Effects of experimental exclusion of scavengers from carcasses of anthrax-infected herbivores on Bacillus anthracis sporulation, survival, and distribution

Abstract

Scavenging of anthrax carcasses has long been hypothesized to play a critical role in the production of the infectious spore stage of Bacillus anthracis after host death, though empirical studies assessing this are lacking. We compared B. anthracis spore production, distribution, and survival at naturally occurring anthrax herbivore carcasses that were either experimentally caged to exclude vertebrate scavengers or left unmanipulated. We found no significant effect of scavengers on soil spore density (P > 0.05). Soil stained with terminally hemorrhaged blood and with nonhemorrhagic fluids exhibited high levels of B. anthracis spore contamination (ranging from 10(3) to 10(8) spores/g), even in the absence of vertebrate scavengers. At most of the carcass sites, we also found that spore density in samples taken from hemorrhagic-fluid-stained soil continued to increase for >4 days after host death. We conclude that scavenging by vertebrates is not a critical factor in the life cycle of B. anthracis and that anthrax control measures relying on deterrence or exclusion of vertebrate scavengers to prevent sporulation are unlikely to be effective.

Fig 1

The site of an anthrax-positive zebra carcass that has been experimentally caged from the date of death is shown on the date of death (A) and 4 days later, after substantial bloating and when the cage was removed (B). A closeup of the same carcass (C) better displays the soil saturated with nonhemorrhagic fluid (the blackened disturbed area surrounding the carcass), which exhibited high levels of B. anthracis spore contamination. A carcass that had been slightly opened prior to caging (D) exhibited a larger area of soil saturated with nonhemorrhagic fluid, as well as substantial maggot activity, 4 days after host death.

Fig 2

Numbers of spg plotted on a log scale by days since host death, experimental exclosure (black) or control (red) treatment, and sample area (with panels showing results for soil collected from hemorrhagic-fluid-stained soil, samples of soil unstained by carcass fluid and taken from within 1- and 3-m radii of the carcass, and soil stained by nonhemorrhagic fluid). Each solid line is from a single carcass, with points representing samples. The dashed lines show the GAMM fitted to the data. Carcasses in the exclosure treatment were excluded from vertebrate scavenging up until the second sampling point (4 days after death), while control carcasses were unmanipulated. The asterisks represent a carcass in the exclosure treatment group that had been scavenged for approximately an hour prior to being caged. All carcasses were those of plains zebras, except for one blue wildebeest. All carcasses were on the same soil type, except for one carcass (outlier).