Parasitoid learning: Current knowledge and implications for biological control

Many hymenopterous parasitoids are biological control agents that contribute significant mortality to economically important arthropod pests of agriculture, forestry, and natural ecosystems. These critically important species forage for food, mates and hosts in complex environments, relying on a variety of stimuli including visual, olfactory, tactile and vibrational cues. In these contexts, learning is often key to optimizing fitness. Here we review current knowledge on the associative learning abilities of both immature and adult parasitoids, specifically learning associated with different kinds of stimuli: (i) reward-associated visual cues, such as colors, shapes and damage patterns; (ii) reward-associated chemical cues, including long- and short-range olfactory cues originating from the plant-host complex or from the host itself, as well as exogenous, nonhost-related odors, and (iii) danger-associated chemical cues that can trigger avoidance behavior. We highlight how the inclusion of associative training with visual and olfactory stimuli in mass-rearing protocols might be exploited to enhance the efficiency of biological control agents against a given target pest. We also discuss the genetic, physiological and ecological factors that can impact parasitoid learning and suggest ways they might be manipulated to optimize rearing conditions for biological control objectives.