Barriers to chimpanzee gene flow at the south-east edge of their distribution.

Populations on the edge of a species' distribution may represent an important source of adaptive diversity, yet these populations tend to be more fragmented and are more likely to be geographically isolated. Lack of genetic exchanges between such populations, due to barriers to animal movement, can not only compromise adaptive potential but also lead to the fixation of deleterious alleles. The south-eastern edge of chimpanzee distribution is particularly fragmented, and conflicting hypotheses have been proposed about population connectivity and viability. To address this uncertainty, we generated both mitochondrial and MiSeq-based microsatellite genotypes for 290 individuals ranging across western Tanzania. While shared mitochondrial haplotypes confirmed historical gene flow, our microsatellite analyses revealed two distinct clusters, suggesting two populations currently isolated from one another. However, we found evidence of high levels of gene flow maintained within each of these clusters, one of which covers an 18,000 km2 ecosystem. Landscape genetic analyses confirmed the presence of barriers to gene flow with rivers and bare habitats highly restricting chimpanzee movement. Our study demonstrates how advances in sequencing technologies, combined with the development of landscape genetics approaches, can resolve ambiguities in the genetic history of critical populations and better inform conservation efforts of endangered species.

The Gombe Ecosystem Health Project: 16 years of program evolution and lessons learned.

Infectious disease outbreaks pose a significant threat to the conservation of chimpanzees (Pan troglodytes) and all threatened nonhuman primates. Characterizing and mitigating these threats to support the sustainability and welfare of wild populations is of the highest priority. In an attempt to understand and mitigate the risk of disease for the chimpanzees of Gombe National Park, Tanzania, we initiated a long-term health-monitoring program in 2004. While the initial focus was to expand the ongoing behavioral research on chimpanzees to include standardized data on clinical signs of health, it soon became evident that the scope of the project would ideally include diagnostic surveillance of pathogens for all primates (including people) and domestic animals, both within and surrounding the National Park. Integration of these data, along with in-depth post-mortem examinations, have allowed us to establish baseline health indicators to inform outbreak response. Here, we describe the development and expansion of the Gombe Ecosystem Health project, review major findings from the research and summarize the challenges and lessons learned over the past 16 years. We also highlight future directions and present the opportunities and challenges that remain when implementing studies of ecosystem health in a complex, multispecies environment.

Gregariousness is associated with parasite species richness in a community of wild chimpanzees.

Increased risk of pathogen transmission through proximity and contact is a well-documented cost of sociality. Affiliative social contact, however, is an integral part of primate group life and can benefit health. Despite its importance to the evolution and maintenance of sociality, the tradeoff between costs and benefits of social contact for group-living primate species remains poorly understood. To improve our understanding of this interplay, we used social network analysis to investigate whether contact via association in the same space and/or physical contact measured through grooming were associated with helminth parasite species richness in a community of wild chimpanzees (Pan troglodytes schweinfurthii). We identified parasite taxa in 381 fecal samples from 36 individuals from the Kasekela community of chimpanzees in Gombe National Park, Tanzania, from November 1, 2006 - October 31, 2012. Over the study period, eight environmentally transmitted helminth taxa were identified. We quantified three network metrics for association and grooming contact, including degree strength, betweenness, and closeness. Our findings suggest that more gregarious individuals - those who spent more time with more individuals in the same space - had higher parasite richness, while the connections in the grooming network were not related to parasite richness. The expected parasite richness in individuals increased by 1.13 taxa (CI: 1.04, 1.22; p = 0.02) per one standard deviation increase in degree strength of association contact. The results of this study add to the understanding of the role that different types of social contact plays in the parasite richness of group-living social primates.

Research and Conservation in the Greater Gombe Ecosystem: Challenges and Opportunities.

The study of chimpanzees in Gombe National Park, Tanzania, started by Jane Goodall in 1960, provided pioneering accounts of chimpanzee behavior and ecology. With funding from multiple sources, including the Jane Goodall Institute (JGI) and grants from private foundations and federal programs, the project has continued for sixty years, providing a wealth of information about our evolutionary cousins. These chimpanzees face two main challenges to their survival: infectious disease - including simian immunodeficiency virus (SIVcpz), which can cause Acquired Immune Deficiency Syndrome (AIDS) in chimpanzees - and the deforestation of land outside the park. A health monitoring program has increased understanding of the pathogens affecting chimpanzees and has promoted measures to characterize and reduce disease risk. Deforestation reduces connections between Gombe and other chimpanzee populations, which can cause loss of genetic diversity. To promote habitat restoration, JGI facilitated participatory village land use planning, in which communities voluntarily allocated land to a network of Village Land Forest Reserves. Expected benefits to people include stabilizing watersheds, improving water supplies, and ensuring a supply of forest resources. Surveys and genetic analyses confirm that chimpanzees persist on village lands and remain connected to the Gombe population. Many challenges remain, but the regeneration of natural forest on previously degraded lands provides hope that conservation solutions can be found that benefit both people and wildlife. Conservation work in the Greater Gombe Ecosystem has helped promote broader efforts to plan and work for conservation elsewhere in Tanzania and across Africa.

Syndromic Surveillance of Respiratory Disease in Free-Living Chimpanzees.

Disease surveillance in wildlife is rapidly expanding in scope and methodology, emphasizing the need for formal evaluations of system performance. We examined a syndromic surveillance system for respiratory disease detection in Gombe National Park, Tanzania, from 2004 to 2012, with respect to data quality, disease trends, and respiratory disease detection. Data quality was assessed by examining community coverage, completeness, and consistency. The data were examined for baseline trends; signs of respiratory disease occurred at a mean frequency of less than 1 case per week, with most weeks containing zero observations of abnormalities. Seasonal and secular (i.e., over a period of years) trends in respiratory disease frequency were not identified. These baselines were used to develop algorithms for outbreak detection using both weekly counts and weekly prevalence thresholds and then compared retrospectively on the detection of 13 respiratory disease clusters from 2005 to 2012. Prospective application of outbreak detection algorithms to real-time syndromic data would be useful in triggering a rapid outbreak response, such as targeted diagnostic sampling, enhanced surveillance, or mitigation.

Socioecological correlates of clinical signs in two communities of wild chimpanzees (Pan troglodytes) at Gombe National Park, Tanzania.

Disease and other health hazards pose serious threats to the persistence of wild ape populations. The total chimpanzee population at Gombe National Park, Tanzania, has declined from an estimated 120 to 150 individuals in the 1960's to around 100 individuals by the end of 2013, with death associated with observable signs of disease as the leading cause of mortality. In 2004, we began a non-invasive health-monitoring program in the two habituated communities in the park (Kasekela and Mitumba) with the aim of understanding the prevalence of health issues in the population, and identifying the presence and impacts of various pathogens. Here we present prospectively collected data on clinical signs (observable changes in health) in the chimpanzees of the Kasekela (n = 81) and Mitumba (n = 32) communities over an 8-year period (2005-2012). First, we take a population approach and analyze prevalence of clinical signs in five different categories: gastrointestinal system (diarrhea), body condition (estimated weight loss), respiratory system (coughing, sneezing etc.), wounds/lameness, and dermatologic issues by year, month, and community membership. Mean monthly prevalence of each clinical sign per community varied, but typically affected <10% of observed individuals. Secondly, we analyze the presence of clinical signs in these categories as they relate to individual demographic and social factors (age, sex, and dominance rank) and simian immunodeficiency virus (SIVcpz) infection status. Adults have higher odds of being observed with diarrhea, loss of body condition, and wounds or lameness when compared to immatures, while males have a higher probability of being observed with wounds or lameness than females. In contrast, signs of respiratory illness appear not to be related to chimpanzee-specific factors and skin abnormalities are very rare. For a subset of known-rank individuals, dominance rank predicts the probability of wounding/lameness in adult males, but does not predict any adverse clinical signs in adult females. Instead, adult females with SIVcpz infection are more likely to be observed with diarrhea, a finding that warrants further investigation. Comparable data are needed from other sites to determine whether the prevalence of clinical signs we observe are relatively high or low, as well as to more fully understand the factors influencing health of wild apes at both the population and individual level. Am. J. Primatol. 80:e22562, 2018. © 2016 Wiley Periodicals, Inc.

Oesophagostomiasis in non-human primates of Gombe National Park, Tanzania.

Oesophagostomum sp. is a parasitic nematode that frequently infects wild chimpanzees. Although nodular lesions are commonly associated with infection, some wild chimpanzee populations seem to tolerate Oesophagostomum nodular lesions while those at Gombe and other sites suffer from associated morbidity and mortality. From August 2004 to December 2013, we examined demographic (i.e., age, sex) and individual correlates (i.e., fecal consistency, Oesophagostomum egg production) to Oesophagostomum-associated pathology in 14 individually recognized chimpanzees at Gombe Stream National Park, Tanzania. In addition, we characterized Oesophagostomum-associated pathology in 14 individual sympatric primates including baboons, colobus, and cercopithecid monkeys. In five chimpanzees, there was no evidence of any significant underlying disease aside from oesophagostomiasis to explain the thin condition or diarrhea. All five of these chimpanzees had moderate to numerous parasitic nodules. In general, nodules were more numerous in older chimpanzees. Three of four chimpanzees with the highest average Oesophagostomum egg counts in feces collected during the year prior to their death had numerous parasitic nodules at necropsy. In contrast, the four chimpanzees with the lowest egg counts had only moderate numbers of nodules. No association (P = 0.74) was noted between frequency of diarrhea in the year prior to death and the number of nodules noted at necropsy. Nodules were also present in all baboons examined documenting pathology associated with Oesophagostomum infection in wild baboons. In contrast, no lesions were noted in colobus or cercopithecid monkeys, although it is uncertain if they are infected as no fecal studies have been completed in these species to date at Gombe. Sequence of DNA isolated from nodules in chimpanzees matched (99%) Oesophagostomum stephanostomum. Further research is needed to identify the types of Oesophagostomum causing lesions in baboons and to determine if baboons suffer from these infections. Am. J. Primatol. 80:e22572, 2018. © 2016 Wiley Periodicals, Inc.

Infanticide in chimpanzees: Taphonomic case studies from Gombe.

OBJECTIVES: We present a study of skeletal damage to four chimpanzee (Pan troglodytes) infanticide victims from Gombe National Park, Tanzania. Skeletal analysis may provide insight into the adaptive significance of infanticide by examining whether nutritional benefits sufficiently explain infanticidal behavior. The nutritional hypothesis would be supported if bone survivorship rates and skeletal damage patterns are comparable to those of monkey prey. If not, other explanations, such as the resource competition hypothesis, should be considered. METHODS: Taphonomic assessment of two chimpanzee infants included description of breakage and surface modification, data on MNE, %MNE, and bone survivorship. Two additional infants were assessed qualitatively. The data were compared to published information on monkey prey. We also undertook a review of published infanticide cases. RESULTS: The cases were intercommunity infanticides (one male and three female infants) committed by males. Attackers partially consumed two of the victims. Damage to all four infants included puncture marks and compression fractures to the cranium, crenulated breaks to long bones, and incipient fractures on ribs. Compared to monkey prey, the chimpanzee infants had an abundance of vertebrae and hand/foot bones. CONCLUSIONS: The cases described here suggest that chimpanzees may not always completely consume infanticide victims, while reports on chimpanzee predation indicated that complete consumption of monkey prey usually occurred. Infanticidal chimpanzees undoubtedly gain nutritional benefits when they consume dead infants, but this benefit may not sufficiently explain infanticide in this species. Continued study of infanticidal and hunting behavior, including skeletal analysis, is likely to be of interest.

Isolation of Treponema DNA from Necrophagous Flies in a Natural Ecosystem.

BACKGROUND: Recently, the World Health Organization launched a campaign to eradicate the tropical disease yaws, caused by the bacterium Treponema pallidum subsp. pertenue; however, for decades researchers have questioned whether flies act as a vector for the pathogen that could facilitate transmission. METHODS: A total of 207 fly specimens were trapped in areas of Africa in which T. pallidum-induced skin ulcerations are common in wild baboons; 88 flies from Tarangire National Park and 119 from Lake Manyara National Park in Tanzania were analyzed by PCR for the presence of T. pallidum DNA. FINDINGS: We report that in the two study areas, T. pallidum DNA was found in 17-24% of wild-caught flies of the order Diptera. Treponemal DNA sequences obtained from many of the flies match sequences derived from nearby baboon T. pallidum strains, and one of the fly species with an especially high prevalence of T. pallidum DNA, Musca sorbens, has previously been shown to transmit yaws in an experimental setting. INTERPRETATION: Our results raise the possibility that flies play a role in yaws transmission; further research is warranted, given how important understanding transmission is for the eradication of this disfiguring disease.

Field immobilization for treatment of an unknown illness in a wild chimpanzee (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania: findings, challenges, and lessons learned.

Infectious diseases are widely presumed to be one of the greatest threats to ape conservation in the wild. Human diseases are of particular concern, and the costs and benefits of human presence in protected areas with apes are regularly debated. While numerous syndromes with fatal outcomes have recently been described, precise identification of pathogens remains difficult. These diagnostic difficulties are compounded by the fact that direct veterinary intervention on wild apes is quite rare. Here we present the unique case of a wild chimpanzee at Gombe National Park that was observed with a severe illness and was subsequently examined and treated in the field. Multiple specimens were collected and tested with the aim of identifying the pathogen responsible for the illness. Our findings represent the first extensive screening of a living wild chimpanzee, yet despite our efforts, the cause and source of illness remain unknown. Nevertheless, our findings represent valuable baseline data for the ape conservation community and for comparison with other recent findings. In addition, we present the case here to demonstrate the planning required and multiple types of expertise necessary to maximize the amount of data obtained from such a rare intervention, and to provide lessons learned for future studies.

Pathologic lesions in chimpanzees (Pan trogylodytes schweinfurthii) from Gombe National Park, Tanzania, 2004-2010.

During a population decline or disease outbreak, the true risk of specific diseases to a wild population is often difficult to determine because of a lack of baseline disease information. To better understand the risk of disease in an endangered and scientifically important population of chimpanzees (Pan trogylodytes schweinfurthii), a health monitoring program was initiated in Gombe National Park, Tanzania. As part of this health monitoring program, comprehensive necropsies with histopathology were conducted on chimpanzees (n = 11; 5 male, 6 female), ranging in age from fetal to 44 yr, that were found dead between August 2004 and January 2010. In contrast to previous reports, respiratory disease was not noted as a cause of morbidity or mortality. Trauma was the most common cause of death in these 11 chimpanzees. All of the chimpanzees greater than 1 yr of age had intestinal and mesenteric parasitic granulomas associated with true strongyles consistent with Oesophagostomum spp. The relative numbers of granulomas increased with age and, in some cases, may have been a cause of weight loss and diarrhea. Simian immunodeficiency virus (SIV)cpz infection was documented in four deceased apes, all of whom exhibited varying amounts of lymphoid depletion including two females with marked CD4+ T cell loss consistent with endstage SIVmac or human immunodeficiency virus infections. Myocardial megalokaryosis was common in chimpanzees greater than 1 mo of age; yet myocardial interstitial fibrosis, a common lesion in captive chimpanzees, was uncommon and only noted in two aged chimpanzees. These findings provide important information on causes of morbidity and mortality in wild chimpanzees, information that can be used to interpret findings during population declines and lead to better management of this population in the context of disease risk.

Demographic and ecological effects on patterns of parasitism in eastern chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania.

From January 2006 to January 2008, we collected 1,045 fecal samples from 90 individually-recognized, free-ranging, eastern chimpanzees (Pan troglodytes schweinfurthii) inhabiting Gombe National Park, Tanzania to determine how patterns of parasitism are affected by demographic and ecological covariates. Seventeen parasite species were recovered, including eight nematodes (Oesophagostomum sp., Necator sp., Probstmayria gombensis, Strongyloides fulleborni, Ascaris sp., Trichuris sp., Abbreviata caucasica, and an unidentified strongyle), 1 cestode (Bertiella sp.), 1 trematode (Dicrocoeliidae), and 7 protozoa (Entamoeba coli, Entamoeba histolytica/dispar, Iodamoeba bütschlii, Troglodytella abrassarti, Troglocorys cava, Balantidium coli, and an unidentified protozoa). Significant differences were observed in interannual infection prevalence and parasite richness between 2006 and 2007. Intercommunity comparisons demonstrated higher prevalence of parasites for the Mitumba compared with Kasekela chimpanzee community. Prevalence of several parasites was strongly correlated with monthly rainfall patterns for both 2006 and 2007. Subadult chimpanzees had lower prevalence for most parasite species compared with adults in both years and also yielded a lower average parasite species richness. No significant differences were observed between males and females in prevalence in 2006. However, in 2007 the prevalence of S. fulleborni and I. bütschlii were higher in males than in females. Parasite prevalence and richness were substantially higher in this multiyear study compared with previous short-term studies of the gastrointestinal parasites of Gombe chimpanzees. This coupled with the significant interannual and interseasonal variation, demonstrated in this study, emphasizes the importance of multiyear monitoring with adequate sample size to effectively determine patterns of parasitism in wild primate populations.

Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz.

African primates are naturally infected with over 40 different simian immunodeficiency viruses (SIVs), two of which have crossed the species barrier and generated human immunodeficiency virus types 1 and 2 (HIV-1 and HIV-2). Unlike the human viruses, however, SIVs do not generally cause acquired immunodeficiency syndrome (AIDS) in their natural hosts. Here we show that SIVcpz, the immediate precursor of HIV-1, is pathogenic in free-ranging chimpanzees. By following 94 members of two habituated chimpanzee communities in Gombe National Park, Tanzania, for over 9 years, we found a 10- to 16-fold higher age-corrected death hazard for SIVcpz-infected (n = 17) compared to uninfected (n = 77) chimpanzees. We also found that SIVcpz-infected females were less likely to give birth and had a higher infant mortality rate than uninfected females. Immunohistochemistry and in situ hybridization of post-mortem spleen and lymph node samples from three infected and two uninfected chimpanzees revealed significant CD4(+) T-cell depletion in all infected individuals, with evidence of high viral replication and extensive follicular dendritic cell virus trapping in one of them. One female, who died within 3 years of acquiring SIVcpz, had histopathological findings consistent with end-stage AIDS. These results indicate that SIVcpz, like HIV-1, is associated with progressive CD4(+) T-cell loss, lymphatic tissue destruction and premature death. These findings challenge the prevailing view that all natural SIV infections are non-pathogenic and suggest that SIVcpz has a substantial negative impact on the health, reproduction and lifespan of chimpanzees in the wild.