to be observed simultaneously. / Thesis (DPhil)--University of Pretoria, 2009. / Zoology and Entomology / unrestricted

Increasing anthropogenic alterations propelled by a growing human population paired with ecological perturbations and climate change has amplified rates of disease transmission at the human-wildlife interface. While attention has focused primarily on diseases that cause high rates of morbidity and mortality, there is a dearth of research on more common, non-lethal “mild” infections. However, despite less obvious and immediate consequences, these infections still have long-term effects on both public health and the conservation of wildlife. Currently, disease research is primarily cross-sectional, with a lack of longitudinal studies, leading to an undervaluation of the dynamic nature of disease systems. In addition to pathogen monitoring, concurrently being able to measure immune system activation will help to clarify the effects of non-lethal diseases on host health and to provide further insights into life-history trade-offs. Here, I investigated malaria parasite (Plasmodium spp.) infections, a “mild” disease, in wild habituated chimpanzees (Pan troglodytes verus) residing in Taï National Park (TNP), Côte d'Ivoire. I used historical biological samples collected from non-human primates (including chimpanzees) and humans, as well as collected mosquitoes within their habitat. First, I identified longitudinal patterns of malaria parasite prevalence detected in chimpanzee faeces; next, I validated a biomarker of immune system activation, urinary neopterin, in wild chimpanzees; and lastly, within a larger ecological framework, I examined the interface of malaria parasite transmission between humans and non-human primates sharing a habitat. With a longitudinal study design, I found substantial intra- and inter-annual fluctuations in the faecal detection of malaria parasites across four non-consecutive sampling periods between 2004 and 2015. Peaks were observed during wet seasons—suggesting that environmental factors relating to vector abundance determine infection patterns. A higher prevalence was also detected in younger individuals, suggesting that the availability of susceptible hosts plays a role. With variations in parasite detection, similar trends should also be observed in health status. Urinary neopterin, an early inflammation marker of the non-specific immune response, increases during malaria parasite infections in humans and has been validated as a marker of immune system activation in laboratory and captive non-human primates. However, it was unclear whether it would be sensitive enough to provide a clear signal in mild diseases against the back-drop of co-infections commonly seen in wildlife. Therefore, we first needed to validate urinary neopterin as a biomarker of immune system activation during severe disease in wild animals. I measured urinary neopterin before, during, and after a severe respiratory outbreak and showed that levels corresponded to respiratory symptoms and predicted mortality. While urinary neopterin is sensitive enough to detect changes in immune system activation during severe disease, future research should still aim to validate its use in mild diseases, such as malaria. Finally, human-to-animal disease transmission is known to occur in TNP, with direct declines in chimpanzee populations observed that resulted from several outbreaks caused by human respiratory diseases. Given the zoonotic origin of malaria parasites in humans, I examined the genetic diversity of malaria parasites infecting humans and non-human primates sharing a habitat. Mosquitoes were also captured to identify potential vectors that may bridge transmission between host species. Only P. malariae was found in both humans and chimpanzees—however, the directionality of cross-species transmission would require a larger sample size to correctly assess. Additionally, no anopheline mosquitoes, the only known vector of mammalian malaria parasites, or mosquitoes positive for human- or great ape-specific malaria parasites were captured—suggesting that transmission events may be rare due to the sparsity of vectors in this region. This thesis shows that malaria epidemiology is a temporally and spatially diverse system that requires the use of longitudinal datasets and diverse sampling schemes. This thesis provides a baseline of data on which future malaria parasite research can build. Additionally, the validation of urinary neopterin will allow researchers to pursue questions on how mild diseases affect host health and to investigate questions relating to strategies and variations in life history trade-offs. This thesis is relevant for research on wildlife disease ecology, eco-immunology, and in the creation of pathogen and health surveillance programs.

Finding food in tropical forests poses a potentially major problem for chimpanzees, whose ranging is thought primarily to be directed at locating suitable food resources: (1) chimpanzees are frugivorous, large bodied and live in large home ranges; (2) they lack specialised sensory or locomotor abilities, and terrestrial travel is known to be costly; but (3) fruits are randomly distributed in space and time. Evidence from studies of captive individuals suggests chimpanzees are capable of remembering the locations of out of sight resources and can compute least distance routes to these resources, but whether this ability translates to the natural foraging behaviour of wild chimpanzees has never been investigated. My observational study was designed to assess how the chimpanzees (Pan troglodytes schweinfurthii) of Budongo Forest, Uganda, locate these patchy resources. I mapped the routes of 14 focal individuals over a 12-month period. I considered how these foraging routes were structured by breaking the path into segments of travel between resources. Consecutive segments of travel between resources were found not to be independent, but assembled into "super-segments" that take in a number of resources along one trajectory. These super-segments are not necessarily directed towards feeding resources, however: travel is not always food directed. Comparisons of actual chimpanzee routes with randomly generated simulations suggest most individuals do not attempt to minimise their travel distances. There is evidence to suggest energetically stressed individuals can remember the locations of recently visited food resources and return to these patches in order to minimise travel distances when necessary, but overall, food is not difficult to find for this community of chimpanzees. I propose this is because males defend a territory with super-abundant food resources, meaning availability is not a limiting factor of foraging. Male chimpanzees can be characterised as convenience feeders, taking food whilst satisfying other, social needs.

Large-scale land-use change across the tropics has led to the decline of animal populations and their habitat. With large investments into mining, hydropower dams and industrial agriculture this trend is likely to continue. Consequently, there is a need for systematic land-use planning to set aside areas for protection and allocate scarce conservation funding effectively. Even though primates are relatively well studied, data-driven systematic planning is still rarely implemented. The overall aim of this dissertation was to investigate population parameters needed for evidence-based conservation planning for the critically endangered western chimpanzee (Pan troglodytes verus) in West Africa. To this end, I compiled density datasets covering the entire geographic range of this taxon from the IUCN SSC A.P.E.S. database and modeled chimpanzee densities as a function of 20 social-ecological variables. I found that western chimpanzees seemingly persist within three social-ecological configurations: rainforests with a low degree of anthropogenic threats, steep areas that are less likely to be developed and are harder to access by humans, and areas with a high prevalence of cultural taboos against hunting chimpanzees. The third configuration of reduced hunting pressure is not yet reflected in commonly implemented conservation interventions, suggesting a need for designing new approaches aimed at reducing the threat of hunting. Based on the modeled density distribution, I estimated that 52,811 (95% CI 17,577-96,564) western chimpanzees remain in West Africa, and identified areas of high conservation value to which conservation interventions should be targeted. These results can be used to inform the expansion of the protected area network in West Africa, to quantify the impact of planned industrial projects on western chimpanzees, and to guide the systematic allocation of conservation funding. In addition, this thesis highlights the unique position of taxon-specific databases of providing access to high-resolution data at the scale needed for conservation planning. Data-driven conservation planning has the potential to enable conservationists to respond more proactively to current and emerging threats, and ultimately improve conservation outcomes.

The mammalian odorant receptor (OR) repertoire is an attractive model to study evolution, because ORs have been subjected to rapid evolution between species, presumably caused by changes of the olfactory system to adapt to the environment. However, functional assessment of ORs in related species remains largely untested. Here we investigated the functional properties of primate and rodent ORs to determine how well evolutionary distance predicts functional characteristics. Using human and mouse ORs with previously identified ligands, we cloned 18 OR orthologs from chimpanzee and rhesus macaque and 17 mouse-rat orthologous pairs that are broadly representative of the OR repertoire. We functionally characterized the in vitro responses of ORs to a wide panel of odors and found similar ligand selectivity but dramatic differences in response magnitude. 87% of human-primate orthologs and 94% of mouse-rat orthologs showed differences in receptor potency (EC50) and/or efficacy (dynamic range) to an individual ligand. Notably dN/dS ratio, an indication of selective pressure during evolution, does not predict functional similarities between orthologs. Additionally, we found that orthologs responded to a common ligand 82% of the time, while human OR paralogs of the same subfamily responded to the common ligand only 33% of the time. Our results suggest that, while OR orthologs tend to show conserved ligand selectivity, their potency and/or efficacy dynamically change during evolution, even in closely related species. These functional changes in orthologs provide a platform for examining how the evolution of ORs can meet species-specific demands. / Dissertation

I tested two pairs of captive chimpanzees (Pan troglodytes) in the informed forager paradigm: a subordinate saw the location of hidden bait, and then searched with a naïve dominant. This paradigm has tested what subjects know about others' states of knowledge, but my focus was to determine how subjects used different movement types and different gaze types to modify their competitive tactics. In particular, I investigated whether chimpanzees follow opponents' gaze to gain information. Learning more about how primates use visual information to predict others' behaviour can shed light on the continuing debate over to what degree apes possess theory of mind capacities. Previous published studies in this paradigm included narratives of ignorant competitors exploiting informed subjects by following their movement and gaze, and informed subjects avoided this exploitation by walking away from hidden food. The subordinate's behaviour can be considered tactical deception, which is a good place to seek strong evidence of second-order intentionality. Analyses with descriptive statistics, however, fail to capture the complexity of these interactions, which range from single decision-making points to larger patterns of following and misleading. I introduced a novel method of statistical analysis, cross correlations, that enabled me to examine behavioural patterns quantitatively that previous authors have only been able to describe in narrative form. Though previous studies on chimpanzees' understanding of gaze found that they were unable to use (human-given) gaze cues to locate hidden food, the subjects I tested followed their conspecific opponent's gaze, and used information gained from the gaze interaction to modify their own movement towards the hidden bait. Dominants adjusted their physical following of the subordinates as the interaction progressed, which reflected their changed states of knowledge. Subordinates used their movement and gaze differentially to manipulate dominants' behaviour, by withholding information and by recruiting towards a less-preferred bait.

Zoological institutions emphasise the importance of excelling in the areas of animal welfare, conservation, education, and research, not only to better the lives of the animals under their care, but to also influence the general population in the pursuit to conserve the natural world. As a result, zoo life is anything but simple. This research project monitored the lives of a captive group of chimpanzees over a two-and-a-half-year period, during which time we explored four research topics while assessing the development of a cognitive research programme and chimpanzee (Pan troglodytes) introductions in a zoo: welfare, cognition, public engagement with science, and animal management. The project’s use of touchscreen technology and on-exhibit research was the first of its kind for the Royal Zoological Society of Scotland’s Edinburgh Zoo. As a result, the researchers placed a great deal of importance not only on assessing the welfare of the chimpanzees throughout training and testing phases, but also assessing the public’s perception of cognitive research being conducted through an internationally broadcast documentary about the project. In the short duration of the project, these research naïve chimpanzees did not fully grasp the concept of video selection in our free-choice activity, but overall, the introduction of a cognitive research programme did not compromise welfare, and the chimpanzees’ repeated interest suggests that chimpanzees found the research to be reinforcing. Partly funded by the BBC, the Chimpcam Project was shown in the UK (broadcast January 2010) and in a variety of other countries, including the United States and Canada (on Animal Planet in 2011). The broadcast allowed us to gather information over the internet on the wider public’s perception of conducting research with great apes in zoos, to complement data collected on visitors to the exhibit itself. Our assessment of the documentary’s impact on public perception showed that it had a positive influence on perceptions of zoo research, scientists, welfare, and the importance of choice for animals. During this research project, a new group of chimpanzees arrived in Edinburgh as part of the international breeding programme for western chimpanzees (Pan troglodytes verus). As the zoo’s focus switched to helping the two chimpanzee groups merge into one, we took the opportunity to apply psychological research to this context, namely the use of video as a research tool and the recognition of the importance of individual differences in response to challenge. The project maintained the cognition and welfare focus by using video introductions (allowing the chimpanzees to watch video footage of the individuals they were about to meet and track the formation of other sub-groups). In addition, personality ratings and chimpanzee behaviour during the visual access period (an animal management technique used prior to physical introductions where the groups could see each other without physical contact) were collected to examine the efficacy of these measures in guiding introductions in order to reduce risk. Personality ratings and behaviours observed during the video introductions could predict the chimpanzees’ behaviour during the physical introductions, however, the visual access period had no predictive power. The welfare implications of the introduction process were also assessed and suggested that: the choice of location (i.e. options of where to be) was more important than the total amount of available space; having individuals removed from your group was more stressful than having individuals added; self-directed behaviour (SDB) performance was context-specific where rubbing significantly increased during periods of uncertainty that were not necessarily negatively valenced; regurgitation and reingestion (R/R) decreased over time; and both in-group members and those of high ranks spent more time grooming others. Overall our data indicate that the chimpanzees coped well with both cognitive challenges and social upheaval during introductions. Despite being regularly studied in captivity and in the wild, chimpanzees have a great deal more to teach us about their world. In order to provide the best welfare for the chimpanzees in our care, we need to understand how research and management practices affect their lives and how the public interpret what we do as researchers. By understanding these aspects of their world, we can better serve those in captivity and influence public opinion on the importance of conserving those in the wild.

Adipositas ist eine polymorphe chronische Erkrankung mit epidemischer Prävalenz. Im katabolen Leptin-Melanocortin-Signalweg ist das Proopiomelanocortin Gen (POMC) ein zentrales Element, das bei Dysfunktion massive Adipositas bewirken kann. Auch eine kürzlich identifizierte intragenische Methylierungsvariante des POMC wurde mit Adipositas assoziiert und deutet somit auf eine mögliche epigenetische Modulation des Gewichtsphänotyps hin. Zur Aufklärung der Relevanz, Stabilität und Entwicklung dieser epigenetischen Modifikation wurden die Funktionalität, Ontogenese und Phylogenese der POMC DNA-Methylierung untersucht. In vitro Analysen zeigten DNA-Methylierungsabhängige Promoteraktivität beider CpG-Inseln (CGIs) des POMC. Diese hier erstmals beschriebene Transkriptionsaktivität der intragenischen CGI weist auf einen alternativen Promoter des POMC hin. Hinsichtlich der Ontogenese konnten in Mensch und Maus postnatal stabile DNA-Methylierungsmuster mit interindividueller Konservierung für beide CGIs des POMC identifiziert werden. Zusätzlich erwiesen sich Gewebeunabhängigkeit der DNA-Methylierungsmuster und ihre pränatale Ausbildung zwischen dem Blastocystenstadium und der frühen Organogenese in der Maus. Die POMC DNA-Methylierungsmuster upstream des Exon3 unterscheiden sich in Mensch und Maus. Der mögliche Einfluss von primatenspezifischen Alu-Elementen im Intron2 des POMC hierauf wurde in verschiedenen Primatenfamilien analysiert. Die Ergebnisse zeigen eine bedingte Assoziation der Alu-Elemente mit der DNA-Methylierung in der entsprechenden Region, lassen jedoch auch weitere Einflussfaktoren vermuten. Insgesamt zeigt diese Arbeit, dass die POMC DNA-Methylierung artspezifisch konserviert ist und in der frühen Embryogenese, vermutlich Alu-abhängig, ausgebildet wird. Dabei könnten stochastische Variationen der DNA-Methylierung die POMC-Aktivität beeinflussen und somit das Risiko für Adipositas erhöhen. / Obesity is a polymorphic chronic disease with epidemic prevalence. Within the catabolic leptin-melanocortin signaling pathway pre-proopiomelanocortin (POMC) is a pivotal element. Dysfunction of POMC, e.g. due to mutations, can cause severe obesity. Moreover, a recently identified intragenic methylation variant of POMC was found to be associated with obesity. Therefore, this indicates potential epigenetic modulation of the weight phenotype. To gain further insight into the relevance, stability, and origin of this epigenetic modification, the functionality, ontogenesis, and phylogenesis of the POMC DNA methylation patterns were analyzed. In vitro analyses revealed DNA methylation-dependent promoter activity of both CpG islands (CGIs) of POMC. Thereby, the intragenic CGI was identified as a potential alternative promoter of POMC, which has not been described before. Regarding the ontogenesis, postnatally stable POMC DNA methylation patterns with interindividual conservation were detected for both CGIs in humans and mice. In addition, it was observed that the POMC DNA methylation patterns are non-tissue-specific, stable upon long time administration of a high fat diet, and develop prenatally between the blastocystal stage and the early organogenesis. The POMC DNA methylation pattern upstream of exon3 differs in humans and mice. A possible influence of primate-specific Alu elements within the intron2 region of POMC was analyzed in various primate families. Results evince a partial association of the Alu elements with the DNA methylation pattern in this particular region, but also suggest an influence of additional factors. Overall, this work demonstrates that DNA methylation of the POMC locus is species-specific highly conserved, and that it is established during early embryogenesis, possibly Alu-triggered. In the course of this, stochastic variances of the POMC DNA methylation might influence the POMC activity and consequently alter the risk to develop obesity.

Afin de sélectionner des plantes ayant des propriétés pharmacologiques, un suivi éthologique et vétérinaire de chimpanzés (Pan troglodytes schweinfurthii), a été conduit, grâce à des méthodes non-invasives (parasitologie, analyses d'urine et observations vétérinaires) dans le Parc National de Kibale, en Ouganda. Des essais biologiques antiparasitaires, antibactériens, antifongiques, antiviraux et cytotoxiques ont été pratiqués in vitro sur 84 extraits bruts, provenant de 24 espèces de plantes. Parmi les nombreux extraits biologiquement actifs, deux binaphtoquinones, isolées de l'écorce de Diospyros abyssinica, et des acétogénines, telles l'annonacine et la gigantétrocine isolées des feuilles et écorces d'Uvariopsis congensis, possèdent une cytotoxicité significative. Deux nouveaux limonoïdes, à forte activité antipaludique, ont été isolés des feuilles de Trichilia rubescens. Ces résultats confirment que le régime alimentaire des chimpanzés peut agir de façon préventive et curative pour améliorer leur santé et pourrait être utilisé pour guider la recherche de nouvelles molécules potentiellement utilisables en médecine humaine.

xvii, 149 p. : ill. (some col.), maps / The ranging behavior of an animal can reveal much about the social and ecological conditions it faces. Food availability, feeding competition, population pressures, metabolic requirements and human influences can all influence the ranging behavior of individuals. For modern humans, the manner in which we move about our world is limited only by access to technology and other cultural factors. Of course, it has not always been that way. Based on recent fossil discoveries, our earliest bipedal ancestors more closely resembled the living great apes in morphology. Consequently, studies of great ape behavior have been used to reconstruct scenarios of early hominin behavior. And while much has been written about chimpanzee ( Pan troglodytes ) ranging in this regard, less is known about bonobos (Pan paniscus ). Along with chimpanzees, bonobos are our closest phylogenetic relative, existing today as a descendant of a common ancestor the Homo and Pan genera shared sometime around six million years ago. Despite their close taxonomic relationship, however, there are a variety of behavioral differences between bonobos and chimpanzees. The aim of this dissertation is to better understand these differences within the context of ranging and social behavior and apply the results to models of early hominin behavior. More specifically, I used a Geographic Information Systems (GIS) approach to examine general bonobo ranging data, the differences in ranging behavior between males and females, and the manner in which neighboring groups interact. Compared with chimpanzees, bonobos at Lomako range over a much smaller total area, are not territorial, and differ in the composition of social parties. In general, female bonobos are more gregarious and cohesive, moving in semi-stable groups I call "cliques", while males are less aggressive and more likely to move independently. These results likely reflect the high levels of food availability for bonobos at Lomako, reducing the level of feeding competition, and emphasizing social and mating strategies in group formation. Consequently, the spectrum of potential early hominin ranging behavior must be expanded from the current chimp-centric perspective. / Committee in charge: Frances White, Chairperson; Stephen Frost, Member; Larry Sugiyama, Member; James Schombert, Outside Member