Parasite passes through predator
Predators, sloppy or not, tend to ingest many parasites along with prey tissues (Johnson et al. 2010). In many cases, these parasites are able to infect the predator and often this trophic transmission is obligatory for their life cycle (Lafferty 1999; Kuris 2003, 2005). However, many parasites are simply digested or, if they are more resilient, pass through the predator digestive tract and are excreted (e.g., fungal pathogens of Daphnia passing through fish guts or viral pathogens of spongy moths (Lymantria dispar ) passing through avian guts; Duffy 2009; Reilly & Hajek 2012). Because many predators are larger and range more widely than their prey, this process of viable parasites passing through predators should promote the spreading of parasites to a larger number of prey over a wider spatial area and could even allow transmission between discrete prey populations.
Parasite resilience is the primary factor that facilitates this type of predator spreading as surviving the potentially harrowing passage through the predator gut is strictly necessary. Whether this condition is met is likely due to a combination of attributes of the parasite (e.g., a digestion-resistant spore) and the predator (e.g., the pH of the digestive tract). If a parasite survives gut passage, predator and prey behavior then interact to determine whether this increases transmission. As noted above, if predators use more space than their prey, then parasites passing through predators should typically increase parasite transmission. However, several factors likely modulate this predator-spreading effect. If prey preferentially avoid predator excrement (Apfelbach et al. 2005; Weinstein et al. 2018a), that should reduce transmission. In contrast, if prey seek out excrement for the nutrients it provides (Weinstein et al. 2018b), this behavior should promote predator-spreading. Moreover, the form in which predators release feces (e.g., in a compact form such as a fecal pellet vs. more diffuse feces; Fig. 2c) is likely to have an impact, though which type of feces leads to parasite spreading likely depends on multiple factors, including the nature of the habitat and prey behavior. For example, in a stratified lake where the prey are filter feeders (e.g., Daphnia ), if predators release diffuse feces that contains infectious transmission stages, those transmission stages might be more likely to stay suspended in the water column where they can be taken up by a new prey individual. In contrast, in a terrestrial environment, the nutrients in more densely packed predator feces increase primary production, attracting prey. In such a system, those compact feces should increase parasite transmission.
The dose-infectivity relationship is also likely to be important (Clayet al. 2021). In cases where the dose-infectivity curve is decelerating, the infectivity of each propagule decreases as they become more abundant. In these cases, the lower parasite densities that would be expected, on average, with diffuse feces might still be sufficient to infect many additional prey (as represented by the dashed line in Fig. 2c). However, if the dose-infectivity curve is accelerating, adding more parasites leads to a greater increase in infections (as compared to a linear relationship where per spore infectivity does not change, and as shown by the solid line in Fig. 2c); in these cases, more concentrated feces might lead to the highest infection levels, though this effect would likely be more geographically restricted. A recent meta-analysis found evidence for accelerating, decelerating, and linear dose-infectivity relationships, but found that decelerating relationships were most common (Clay et al. 2021) – which would mean that predators that release diffuse feces might, on average, be more likely to spread disease, since that feces would cover a wider area while still being infectious.
Study of predator-spreading via parasites passing through predators requires the use of excrement analysis and necropsy of predators to identify parasites of their prey that they excrete but by which they are not infected. Ideally, these studies would seek not only to determine the presence/abundance of the parasite (e.g., via microscopy or molecular approaches), but also whether transmission stages are still viable. If a system has a parasite that survives gut passage and does not infect the predator, then a range of experimental manipulations could be devised to test whether the presence of a predator, or even just the predator’s parasite-laced feces, increases parasite transmission and/or facilitates transmission from one population to another. The role of a predator-spreader in such a system could also be detected using parasite genetic information: if parasites that pass through predators show minimal genetic structure over long distances with respect to prey movement then it is likely that predator-spreading plays a key role in transmission.