Season of death, pathogen persistence and wildlife behaviour alter number of anthrax secondary infections from environmental reservoirs.

An important part of infectious disease management is predicting factors that influence disease outbreaks, such as R, the number of secondary infections arising from an infected individual. Estimating R is particularly challenging for environmentally transmitted pathogens given time lags between cases and subsequent infections. Here, we calculated R for Bacillus anthracis infections arising from anthrax carcass sites in Etosha National Park, Namibia. Combining host behavioural data, pathogen concentrations and simulation models, we show that R is spatially and temporally variable, driven by spore concentrations at death, host visitation rates and early preference for foraging at infectious sites. While spores were detected up to a decade after death, most secondary infections occurred within 2 years. Transmission simulations under scenarios combining site infectiousness and host exposure risk under different environmental conditions led to dramatically different outbreak dynamics, from pathogen extinction (R < 1) to explosive outbreaks (R > 10). These transmission heterogeneities may explain variation in anthrax outbreak dynamics observed globally, and more generally, the critical importance of environmental variation underlying host-pathogen interactions. Notably, our approach allowed us to estimate the lethal dose of a highly virulent pathogen non-invasively from observational studies and epidemiological data, useful when experiments on wildlife are undesirable or impractical.

The persistence of time: the lifespan of Bacillus anthracis spores in environmental reservoirs.

Anthrax is a lethal bacterial zoonosis primarily affecting herbivorous wildlife and livestock. Upon host death Bacillus anthracis vegetative cells form spores capable of surviving for years in soil. Anthrax transmission requires host exposure to large spore doses. Thus, conditions that facilitate higher spore concentrations or promote spore survival will increase the probability that a pathogen reservoir infects future hosts. We investigated abiotic and pathogen genomic variation in relation to spore concentrations in surface soils (0-1 cm depth) at 40 plains zebra (Equus quagga) anthrax carcass sites in Namibia. Specifically, how initial spore concentrations and spore survival were affected by seasonality associated with the timing of host mortality, local soil characteristics, and pathogen genomic variation. Zebras dying of anthrax in wet seasons-the peak season for anthrax in Etosha National Park-had soil spore concentrations 1.36 orders of magnitude higher than those that died in dry seasons. No other variables considered affected spore concentrations, and spore survival rates did not differ among sites. Surface soils at these pathogen reservoirs remained culture positive for a range of 3.8-10.4 years after host death. Future research could evaluate if seasonal patterns in spore concentrations are driven by differences in sporulation success or levels of terminal bacteremia.

The roles of environmental variation and parasite survival in virulence-transmission relationships.

Disease outbreaks are a consequence of interactions among the three components of a host-parasite system: the infectious agent, the host and the environment. While virulence and transmission are widely investigated, most studies of parasite life-history trade-offs are conducted with theoretical models or tractable experimental systems where transmission is standardized and the environment controlled. Yet, biotic and abiotic environmental factors can strongly affect disease dynamics, and ultimately, host-parasite coevolution. Here, we review research on how environmental context alters virulence-transmission relationships, focusing on the off-host portion of the parasite life cycle, and how variation in parasite survival affects the evolution of virulence and transmission. We review three inter-related 'approaches' that have dominated the study of the evolution of virulence and transmission for different host-parasite systems: (i) evolutionary trade-off theory, (ii) parasite local adaptation and (iii) parasite phylodynamics. These approaches consider the role of the environment in virulence and transmission evolution from different angles, which entail different advantages and potential biases. We suggest improvements to how to investigate virulence-transmission relationships, through conceptual and methodological developments and taking environmental context into consideration. By combining developments in life-history evolution, phylogenetics, adaptive dynamics and comparative genomics, we can improve our understanding of virulence-transmission relationships across a diversity of host-parasite systems that have eluded experimental study of parasite life history.

Disease or drought: environmental fluctuations release zebra from a potential pathogen-triggered ecological trap.

When a transmission hotspot for an environmentally persistent pathogen establishes in otherwise high-quality habitat, the disease may exert a strong impact on a host population. However, fluctuating environmental conditions lead to heterogeneity in habitat quality and animal habitat preference, which may interrupt the overlap between selected and risky habitats. We evaluated spatio-temporal patterns in anthrax mortalities in a plains zebra (Equus quagga) population in Etosha National Park, Namibia, incorporating remote-sensing and host telemetry data. A higher proportion of anthrax mortalities of herbivores was detected in open habitats than in other habitat types. Resource selection functions showed that the zebra population shifted habitat selection in response to changes in rainfall and vegetation productivity. Average to high rainfall years supported larger anthrax outbreaks, with animals congregating in preferred open habitats, while a severe drought forced animals into otherwise less preferred habitats, leading to few anthrax mortalities. Thus, the timing of anthrax outbreaks was congruent with preference for open plains habitats and a corresponding increase in pathogen exposure. Given shifts in habitat preference, the overlap in high-quality habitat and high-risk habitat is intermittent, reducing the adverse consequences for the population.

DUST-BATHING BEHAVIORS OF AFRICAN HERBIVORES AND THE POTENTIAL RISK OF INHALATIONAL ANTHRAX.

: Anthrax in herbivorous wildlife and livestock is generally assumed to be transmitted via ingestion or inhalation of Bacillus anthracis spores. Although recent studies have highlighted the importance of the ingestion route for anthrax transmission, little is known about the inhalational route in natural systems. Dust bathing could aerosolize soilborne pathogens such as B. anthracis, exposing dust-bathing individuals to inhalational infections. We investigated the potential role of dust bathing in the transmission of inhalational anthrax to herbivorous wildlife in Etosha National Park, Namibia, an area with endemic seasonal anthrax outbreaks. We 1) cultured soils from dust-bathing sites for the presence and concentration of B. anthracis spores, 2) monitored anthrax carcass sites, the locations with the highest B. anthracis concentrations, for evidence of dust bathing, including a site where a zebra died of anthrax on a large dust bath, and 3) characterized the ecology and seasonality of dust bathing in plains zebra ( Equus quagga), blue wildebeest ( Connochaetes taurinus), and African savanna elephant ( Loxodonta africana) using a combination of motion-sensing camera traps and direct observations. Only two out of 83 dust-bath soils were positive for B. anthracis, both with low spore concentrations (≤20 colony-forming units per gram). We also detected no evidence of dust baths occurring at anthrax carcass sites, perhaps due to carcass-induced changes in soil composition that may deter dust bathing. Finally, despite observing some seasonal variation in dust bathing, preliminary evidence suggests that the seasonality of dust bathing and anthrax mortalities are not correlated. Thus, although dust bathing creates a dramatic cloud of aerosolized soil around an individual, our microbiologic, ecologic, and behavioral results in concert demonstrate that dust bathing is highly unlikely to transmit inhalational anthrax infections.

Lethal exposure: An integrated approach to pathogen transmission via environmental reservoirs.

To mitigate the effects of zoonotic diseases on human and animal populations, it is critical to understand what factors alter transmission dynamics. Here we assess the risk of exposure to lethal concentrations of the anthrax bacterium, Bacillus anthracis, for grazing animals in a natural system over time through different transmission mechanisms. We follow pathogen concentrations at anthrax carcass sites and waterholes for five years and estimate infection risk as a function of grass, soil or water intake, age of carcass sites, and the exposure required for a lethal infection. Grazing, not drinking, seems the dominant transmission route, and transmission is more probable from grazing at carcass sites 1-2 years of age. Unlike most studies of virulent pathogens that are conducted under controlled conditions for extrapolation to real situations, we evaluate exposure risk under field conditions to estimate the probability of a lethal dose, showing that not all reservoirs with detectable pathogens are significant transmission pathways.