Constitutive exposure to the volatile methyl salicylate reduces per‐capita foraging efficiency of a generalist predator to learned prey associations

Abstract

Understanding the factors that influence the ability of predators to find and kill herbivores is central to enhancing their impact on prey populations, but few studies have tested the impact of these factors on predation rates in realistic foraging environments. Using the tri‐trophic system consisting of tomato, Solanum lycopersicum L. (Solanaceae), hornworm caterpillars, Manduca sexta L. (Lepidoptera: Sphingidae), and the predaceous stink bug Podisus maculiventris (Say) (Hemiptera: Pentatomidae), we measured the effects of associative learning and plant volatile camouflage on predator behavior and foraging efficiency in field enclosures. To do so, we compared experienced vs. naive individuals under varying environmental contexts. Experienced predators were those with prior exposure to induced volatiles from the tomato–caterpillar association, whereas naive predators had not experienced tomato, only prey (caterpillars). We varied their environmental foraging matrix using either (1) tomato surrounded by basil (Ocimum basilicum L.; Lamiaceae) or (2) tomato exposed to the synthetic volatile, methyl salicylate (MeSA). We found that (1) experienced predators were more efficient than naive 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. These differences corresponded with distinct shifts in predator foraging; for example, experienced individuals were less stationary and exhibited unique behaviors such as stylet extension. Taken together, these results suggest that it is possible to improve the function of generalist predators in suppressing prey by coupling odors with food. However, constitutive emission of volatiles to attract natural enemies may ultimately camouflage neighboring plants, reducing the benefits of orientation to learned stimuli such as induced volatiles.

Methyl Salicylate Can Benefit Ornamental Pest Control, and Does Not Alter Per Capita Predator Consumption at Close-Range

“…Puente et al's (2008) model predicts that once a natural enemy is in the vicinity, there is a possibility that synthetic HIPVs will saturate the system and interfere with its search for pests. This is supported by a field cage study where synthetic MeSA lures near tomatoes reduced per capita predation by a stink bug (Vidal-Gomez et al, 2018). Yet, other HIPVs have suggested the opposite effect.…”

“…However, another study that examined per capita predator efficiency found a negative impact. The number of Podisus maculiventris (Say) (Hemiptera: Pentatomidae) nymphs observed on plants was 26% lower and predation on caterpillars was 22% lower on tomatoes caged with MeSA than untreated tomatoes (Vidal-Gomez et al, 2018). The constitutive emission of MeSA was suggested to camouflage necessary odors and reduce predator efficiency.…”

“…Podisus maculiventris and C. rufilabris were lab-reared while the others were field-collected. Both naïve and experienced P. maculiventris fed less in the presence of MeSA (Vidal-Gomez et al, 2018). The lady beetles would be considered experienced since they were maintained on aphid-infested plants that may have produced various HIPVs.…”

The threat of parasitism impairs immune function in host caterpillars

“…P. maculiventris is a generalist omnivore, native to North America, that consumes soft‐bodied insects and plant phloem (Thaler et al, 2012). They are also reared as a biological control agent for larval insect pests and known to attack M. sexta (Kelly et al, 2012; Vidal‐Gomez et al, 2018). C. congregata is a gregarious parasitoid that prefers ovipositing in the 2nd and 3rd larval instars of their host.…”

“…They were provided with bean plants, and water and were given mealworms ( Tenebrio molitor L.) as a prey source twice a week. More thorough explanations of insect colony husbandry and origin are described in Garvey et al (2020) for M. sexta / C. congregata and Vidal‐Gomez et al (2018) for P. maculiventris so a brief description is provided above.…”