Ape Populations Research Articles

Pathogens as drivers of population declines: The importance of systematic monitoring in great apes and other threatened mammals

Until recently, the focus of great ape behavioural and ecological research has been distinct from the focus of scientists working in medical and veterinary sciences. More scientists are calling for a connection between medical and field research due to recent disease outbreaks in great apes, including Ebola, and indications of cross-transmission of Ebola and other viruses between primates and humans. A major limitation to progress is the lack of information on infectious diseases and their transmission in wild primates. Here, we present examples of successful pathogen detection in wild great apes and describe approaches and techniques that can be used in the field, focusing in particular on investigation of deaths and non-invasive sample collection. This interdisciplinary approach is providing new insights to infectious diseases of great apes and is helping to protect the health of great ape populations. This framework can also be applied to other mammals under threat from infectious diseases, including African wild dogs, seals and Tasmanian devils. In addition to providing benefits for great ape conservation, research that integrates infectious disease with primate ecology provides insights to emerging diseases in humans and the role of disease in primate evolution.

Genetic Signature of Anthropogenic Population Collapse in Orang-utans

Great ape populations are undergoing a dramatic decline, which is predicted to result in their extinction in the wild from entire regions in the near future. Recent findings have particularly focused on African apes, and have implicated multiple factors contributing to this decline, such as deforestation, hunting, and disease. Less well-publicised, but equally dramatic, has been the decline in orang-utans, whose distribution is limited to parts of Sumatra and Borneo. Using the largest-ever genetic sample from wild orang-utan populations, we show strong evidence for a recent demographic collapse in North Eastern Borneo and demonstrate that this signature is independent of the mutation and demographic models used. This is the first demonstration that genetic data can detect and quantify the effect of recent, human-induced deforestation and habitat fragmentation on an endangered species. Because current demographic collapses are usually confounded by ancient events, this suggests a much more dramatic decline than demographic data alone and emphasises the need for major conservation efforts.

Bioactive properties of plant species ingested by chimpanzees (Pan troglodytes schweinfurthii) in the Kibale National Park, Uganda

We measured the biological activities of a selected sample (84 crude extracts) of 24 species eaten by wild chimpanzees (Pan troglodytes schweinfurthii) in the Kibale National Park, western Uganda, to assess their potential chemotherapeutic values. Antibacterial, antimalarial, and/or antileishmania activities were observed in some crude extracts, and five of these extracts showed a significant cytotoxicity against human tumor cells. Active compounds isolated from three plant parts occasionally ingested by chimpanzees (Diospyros abyssinica (Ebenaceae) bark, Uvariopsis congensis (Annonaceae) leaves, and Trichilia rubescens (Meliaceae) leaves) showed highly significant medicinal properties. Two novel antiparasitic limonoids were isolated from Trichilia rubescens and their molecular structures were determined. In addition to elucidating the natural equilibrium maintained between hosts and pathogens, our investigation of the diet of wild chimpanzees may serve as a guideline to discovering plants with bioactive properties that should be preserved from destruction because of their health maintenance value for great ape populations.

Recombination in the Genesis and Evolution of Hepatitis B Virus Genotypes

Hepatitis B virus (HBV) infection is widely distributed in both human and ape populations throughout the world and is a major cause of human morbidity and mortality. HBV variants are currently classified into the human genotypes A to H and species-associated chimpanzee and gibbon/orangutan groups. To examine the role of recombination in the evolution of HBV, large-scale data retrieval and automated phylogenetic analysis (TreeOrder scanning) were carried out on all available published complete genome sequences of HBV. We detected a total of 24 phylogenetically independent potential recombinants (different genotype combinations or distinct breakpoints), eight of which were previously undescribed. Instances of intergenotype recombination were observed in all human and ape HBV variants, including evidence for a novel gibbon/genotype C recombinant among HBV variants from Vietnam. By recording sequence positions in trees generated from sequential fragments across the genome, violations of phylogeny between trees also provided evidence for frequent intragenotype recombination between members of genotypes A, D, F/H, and gibbon variants but not in B, C, or the Asian B/C recombinant group. In many cases, favored positions for both inter- and intragenotype recombination matched positions of phylogenetic reorganization between the human and ape genotypes, such as the end of the surface gene and the core gene, where sequence relationships between genotypes changed in the TreeOrder scan. These findings provide evidence for the occurrence of past, extensive recombination events in the evolutionary history of the currently classified genotypes of HBV and potentially in changes in its global epidemiology and associations with human disease.

Is the chimpanzee, Pan troglodytes, an endangered species? It depends on what “endangered” means

I review information on the status in the wild of the robust chimpanzee, Pan troglodytes, and consider whether this evidence is consistent with the designation of P. troglodytes as Endangered in the International Union for the Conservation of Nature and Natural Resources (IUCN) Red List, and with public statements to the effect that great apes as a whole will be extinct within a few decades. Chimpanzees remain widespread in tropical Africa, occurring in a variety of forested habitats. Estimates of total surviving numbers have increased from about 200,000 in the 1980s to a maximum of almost 300,000 in 2003. However, this apparent increase comes about from new survey data, rather than representing a measured increase in actual population numbers. Infectious disease decimated several chimpanzee populations during the 1990s, and data from parts of Gabon, extrapolated to that country as a whole, suggest a major decline in great ape populations caused by disease and hunting. However, accurate data on population numbers are absent for the majority of wild chimpanzee populations. I found reports of the presence of Pan troglodytes in at least 51 national parks in at least 19 countries; some of these parks have been established very recently. Chimpanzees also occur in many non-park conservation areas. A set of large, well-protected parks could safeguard chimpanzees for the foreseeable future. Although many African parks do not function well at present, mechanisms to improve their function are understood and available. By a strict application of IUCN threat criteria, P. troglodytes can be considered Endangered, based on estimated rates of past decline and on the species' long generation time. Relatively speaking, however, P. troglodytes is less endangered than are orangutans or gorillas, and the species is unlikely to go extinct by the year 2100, especially if existing conservation measures improve. The IUCN threat-rating system has become overly complex; the system can produce results that do not accord with common sense and these results must therefore be interpreted with care.

Introduction to the International Symposium on African Great Apes

This special issue consists of selected papers presented to the international symposium entitled ‘African Great Apes: Evolution, Diversity and Conservation’ held at Kyoto on 3–5 March 2004. It was organized as a part of the 21st century COE program of Kyoto University (A 14) ‘‘Formation of a strategic base for the multidisciplinary study of biodiversity.’’ The goal of this program is threefold: to promote world-class research by unifying traditional field research at Kyoto University with new developments in molecular biology; to construct a basic academic discipline of ‘‘Biodiversity Science;’’ and to implement postgraduate education under a unified system of macroand micro-biology. The aim of this symposium was to evaluate our current knowledge of the African great apes from recent and ongoing field research and to consider its relevance to evolutionary anthropology. This symposium was based on two previous conferences sponsored by the Wenner-Gren Foundation. One is ‘‘The Great Apes’’ organized by Jane Goodall and David Hamburg and held at Burg Wartenstein, Austria in 1974. The other is ‘‘The Great Apes Revisited’’ organized by William McGrew, Linda Marchant, and Toshisada Nishida, and held at Cabo San Lucas, Mexico in 1994. The first conference provided the first reliable information on the social organization of the great apes using newly acquired results from field studies of habituated subjects. Data on chimpanzees and gorillas were limited to a single species from Gombe, Mahale, and the Virunga Volcanoes. Field research on bonobos had just been initiated and was introduced in preliminary reports. The second conference included new information from various study sites and different subspecies. Special topics such as party size, mating, positional behavior, nesting, and laterality were compared within and between species. Studies of sympatric chimpanzees and gorillas were first reported and discussed in terms of ecological competition and niche differentiation. Since then, new study sites have been established to facilitate inter-group, inter-regional, and inter-species comparisons, while methodological advances have yielded new insights into African great ape ecology and behavior. For example, Global Positioning Systems (GPS) have permitted us to monitor populations more precisely over larger geographic areas. Genetic analyses have allowed us to determine the paternity of individuals, sometimes with surprising results not predicted by behavioral observations. Despite these advances, the recent collapse of the economies and volatile political situations of countries that harbor the great apes in Africa have resulted in a prominent increase in habitat destruction and poaching. Frequent civil wars and disease outbreaks, such as Ebola, have caused a significant decline in ape populations in Central Africa. The African great apes are now in danger of extinction and worldwide conservation measures are needed to save them. Six topics were selected for discussion in this symposium: (1) Behavioral diversity and origins of human culture; (2) Sympatry and coexistence of African great apes; (3) Natural environments and evolution of African great apes; (4) The significance of Pan social behavior; (5) Contributions of African great apes to biodiversity; and (6) Great apes as the World Heritage Species. Talks focused on how studies of the African great apes contribute to the field of evolutionary anthropology and on conservation planning for their survival. Old and new topics were discussed and compared with previous conferences. We hope that the papers in this special issue will add to our understanding of the African great apes as well as human beings and will promote our coexistence with them, our closest evolutionary relatives. J. Yamagiwa (&) Kyoto University, Kyoto, Japan E-mail: yamagiwa@jinrui.zool.kyoto-u.ac.jp

Genetic diversity among African great apes based on mitochondrial DNA sequences

The mitochondrial DNA D-Loop region was sequenced, analyzed and used as a molecular marker for populations of chimpanzee (Pan troglodytes), bonobo (P. paniscus) and gorilla (Gorilla gorilla and G. beringei), and also compared with data previously reported for these taxa. In Gorilla, a main disjunction between western (G. gorilla) and eastern (G. beringei, including G. b. graueri) species was observed, as well as high mitochondrial diversity within the western species. The genetic distance values within G. gorilla (0.14) were higher than those between subspecies (eastern lowland and mountain 0.12). Likewise, values of genetic diversity within this species (0.05) were higher than those between species (western and eastern lowland gorilla 0.04). Similarly, in genus Pan a main differentiation between western (P. t. verus) and central forms (P. t. troglodytes and P. t. schweinfurthii) was observed. The obtained values of genetic distance and genetic diversity revealed that the central subspecies are closer to each other than either of them is to the western one, while bonobos composed a distinct clade that expresses a well-defined specific identity. The current distribution, phylogeny and levels of genetic diversity in African great ape populations are consistent with the hypothesis that Pleistocene climatic events led to cyclical periods of isolation in forest refugia followed by expansion and dispersal. The implications of this high level of genetic diversity for taxonomic classification, wildlife management and conservation are discussed.

Disease Risk Assessment in African Great Apes Using Geographic Information Systems

This unique study illustrates the potential application of Geographic Information Systems (GIS) to generate hypotheses regarding which African great ape populations, including bonobos (Pan paniscus), chimpanzees (Pan troglodytes), and gorillas (Gorilla gorilla and Gorilla beringei), are at increased risk from human diseases. Human demographic data and core human health indicator data for the African great ape range countries were obtained. Human population density and percent annual human population growth rate were used as combined indicators of environmental stress/vulnerability (as a proxy measure of human–great ape contact), and infant mortality rate (IMR) and healthy life expectancy (HALE) were used as separate indicators of disease burden among the human populations living in the great ape range countries. Cut-off values were determined and, using GIS, these indicators were analyzed to create maps of critical areas (countries) with both environmental stress and high burden of human diseases. When using IMR as the indicator of disease burden, the great ape range countries identified as critical areas included Benin, Guinea-Bissau, Ivory Coast, Liberia, Nigeria, and Tanzania. Cameroon and Uganda were also identified as critical areas when using HALE as the indicator of disease burden; however, Benin was excluded. Validation of these results would allow for targeted interventions thereby maximizing the use of limited resources. Improvements in public health infrastructure in these critical areas would benefit the human populations that have unmet health needs as well as these endangered species.

Frequent infection of Hylobates pileatus (pileated gibbon) with species-associated variants of hepatitis B virus in Cambodia

As well as being distributed widely in human populations, hepatitis B virus (HBV) infections occur frequently in chimpanzee, gibbon and other ape populations in sub-Saharan Africa and South-East Asia. To investigate the frequency and genetic relationships of HBV infecting gibbons in Cambodia, pileated gibbons (Hylobates pileatus) that were originally wild-caught were screened for surface antigen. Twelve of 26 (46 %) were positive, of which 11 were positive for HBV DNA. Phylogenetic analysis of complete genome sequences revealed two distinct genetic groups in the gibbon/orangutan clade. Three were similar to previously described variants infecting H. pileatus in Thailand and eight formed a distinct clade, potentially representing distinct strains of HBV circulating in geographically separated populations in South-East Asia. Because of the ability of HBV to cross species barriers, large reservoirs of infection in gibbons may hamper ongoing attempts at permanent eradication of HBV infection from human populations in South-East Asia through immunization.

Determination of ape distribution and population size using ground and aerial surveys: a case study with orang‐utans in lower Kinabatangan, Sabah, Malaysia

AbstractBecause of the difficulties encountered in detecting many large tropical forest‐dwelling species in their natural habitat, precise figures concerning the distribution, number and trends of many populations remain deficient. In tropical forests, ground surveys are generally carried out by counting objects along straight lines. These counts require a strict compliance with the line‐transect methodology before (proper design of the census), during (careful data collection) and after (accurate and correct data processing and analysis) the census itself. In addition, the major source of bias when estimating population size and/or trends comes from the extrapolation of estimates obtained in small sampling areas to the larger, and often incompletely known, distribution of the population. In the Kinabatangan floodplain (Sabah, Malaysia), helicopter surveys were useful in directly assessing the distribution of orang‐utans and were a major advantage in the precise estimation of the size of the orang‐utan population surviving in this region. Our survey showed that about 1100 orang‐utans remain in the multiple‐use forests of the Kinabatangan floodplain. These results provide new evidence on orang‐utan adaptation to habitat disturbance and indicate the potential of the Kinabatangan multiple‐use forests for orang‐utan conservation. Helicopter surveys appear to be a promising alternative to ground survey for precise distribution assessment and for monitoring population trends of apes throughout their entire range in Asia and in some parts of Africa.

Life history of wild Sumatran orangutans ( Pongo abelii)

We present life history data on wild Sumatran orangutans gleaned from a 32-year and a 5.5-year study. Estimated age at first reproduction was 15.4 years. At 9.3 years, the average interbirth interval for this population is the longest ever recorded for any great ape population, significantly longer than that of a Bornean orangutan population. We find that age-specific mortality of Sumatran orangutans does not differ between sexes and is significantly lower than that of wild chimpanzees. We conclude that orangutan life history is the slowest among extant great apes. In accordance with their slow life history, longevity in the wild is estimated to be at least 58 years for males and at least 53 for females. We find no evidence for menopause. These data suggest that compared to the ancestral state, humans have undergone less of an increase in longevity than commonly assumed, and have experienced selection on earlier cessation of reproduction.

Anthrax kills wild chimpanzees in a tropical rainforest.

Infectious disease has joined habitat loss and hunting as threats to the survival of the remaining wild populations of great apes. Nevertheless, relatively little is known about the causative agents. We investigated an unusually high number of sudden deaths observed over nine months in three communities of wild chimpanzees (Pan troglodytes verus) in the Taï National Park, Ivory Coast. Here we report combined pathological, cytological and molecular investigations that identified Bacillus anthracis as the cause of death for at least six individuals. We show that anthrax can be found in wild non-human primates living in a tropical rainforest, a habitat not previously known to harbour B. anthracis. Anthrax is an acute disease that infects ruminants, but other mammals, including humans, can be infected through contacting or inhaling high doses of spores or by consuming meat from infected animals. Respiratory and gastrointestinal anthrax are characterized by rapid onset, fever, septicaemia and a high fatality rate without early antibiotic treatment. Our results suggest that epidemic diseases represent substantial threats to wild ape populations, and through bushmeat consumption also pose a hazard to human health.

Densities, Distributions, and Seasonal Movements of Gorillas and Chimpanzees in Swamp Forest in Northern Congo

The conservation of gorillas (Gorilla spp.) and chimpanzees (Pan troglodytes) depends upon knowledge of their densities and distribution throughout their ranges. However, information about ape populations in swamp forests is scarce. Here we build on current knowledge of ape populations by conducting line transect surveys of nests throughout a reserve dominated by swamp forest: the Lac Tele Community Reserve in northern Congo. We estimated gorilla and chimpanzee densities, distributions across habitats, and seasonal changes in abundance. Gorilla density was 2.9 gorillas km−2, but densities varied by habitat (0.3–5.4 gorillas km−2) with highest densities in swamp forest and terra firma mixed forest. Average chimpanzee density is 0.7 chimpanzees km−2 (0.1–1.3 chimpanzees km−2), with highest densities in swamp forest. Habitat was the best predictor of ape nest abundance, as neither the number of human indices nor the distance from the nearest village predicted nest abundance. We recorded significantly greater numbers of apes in terra firma forest during the high-water season than the low-water season, indicating that many gorillas and chimpanzees are at times concentrated in terra firma forest amid a matrix of swamp forest. Seasonally high numbers of apes on terra firma forest islands easily accessible to local people may expose them to substantial hunting pressure. Conversely, the nearly impenetrable nature of swamp forests and their low value for logging makes them promising sites for the conservation of apes.

Ape Populations and Ebola

Ape Populations and Ebola

Ebola and the decline of gorilla Gorilla gorilla and chimpanzee Pan troglodytes populations in Minkebe Forest, north-eastern Gabon

During 1998–2000 extremely low densities of gorillas Gorilla gorilla gorilla and chimpanzees Pan troglodytes troglodytes were found in the Minkebe Forest block in north-eastern Gabon. When compared with data collected before 1994, these data suggest a catastrophic decline in ape populations in the area. We believe that this decline was caused by a disease epidemic. The period of decline corresponds with the Ebola outbreaks of 1994 and 1996 that occurred in the human population in the same area. Deaths of gorillas and chimpanzees were associated with both Ebola outbreaks. Data from nearby sites indicate that the epidemic was limited to the Minkebe Forest. Occurrence of such epidemic die-offs should be taken into account in conservation strategies for the long-term survival of ape populations. At the time of writing, an Ebola epidemic among humans in the Zadié Department east of Minkebe Forest has resulted in 53 deaths. In the neighbouring Republic of Congo, authorities have reported 43 deaths and at least 12 other cases of Ebola. These epidemics are believed to be linked to the handling and eating of dead apes.

Foci of endemic simian immunodeficiency virus infection in wild-living eastern chimpanzees (Pan troglodytes schweinfurthii).

Simian immunodeficiency virus of chimpanzees (SIVcpz) is the immediate precursor to human immunodeficiency virus type 1 (HIV-1), yet remarkably, the distribution and prevalence of SIVcpz in wild ape populations are unknown. Studies of SIVcpz infection rates in wild chimpanzees are complicated by the species' endangered status and by its geographic location in remote areas of sub-Saharan Africa. We have developed sensitive and specific urine and fecal tests for SIVcpz antibody and virion RNA (vRNA) detection and describe herein the first comprehensive prevalence study of SIVcpz infection in five wild Pan troglodytes schweinfurthii communities in east Africa. In Kibale National Park in Uganda, 31 (of 52) members of the Kanyawara community and 39 (of approximately 145) members of the Ngogo community were studied; none were found to be positive for SIVcpz infection. In Gombe National Park in Tanzania, 15 (of 20) members of the Mitumba community, 51 (of 55) members of the Kasekela community, and at least 10 (of approximately 20) members of the Kalande community were studied. Seven individuals were SIVcpz antibody and/or vRNA positive, and two others had indeterminate antibody results. Based on assay sensitivities and the numbers and types of specimens analyzed, we estimated the prevalence of SIVcpz infection to be 17% in Mitumba (95% confidence interval, 10 to 40%), 5% in Kasekela (95% confidence interval, 4 to 7%), and 30% in Kalande (95% confidence interval, 15 to 60%). For Gombe as a whole, the SIVcpz prevalence was estimated to be 13% (95% confidence interval, 7 to 25%). SIVcpz infection was confirmed in five chimpanzees by PCR amplification of partial pol and gp41/nef sequences which revealed a diverse group of viruses that formed a monophyletic lineage within the SIVcpzPts radiation. Although none of the 70 Kibale chimpanzees tested SIVcpz positive, we estimated the likelihood that a 10% or higher prevalence existed but went undetected because of sampling and assay limitations; this possibility was ruled out with 95% certainty. These results indicate that SIVcpz is unevenly distributed among P. t. schweinfurthii in east Africa, with foci or "hot spots" of SIVcpz endemicity in some communities and rare or absent infection in others. This situation contrasts with that for smaller monkey species, in which infection rates by related SIVs are generally much higher and more uniform among different groups and populations. The basis for the wide variability in SIVcpz infection rates in east African apes and the important question of SIVcpz prevalence in west central African chimpanzees (Pan troglodytes troglodytes) remain to be elucidated.

Catastrophic ape decline in western equatorial Africa.

Because rapidly expanding human populations have devastated gorilla (Gorilla gorilla) and common chimpanzee (Pan troglodytes) habitats in East and West Africa, the relatively intact forests of western equatorial Africa have been viewed as the last stronghold of African apes. Gabon and the Republic of Congo alone are thought to hold roughly 80% of the world's gorillas and most of the common chimpanzees. Here we present survey results conservatively indicating that ape populations in Gabon declined by more than half between 1983 and 2000. The primary cause of the decline in ape numbers during this period was commercial hunting, facilitated by the rapid expansion of mechanized logging. Furthermore, Ebola haemorrhagic fever is currently spreading through ape populations in Gabon and Congo and now rivals hunting as a threat to apes. Gorillas and common chimpanzees should be elevated immediately to 'critically endangered' status. Without aggressive investments in law enforcement, protected area management and Ebola prevention, the next decade will see our closest relatives pushed to the brink of extinction.

Habituating the great apes: the disease risks

All six great apes, gorillas Gorilla gorilla and G. beringei, chimpanzees Pan troglodytes and P. paniscus, and orang-utans Pongo pygmaeus and P. abelii, are categorized as Endangered on the 2000 IUCN Red List and face many threats to their continued existence in the wild. These threats include loss of habitat to settlement, logging and agriculture, illegal hunting for bushmeat and traditional medicine, the live ape trade, civil unrest and infectious diseases. The great apes are highly susceptible to many human diseases, some of which can be fatal while others can cause marked morbidity. There is increasing evidence that diseases can be transmitted from humans to free-living habituated apes, sometimes with serious consequences. If protective measures are not improved, ape populations that are frequently in close contact with people will eventually be affected by the inadvertent transmission of human diseases. This paper describes the risks, sources and circumstances of infectious disease transmission from humans to great apes during and consequent upon habituation for tourism and research. A major problem is that the regulations that protect habituated apes from the transmission of disease from people are often poorly enforced. Suggestions are made for improving the enforcement of existing regulations governing ape-based tourism, and for minimizing the risk of disease transmission between humans, both local people and international visitors, and the great apes.

Modern African ape populations as genetic and demographic models of the last common ancestor of humans, chimpanzees, and gorillas.

In order to fully understand human evolutionary history through the use of molecular data, it is essential to include our closest relatives as a comparison. We provide here estimates of nucleotide diversity and effective population size of modern African ape species using data from several independent noncoding nuclear loci, and use these estimates to make predictions about the nature of the ancestral population that eventually gave rise to the living species of African apes, including humans. Chimpanzees, bonobos, and gorillas possess two to three times more nucleotide diversity than modern humans. We hypothesize that the last common ancestor (LCA) of these species had an effective population size more similar to modern apes than modern humans. In addition, estimated dates for the divergence of the Homo, Pan, and Gorilla lineages suggest that the LCA may have had stronger geographic structuring to its mtDNA than its nuclear DNA, perhaps indicative of strong female philopatry or a dispersal system analogous to gorillas, where females disperse only short distances from their natal group. Synthesizing different classes of data, and the inferences drawn from them, allows us to predict some of the genetic and demographic properties of the LCA of humans, chimpanzees, and gorillas.

On the Conservation of Apes in Africa

Recent advances in conservation biology are discussed for the future of the wild African apes. Forest destruction in the continent and fragmentation of the ape populations give rise to the serious possibility of continuous local extinction of apes. The spatial design of protected areas (single large or several small), the effective population size, the MVP, the Allee's effect, and synecological factors are considered. The participants who are concerned about conservation of the apes can contribute to their survival with these scientific understandings. Some personal opinions are proposed for the survival of apes.