Evaluating the role of North American scavengers in the transmission of chronic wasting disease prions to cervids

Abstract

Many scavenging species have been categorized as pests or potential disease vectors, and as a result, management actions toward scavengers are frequently focused on removal. However, scavengers can play important ecological roles, and there is a growing need to define their impact on ecological systems and processes. In the context of disease ecology, their influence is inherently complex, as their interactions at and with carcasses can either mitigate or facilitate the pathogen transmission. Chronic wasting disease (CWD) is a transmissible prion disease afflicting cervids – a taxon that is important to multiple stakeholders. The disease is invariably fatal, and prions persist in the environment for years. Scavengers have been implicated in CWD transmission due to their interactions with infected carcasses, and recent studies have begun to quantify the extent of their involvement. In Chapter 1, we explored scavenger activities at 20 cervid carcasses in northern Colorado, USA using data gathered from camera traps from January 2022 to May 2023. Specifically, we characterized the species community at cervid carcasses, described carcass utilization patterns, identified landscape factors associated with scavenger diversity at carcass sites, and determined correlates of scavenger foraging duration. Black-billed magpies (Pica hudsonia) and coyotes (Canis latrans) comprised 63.9% of species detections at carcasses. We found that site-level species diversity decreased as human modifications to the landscape increased and foraging bout duration decreased as carcasses aged and as temperatures increased. Foraging time at carcasses varied by species, with common ravens (Corvus corax) and black bears (Ursus americanus) spending the greatest time foraging on carcasses. While observability of carcass tissues consumed was limited, we found that most scavengers consumed muscle (tissue with relatively low prion loads), except for turkey vultures (Cathartes aura) who preferred abdominopelvic cavity organs. This chapter underscores the complex interplay between temporal, environmental, and species-specific factors in determining scavengers' role in transmission dynamics, with broader implications for understanding the cascading effects of scavenger activity on ecosystem health. In Chapter 2, we explored the contributions of coyotes to CWD epidemiology. This species is of particular interest in this system given their ubiquity across North America, proclivity for scavenging from cervid carcasses, and the retention of prion infectivity post-passage by coyotes. To further quantify coyotes' role in CWD ecology, we conducted controlled feeding experiments to examine the fate of three concentrations of CWD prions post-passage through the digestive tracts of eight adult coyotes. We utilized real-time quaking induced conversion (RT-QuIC) to serially determine the relative amount of prions in coyote feces after three levels of exposure: low (0.1% [4 Log10LD50/g] CWD positive brain homogenate [BH]), moderate (1% [6 Log10LD50/g] CWD positive BH), and high (10% [8 Log10LD50/g] CWD positive BH). We found that coyotes are remarkably efficient neutralizers of CWD; we recovered less than 1% of ingested prions from fecal samples across all tested exposure levels. Additionally, we found no evidence of prion seeding activity in the tissues of study animals after necropsy, indicating that coyotes neutralize, rather than sequester, ingested prions. Our findings demonstrate that coyotes provide an important ecosystem service by consuming CWD-positive tissues, effectively mitigating the environmental accumulation of one of the most environmentally robust pathogens known at carcass sites.