The goal of this study was to examine several aspects of the population genetics and population biology of the Nigeria-Cameroon chimpanzee at seven sampling locations in the south of Taraba State, Nigeria. Three of the sampling locations are within GGNP and two are situated just outside the southern boundary of GGNP. The final two sampling locations are found within Ngel Nyaki forest reserve, at each of the two forest fragments inside the reserve. Ngel Nyaki forest reserve was the focus of the study and the principal goal was to 16 determine if the community of chimpanzees at Ngel Nyaki forest reserve has become isolated from the chimpanzees at GGNP using microsatellite loci extracted from non-invasive sources of DNA. In Chapter two, the methods used to extract and amplify the DNA and the protocols used to confirm the genotypes are outlined. Chapter three examines the population structure of the chimpanzees among the regions sampled in this study, particularly addressing the question as to whether the chimpanzees at Ngel Nyaki forest reserve are isolated from the chimpanzees at GGNP. Chapter four investigates patterns of sex biased dispersal in the Nigeria-Cameroon chimpanzee. In Chapter five, population viability analysis is used to determine the fate of the chimpanzees at Ngel Nyaki forest reserve under a range of management scenarios. Chapter six summarizes the conclusions of the study and presents a conservation strategy to ensure the viability of the population of chimpanzees at Ngel Nyaki forest reserve.

Title from second page of PDF document. Includes bibliographical references (p. 145-173).

Les canaux semi-circulaires présentent un grand intérêt dans l'évolution. Des travaux récents ont montré que pour certains caractères, le génome humain est plus étroitement lié à celui du bonobo ou du chimpanzé que ces derniers entre eux. Dans ce contexte, il est important de comprendre le degré auquel les différences morphologiques et structurales entre ces trois espèces, reflètent les connaissances phylogéniques actuelles. Cette étude vise à comparer la variabilité anatomique des canaux semi-circulaires à partir de 260 examens tomodensitométriques d'homo sapiens, pan paniscus et pan troglodytes existants. Nous appliquons un modèle mathématique valide avec des examens micro tomodensitométriques et une quantification de l'erreur de mesure. Principalement, nous trouvons que les humains et les bonobos partagent plus de similarités entre eux qu'avec les chimpanzés par rapport a l'orientation tridimensionnelle de leurs canaux semi-circulaires, un résultat qui ne cadre pas avec les connaissances phylogénétiques actuelles. Une première hypothèse consiste en une évolution convergente dans laquelle les bonobos et les humains produisent indépendamment, des phénotypes semblables, peut-être en réponse aux pressions de sélection similaires éventuellement associées à des adaptations posturales. Une deuxième explication possible et plus parcimonieuse, c'est que la morphologie labyrinthique partagée entre le bonobo et l'homme représente la condition ancestrale à partir de laquelle les chimpanzés se sont déviés par la suite. La symétrie remarquable des CSC est le deuxième résultat majeur de cette étude pour ses implications dans la taphonomie. Il a le potentiel pour enquêter sur les fossiles altérés, déduire la probabilité de déformation post-mortem qui peut conduire à des difficultés dans la compréhension de la variation taxonomique, des relations phylogénétiques et de la morphologie fonctionnelle. / For some traits, the human genome is more closely related to either the bonobo or the chimpanzee genome than these are to each other. Therefore, it becomes crucial to understand whether morphological differences between humans, chimpanzees and bonobos reflect the well known phylogeny. Here we investigate intra and extra labyrinthine semicircular canals morphology using 260 computed tomography scans of homo sapiens, pan paniscus and pan troglodytes. We apply a mathematical model validated with micro-computed tomography scans and measurement error quantification. We find striking differences between, on the one hand, humans and bonobos and, on the other hand, chimpanzees concerning the 3D orientation of their semicircular canals. This finding does not fit with the phylogenetic knowledge. The first hypothesis is convergent evolution in which bonobos and humans produce independently similar phenotypes possibly in response to similar selection pressure maybe associated with postural adaptations. A second possible and more parsimonious explanation is that the bonobo-human labyrinthine shared morphology represents the ancestral condition with chimpanzees being subsequently derived. The remarkable symmetry of the SCC is the second major result of this study for its implications in taphonomy. It has the potential to investigate altered fossil, inferring the probability of post-mortem deformation which can lead to difficulties in understanding taxonomic variation, phylogenetic relationships, and functional morphology.

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.