Exposure and immunity to generalist pathogens differ among host species and vary across spatial scales. Anthrax, caused by a multi-host bacterial pathogen, Bacillus anthracis , is enzootic in Kruger National Park (KNP), South Africa and Etosha National Park (ENP), Namibia. These parks share many of the same potential host species, yet the main anthrax host in one (greater kudu ( Tragelaphus strepsiceros ) in KNP and plains zebra ( Equus quagga ) in ENP) is only a minor host in the other. We investigated species and spatial patterns in anthrax mortalities, B. anthracis exposure, and the ability to neutralize the anthrax lethal toxin to determine if observed host mortality differences between locations could be attributed to population-level variation in pathogen exposure and/or immune response. Using serum collected from zebra and kudu in high and low incidence areas of each park (18- 20 samples/species/area), we estimated pathogen exposure from anti-protective antigen (PA) antibody response using enzyme-linked immunosorbent assay (ELISA) and lethal toxin neutralization with a toxin neutralization assay (TNA). Serological evidence of pathogen exposure followed mortality patterns within each system (kudus: 95% positive in KNP versus 40% in ENP; zebras: 83% positive in ENP versus 63% in KNP). Animals in the high-incidence area of KNP had higher anti-PA responses than those in the low-incidence area, but there were no significant differences in exposure by area within ENP. Toxin neutralizing ability was higher for host populations with lower exposure prevalence, i.e., higher in ENP kudus and KNP zebras than their conspecifics in the other park. These results indicate that host species differ in their exposure to and adaptive immunity against B. anthracis in the two parks. These patterns may be due to environmental differences such as vegetation, rainfall patterns, landscape or forage availability between these systems and their interplay with host behavior (foraging or other risky behaviors), resulting in differences in exposure frequency and dose, and hence immune response.
more »
« less
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.
more »
« less
- NSF-PAR ID:
- 10260016
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 288
- Issue:
- 1952
- ISSN:
- 0962-8452
- Page Range / eLocation ID:
- 20210582
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
more » « less
Abstract Environmental factors are common forces driving infectious disease dynamics. We compared interannual and seasonal patterns of anthrax infections in two multihost systems in southern Africa: Etosha National Park, Namibia, and Kruger National Park, South Africa. Using several decades of mortality data from each system, we assessed possible transmission mechanisms behind anthrax dynamics, examining (1) within‐ and between‐species temporal case correlations and (2) associations between anthrax mortalities and environmental factors, specifically rainfall and the Normalized Difference Vegetation Index (NDVI), with empirical dynamic modeling. Anthrax cases in Kruger had wide interannual variation in case numbers, and large outbreaks seemed to follow a roughly decadal cycle. In contrast, outbreaks in Etosha were smaller in magnitude and occurred annually. In Etosha, the host species commonly affected remained consistent over several decades, although plains zebra (
Equus quagga ) became relatively more dominant. In Kruger, turnover of the main host species occurred after the 1990s, where the previously dominant host species, greater kudu (Tragelaphus strepsiceros ), was replaced by impala (Aepyceros melampus ). In both parks, anthrax infections showed two seasonal peaks, with each species having only one peak in a year. Zebra, springbok (Antidorcas marsupialis ), wildebeest (Connochaetes taurinus ), and impala cases peaked in wet seasons, while elephant (Loxodonta africana ), kudu, and buffalo (Syncerus caffer ) cases peaked in dry seasons. For common host species shared between the two parks, anthrax mortalities peaked in the same season in both systems. Among host species with cases peaking in the same season, anthrax mortalities were mostly synchronized, which implies similar transmission mechanisms or shared sources of exposure. Between seasons, outbreaks in one species may contribute to more cases in another species in the following season. Higher vegetation greenness was associated with more zebra and springbok anthrax mortalities in Etosha but fewer elephant cases in Kruger. These results suggest that host behavioral responses to changing environmental conditions may affect anthrax transmission risk, with differences in transmission mechanisms leading to multihost biseasonal outbreaks. This study reveals the dynamics and potential environmental drivers of anthrax in two savanna systems, providing a better understanding of factors driving biseasonal dynamics and outbreak variation among locations. -
Background The distribution of resources can affect animal range sizes, which in turn may alter infectious disease dynamics in heterogenous environments. The risk of pathogen exposure or the spatial extent of outbreaks may vary with host range size. This study examined the range sizes of herbivorous anthrax host species in two ecosystems and relationships between spatial behavior and patterns of disease outbreaks for a multi-host environmentally transmitted pathogen. Methods We examined range sizes for seven host species and the spatial extent of anthrax outbreaks in Etosha National Park, Namibia and Kruger National Park, South Africa, where the main host species and numbers of cases differ. We evaluated host range sizes using the local convex hull method at different temporal scales, within-individual temporal range overlap, and relationships between ranging behavior and species contributions to anthrax cases in each park. We estimated the spatial extent of annual anthrax mortalities and evaluated whether the extent was correlated with case numbers of a given host species. Results Range size differences among species were not linearly related to anthrax case numbers. In Kruger the main host species had small range sizes and high range overlap, which may heighten exposure when outbreaks occur within their ranges. However, different patterns were observed in Etosha, where the main host species had large range sizes and relatively little overlap. The spatial extent of anthrax mortalities was similar between parks but less variable in Etosha than Kruger. In Kruger outbreaks varied from small local clusters to large areas and the spatial extent correlated with case numbers and species affected. Case numbers of secondary host species with larger range sizes were positively correlated with the spatial extent of outbreaks in both parks. Conclusions Our results provide new information on the spatiotemporal structuring of ranging movements of anthrax host species in two ecosystems. The results linking anthrax dynamics to host space use are correlative, yet suggest that, though partial and proximate, host range size and overlap may be contributing factors in outbreak characteristics for environmentally transmitted pathogens.more » « less
-
more » « less
Abstract Movement behavior is an important contributor to habitat selection and its incorporation in disease risk models has been somewhat neglected. The habitat preferences of host individuals affect their probability of exposure to pathogens. If preference behavior can be incorporated in ecological niche models (ENMs) when data on pathogen distributions are available, then variation in such behavior may dramatically impact exposure risk. Here we use data from the anthrax endemic system of Etosha National Park, Namibia, to demonstrate how integrating inferred movement behavior alters the construction of disease risk maps. We used a Maximum Entropy (MaxEnt) model that associated soil, bioclimatic, and vegetation variables with the best available pathogen presence data collected at anthrax carcass sites to map areas of most likely
Bacillus anthracis (the causative bacterium of anthrax) persistence. We then used a hidden Markov model (HMM) to distinguish foraging and non-foraging behavioral states along the movement tracks of nine zebra (Equus quagga ) during the 2009 and 2010 anthrax seasons. The resulting tracks, decomposed on the basis of the inferred behavioral state, formed the basis of step-selection functions (SSFs) that used the MaxEnt output as a potential predictor variable. Our analyses revealed different risks of exposure during different zebra behavioral states, which were obscured when the full movement tracks were analyzed without consideration of the underlying behavioral states of individuals. Pathogen (or vector) distribution models may be misleading with regard to the actual risk faced by host animal populations when specific behavioral states are not explicitly accounted for in selection analyses. To more accurately evaluate exposure risk, especially in the case of environmentally transmitted pathogens, selection functions could be built for each identified behavioral state and then used to assess the comparative exposure risk across relevant states. The scale of data collection and analysis, however, introduces complexities and limitations for consideration when interpreting results. -
Bacillus anthracis , the etiological agent of anthrax, is a well-established model organism. For B. anthracis and most other infectious diseases, knowledge regarding transmission and infection parameters in natural systems, in large part, comprises data gathered from closely controlled laboratory experiments. Fatal, natural anthrax infections transmit the bacterium through new host−pathogen contacts at carcass sites, which can occur years after death of the previous host. For the period between contact and death, all of our knowledge is based upon experimental data from domestic livestock and laboratory animals. Here we use a noninvasive method to explore the dynamics of anthrax infections, by evaluating the terminal diversity of B. anthracis in anthrax carcasses. We present an application of population genetics theory, specifically, coalescence modeling, to intrainfection populations of B. anthracis to derive estimates for the duration of the acute phase of the infection and effective population size converted to the number of colony-forming units establishing infection in wild plains zebra ( Equus quagga ). Founding populations are small, a few colony-forming units, and infections are rapid, lasting roughly between 1 d and 3 d in the wild. Our results closely reflect experimental data, showing that small founding populations progress acutely, killing the host within days. We believe this method is amendable to other bacterial diseases from wild, domestic, and human systems.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rspb.2021.0582
