Enemy-Risk Effects in Space
At smaller spatial scales, enemy risk may alter microhabitat use as pests seek refuges or move to lower-quality parts of the plant (Lee et al. 2011; Paterson et al. 2013; Calvet et al. 2018). Pest fitness may be affected by decreased foraging time due to refuge use or consistent foraging on lower-quality resources. Some pests, particularly aphids, will drop off a plant in response to enemy risk (Humphreys & Ruxton 2019). This behavior incurs significant costs, as dropping reduces feeding time (Nelson & Rosenheim 2006; Nelson 2007). It may also expose pests to a new set of mortality sources, such as ground-dwelling enemies or increased exposure to extreme temperatures. Conversely, increased refuge use due to enemy risk may decrease pesticide exposure (Jallow & Hoy 2005; Martini et al. 2012). Additionally, shifts in microhabitat use by pests may reduce the reliability of field sampling methods based on inspections of certain parts of the plant (R. E. Southwood & Henderson 2000).
At larger spatial scales, enemies may influence pest dispersal and habitat selection at within-field and between-field scales. Foraging models, such as the Ideal Free Distribution (IFD), are often used to predict pest movement and abundance within a patchy habitat, but the inclusion of mobile enemies and prey perception of enemies can drastically alter those predictions (Sih et al. 1998; Brown & Kotler 2004; Fraker & Luttbeg 2012). Natural enemies can change the threshold at which pests disperse, either increasing dispersal by making patches riskier, or decreasing dispersal by making the movement between patches riskier (Sih & Wooster 1994; Hammill et al. 2015). Modeling work has shown that this can lead to seemingly counterintuitive results at the metapopulation level; if prey immigration is not affected by enemy presence, but emigration is reduced by it, then prey density can be higher in patches with enemies. Whether or not natural enemy distributions match the distributions of their prey can depend on mobility of the pests and enemies, the resource needs of each, and other density-dependent effects for each population (Winder et al. 2001; Nachman 2006; Pearce & Zalucki 2006). In general, understanding how natural enemies affect spatial patterns of pest abundance, such as higher density near field borders, may allow for more precise pest sampling and pesticide spraying, increasing the efficacy and cost effectiveness of these methods. Boxes 5, 6, and 7 all describe particular cases in which enemy-induced dispersal aids or hinders specific pest management goals, including disease transmission, pesticide resistance, and trap-cropping.
Arthropod movement between fields is of particular interest when considering field-scale implementation of biocontrol. Under a classical biocontrol program, where the goal is typically for an agent to disperse widely and match the pest range, enemy-induced dispersal may not be a cause for alarm, as the enemy would be predicted to follow its prey. However, if enemy dispersal does not match pest dispersal, certain augmentative biocontrol releases may simply result in the pest problem being pushed from one farm to another. For example, flightless morphs of ladybeetles have been shown to control aphid populations more effectively due to their longer residency time in the crop (Koch 2003). However, some ladybeetles can induce strong increases in alate production (Kaplan & Thaler 2012) and aphid dispersal, potentially exporting the pest problem.
Finally, oviposition site selection can be strongly influenced by enemy presence. Many arthropods can detect enemies when making oviposition choices and prefer low-risk sites (Kraus & Vonesh 2010; Livingston et al. 2017), which may lead to heterogeneous patterns within or between fields. If natural enemies are in fields prior to oviposition, they may even completely deter pest establishment, referred to as biotic resistance (Gruner 2005; Wanger et al. 2011). This would be more likely to occur with generalist predators, since their populations may be sustained by other species prior to the arrival of the target pest. Conservation biological control, being most focused on supporting native enemy populations, utilizes biotic resistance most strongly, though any natural enemy with sufficient density prior to pest establishment may help prevent establishment.