Abstract

Animals can alter their foraging behavior through associative learning, where an encounter with an essential resource (e.g., food or a reproductive opportunity) is associated with nearby environmental cues (e.g., volatiles). This can subsequently improve the animal’s foraging efficiency. However, when these associated cues are encountered again, the anticipated resource is not always present. Such an unrewarding experience, also called a memory-extinction experience, can change an animal’s response to the associated cues. Although some studies are available on the mechanisms of this process, they rarely focus on cues and rewards that are relevant in an animal’s natural habitat. In this study, we tested the effect of different types of ecologically relevant memory-extinction experiences on the conditioned plant volatile preferences of the parasitic wasp Cotesia glomerata that uses these cues to locate its caterpillar hosts. These extinction experiences consisted of contact with only host traces (frass and silk), contact with nonhost traces, or oviposition in a nonhost near host traces, on the conditioned plant species. Our results show that the lack of oviposition, after contacting host traces, led to the temporary alteration of the conditioned plant volatile preference in C. glomerata, but this effect was plant species-specific. These results provide novel insights into how ecologically relevant memory-extinction experiences can fine-tune an animal’s foraging behavior. This fine-tuning of learned behavior can be beneficial when the lack of finding a resource accurately predicts current, but not future foraging opportunities. Such continuous reevaluation of obtained information helps animals to prevent maladaptive foraging behavior.

Highlights

  • Foraging for resources in a complex environment is a demanding task for animals

  • We determined whether a conditioned preference for a particular plant species was influenced by an extinction experience 10 min after the rewarding experience

  • There was a marginally significant effect of the interaction between plant species and extinction treatment on parasitoid behavior (Figure 2, generalized linear mixed models (GLMMs), X32 = 6.64, P = 0.084), indicating that the effect of the extinction treatments may be different on the two plant species used for conditioning

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Summary

Introduction

Natural environments are highly complex and variable in time and space, which has led to the evolution of behavioral adaptations to optimize foraging efficiency (Raine et al 2006; Hilker and McNeil 2008; Eliassen et al 2009) One such adaptation is associative learning, where an encounter with a resource is associated with the perception of nearby environmental cues, such as the classical example of the sound of a bell signaling food for Pavlov’s dogs (Clark 2004), and bees associating volatiles and colors of flowers with nectar (Hazlett 1994; Dukas 1999a; Menzel 1999; Eisenhardt 2012; Haverkamp and Smid 2020).

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