Associative Learning of the Generalist Predator Podisus maculiventris to Herbivore-Induced Plant Volatiles

Ulianova Vidal-Gomez, Purdue University

Abstract

Following herbivore attack, plants produce volatile organic compounds (HIPVs for herbivore-induced plant volatiles) that allow predators to find and consume herbivores. The generalist predator Podisus maculiventris likely uses HIPVs in its foraging decisions. I hypothesized that the behavioral responses of this predator to HIPVs are acquired via associative learning, as suggested by theoretical predictions linking natural enemy host range with odor preferences. To evaluate P. maculiventris learning capabilities across different levels of biological organization, I use the tri-trophic system consisting of tomato (Solanum lycopersicum ), hornworm caterpillars (Manduca sexta), and the predaceous stinkbug Podisus maculiventris to answer the following questions: (1) Does P. maculiventris innately respond to specific host-plant volatiles? Are P. maculiventris olfactory preferences modified by experience? Specifically, I assessed whether and how this generalist predator acquires preference to host-plant volatiles after being exposed to the HIPV-prey association. First, naïve (i.e., lab reared in colony) and experienced (i.e., field collected) individuals were allowed to choose between scents released by caterpillar (M. sexta) damaged tomato plants vs. undamaged plants. Additionally, conditioned females, a group that previously experienced the tomato plant-M. sexta association, were tested for their preference in field enclosures. I found that only field-collected males showed orientation to odors released by caterpillar-damaged plants and naïve lab-reared individuals showed no preference. When conditioned females were tested in the field, they clearly chose M. sexta damaged plants (Chapter 1). (2) Is P. maculiventris olfactory processing affected by the number of associations/reinforcements, developmental stages and memory? Do naïve predators differ from HIPV-conditioned ones at a neurophysiological level? Here, I trained individual predators to associate a conditioned stimulus (the synthetic HIPV methyl salicylate, or MeSA) with an unconditioned stimulus (hemolymph extracted from the tobacco hornworm M. sexta as food). Subsequently, I assessed adult and nymph preferences toward MeSA. I found that: (1) Conditioned nymphs showed an orientation response to MeSA, whereas adults did not display a strong preference upon conditioning, suggesting that olfactory learning abilities vary with developmental stage, (2) Nymphs that responded positively to MeSA retained this association for ca. 6 days, which indicates long term memory formation, (3) The response of nymphs was the same regardless of the number of volatile-food pairings, and (4) Differences in olfactory processing between nymphs and adults are displayed at a neurophysiological level in the brain information processing centers (Chapter 2). (3) Does learning improve P. maculiventris foraging efficiency in complex odor environments? In this part of the study, I measured the effects of associative learning and plant volatile camouflage on predator behavior and foraging efficiency in field enclosures. To do so, I compared experienced vs. naïve individuals in simple vs. complex environments. “Simple” habitats consisted of tomato alone, whereas “complex” environments were created using either: (1) tomato surrounded by basil, or (2) tomato exposed to the synthetic volatile, methyl salicylate (MeSA). I found that: (1) experienced predators were more efficient than naïve predators, capturing 28% more prey, (2) the tomato-basil combination did not affect predator-prey interactions, and (3) constitutive emission of synthetic MeSA caused a 22% reduction in P. maculiventris predation rate. Additionally, I documented that these ecological differences correspond with distinct shifts in predator foraging behaviors (Chapter 3). Overall, these results not only suggest that associative learning is the mechanism underlying HIPV attraction, but also that P. maculiventris can be conditioned to natural and synthetic HIPVs, specifically, MeSA. This study also enhances our understanding of olfactory processing across predator development, an area that is unexplored in any arthropod species.

Degree

Ph.D.

Advisors

Kaplan, Purdue University.

Subject Area

Entomology

COinS