Soil ingestion, nutrition and the seasonality of anthrax in herbivores of Etosha National Park

Abstract

Abstract. Anthrax, caused by the bacterium Bacillus anthracis, is a seasonally occurring infectious disease affecting primarily herbivorous wildlife and livestock. The seasonality of anthrax outbreaks varies among locations, making it difficult to develop a single consistent ecological description of this disease. Over 44 years of mortality surveillance, most anthrax cases in Etosha National Park, Namibia are observed in the wet season, although elephants have an anthrax mortality peak in the dry season. Focusing on three host species (plains zebra, Equus quagga; African elephant, Loxodonta africana; and springbok, Antidorcas marsupialis) occupying the endemic anthrax area of Etosha National Park, Namibia, we tested two commonly posited causes of anthrax seasonality in herbivores: increased pathogen exposure due to greater soil contact, and increased host susceptibility due to seasonal nutritional stress. These hypotheses were assessed using fecal sampling and measurement of the percentage of fecal silicates as an index of soil ingestion and fecal nitrogen, phosphorus and crude fiber as nutritional indices. Nutritional quality for all three species was higher in wet than dry seasons. Comparing among wet seasons, nutritional indices showed either a decline in nutrition with increasing rainfall or no significant pattern. All three species had greater soil ingestion in the wet season than the dry season. Higher soil contact during the anthrax peak suggests that anthrax seasonality may in part be due to heightened exposure to B. anthracis in wet seasons, for zebra and springbok. Elephant anthrax deaths do not correspond with the season of increased soil ingestion or grazing, suggesting that other behavioral mechanisms may overshadow foraging-based risk factors for this species. Nutritional stress is unlikely the primary causative factor in wet season anthrax systems, although nutritional stress sufficient to reduce resistance is difficult to assess non-invasively in wild herbivores. In contrast, increased soil ingestion may be an important predisposing factor for wet season anthrax outbreaks. Ultimately, the amount of soil ingested and its importance in the transmission of soil-borne pathogens will vary based on foraging behaviors, intake rates, grassland structure and on the likelihood that foraging areas intersect with pathogen aggregations in the environment.

Gastrointestinal helminths may affect host susceptibility to anthrax through seasonal immune trade-offs

“…Previous work in ENP has demonstrated that ungulates ingest significantly more soil in the wet season, likely leading to increased exposure to B. anthracis at that time [27]. In support of this, we found that anti-PA titer prevalence was significantly, positively related to rainfall in the PA GEE ( Figure 3B), likely reflecting this increased exposure to B. anthracis during the wet season, with a subsequent immune response if hosts are exposed to sublethal doses [32].…”

“…These new helminth infections are constrained to the wet season; the eggs and larvae require for survival moisture and moderate temperatures over the 1-2 week period of development in the external environment before they become infectious to new hosts [23,24]. The wet season is also when ENP plains ungulates experience annual outbreaks of anthrax, a bacterial infection caused by the ingestion of Bacillus anthracis spores from the environment [25,26]; zebra account for 52% of all anthrax cases in ENP, and 57% of all anthrax cases occur in March and April at the middle and end of the rainy season [27]. The reasons for anthrax seasonality, however, are not yet understood.…”

“…There is as yet no definitive evidence that anthrax can multiply in the soil in natural systems [25]; though see [29,30], and thus anthrax spore levels likely do not increase under seasonal conditions. Given the endemic nature of anthrax in ENP, the prolonged survival times of spores in the environment [28,31], the fact that anthrax deaths and sublethal infections do occur throughout the year in this system [32], it is likely that animals come into contact with anthrax spores in all seasons, though some hosts may also ingest more B. anthracis in soil during wetter times [27]. While multiple factors are likely involved in the timing of anthrax outbreaks, we hypothesize that seasonal changes in host coinfection and immune factors may influence host susceptibility to this environmental pathogen.…”

Effects of Experimental Exclusion of Scavengers from Carcasses of Anthrax-Infected Herbivores on Bacillus anthracis Sporulation, Survival, and Distribution

“…Blowflies have been suspected to play an important role in anthrax transmission in Kruger National Park, South Africa, because of their propensity to ingest material at carcass sites and then regurgitate it on vegetation at heights preferred by the browsing species most frequently infected in that system (36,37). In ENP, however, while we observed similar blowfly feeding preferences (but far fewer flies), the outbreaks occur primarily in grazers and appear more likely to be due to the direct ingestion of contaminated soil (6,20).…”

“…The resulting vegetative cells rapidly reproduce in the blood and produce toxins, killing the host within days (3)(4)(5). Along with exposure-related host behavior, species variation in lethal doses, and individual-specific variation in immunity, spore production (i.e., sporulation) and survival play a critical role in anthrax transmission (1,5,6).…”