Learned predators enhance biological control via organizational upward and trophic top-down cascades

Learning is a behavioural change based on memory of previous experiences and a ubiquitous phenomenon in animals. Learning effects are commonly life-stage- and age-specific. In many animals, early life experiences lead to pervasive and persistent behavioural changes. There is broad consensus that learning has far-reaching implications to biological control. Proximate and ultimate factors of individual learning by parasitoids and true predators are relatively well understood, yet the consequences of learning to higher organizational levels, populations and communities, and top-down trophic cascades are unexplored. We addressed this issue using a tri-trophic system consisting of predatory mites Amblyseius swirskii, Western flower thrips Frankliniella occidentalis and whole common bean plants, Phaseolus vulgaris. F. occidentalis are notorious horticultural pests that are difficult to control. Therefore, practitioners have much to gain by optimizing biological control of thrips. Previous studies have shown that early life experience of thrips by A. swirskii improves foraging on thrips later in life due to decreased prey recognition times and increased predation rates, together enhancing predator fecundity. Here, we hypothesized that early learning by A. swirskii enhances biological control of thrips via immediate and cascading effects. We predicted that release of thrips-experienced predators enhances predator population growth and thrips suppression and reduces plant damage as compared to release of thrips-naive predators. The behavioural changes brought about by early learning cascaded up to the population and community levels. Thrips-experienced predators caused favourable immediate and cascading effects that could not be compensated for in populations founded by thrips-naive predators. Populations founded by thrips-experienced predators grew faster, reached higher abundances, were more efficacious in suppressing an emerging thrips population and kept plant damage at lower levels than populations founded by thrips-naive predators. Plant fecundity correlated negatively with thrips abundance and positively with predatory mite abundance. Improved biological control was mainly due to thrips-experienced founders providing for a head-start in predator population growth and thrips suppression. Synthesis and applications. Our study suggests that learned natural enemies have high potential to optimize augmentative biological control on a larger scale due to favourably modulating organizational upward and trophic top-down cascades.