Insect Odorscapes: From Plant Volatiles to Natural Olfactory Scenes

Abstract

Olfaction is an essential sensory modality for insects and their olfactory environment is mostly made up of plant-emitted volatiles. The terrestrial vegetation produces an amazing diversity of volatile compounds, which are then transported, mixed, and degraded in the atmosphere. Each insect species expresses a set of olfactory receptors that bind part of the volatile compounds present in its habitat. Insect odorscapes are thus defined as species-specific olfactory spaces, dependent on the local habitat, and dynamic in time. Manipulations of pest-insect odorscapes are a promising approach to answer the strong demand for pesticidefree plant-protection strategies. Moreover, understanding their olfactory environment becomes a major concern in the context of global change and environmental stresses to insect populations. A considerable amount of information is available on the identity of volatiles mediating biotic interactions that involve insects. However, in the large body of research devoted to understanding how insects use olfaction to locate resources, an integrative vision of the olfactory environment has rarely been reached. This article aims to better apprehend the nature of the insect odorscape and its importance to insect behavioral ecology by reviewing the literature specific to different disciplines from plant ecophysiology to insect neuroethology. First, we discuss the determinants of odorscape composition, from the production of volatiles by plants (section "Plant Metabolism and Volatile Emissions") to their filtering during detection by the olfactory system of insects (section "Insect Olfaction: How Volatile Plant Compounds Are Encoded and Integrated by the Olfactory System"). We then summarize the physical and chemical processes by which volatile chemicals distribute in space (section "Transportation of Volatile Plant Compounds and Spatial Aspects of the Odorscape") and time (section "Temporal Aspects: The Dynamics of the Odorscape") in the atmosphere. The following sections consider the ecological importance of background odors in odorscapes and how insects adapt to their olfactory environment. Habitat provides an odor background and a sensory context that modulate the responses of insects to pheromones and other olfactory signals (section "Ecological Importance of Odorscapes"). In addition, insects do not respond inflexibly to single elements in their odorscape but integrate several components of their environment (section "Plasticity and Adaptation to Complex and Variable Odorscapes"). We finally discuss existing methods of odorscape manipulation for sustainable pest insect control and potential future developments in the context of agroecology (section "Odorscapes in Plant Protection and Agroecology").

Volatiles of bacteria associated with parasitoid habitats elicit distinct olfactory responses in an aphid parasitoid and its hyperparasitoid

“…Moreover, we have to take into account that often just a fraction of the volatile compounds present in the environment can be detected and subsequently cause a behavioural response in insects (Bruce & Pickett, ). Therefore, insect behaviour does not always reflect complete mVOC profiles, but rather the concentration and ratio of a select number of compounds that are detected by the insects (Conchou et al, ).…”

Adaptive evolution of olfactory degeneration in recently flightless insects

“…While it seems obvious that flight must have generated selective pressure for rapid olfactory transduction (the transformation of olfactory stimuli into action potentials), there is still surprisingly little direct evidence with which to assess this hypothesis (13–17). This lack of research on the evolutionary lability of temporal acuity of olfaction stands in stark contrast to the many studies on the evolution of odor specificity, which demonstrate rapid evolutionary adaptation of the olfactory system to the animals’ chemical environments (13, 18–25).…”

The fate of methyl salicylate in the environment and its role as signal in multitrophic interactions

“…The observation that a substantial fraction of MeSA can partition to aerosol particles is consistent with previous studies (Karl et al, 2008;Liyana-Arachchi et al, 2013), and should be an important focus when investigating signalling among biotic entities. Indeed, MeSA is perceived at the same time and location as many other semiochemicals within an odorscape, by a variety of organisms (Conchou et al, 2019;Xu and Turlings, 2018). Here, MeSA can serve the dual role of a synergetic compound with insect pheromones, for example in facilitating the orientation to a sexual partner (Xu and Turlings, 2018), or antagonistically, by hampering this orientation (Rouyar et al, 2015), depending on the volatile, plant and insect species.…”