Bridging biotremology and chemical ecology: a new terminology.

Living organisms use both chemical and mechanical stimuli to survive in their environment. Substrate-borne vibrations play a significant role in mediating behaviors in animals and inducing physiological responses in plants, leading to the emergence of the discipline of biotremology. Biotremology is experiencing rapid growth both in fundamental research and in applications like pest control, drawing attention from diverse audiences. As parallels with concepts and approaches in chemical ecology emerge, there is a pressing need for a shared standardized vocabulary in the area of overlap for mutual understanding. In this article, we propose an updated set of terms in biotremology rooted in chemical ecology, using the suffix '-done' derived from the classic Greek word 'δονέω' (pronounced 'doneo'), meaning 'to shake'.

Leafhopper males compensate for unclear directional cues in vibration-mediated mate localization.

Ambient noise and transmission properties of the substrate pose challenges in vibrational signal-mediated mating behavior of arthropods, because vibrational signal production is energetically demanding. We explored implications of these challenges in the leafhopper Aphrodes makarovi (Insecta: Hemiptera: Cicadellidae) by exposing males to various kinds of vibrational noise on a natural substrate and challenging them to find the source of the female playback. Contrary to expectations, males exposed to noise were at least as efficient as control males on account of similar searching success with less signaling effort, while playing back male-female duets allowed the males to switch to satellite behavior and locate the target without signaling, as expected. We found altered mitochondrial structure in males with high signaling effort that likely indicate early damaging processes at the cellular level in tymbal muscle, but no relation between biochemical markers of oxidative stress and signaling effort. Analysis of signal transmission revealed ambiguous amplitude gradients, which might explain relatively low searching success, but it also indicates the existence of behavioral adaptations to complex vibrational environments. We conclude that the observed searching tactic, emphasizing speed rather than thorough evaluation of directional cues, may compensate for unclear stimuli when the target is near.

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.

Hay meadow vibroscape and interactions within insect vibrational community.

Our experiences shape our knowledge and understanding of the world around us. The natural vibrational environment (vibroscape) is hidden to human senses but is nevertheless perceived and exploited by the majority of animals. Here, we show that the vibroscape recorded on plants in a temperate hay meadow is a dynamic low-frequency world, rich in species-specific vibrational signals. The overall vibroscape composition changed throughout the season and also depended on the plant species, as well as on the spatial position of individual plants within the meadow. Within the studied community, vibrationally signaling species sharing this communication channel avoided interference primarily by partitioning vibrational space on a fine temporal scale. The vibroscape is a reliable source of information in the environment and expands our understanding of ecological and evolutionary processes.

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.

Variation in plant leaf traits affects transmission and detectability of herbivore vibrational cues.

Many insects use plant-borne vibrations to obtain important information about their environment, such as where to find a mate or a prey, or when to avoid a predator. Plant species can differ in the way they vibrate, possibly affecting the reliability of information, and ultimately the decisions that are made by animals based on this information. We examined whether the production, transmission, and possible perception of plant-borne vibrational cues is affected by variation in leaf traits. We recorded vibrations of 69 Spodoptera exigua caterpillars foraging on four plant species that differed widely in their leaf traits (cabbage, beetroot, sunflower, and corn). We carried out a transmission and an airborne noise absorption experiment to assess whether leaf traits influence amplitude and frequency characteristics, and background noise levels of vibrational chewing cues. Our results reveal that species-specific leaf traits can influence transmission and potentially perception of herbivore-induced chewing vibrations. Experimentally-induced vibrations attenuated stronger on plants with thicker leaves. Amplitude and frequency characteristics of chewing vibrations measured near a chewing caterpillar were, however, not affected by leaf traits. Furthermore, we found a significant effect of leaf area, water content and leaf thickness-important plant traits against herbivory, on the vibrations induced by airborne noise. On larger leaves higher amplitude vibrations were induced, whereas on thicker leaves containing more water airborne noise induced higher peak frequencies. Our findings indicate that variation in leaf traits can be important for the transmission and possibly detection of vibrational cues.

Female competition for availability of males in insects: the Nezara viridula (Linnaeus, 1758) model.

Multimodal communication in solitary stinkbugs enables them to meet, mate and copulate. Many plant-dwelling species exchange information during the calling phase of mating behavior using substrate-borne vibratory signals. A female-biased gender ratio induces rivalry and competition for a sexual partner. Female competition for males, first described among Heteroptera in three stinkbug species, revealed species specific differences and opened the question of plasticity in individually emitted temporal and frequency signal characteristics during calling and rival alternation. To address this question and gain an insight into the mechanisms underlying stinkbug female rivalry, we compared the characteristics of alternated signals in the southern green stinkbug Nezara viridula (Linnaeus, 1758) (Hemiptera: Pentatomidae). Compared to male rivalry, female rivalry is more complex, lasts longer and runs through successive phases by a combination of different song types. The male pheromone triggers alternation between females, producing song pulses that occasionally overlap each other. One female initiates the rivalry by changing individual pulses into pulse trains of three different types. The competing female alternates with pulses of changed temporal characteristics at lower levels of rivalry and by varying the frequency characteristics of pulse trains at higher levels. During female rivalry, the male either stops responding or occasionally emits calling and courtship signals in response to the female that has produced signals of steady temporal characteristics. Female rivalry shows complex and species specific patterns of information exchange at different levels with a broad-range variation of temporal and frequency characteristics of, until now, unidentified vibratory emissions.

Substrate-Borne Vibrational Communication in the Vector of Apple Proliferation Disease Cacopsylla picta (Hemiptera: Psyllidae).

Cacopsylla picta (Förster, 1848) (Hemiptera: Pysllidae) is the main vector of apple proliferation, a phytoplasma-caused disease. It represents one of the most severe problems in apple orchards, and therefore, there is a mandatory requirement to chemically treat against this pest in the European Union. Sexual communication using substrate-borne vibrations was demonstrated in several psyllid species. Here, we report the characteristics of the vibrational signals emitted by C. picta during courtship behavior. The pair formation process can be divided into two main phases: identification and courtship. Females initiate the communication on the host plant by emitting trains of vibrational pulses and, during courtship, if males reply, by emitting a signal consisting of a series of pre-pulses and a 'buzz', a duet is established. Moreover, a scanning electron microscopy investigation showed the presence of a stridulatory structure on the thorax and wings of both sexes, whereas the video recordings elucidated associated wing movement. The results provide new information about the biology of this phytoplasma vector and could form a basis of an environmentally friendly pest management strategy.

On the spot: utilization of directional cues in vibrational communication of a stink bug.

Although vibrational signalling is among the most ancient and common forms of communication, many fundamental aspects of this communication channel are still poorly understood. Here, we studied mechanisms underlying orientation towards the source of vibrational signals in the stink bug Nezara viridula (Hemiptera, Pentatomidae), where female vibrational song enables male to locate her on the bean plant. At the junction between the main stem and the leaf stalks, male placed his legs on different sides of the branching and orientation at the branching point was not random. Analyses of signal transmission revealed that only a time delay between the arrival of vibrational wave to receptors located in the legs stretched across the branching was a reliable directional cue underlying orientation, since, unexpectedly, the signal amplitude at the branching point was often higher on the stalk away from the female. The plant and the position of the vibrational source on the plant were the most important factors influencing the unpredictability of the amplitude cue. Determined time delays as short as 0.5 ms resulted in marked changes in interneuron activity and the decision model suggests that the behavioural threshold is in the range between 0.3 and 0.5 ms.

Mating behavior of Psammotettix alienus (Hemiptera: Cicadellidae).

The Wheat dwarf virus, the causal agent of the wheat dwarf disease, is transmitted by leafhoppers from the genus Psammotettix and currently the main protection strategy is based on the use of insecticide treatments. Sustainable management strategies for insect vectors should include methods that are targeted to disrupt reproductive behavior and here we investigated the mating behavior of Psammotettix alineus (Dahlbom 1850) in order to determine the role of vibrational signals in intra-specific communication and pair formation. Both genders spontaneously emit species- and sex-specific calling songs that consisted of regularly repeated pulse trains and differ primarily in pulse train duration and pulse repetition time. Females preferred the conspecific male calling song. After a coordinated exchange of pulse trains, the male approached the stationary female. During the close range courtship and also immediately prior to copulatory attempts distinct male vibrational signals associated with wing flapping and wing vibrations were recorded from the substrate. In the presence of a receptive female, competing males emitted vibrational signals most likely aimed to interfere with male-female interaction. Mated females regained sexual receptivity after they laid eggs. Although results suggest that the viruliferous status of insects may have an effect on vibrational songs, our current results did not reveal a significant effect of virus on leafhopper performance in mating behavior. However, this study also suggests, that detailed understanding of plant-vector-virus interactions relevant for vector mating behavior is essential for trying new approaches in developing future control practices against plant viruses transmitted by insect vectors.

The Effect of Timing of Female Vibrational Reply on Male Signalling and Searching Behaviour in the Leafhopper Aphrodes makarovi.

Sexual communication in animals often involves duetting characterized by a coordinated reciprocal exchange of acoustic signals. We used playback experiments to study the role of timing of a female reply in the species-specific duet structure in the leafhopper Aphrodes makarovi (Hemiptera: Cicadellidae). In leafhoppers, mate recognition and location is mediated exclusively by species- and sex-specific substrate-borne vibrational signals and a female signal emitted in reply to male advertisement calls is essential for recognition and successful location of the female. In A. makarovi, males have to initiate each exchange of vibrational signals between partners, and in a duet the beginning of a female reply overlaps the end of the male advertisement call. Results of playback treatments in which female replies were delayed and did not overlap with the male call revealed that in order to trigger an appropriate behavioural response of the male, female reply has to appear in a period less than 400 ms after the end of the initiating male call. Results also suggest that males are not able to detect a female reply while calling, since female reply that did not continue after the end of male call triggered male behaviour similar to behaviour observed in the absence of female reply. Together, our results show that vibrational duets are tightly coordinated and that the species-specific duet structure plays an important role in mate recognition in location processes.

Interference of Overlapping Insect Vibratory Communication Signals: An Eushistus heros Model.

Plants limit the range of insect substrate-borne vibratory communication by their architecture and mechanical properties that change transmitted signal time, amplitude and frequency characteristics. Stinkbugs gain higher signal-to-noise ratio and increase communication distance by emitting narrowband low frequency vibratory signals that are tuned with transmission properties of plants. The objective of the present study was to investigate hitherto overlooked consequences of duetting with mutually overlapped narrowband vibratory signals. The overlapped vibrations of the model stinkbug species Eushistus heros, produced naturally or induced artificially on different plants, have been analysed. They represent female and male strategies to preserve information within a complex masked signal. The brown stinkbugs E. heros communicate with species and gender specific vibratory signals that constitute characteristic duets in the calling, courtship and rivalry phases of mating behaviour. The calling female pulse overlaps the male vibratory response when the latency of the latter is shorter than the duration of the female triggering signal or when the male response does not inhibit the following female pulse. Overlapping of signals induces interference that changes their amplitude pattern to a sequence of regularly repeated pulses in which their duration and the difference between frequencies of overlapped vibrations are related inversely. Interference does not occur in overlapped narrow band female calling pulses and broadband male courtship pulse trains. In a duet with overlapped signals females and males change time parameters and increase the frequency difference between signals by changing the frequency level and frequency modulation pattern of their calls.

Secondary spectral components of substrate-borne vibrational signals affect male preference.

Animal sexual signals contain information about both compatibility and quality of the signaller, but combined with influence of the signalling medium, the complexity of mate selection makes it difficult to separate different components of this process. We approached the problem of teasing apart different functions of sexual signals by using the planthopper Hyalesthes obsoletus, which uses unimodal vibrational communication, as a model. Vibrational signals are known to encode information about identity in their temporal pattern, while a useful cue for quality may reside in their spectral properties. In this study, we demonstrate a connection between spectral properties and attractiveness of female signals based on male behavioural response to signal playback. Artificially increasing the amplitude of high-frequency components increases signal attractiveness and vice versa, which indicates that spectral properties could function as an index of quality. Presence of high-frequency spectral components might indicate a larger or healthier individual, but direct connection with female fitness is not yet clear. In addition, we found that H. obsoletus males are able to exploit female pulses as directional cues and can discriminate between female signals of different attractiveness coming from spatially separated sources.

Manipulating behaviour with substrate-borne vibrations--potential for insect pest control.

This review presents an overview of the potential use of substrate-borne vibrations for the purpose of achieving insect pest control in the context of integrated pest management. Although the importance of mechanical vibrations in the life of insects has been fairly well established, the effect of substrate-borne vibrations has historically been understudied, in contrast to sound sensu stricto. Consequently, the idea of using substrate-borne vibrations for pest control is still in its infancy. This review therefore focuses on the theoretical background, using it to highlight potential applications in a field environment, and lists the few preliminary studies that have been or are being performed. Conceptual similarities to the use of sound, as well as limitations inherent in this approach, are also noted.

The process of pair formation mediated by substrate-borne vibrations in a small insect.

The ability to identify and locate conspecifics depends on reliable transfer of information between emitter and receiver. For a majority of plant-dwelling insects communicating with substrate-borne vibrations, localization of a potential partner may be a difficult task due to their small body size and complex transmission properties of plants. In the present study, we used the leafhopper Scaphoideus titanus as a model to investigate duetting and mate searching associated with pair formation. Studying these insects on a natural substrate, we showed that the spatio-temporal structure of a vibrational duet and the perceived intensity of partner's signals influence the mating behaviour. Identification, localization and courtship stages were each characterized by a specific duet structure. In particular, the duet structure differed in synchronization between male and female pulses, which enables identification of the partner, while the switch between behavioural stages was associated with the male-perceived intensity of vibrational signals. This suggests that males obtain the information about their distance from the female and optimize their strategy accordingly. More broadly, our results show that even in insects smaller than 1cm, vibrational signals provide reliable information needed to find a mating partner.

Substrate vibrations during courtship in three Drosophila species.

While a plethora of studies have focused on the role of visual, chemical and near-field airborne signals in courtship of Drosophila fruit flies, the existence of substrate-borne vibrational signals has been almost completely overlooked. Here we describe substrate vibrations generated during courtship in three species of the D. melanogaster group, from the allegedly mute species D. suzukii, its sister species D. biarmipes, and from D. melanogaster. In all species, we recorded several types of substrate vibrations which were generated by locomotion, abdominal vibrations and most likely through the activity of thoracic wing muscles. In D. melanogaster and D. suzukii, all substrate vibrations described in intact males were also recorded in males with amputated wings. Evidence suggests that vibrational signalling may be widespread among Drosophila species, and fruit flies may provide an ideal model to study various aspects of this widespread form of animal communication.

Exploitation of insect vibrational signals reveals a new method of pest management.

Food production is considered to be the main source of human impact on the environment and the concerns about detrimental effects of pesticides on biodiversity and human health are likely to lead to an increasingly restricted use of chemicals in agriculture. Since the first successful field trial, pheromone based mating disruption enabled sustainable insect control, which resulted in reduced levels of pesticide use. Organic farming is one of the fastest growing segments of agriculture and with the continuously growing public concern about use of pesticides, the main remaining challenge in increasing the safety of the global food production is to identify appropriate alternative mating disruption approaches for the numerous insect pests that do not rely on chemical communication. In the present study, we show for the first time that effective mating disruption based on substrate-borne vibrational signals can be achieved in the field. When disruptive vibrational signals were applied to grapevine plants through a supporting wire, mating frequency of the leafhopper pest Scaphoideus titanus dropped to 9 % in semi-field conditions and to 4 % in a mature vineyard. The underlying mechanism of this environmentally friendly pest-control tactic is a masking of the vibrational signals used in mate recognition and location. Because vibrational communication is widespread in insects, mating disruption using substrate vibrations can transform many open field and greenhouse based farming systems.

Inter-plant vibrational communication in a leafhopper insect.

Vibrational communication is one of the least understood channels of communication. Most studies have focused on the role of substrate-borne signals in insect mating behavior, where a male and a female establish a stereotyped duet that enables partner recognition and localization. While the effective communication range of substrate-borne signals may be up to several meters, it is generally accepted that insect vibrational communication is limited to a continuous substrate. Until now, interplant communication in absence of physical contact between plants has never been demonstrated in a vibrational communicating insect. With a laser vibrometer we investigated transmission of natural and played back vibrational signals of a grapevine leafhopper, Scaphoideus titanus, when being transmitted between leaves of different cuttings without physical contact. Partners established a vibrational duet up to 6 cm gap width between leaves. Ablation of the antennae showed that antennal mechanoreceptors are not essential in detection of mating signals. Our results demonstrate for the first time that substrate discontinuity does not impose a limitation on communication range of vibrational signals. We also suggest that the behavioral response may depend on the signal intensity.