Changes in prey behavior
Prey organisms respond behaviorally to predation pressure in a variety
of ways, many of which can increase parasite transmission, leading to
behaviorally mediated predator-spreading. These predator-spreading
behavioral changes are a type of “non-consumptive” or
“trait-mediated” effect of predators on parasites via their prey
(Schmitz et al. 1997, 2000; Preisser et al. 2007; Daversaet al. 2019). Behaviorally mediated effects tend to fall into one
of two categories: (i) increased contact rates between prey individuals
and (ii) decreased parasite avoidance behaviors. Behavioral
predator-spreading is relatively well studied in aquatic systems.
Trinidadian guppies shoal in larger groups when under high predation and
this higher group size increases transmission rates ofGyrodactylus parasites, resulting in higher burdens of this
ectoparasite (Stephenson et al. 2015). Alternatively, wood frog
tadpoles (Lithobates sylvaticus ) increase their active time in
the presence of trematode parasites to avoid infection; however, in the
presence of parasites and predators, they decrease activity to avoid
predation, increasing their susceptibility to trematode infection
(Szuroczki & Richardson 2012). Both these examples share a common
pattern: a prey behavior that impacts parasite transmission is disrupted
or altered by the presence of predators.
Behaviorally mediated predator spreading should be possible in many
systems where prey alter behavior substantially in response to
predators, and a few types of identifiable behavior modifications are
most suspect. Any prey that displays conflicting parasite avoidance and
predator avoidance behavior is likely to sacrifice one for the other
when confronted with both natural enemies (Weinstein et al.2018a). Alternatively, predator response behavior that increases prey
group sizes or interaction frequencies should directly increase parasite
transmission through increased contact rates (Anderson & May 1979).
However, system specific knowledge about parasite-prey pairs may
illuminate additional types of predator induced behavior that could
amplify parasitism. Parasite induced behavioral changes are frequently
discussed when they increase predation in trophically transmitted
parasites (Lafferty 1999; Kuris 2003, 2005). Although such behavioral
changes are generally considered maladaptive in non-trophically
transmitted parasites, mechanical predator spreading processes discussed
above may result in a selective pressure for parasite behavior
manipulation even in non-trophically transmitted parasites.
Behaviorally mediated predator-spreading has been reasonably well
studied in aquatic systems but relatively unstudied in terrestrial
systems. However, similar behavioral changes could result in increased
parasitism in terrestrial systems. For example, the beetleLeptinotarsa decemlineata is attacked by predators above ground
but parasites belowground (Ramirez & Snyder 2009); if beetles shift
habitat use in response to predator cues, this behavior should increase
parasitism. For example, an aphid (Microlophium carnosum )
experiences increased parasitism by a fungal pathogen (Pandora
neoaphidis ) at the population level in the presence of coccinellid
predators (Baverstock et al. 2009). When aphids perceive
potential predators they flee by dropping from their host plant and
subsequently colonizing the same or another plant. This process exposes
the aphids to substantially more leaf surface area and therefore fungal
spores than if they remained on a single leaf (Baverstock et al.2008).
Researchers could specifically target systems where predator presence
substantially alters prey space-use behavior or contact networks to test
the downstream effects on parasitism. Regardless of the system, it is
extremely important to appropriately measure behavioral changes due to
predator presence in a way that relates directly to how those behaviors
may affect transmission.