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.