Stink Bug Communication and Signal Detection in a Plant Environment

Abstract

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.

Keywords: Pentatominae stink bugs; biotremology; communication; evolution; host plants; plant-dwelling insects; sensory system; signals; transmission medium.

Figure 1

Schematic drawing showing the signals that are produced in plant–stink bug communication at different spatial scales (i.e., distances).

Figure 2

Specificity of chemical and vibrational signals in four Neotropical stink bugs species. Species-specificity of male sex-pheromone: (1) methyl 2,6,10-trimethyltridecanoate, (2) methyl 2,6,10-trimethyldodecanoate, (3) (2E,4Z)-methyl deca-2,4-dienoate, (4) 7R-β-sesquiphellandrene, (5) trans-(Z)-(4S) bisabolene epoxide, and (6) cis-(Z)-(4S) bisabolene epoxide. Vibratory signals represent female and male calling signals of each species. Time scales are in seconds (s).

Figure 3

Vibratory signals in stink bugs produced by different mechanisms. Examples of abdominal vibration signals, tremulation and percussion signals of a P. maculiventris male, and a buzzing signal produced by an E. heros female. The signals recorded from the loudspeaker membrane (left), and from the plant (right) indicate the influence of the substrate properties on the signal characteristics. Shown are oscillograms of 1–2 pulses or pulse trains with the frequency spectra. New data and new data analysis [64].

Figure 4

Male preference curves for frequency (left) and duration (right) compared to spectrum and duration of female calling song (FCS) and female courtship song (FCrS) signals in N. viridula. Shown are the frequency spectrum (left) and duration (right) of a FCS signal characteristic of the mean frequency and duration for the population, with the proportion of males (N = 23, N = 14) responding to synthesized signals varying in dominant frequency (left) and duration (right), while other signal parameters were kept constant (i.e. at the mean value for the population). New data analysis according to [64].

Figure 5

Central projections and physiological responses of vibratory receptor neurons in stink bugs. The micrograph shows anterograde staining of a single mesothoracic FCO (left) and a group of metathoracic FCO/SGO sensory neurons (right) terminating in the central ganglion. The dashed line outlines the area of the medial ventral association center (mVAC). The dashed vertical line shows the midline of the ganglion (adapted from Nishino et al. 2016, with permission from Springer Nature). Top right are combined drawings of intracellularly stained sensory neurons of N. viridula morphologically corresponding to FCO (left) and SGO (right) afferents. Bottom right recordings are example traces of responses from the neurons projecting to the mesothoracic segment (second) of the central ganglion. The stimuli are 100 ms long sinusoidal vibrations of the indicated frequencies and intensities. The two neurons physiologically correspond to the low-frequency (LFR1; FCO neuron) and the middle-frequency (MFR; SGO neuron) receptor types. The diagram shows mean threshold curves of the middle leg LFR1, MFR, and high-frequency (HFR) receptors physiologically characterized in N. viridula (adapted from Čokl et al. 2006 [63], with permission from Springer Nature, and from [124], with permission from Taylor&Francis Group).

Figure 6

Directional vibratory cues and information coding in the central nervous system of N. viridula. Schematic representation of the setup used to measure the transmission of the female’s calling signals across the stem-stalk node of a plant, a relevant decision point for the searching male (top left). The signals emitted by the female on a leaf were measured at the indicated points (red) on the same (ipsi) and the opposite petiole (contra) using two laser vibrometers. Bottom left is the distribution of time differences (Δt) and RMS amplitude difference (ΔA) of the vibration signals (n = 55) recorded simultaneously at the two points. Values below 0 on the y-axis indicate signals with a higher amplitude on the contralateral stalk. Only the difference in arrival time of signals as they reach the male legs straddling the crossing is a reliable directional cue to the calling female. The diagram on the right shows the effect of a time delay in the onset of leg stimulation on the response latency of eleven thoracic vibratory interneurons of N. viridula. The symbols used indicate the applied configuration of leg stimulation, which is schematized on the left of the diagram. The responses show directional sensitivity (i.e., they depend on the side stimulated first). Dominant is the side with the strongest impact (Adapted from Prešern et al., 2018, [70] with permission).