Enemy-Risk Effects and Bottom-Up Effects
Interactions between top-down and bottom-up pressures have received much attention in broader natural enemy ecology, but specific breakdown of CEs and NCEs has been less common (but see Kaplan & Thaler 2010, 2012; Thaler et al. 2014). A general framework for understanding the role of plant defenses in altering the CE:NCE ratio focuses on the cost-benefit ratio of engaging in anti-enemy behavior. An enemy avoidance behavior that reduces foraging time may have a higher relative cost if food quality is low, leading to a reduction in that behavior and resulting NCEs. The degree to which plant defenses shift the tradeoff between foraging and enemy avoidance can depend on whether the pest is a generalist or specialist (Kaplan et al. 2014). Though a reduction in only NCEs would shift the CE:NCE ratio towards consumptive effects, plant defenses can also affect rates of enemy consumption. Generalist enemies may reduce consumption of a particular prey if plant quality or defenses reduce prey biomass, prey quality, or the chemical cues used by enemies to locate prey (Kersch-Becker et al. 2017).
Bottom-up effects do not always affect anti-enemy behaviors simply by changing the cost-benefit ratio of those behaviors. Additive effects may be possible if pests respond to plant defenses and enemy risk in qualitatively different ways. For example, phytohormones have been shown to reduce aphid population growth, while natural enemies induce production of winged morphs (Kaplan & Thaler 2012). Here, the pathways operate independently, leading to additive effects of anti-enemy behavior and plant defense. In other studies, short-distance dispersal and plant defenses have been shown to interact strongly, with low plant quality and natural enemies synergistically increasing aphid dispersal (Kersch-Becker & Thaler 2015). Additionally, the effects of reduced plant quality and NCEs may occur on longer timescales than CEs. Pests can exploit these longer timescales by engaging in compensatory mechanisms to reduce the overall negative effects. Caterpillars facing predation risk will can their feeding rate but temporarily increase conversion efficiency to maintain a normal growth rate (Thaler et al. 2012). However, this cannot continue forever and may be dependent on the threat duration (Kaplan et al. 2014).
Finally, many biocontrol agents are omnivorous, meaning plant defenses may affect their fitness directly. If high-quality plants increase omnivorous enemy populations, consumption of prey may increase. However, high-quality plants may also reduce the omnivore’s need to forage for prey, reducing per-capita consumptive rates and NCEs. The interactions between plant defenses and natural enemies are numerous, including risk effect pathways and others not discussed here, which have been more thoroughly reviewed elsewhere (Pappas et al. 2017). Due to these complexities, studies aiming to assess enemy-risk effects in the field should consider what interactions with bottom-up effects may occur.