Vibration receptor organs in the insect leg: neuroanatomical diversity and functional principles.

Detecting substrate vibrations is essential for insects in different behavioural contexts. These vibrational behaviours are mediated by mechanoreceptor organs detecting and processing vibrational stimuli transmitted in the environment. We discuss recently gained insights about the functional principles of insect vibration receptors, mainly leg chordotonal organs highly sensitive to vibrational stimuli, and the mechanisms of their diversification in neuroanatomy and functional morphology, in relation to the attachment structures and mechanical coupling. The two main input pathways for vibration stimuli transferred by the insect legs to vibrosensory organs via the cuticle and via the hemolymph are fundamental for explaining sensory specialisations. The vibroreceptor organs can diversify in their neuroanatomy and morphology in several key aspects. This provides the structural basis for complex adaptations in sensory evolution.

Functional Diversity of Vibrational Signaling Systems in Insects.

Communication by substrate-borne mechanical waves is widespread in insects. The specifics of vibrational communication are related to heterogeneous natural substrates that strongly influence signal transmission. Insects generate vibrational signals primarily by tremulation, drumming, stridulation, and tymbalation, most commonly during sexual behavior but also in agonistic, social, and mutualistic as well as defense interactions and as part of foraging strategies. Vibrational signals are often part of multimodal communication. Sensilla and organs detecting substrate vibration show great diversity and primarily occur in insect legs to optimize sensitivity and directionality. In the natural environment, signals from heterospecifics, as well as social and enemy interactions within vibrational communication networks, influence signaling and behavioral strategies. The exploitation of substrate-borne vibrational signaling offers a promising application for behavioral manipulation in pest control.

Vibration detection in arthropods: Signal transfer, biomechanics and sensory adaptations.

In arthropods, the detection of vibrational signals and stimuli is essential in several behaviours, including mate recognition and pair formation, prey detection, and predator evasion. These behaviours have been studied in several species of insects, arachnids, and crustaceans for vibration production and propagation in the environment. Vibration stimuli are transferred over the animals' appendages and the body to vibrosensory organs. Ultimately, the stimuli are transferred to act on the dendrites of the mechanosensitive sensilla. We refer to these two different levels of transfer as macromechanics and micromechanics, respectively. These biomechanical processes have important roles in filtering and pre-processing of stimuli, which are not carried out by neuronal components of sensory organs. Also, the macromechanical transfer is posture-dependent and enables behavioural control of vibration detection. Diverse sensory organs respond to vibrations, including cuticular sensilla (slit sensilla, campaniform sensilla) and internal chordotonal organs. These organs provide various adaptations, as they occur at diverse body positions with different mechanical couplings as input pathways. Macromechanics likely facilitated evolution of vibrosensory organs at specific body locations. Thus, vibration detection is a highly complex sensory capacity, which employs body and sensory mechanics for signal filtering, amplification, and analysis of frequency, intensity and directionality.

Are all auditory sensilla of bushcrickets bimodal? Comment on: R. D. Zhantiev and O. S. Korsunovskaya, Functions of chordotonal sensilla in bushcrickets (Orthoptera, Tettigoniidae); Entomological Review, 2021, vol. 101 (6), pp. 755-766.

Detection of sound and substrate vibration is crucial for the survival and reproduction of many animals, particularly insects. Bushcrickets (Orthoptera, Tettigoniidae), developed a large mechanosensory organ complex in their legs to detect such stimuli. As demonstrated by various studies in the past, sensilla in distinct functional groups form specialized vibratory organs (the subgenual organ and the accessory organ), respond sensitively to both vibration and sound (in the intermediate organ [IO]), or mediate hearing (in the crista acustica [CA]; the tympanal hearing organ). In their recent publication, Zhantiev and Korsunovskaya addressed auditory and vibratory sensitivity in the IO and the CA in two species of bushcrickets, using single-cell recording and staining of sensory neurons from their soma in an isolated foreleg. Their main finding was that not only the IO but also the complete CA contains bimodal sensilla responding with high sensitivity to both sound and vibration, which would be a true change in the paradigm of how the auditory/vibratory sense in Orthoptera works. In addition, they revealed vibratory tuning of the IO sensilla, which differs largely from that in previous studies. We propose three major experimental causes of such discrepancies: calibration, experiments with isolated legs, and differences in the sites of recording. To judge the causes of these discrepancies more adequately, a detailed comparison of methods and a number of control experiments are needed. This will deepen our understanding of sensory adaptations and specialization of insect mechanosensory organs to stimuli entering the system by different input pathways.

Stink Bug Communication and Signal Detection in a Plant Environment.

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.

Vibrational signalling, an underappreciated mode in cricket communication.

Signalling via substrate vibration represents one of the most ubiquitous and ancient modes of insect communication. In crickets (Grylloidea) and other taxa of tympanate Ensifera, production and detection of acoustic and vibrational signals are closely linked functionally and evolutionarily. Male stridulation produces both acoustic and vibrational signal components, the joint perception of which improves song recognition and female orientation towards the signaller. In addition to stridulation, vibrational signalling mainly through body tremulation and/or drumming with body parts on the substrate has long been known to be part of crickets' close-range communication, including courtship, mate guarding and aggression. Such signalling is typically exhibited by males, independently or in conjunction with stridulation, and occurs literally in all cricket lineages and species studied. It is further also part of the aggressive behaviour of females, and in a few cricket groups, females respond vibrationally to acoustic and/or vibrational signals from males. The characteristics and function of these signals have remained largely unexplored despite their prevalence. Moreover, the communication potential and also ubiquity of cricket vibrational signals are underappreciated, limiting our understanding of the function and evolution of the cricket signalling systems. By providing a concise review of the existing knowledge of cricket perception of vibrations and vibrational signalling behaviour, we critically comment on these views, discuss the communication value of the emitted signals and give some methodological advice respecting their registration and control. The review aims to increase awareness, understanding and research interest in this ancient and widespread signalling mode in cricket communication.

A male-produced aggregation-sex pheromone of the beetle Arhopalus rusticus (Coleoptera: Cerambycidae, Spondylinae) may be useful in managing this invasive species.

The longhorned beetle Arhopalus rusticus (Coleoptera: Cerambycidae, Spondylinae) is a common species in conifer forests of the Northern Hemisphere, but with global trade, it has invaded and become established in New Zealand, Australia, and South America. Arhopalus rusticus is a suspected vector of the phytopathogenic nematode, Bursaphelenchus xylophilus, the causative agent of pine wilt disease, which is a major threat to pine forests worldwide. Here, we report the identification of a volatile, male-produced aggregation-sex pheromone for this species. Headspace odours from males contained a major male-specific compound, identified as (2 S, 5E)-6,10-dimethyl-5,9-undecadien-2-ol (common name (S)-fuscumol), and a minor component (E)-6,10-dimethyl-5,9-undecadien-2-one (geranylacetone). Both compounds are known pheromone components for species in the same subfamily. In field trials in its native range in Slovenia, (S)-fuscumol was significantly more attractive to beetles of both sexes, than racemic fuscumol and a blend of host plant volatiles commonly used as an attractant for this species. Fuscumol-baited traps also caught significant numbers of another spondylidine species, Spondylis buprestoides (L.), and a rare click beetle, Stenagostus rufus (De Geer). The pheromone can be exploited as a cost-effective and environmentally safe tool for detection and monitoring of this invasive species at ports of entry, and for monitoring the beetle's distribution and population trends in both endemic and invasive populations.

Low-frequency vibration transmission and mechanosensory detection in the legs of cave crickets.

Vibrational communication is common in insects and often includes signals with prominent frequency components below 200 Hz, but the sensory adaptations for their detection are scarcely investigated. We performed an integrative study of the subgenual organ complex in Troglophilus cave crickets (Orthoptera: Rhaphidophoridae), a mechanosensory system of three scolopidial organs in the proximal tibia, for mechanical, anatomical and physiological aspects revealing matches to low frequency vibration detection. Microcomputed tomography shows that a part of the subgenual organ sensilla and especially the accessory organ posteriorly in this complex are placed closely underneath the cuticle, a position suited to evoke responses to low-frequency vibration via changes in the cuticular strain. Laser-Doppler vibrometry shows that in a narrow low-frequency range the posterior tibial surface reacts stronger to low frequency sinusoidal vibrations than the anterior tibial surface. This finding suggests that the posterior location of sensilla in tight connection to the cuticle, especially in the accessory organ, is adapted to improve detectability of low-frequency vibration signals. By electrophysiological recordings we identify a scolopidial receptor type tuned to 50-300 Hz vibrations, which projects into the central mechanosensory region specialised for processing low-frequency vibratory inputs, and most likely originates from the accessory organ or the posterior subgenual organ. Our findings contribute to understanding of the mechanical and neuronal basis of low-frequency vibration detection in insect legs and their highly differentiated sensory systems.

The mechanical leg response to vibration stimuli in cave crickets and implications for vibrosensory organ functions.

We investigate the influence of leg mechanics on the vibration input and function of vibrosensitive organs in the legs of the cave cricket Troglophilus neglectus, using laser Doppler vibrometry. By varying leg attachment, leg flexion, and body posture, we identify important influences on the amplitude and frequency parameters of transmitted vibrations. The legs respond best to relatively high-frequency vibration (200-2000 Hz), but in strong dependence on the leg position; the response peak shifts progressively over 500-1400 Hz towards higher frequencies following leg flexion. The response is amplified most strongly on the tibia, where specialised vibrosensory organs occur, and the response amplitude increases with the increasing frequency. Leg responses peaking at 800 and 1400 Hz closely resemble the tuning of the intermediate organ receptors in the proximal tibia of T. neglectus, which may be highly sensitive to positional change. The legs of free-standing animals with the abdomen touching the vibrating substrate show a secondary response peak below 150 Hz, induced by body vibration. Such responses may significantly increase the sensitivity of low-frequency receptors in the tibial accessory organ and the femoral chordotonal organ. The cave cricket legs appear suitable especially for detection of high-frequency vibration.