Dynamics of a morbillivirus at the domestic-wildlife interface: Canine distemper virus in domestic dogs and lions.

Morbilliviruses cause many diseases of medical and veterinary importance, and although some (e.g., measles and rinderpest) have been controlled successfully, others, such as canine distemper virus (CDV), are a growing concern. A propensity for host-switching has resulted in CDV emergence in new species, including endangered wildlife, posing challenges for controlling disease in multispecies communities. CDV is typically associated with domestic dogs, but little is known about its maintenance and transmission in species-rich areas or about the potential role of domestic dog vaccination as a means of reducing disease threats to wildlife. We address these questions by analyzing a long-term serological dataset of CDV in lions and domestic dogs from Tanzania's Serengeti ecosystem. Using a Bayesian state-space model, we show that dynamics of CDV have changed considerably over the past three decades. Initially, peaks of CDV infection in dogs preceded those in lions, suggesting that spill-over from dogs was the main driver of infection in wildlife. However, despite dog-to-lion transmission dominating cross-species transmission models, infection peaks in lions became more frequent and asynchronous from those in dogs, suggesting that other wildlife species may play a role in a potentially complex maintenance community. Widespread mass vaccination of domestic dogs reduced the probability of infection in dogs and the size of outbreaks but did not prevent transmission to or peaks of infection in lions. This study demonstrates the complexity of CDV dynamics in natural ecosystems and the value of long-term, large-scale datasets for investigating transmission patterns and evaluating disease control strategies.

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.

Serologic surveillance of anthrax in the Serengeti ecosystem, Tanzania, 1996-2009.

Bacillus anthracis, the bacterium that causes anthrax, is responsible for varying death rates among animal species. Difficulties in case detection, hazardous or inaccessible carcasses, and misdiagnosis hinder surveillance. Using case reports and a new serologic assay that enables multispecies comparisons, we examined exposure to and illness caused by B. anthracis in different species in the Serengeti ecosystem in Tanzania during 1996-2009 and the utility of serosurveillance. High seroprevalence among carnivores suggested regular nonfatal exposure. Seropositive wildebeest and buffalo showed that infection was not invariably fatal among herbivores, whereas absence of seropositivity in zebras and frequent detection of fatal cases indicated high susceptibility. Exposure patterns in dogs reflected known patterns of endemicity and provided new information about anthrax in the ecosystem, which indicated the potential of dogs as indicator species. Serosurveillance is a valuable tool for monitoring and detecting anthrax and may shed light on mechanisms responsible for species-specific variability in exposure, susceptibility, and mortality rates.

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.

Chimpanzee deaths at Mahale caused by a flu-like disease.

A flu-like disease spread among chimpanzees (Pan troglodytes schweinfurthii) of the M group at Mahale Mountains National Park, Tanzania, from June to July 2006. This epizootic or epidemic killed up to 12 chimpanzees. The obvious evidence of their deaths came from finding the bodies of three infants who had previously shown some symptoms of the disease. At least one of these infants died of pneumonia. In addition, nine chimpanzees were missing after the outbreak. These individuals were assumed to have been killed by this epizootic because most of them had contact with the infected individuals on the last days they were observed. We also found two dead bodies during this period, which were thought to be those of two missing individuals. We confirmed 23 (35.4%) of 65 individuals of the M group showed some symptoms of the disease, although most of them (20/23) did not die. More than half of them (14/23) had kin showing symptoms. Since this epizootic may have been caused by contact with humans, it will be necessary to establish and follow appropriate protocols for researchers, tourists, and park staff to observe chimpanzees, and to explore the mechanism of disease transmission from humans to chimpanzees and among chimpanzees.

Sleeping sickness--a re-emerging disease in the Serengeti?

Sleeping sickness is a re-emerging disease in the Serengeti ecosystem affecting both local people and tourists. Here we report the results of a survey to assess the prevalence of trypanosomiasis in both domestic and wild animals from this area. Five hundred and eighteen cattle samples were collected from 12 villages that bordered the Serengeti National Park and 220 samples from 15 different wild animal species were collected from within the park. PCR analysis, directed against the human serum resistance associated gene SRA, identified human infective Trypanosoma brucei rhodesiense parasites in both cattle and warthogs.

Predictability of anthrax infection in the Serengeti, Tanzania.

Anthrax is endemic throughout Africa, causing considerable livestock and wildlife losses and severe, sometimes fatal, infection in humans. Predicting the risk of infection is therefore important for public health, wildlife conservation and livestock economies. However, because of the intermittent and variable nature of anthrax outbreaks, associated environmental and climatic conditions, and diversity of species affected, the ecology of this multihost pathogen is poorly understood.We explored records of anthrax from the Serengeti ecosystem in north-west Tanzania where the disease has been documented in humans, domestic animals and a range of wildlife. Using spatial and temporal case-detection and seroprevalence data from wild and domestic animals, we investigated spatial, environmental, climatic and species-specific associations in exposure and disease.Anthrax was detected annually in numerous species, but large outbreaks were spatially localized, mostly affecting a few focal herbivores.Soil alkalinity and cumulative weather extremes were identified as useful spatial and temporal predictors of exposure and infection risk, and for triggering the onset of large outbreaks.Interacting ecological and behavioural factors, specifically functional groups and spatiotemporal overlap, helped to explain the variable patterns of infection and exposure among species.Synthesis and applications. Our results shed light on ecological drivers of anthrax infection and suggest that soil alkalinity and prolonged droughts or rains are useful predictors of disease occurrence that could guide risk-based surveillance. These insights should inform strategies for managing anthrax including prophylactic livestock vaccination, timing of public health warnings and antibiotic provision in high-risk areas. However, this research highlights the need for greater surveillance (environmental, serological and case-detection-orientated) to determine the mechanisms underlying anthrax dynamics.

Climate extremes promote fatal co-infections during canine distemper epidemics in African lions.

Extreme climatic conditions may alter historic host-pathogen relationships and synchronize the temporal and spatial convergence of multiple infectious agents, triggering epidemics with far greater mortality than those due to single pathogens. Here we present the first data to clearly illustrate how climate extremes can promote a complex interplay between epidemic and endemic pathogens that are normally tolerated in isolation, but with co-infection, result in catastrophic mortality. A 1994 canine distemper virus (CDV) epidemic in Serengeti lions (Panthera leo) coincided with the death of a third of the population, and a second high-mortality CDV epidemic struck the nearby Ngorongoro Crater lion population in 2001. The extent of adult mortalities was unusual for CDV and prompted an investigation into contributing factors. Serological analyses indicated that at least five "silent" CDV epidemics swept through the same two lion populations between 1976 and 2006 without clinical signs or measurable mortality, indicating that CDV was not necessarily fatal. Clinical and pathology findings suggested that hemoparsitism was a major contributing factor during fatal epidemics. Using quantitative real-time PCR, we measured the magnitude of hemoparasite infections in these populations over 22 years and demonstrated significantly higher levels of Babesia during the 1994 and 2001 epidemics. Babesia levels correlated with mortalities and extent of CDV exposure within prides. The common event preceding the two high mortality CDV outbreaks was extreme drought conditions with wide-spread herbivore die-offs, most notably of Cape buffalo (Syncerus caffer). As a consequence of high tick numbers after the resumption of rains and heavy tick infestations of starving buffalo, the lions were infected by unusually high numbers of Babesia, infections that were magnified by the immunosuppressive effects of coincident CDV, leading to unprecedented mortality. Such mass mortality events may become increasingly common if climate extremes disrupt historic stable relationships between co-existing pathogens and their susceptible hosts.

Exploring reservoir dynamics: a case study of rabies in the Serengeti ecosystem.

Knowledge of infection reservoir dynamics is critical for effective disease control, but identifying reservoirs of multi-host pathogens is challenging. Here, we synthesize several lines of evidence to investigate rabies reservoirs in complex carnivore communities of the Serengeti ecological region in northwest Tanzania, where the disease has been confirmed in 12 carnivore species.Long-term monitoring data suggest that rabies persists in high-density domestic dog Canis familiaris populations (> 11 dogs km(-2)) and occurs less frequently in lower-density (< 5 dogs km(-2)) populations and only sporadically in wild carnivores.Genetic data show that a single rabies virus variant belonging to the group of southern Africa canid-associated viruses (Africa 1b) circulates among a range of species, with no evidence of species-specific virus-host associations.Within-species transmission was more frequently inferred from high-resolution epidemiological data than between-species transmission. Incidence patterns indicate that spill-over of rabies from domestic dog populations sometimes initiates short-lived chains of transmission in other carnivores.Synthesis and applications. The balance of evidence suggests that the reservoir of rabies in the Serengeti ecosystem is a complex multi-host community where domestic dogs are the only population essential for persistence, although other carnivores contribute to the reservoir as non-maintenance populations. Control programmes that target domestic dog populations should therefore have the greatest impact on reducing the risk of infection in all other species including humans, livestock and endangered wildlife populations, but transmission in other species may increase the level of vaccination coverage in domestic dog populations necessary to eliminate rabies.

The conservation relevance of epidemiological research into carnivore viral diseases in the serengeti.

Recent outbreaks of rabies and canine distemper in wildlife populations of the Serengeti show that infectious disease constitutes a significant cause of mortality that can result in regional extirpation of endangered species even within large, well-protected areas. Nevertheless, effective management of an infectious disease depends critically on understanding the epidemiological dynamics of the causative pathogen. Pathogens with short infection cycles cannot persist in small populations in the absence of a more permanent reservoir of infection. Development of appropriate interventions requires detailed data on transmission pathways between reservoirs and wildlife populations of conservation concern. Relevant data can be derived from long-term population monitoring, epidemic and case-surveillance patterns, genetic analyses of rapidly evolving pathogens, serological surveys, and intervention studies. We examined studies of carnivore diseases in the Serengeti. Epidemiological research contributes to wildlife conservation policy in terms of management of endangered populations and the integration of wildlife conservation with public health interventions. Long-term, integrative, cross-species research is essential for formulation of effective policy for disease control and optimization of ecosystem health.