Substrate-borne Communication Research Articles

Vibrational and acoustic communication in fishes: The overlooked overlap between the underwater vibroscape and soundscape.

Substrate-borne communication via mechanical waves is widespread throughout the animal kingdom but has not been intensively studied in fishes. Families such as the salmonids and sculpins have been documented to produce vibratory signals. However, it is likely that fish taxa on or close to the substrate that produce acoustic signals will also have a vibratory component to their signal due to their proximity to substrates and energy transfer between media. Fishes present an intriguing opportunity to study vibrational communication, particularly in the context of signal production and detection, detection range, and how vibratory signals may complement or replace acoustic signals. It is highly likely that the vibrational landscape, the vibroscape, is an important component of their sensory world, which certainly includes and overlaps with the soundscape. With the wide range of anthropogenic activities modifying underwater substrates, vibrational noise presents similar risks as acoustic noise pollution for fishes that depend on vibrational communication. However, in order to understand vibrational noise, more empirical studies are required to investigate the role of vibrations in the fish environment.

Substrate-borne vibrations used during acoustic communication and the existence of courtship songs in some species of the genus Anaxipha (Saussure) (Orthoptera: Trigonidiidae: Trigonidiinae)

Anaxipha (Saussure, 1874) are small, swordtail crickets found in much of eastern North America. Many species within the genus Anaxipha were only recently described and their calling songs characterized. However, little is known about their courtship songs or use of substrate-borne communication (drumming). This study is the first documentation of the existence of courtship songs and substrate-borne vibrational communication in the genus. Courtship songs and substrate-borne vibrational communication were first detected in the following species: Anaxipha exigua (Say, 1825), A. tinnulacita Walker & Funk, 2014, A. tinnulenta Walker & Funk, 2014, and A. thomasi Walker & Funk, 2014. When in the presence of a conspecific female, males of all four species perform courtship songs that are distinctly different in pattern of echeme delivery and syllable details compared to their respective calling songs. Additionally, males of all four species exhibited drumming behavior during courtship singing and variably during calling songs. Examination of video recordings of males drumming during courtship singing showed that they are apparently using the sclerotized portion of their mandibles to impact the substrate on which they are perched to create vibrations. Courtship song and drumming bout characteristics were statistically different among the four species studied here, although A. tinnulacita and A. tinnulenta were similar in some measurements. Drumming during calling songs was common only in A. tinnulacita, where drumming occurs predominately during the first forty percent and last twenty percent of the long echemes of calling songs. Additional study is needed to further explore the use of substrate-borne vibrational communication in this genus.

Stink Bug Communication and Signal Detection in a Plant Environment.

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.

Drosophila females receive male substrate-borne signals through specific leg neurons during courtship

SummarySubstrate-borne vibratory signals are thought to be one of the most ancient and taxonomically widespread communication signals among animal species, including Drosophila flies.1, 2, 3, 4, 5, 6, 7, 8, 9 During courtship, the male Drosophila abdomen tremulates (as defined in Busnel et al.10) to generate vibrations in the courting substrate.8,9 These vibrations coincide with nearby females becoming immobile, a behavior that facilitates mounting and copulation.8,11, 12, 13 It was unknown how the Drosophila female detects these substrate-borne vibratory signals. Here, we confirm that the immobility response of the female to the tremulations is not dependent on any air-borne cue. We show that substrate-borne communication is used by wild Drosophila and that the vibrations propagate through those natural substrates (e.g., fruits) where flies feed and court. We examine transmission of the signals through a variety of substrates and describe how each of these substrates modifies the vibratory signal during propagation and affects the female response. Moreover, we identify the main sensory structures and neurons that receive the vibrations in the female legs, as well as the mechanically gated ion channels Nanchung and Piezo (but not Trpγ) that mediate sensitivity to the vibrations. Together, our results show that Drosophila flies, like many other arthropods, use substrate-borne communication as a natural means of communication, strengthening the idea that this mode of signal transfer is heavily used and reliable in the wild.3,4,7 Our findings also reveal the cellular and molecular mechanisms underlying the vibration-sensing modality necessary for this communication.

Stink Bug Communication with Multimodal Signals Transmitted through Air and Substrate

This review represents complex mechanisms and processes of multimodal communication in stink bugs. During reproductive behavior the airborne and substrate-borne signals enable mate recognition, mediate directionality of movement, eliminate rivals and motivate partners for copulation. Species specific characteristics prevent hybridization at various levels of mating behavior. Male sex and/or aggregation pheromones as uni- or multicomponent signals attract mates to land on the same plant and there, trigger females to call males by vibratory signals, transmitted through the plant. Communication during courtship runs at short distance with visual, airborne, substrate-borne and contact chemical and mechanical signals. Abdomen vibrations produce the main repertoire of female and male calling, courtship and rival vibratory signals. To increase their informational value, stink bugs tune signal frequency, amplitude and temporal characteristics with mechanical properties of plants. The airborne component of species non-specific and high amplitude signals, produced by body tremulation and wing buzzing enables communication contact between mates standing on mechanically isolated plants. Female vibratory signals increase the amount of male emitted pheromone and the latter keeps female calling. Interaction, synergy and characteristics of visual, contact chemical and vibratory signals, exchanged during courtship remain under-investigated. Female and male competition for access to copulation in imbalanced sex conditions is characterized by duetting with rival song vibratory signals. Different receptors in and on different parts of the body are able to detect with high sensitivity multimodal airborne and substrate-borne communication signals. The relevance of the multimodal communication for the reproductive success of stink bugs is discussed.

Gular pouch diversity in the Chamaeleonidae.

Numerous chameleon species possess an out-pocketing of the trachea known as the gular pouch. After surveying more than 250 specimens, representing nine genera and 44 species, we describe two different morphs of the gular pouch. Species of the genera Bradypodion and Chamaeleo, as well as Trioceros goetzei, all possess a single gular pouch (morph one) formed from ventral expansion of soft tissue where the larynx and trachea meet. Furcifer oustaleti and Furcifer verrucosus possess from one to four gular pouches (morph two) formed by the expansion of soft tissue between sequential hyaline cartilage rings of the trachea. In Trioceros melleri, examples of both morphs of the gular pouch were observed. Morphometric data are presented for 100 animals representing eight species previously known to possess a gular pouch and two additional species, Bradypodion thamnobates and Bradypodion transvaalense. In the species with the absolutely and relatively largest gular pouch, Chamaeleo calyptratus, a significant difference was found between sexes in its width and volume, but not its length. In C. calyptratus, we show that an inflated gular pouch is in contact with numerous hyoid muscles and the tongue. Coupled with the knowledge that C. calyptratus generates vibrations from the throat region, we posit that the tongue (M. accelerator linguae and M. hyoglossus) and supporting hyoid muscles (i.e., Mm. sternohyoideus profundus et superficialis and Mm. mandibulohyoideus) are involved in the production of vibrations to produce biotremors that are amplified by the inflated gular pouch and used in substrate-borne communication.

The flightin gene is necessary for the emission of vibrational signals in the rice brown planthopper (Nilaparvata lugens Stǻl)

In duet-based courtship, species- and sex-specific vibrational signals enable animals to identify the species and sex of the singer and also provide the necessary information with which to locate a partner. Substrate-borne communication has been described in a wide variety of insects. Here, we focus on the gene necessary for the emission of male vibrational signals and whether the male song fulfills such a functional role in the mating system of the brown planthopper (BPH, Nilaparvata lugens). We generated mute BPH adult males via RNA interference (RNAi) of the flightin gene, which encodes a myosin-binding protein expressed exclusively in the dorsal longitudinal muscle (DLM) in the basal two abdominal segments used for driving the vibration of the male-specific tymbal structure in short-winged (brachypterous) BPH adults. Transmission electron microscopy (TEM) observation showed that flightin knockdown disrupted the normal sarcomere structure of the abdominal DLM. No courtship song could be detected in the brachypterous males after RNAi treatment. Behavior and competition trials showed that the lack of male courtship songs prolonged copulation latency and even caused female rejection. Unexpectedly, the mute males exhibited greater competitiveness when competing against normal males.

Egg-guarding behavior of the treehopper Ennya chrysura (Hemiptera: Membracidae): female aggregations, egg parasitism, and a possible substrate-borne alarm signal.

Treehoppers are known for their substrate-borne communication and some of them also for their subsocial behavior. Following a more general study of the natural history and substrate-borne signal repertoire of the treehopper Ennya chrysura, the objective of this paper was to explore in greater depth the signals and other behaviors associated specifically to egg-guarding. Theese were studied both in natural and laboratory conditions between July, 2000 and March, 2004. The spacial distribution of egg guarding females was studied in the natural population; recording equipment and playback experiments were used in the laboratory and then analyzed digitally. Under natural conditions (San Antonio de Escazú, Costa Rica), female E. chrysura guard their egg masses and egg-guarding was associated with lower parasitism of the eggs from the wasps Gonatocerus anomocerus and Schizophragma sp. (Mymaridae). Females tended to place their eggs close to other egg-guarding females and they produced substrate-borne vibrations when disturbed. An aggregated pattern under natural conditions was confirmed by calculating dispersion indices from egg-clutch data obtained from 66 leaves in the field. The disturbance signal was characterized from laboratory recordings of substrate-borne vibrations of 10 egg-guarding females. Experiments conducted in the laboratory with 18 egg-guarding females showed that those which were previously exposed to the disturbance signal of another female moved slightly or vibrated more during playbacks and that they reacted more quickly and exhibited more deffensive behaviors in response to a tactile stimulus. The signals produced while defending against egg parasites may therefore function as an alarm and favor aggregating behavior of egg-guarding females.

Singing in the Namoroka Caves, First Record In Situ for a Cave Dwelling Insect: Typhlobrixia namorokensis (Hemiptera, Fulgoromorpha, Cixiidae)

This is the first substrate-borne communication record of the troglobitic planthopper Typhlobrixia namorokensis in the caves of the Ambovonomby network, Namoroka Tsingy, Madagascar. A supplementary morphological description of the male genitalia is provided and, for the first time, female genitalia of T. namorokensis are characterized. Molecular data were obtained for T. namorokensis; molecular analysis also reveals the presence of another (yet unidentified) cavernicolous cixiid in the Antsifotra caves network. The evolutionary origin of T. namorokensis is discussed. Its adaptation to caves and its behaviour allows its identification as a true troglobiont. Its vibrational signal structure is compared to the calls of other cave-dwelling cixiids.

Species Recognition During Substrate-Borne Communication in Nezara viridula (L.) (Pentatomidae: Heteroptera)

The information code in the temporal and spectral characteristics of the substrate-borne communication signals produced by insects has been primarily studied in insects in the suborder Auchenorrhyncha. In the present study we investigated which of the female calling song (FCS) parameters in Nezara viridula (L.) (Heteroptera, Pentatomidae) are essential for recognition by conspecific males. In playback experiments we measured male vibrational responsiveness to FCS signals varying in the durations of pulse trains and inter-pulse train intervals, repetition times, duty cycles, and dominant frequencies, and determined the preference range for each specific parameter. Males were able to distinguish songs of different temporal and frequency parameters and responded best to values characteristic of the song of conspecific females. Signal recognition is achieved on the basis of two temporal filters tuned to the durations of the pulse train and inter-pulse train interval. Males responded best to the dominant frequency characteristic of conspecific songs, which are tuned to the resonant properties of the herbaceous plants used for intraspecific signal transmission during communication.

Tuning of host plants with vibratory songs ofNezara viridulaL(Heteroptera: Pentatomidae)

Songs of the southern green stink bug Nezara viridula L, recorded on a non-resonant loudspeaker membrane, reflect frequency characteristics of body vibrations. The song dominant frequency directly depends on the repetition rate of potentials recorded from synchronously contracting muscles that vibrate the abdomen during singing. Spectra of naturally emitted signals recorded on the pronotum of a singing bug or on a plant contain peaks characteristic of plant resonant spectra. The dominant resonant frequency of sound-induced vibrations in bean and other stink bug host plants ranges between 160 and 215 Hz and subdominant peaks do not exceed 600 Hz. There is no correlation between spectral peak positions and recording points on a plant. The dominant resonance peak corresponds to the best frequency sensitivity of N. viridula middle frequency subgenual receptor cell. Subdominant peaks around and below 100 Hz lie close to the dominant frequency of body vibrations during singing and to the range of best frequency sensitivity of low frequency receptor cells. Tuning of plant resonant frequencies with spectral properties of songs and frequency sensitivity of sensory organs is discussed in the context of stink bug substrate-borne communication.