Abstract

Simple SummaryPlant-dwelling stink bugs communicate with chemical and plant-borne vibratory signals that are altered when transmitted through the substrate and air. Mates are attracted to the same plant by pheromones, where they exchange information through mechanical and close-range chemical signals. Plants absorb odor molecules from insects and produce kairomones that can enhance or reduce insect responses to pheromones. Long-range communication between stink bug mates in the field occurs exclusively via pheromones. The species specificity of the sex-pheromones guarantees their success in finding mates in the plant environment. Substrate-borne communication occurs in a narrow frequency range that is tuned to the mechanical properties of the plant. Vibratory signals are transmitted with low attenuation and with altered frequency, amplitude, and temporal characteristics. The frequency sensitivity of the subgenual organ is tuned to the low-frequency resonant properties of the plants. Recognition is encoded in the vibratory signal species- and sex-specific temporal parameters and directionality in the time delay between signals arriving from different directions. The characteristics of behaviorally described multimodal close-range communication on a plant are under-investigated. Studies of neuronal processing of multimodal sensory signals in the stink bug brain are needed to understand how their integration affects behavioral responses. Plants influenced the evolution of plant-dwelling stink bugs’ systems underlying communication with chemical and substrate-borne vibratory signals. Plant volatiles provides cues that increase attractiveness or interfere with the probability of finding a mate in the field. Mechanical properties of herbaceous hosts and associated plants alter the frequency, amplitude, and temporal characteristics of stink bug species and sex-specific vibratory signals. The specificity of pheromone odor tuning has evolved through highly specific odorant receptors located within the receptor membrane. The narrow-band low-frequency characteristics of the signals produced by abdomen vibration and the frequency tuning of the highly sensitive subgenual organ vibration receptors match with filtering properties of the plants enabling optimized communication. A range of less sensitive mechanoreceptors, tuned to lower vibration frequencies, detect signals produced by other mechanisms used at less species-specific levels of communication in a plant environment. Whereas the encoding of frequency-intensity and temporal parameters of stink bug vibratory signals is relatively well investigated at low levels of processing in the ventral nerve cord, processing of this information and its integration with other modalities at higher neuronal levels still needs research attention.

Highlights

  • Most insects spend their life in a plant environment

  • Receptor organs with specific morphology and function are described as constitutive elements of the complex multimodal sensory system of the stink bug, which is capable of detecting, encoding, and extracting the information preserved in the parameters of the signals transmitted in the plant environment

  • Recordings from individual sensory neurons during vibration of the legs of N. viridula revealed a group of low-frequency receptor (LFR) neurons characterized by highest frequency sensitivity between 40 and 75 Hz, a phase-coupled response pattern below 150 Hz, response latencies between 10 and 13 ms to 100 Hz vibratory stimuli, and thresholds following the line of equal displacement values around 0.1 μm [117,118] (Figure 5)

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Summary

Introduction

Herbivorous stink bugs of the family Pentatomidae (Heteroptera) represent a well-studied example of how plants determine the evolution of multimodal sexual and mating communication processes at the emitter and receiver sides. Mating behavior and communication have been described in more than 35 stink bug species of the subfamily Pentatominae [13,14,15]. The present review aims to highlight the key role of plants in the multimodal airborne and substrate-borne communication of stink bugs in the field. Receptor organs with specific morphology and function are described as constitutive elements of the complex multimodal sensory system of the stink bug, which is capable of detecting, encoding, and extracting the information preserved in the parameters of the signals transmitted in the plant environment. We present mechanisms of central nervous processing of vibratory signals that shape the stink bug’s orientation and recognition behavior on a plant

Long-Range Sex Pheromone Communication in Stink Bugs in a Plant Environment
Multimodal Communication on a Plant
Plants as the Vibratory Signal Transmission Medium
The Effect of Noise on Signal Transmission on Plants
Detection of Vibratory Signals on a Plant
Vibration Receptor Organs
Central Projections of the Vibration Receptor Neurons
Processing of Vibratory Input in the Ventral Nerve Cord
Frequency and Time Pattern Coding in Ventral Nerve Cord Neurons
Neuronal Basis of Vibrational Directionality and Mate Recognition on a Plant
Findings
Concluding Remarks
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