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.