The role of signals of different modalities in initiating vibratory communication in Nezara viridula

Signals of different modalities are involved in the behaviour of the green stink bug, Nezara viridula (L.) (Pentatomidae, Heteroptera). Long range attraction is mediated by male pheromones, resulting in aggregation of bugs on the same plant where vibratory signals, vision and various chemical signals become important. Both males and females sing spontaneously. When both are on the plant, males start vibratory communication as often as females. Females induce the exchange of vibratory signals spontaneously or triggered by the male pheromone while males initiate the duet either spontaneously or after seeing the female. Males and females sing spontaneously and respond to signals of different modalities more often in the daylight than in the dark. Long lasting autonomous emission of the female calling song is present when triggered by the male pheromone and males respond to female calling predominantly by the emission of the courtship song.     

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.     

Species Recognition During Substrate-Borne Communication in <Emphasis Type="Italic">Nezara viridula</Emphasis> (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.     

The structure and function of songs emitted by southern green stink bugs from Brazil, Florida, Italy and Slovenia

Nezara viridula (L.) (Pentatomidae: Heteroptera) from Brazil, Florida, Italy and Slovenia, communicate by vibratory songs associated with long‐range calling and close‐range courting, rivalry and repelling. Each song is composed of spectrally and temporally different units. Spectrally different pulses of duration less than 300 ms are present in the male calling song. The female calling song is characterized by pulse trains composed of pulses shorter than 150 ms and pulse trains composed of a longer (> 700 ms) and shorter (< 250 ms) pulse. Shorter and longer pulses have different spectral characteristics. The male and female courtship songs are characterized by fusion of shorter (< 150 ms) pulses into a pulse train usually followed by a shorter (< 200 ms) postpulse in the case of the male courtship song. The female repelling song is a several seconds long vibration of irregular temporal structure. The short (< 400 ms) male rival song pulses are frequency modulated. The dominant frequency peaks of the songs investigated lie between 70 and 130 Hz. The dominant frequency and the microstructure of song spectra show no population specificity. The average duration varies more in calling than in courtship songs. The repetition time varies extensively in songs of different populations. Normal communication followed by copulation was observed between mates from Slovenia and Brazil and between mates from Florida and Italy. The potential role of different temporal and spectral parameters for species recognition and mate location is discussed in view of the expected distortion of the characteristic signal structure during transmission through plants.     

Search behaviour of two hemipteran species using vibrational communication

The ability of conspecifics to recognize and locate each other in the environment depends on the efficiency of intraspecific communication. We compared the mate searching strategies of southern green stinkbug Nezara viridula (male searches for a continuously calling female) and the leafhopper Aphrodes makarovi (partners form a precisely coordinated duet). Males of both species were tested on plants in playback experiments. One leaf was vibrated with unaltered conspecific female signals or with various conspecific signals using modified temporal parameters. The results showed that the onset of searching was faster in A. makarovi than in N. viridula. Changes in temporal parameters of female replies had negative effect on the searching behaviour of A. makarovi. Males located the source of longer female replies faster than the short female call and they failed to locate the source of a female reply with temporal parameters outside the species-specific values. In contrast, in N. viridula, searching males successfully located also the source of a female song with parameters outside the species-specific values. The results are discussed with regard to male behavioural strategies in species with different vibrational communication systems and different male mating investment.     

Predatory bug <Emphasis Type="Italic">Picromerus bidens</Emphasis> communicates at different frequency levels

The Asopinae (Heteroptera: Pentatomidae) are a subfamily of stinkbugs with predaceous feeding habits and poorly understood communication systems. In this study we recorded vibratory signals emitted by Picromerus bidens L. on a non-resonant substrate and investigated their frequency characteristics. Males and females produced signals by vibration of the abdomen and tremulation. The female and male songs produced by abdominal vibrations showed gender-specific time structure. There were no differences in the temporal patterns of male or female tremulatory signals. The signals produced by abdominal vibrations were emitted below 600 Hz whereas tremulatory signals had frequency ranges extending up to 4 kHz. Spectra of male vibratory signals produced by abdominal vibrations contained different peaks, each of which may be dominant within the same song sequence. Males alternated with each other during production of rivalry signals, using different dominant frequency levels. We show that the vibratory song repertoire of P. bidens is broader than those of other predatory stinkbugs that have been investigated. The emission of vibrational signals with different dominant frequencies but the same production mechanism has not yet been described in heteropteran insects, and may facilitate location of individual sources of vibration within a group.     

Limited flexibility in female Pacific field cricket (Teleogryllus oceanicus) exploratory behaviors in response to perceived social environment

How populations adapt, or not, to rapid evolution of sexual signals has important implications for population viability, but is difficult to assess due to the paucity of examples of sexual signals evolving in real time. In Hawaiian populations of the Pacific field cricket (Teleogryllus oceanicus), selection from a deadly parasitoid fly has driven the rapid loss of a male acoustic signal, calling song, that females use to locate and evaluate potential mates. In this newly quiet environment where many males are obligately silent, how do phonotactic females find mates? Previous work has shown that the acoustic rearing environment (presence or absence of male calling song) during late juvenile stages and early adulthood exposes adaptive flexibility in locomotor behaviors of males, as well as mating behaviors in both sexes that helps facilitate the spread of silent (flatwing) males. Here, we tested whether females also show acoustically induced plasticity in walking behaviors using laboratory‐reared populations of T. oceanicus from Kauai (HI; >90% flatwings), Oahu (HI; ~50% flatwings), and Mangaia (Cook Islands; no flatwings or parasitoid fly). Though we predicted that females reared without song exposure would increase walking behaviors to facilitate mate localization when song is rare, we discovered that, unlike males, female T. oceanicus showed relatively little plasticity in exploratory behaviors in response to an acoustic rearing environment. Across all three populations, exposure to male calling song during development did not affect latency to begin walking, distance walked, or general activity of female crickets. However, females reared in the absence of song walked slower and showed a marginally non‐significant tendency to walk for longer durations of time in a novel environment than those reared in the presence of song. Overall, plasticity in female walking behaviors appears unlikely to have facilitated sexual signal loss in this species.     

Sound production in Parapellopedon instabilis (Rehn, 1906) (Orthoptera: Gomphocerinae)

The sounds produced by Parapellopedon instabilis (Rehn, 1906), are described for the first time on the basis of recordings made, in captivity, with an analogical tape recorder. The signals were digitized in the laboratory and analyzed using a software. Three types of song are described: the male calling song, typical of the gomphocerinae species, the female’s agreement song, less organized temporally and unusually loud for a gomphocerinae species, and disturbance songs among males and among females, which follow the typical structure of these signals in the subfamily. Oscillograms and frequency spectra of all songs are given. The stridulatory file of both sexes, male and female, are described.     

The Influence of Substrate on Male Responsiveness to the Female Calling Song in Nezara viridula

The female calling song (FCS) of the southern green stink bug Nezara viridula is composed of vibrational pulse trains that include either short pulses and a long pulse (FCS-1) or just short pulses (FCS-2). Their function in communication was studied by investigating male vibratory responses to natural and artificial signals on artificial and natural substrates. On a loudspeaker membrane, FCS-1 triggered in males from a Slovene and a French population significantly more courtship songs (MCrS) than FCS-2. Experiments with artificial signals showed that male responses are modulated by the duration of pulse trains and pulse repetition time. On a bean plant, males of both populations responded in the same way to the two types of female calling song pulse trains. Moreover, a laser vibrometer study of the transmission of different natural and artificial vibratory signals through the bean plant showed that the pulses of a high repetition rate are prolonged and fused at distances from the emitter. We conclude that female calling song pulse trains of different temporal structure have the same function in vibrational communication of the species. The temporal and spectral structures of the female calling songs of N. viridula are discussed in terms of effective transmission through plants.     

Intraspecific acoustic communication and mechanical sensitivity of the tympanal ear of the gypsy moth Lymantria dispar

Tympanal ears of female gypsy moths Lymantria dispar dispar (L.) (Lepidoptera: Erebidae: Lymantriinae) are reportedly more sensitive than ears of conspecific males to sounds below 20 kHz. The hypothesis is tested that this differential sensitivity is a result of sex‐specific functional roles of sound during sexual communication, with males sending and females receiving acoustic signals. Analyses of sounds produced by flying males reveal a 33‐Hz wing beat frequency and 14‐kHz associated clicks, which remain unchanged in the presence of female sex pheromone. Females exposed to playback sounds of flying conspecific males respond with wing raising, fluttering and walking, generating distinctive visual signals that may be utilized by mate‐seeking males at close range. By contrast, females exposed to playback sounds of flying heterospecific males (Lymantria fumida Butler) do not exhibit the above behavioural responses. Laser Doppler vibrometry reveals that female tympana are particularly sensitive to frequencies in the range produced by flying conspecific males, including the 33‐Hz wing beat frequency, as well as the 7‐kHz fundamental frequency and 14‐kHz dominant frequency of associated clicks. These results support the hypothesis that the female L. dispar ear is tuned to sounds of flying conspecific males. Based on previous findings and the data of the present study, sexual communication in L. dispar appears to proceed as: (i) females emitting sex pheromone that attracts males; (ii) males flying toward calling females; and (iii) sound signals from flying males at close range inducing movement in females, which, in turn, provides visual signals that could orient males toward females.     

Mate location in the southern green stink bug,Nezara Viridula (Heteroptera: Pentatomidae), mediated through substrate-borne signals on ivy

We observed mate location behavior in Nezara viridulaon the ivy Hedera helix.The female stays motionless on the plant stem, calling with rhythmic repetitions of her calling song. The male walks on the plant, answering with his calling and courtship songs. On encountering petioles or branching points, the male stops and straddles his legs across the fork. Only after another repetition of the female's call does the male proceed to walk again. This behavior may enable the male to compare the vibrations in the two substrates and choose the stronger one to follow. On plants where visual and airborne acoustic communication can be prevented by leaves, substrateborne vibrational signals perceived by receptors in legs would enhance the likelihood of mate location in N. viridula.     

Temporal processing of vibratory communication signals at the level of ascending interneurons in Nezara viridula (Hemiptera: Pentatomidae)

During mating, males and females of N. viridula (Heteroptera: Pentatomidae) produce sex- and species-specific calling and courtship substrate-borne vibratory signals, grouped into songs. Recognition and localization of these signals are fundamental for successful mating. The recognition is mainly based on the temporal pattern, i.e. the amplitude modulation, while the frequency spectrum of the signals usually only plays a minor role. We examined the temporal selectivity for vibratory signals in four types of ascending vibratory interneurons in N. viridula. Using intracellular recording and labelling technique, we analyzed the neurons' responses to 30 pulse duration/interval duration (PD/ID) combinations. Two response arrays were created for each neuron type, showing the intensity of the responses either as time-averaged spike counts or as peak instantaneous spike rates. The mean spike rate response arrays showed preference of the neurons for short PDs (below 600 ms) and no selectivity towards interval duration; while the peak spike rate response arrays exhibited either short PD/long ID selectivity or no selectivity at all. The long PD/short ID combinations elicited the weakest responses in all neurons tested. No response arrays showed the receiver preference for either constant period or duty cycle. The vibratory song pattern selectivity matched the PD of N. viridula male vibratory signals, thus pointing to temporal filtering for the conspecific vibratory signals already at level of the ascending interneurons. In some neurons the responses elicited by the vibratory stimuli were followed by distinct, regular oscillations of the membrane potential. The distance between the oscillation peaks matched the temporal structure of the male calling song, indicating a possible resonance based mechanism for signal recognition.     

FEMALE CHOICE FOR AN INDICATOR OF MALE SIZE IN THE SONG OF THE BLACK-HORNED TREE CRICKET,OECANTHUS NIGRICORNIS (ORTHOPTERA: GRYLLIDAE: OECANTHINAE)

The calling song of male crickets, including Oecanthus nigricornis (Walker), attracts females for mating and provides a model system of sexual communication. We give the first conclusive identification of a feature of cricket song that is both attractive to females and indicates a phenotypic feature (body size) that determines male mating success and female reproductive benefits. We do this by first testing for correlations between song characteristics and aspects of male phenotype that are hypothesized to indicate male quality. We show that song is a reliable indicator of male size and male age, and that large male size is associated with increased female fecundity. We then use playbacks of synthetic songs that mimic natural variation in song parameters to study song preferences and we compare preferences under different presentation regimes to determine whether choices are based on relative song quality or some fixed criterion. Females show a preference for the lower frequency songs produced by large males, but only during simultaneous playbacks. Thus female choice is based on the relative quality of calls that can be sampled simultaneously. These results provide strong support for the hypothesis that females use variation in calling song to assess male mate quality.     

Sexual signal loss,pleiotropy, and maintenance of a male reproductive polymorphism in crickets

Pleiotropy between male signals and female preferences can facilitate evolution of sexual communication by maintaining coordination between the sexes. Alternatively, it can favor variation in the mating system, such as a reproductive polymorphism. It is unknown how common either of these scenarios is in nature. In Pacific field crickets (Teleogryllus oceanicus) on Kauai, Hawaii, a mutation (flatwing) that segregates as a single locus is responsible for the rapid loss of song production in males. We used outbred cricket colonies fixed for male wing morph to investigate whether homozygous flatwing and normal-wing (wild-type) females differ in responsiveness to male calling song and propensity to mate when paired with either a flatwing or normal-wing male in the presence or absence of courtship song. Flatwing females were less likely to mount a male than normal-wing females. Females of both genotypes showed a preference for normal-wing males and were more likely to mate in the presence of courtship song; normal-wing females were particularly likely to mate with song. Our results show that negative pleiotropy between obligate male silence and female mating behavior can constrain the evolution of sexual signal loss and contribute to the maintenance of a male reproductive polymorphism in the wild.     

Vibrational communication and mating behaviour of Dichelops melacanthus (Hemiptera: Pentatomidae) recorded from loudspeaker membranes and plants

Vibrational communication is important for successful mating in various stink bugs species. The vibrational signals from males and females of Dichelops melacanthus Dallas (Hemiptera: Pentatomidae) are recorded from a nonresonant substrate (i.e. a loudspeaker membrane) to characterize the temporal and spectral properties of these vibrational signals, as well as on a resonant substrate (i.e. bean plants) to obtain information about how these signals are altered when they are transmitted through the plants. On the loudspeaker membrane, D. melacanthus males and females emit only one male or one female song, respectively. However, when the insects are placed on bean leaves, a more complex repertoire is recorded, with three different songs for each sex. The first female and male songs appear to have calling functions and the third male and female songs are emitted during courtship. The second female and male songs are emitted after the first song, although their functions in mating behaviour are not clear. The identified repertoire is similar to those of other Neotropical stink bugs, starting with songs 1 and 2 and developing into song 3. Frequency modulation is observed in the female songs recorded from the loudspeaker membrane and the plants. The signals recorded from plants present higher harmonic peaks compared with the signals recorded from the loudspeaker membrane. The presence of species and sex‐specific songs during mating confirms the important role of vibrational communication in mate location and recognition. The temporal and spectral characteristic signals are influenced by the substrate used to record the songs emitted by D. melacanthus.     

Percussion signals of Lygus rugulipennis Poppius (Heteroptera: Miridae)

The European tarnished plant bug (Lygus rugulipennis Poppius) is among the most serious pests in the family Miridae, and therefore there is increasing interest in understanding the behaviour of this species. In the present study, laboratory recordings were taken using a laser vibrometer on adult males and females to ascertain whether acoustic signals are involved in intraspecific communication. Recordings were both carried out on plant and loudspeaker membrane substrates. Males and females emitted vibratory signals and the present results indicate that these signals are important during courtship. The basic signal characteristics measured were the dominant frequency, pulse duration, repetition time and number of pulses per group within the signal. Male and female signals did not differ in respect to any of these characteristics. Plant recorded signals were longer because of different mechanical properties of substrates. Additionally, the high frequency components were attenuated due to the low-pass filtering properties of plants. As this is the first study on vibratory communication of the European tarnished plant bug, we believe these findings may contribute considerably to the better understanding of the mating behavior of this important pest species.     

The acoustic behaviour of the bushcricket Tettigonia cantans II. Transmission of airborne-sound and vibration signals in the biotope

The airborne-sound and the vibratory signals produced by stridulating $\text{Tettigonia cantans}$ males, and the transmission of these signals in the natural biotope were investigated.The song of $\text{T. cantans}$ is composed of repeated uniform syllables with a rate of ca. 30/sec. Intensity approaches 100 dB SPL, 10 cm away from the animal. The spectrum shows three dominant frequency ranges around 8, 16 and 32 kHz.Airborne transmission of the song in such vegetation layers as are found in the biotopes of $\text{T. cantans}$ shows an excess attenuation which increases with frequency. The relative intensities of the frequency components of the song vary as a result of the kind of vegetation, the positions of emitter and receiver, and the separation distance. These relative differences in intensity may be useful during the phonotactic approach to conspecific partners, providing a measure of the distance from the sound source.Stridulating males also produce vibratory signals in the plants they sit on. The spectrum of these signals includes frequencies up to 8 kHz, the first dominant frequency of the song: low frequency components are induced in the plants via the legs and abdomen of the animal. The vibratory signals are transmitted mainly in the form of bending waves. Near the animal, amplitude modulation corresponds to that of the song. At greater distances, reflections and frequency-dependent propagation velocities, cause distortions of this time pattern. Transmission depends greatly on the mechanical properties of the particular plant, attenuation values of 20–50 dB/m being found. Nevertheless, in most cases, vibratory signals may be perceived up to 1.5 – 2 metres away from a stridulating male.     

Vibratory signals of four Neotropical stink bug species

Abstract. The stink bugs Acrosternum impicticorne, Euschistus heros, Piezodorus guildinii and Thyanta perditor (Heteroptera: Pentatomidae) feed and mate on the same host plants and constitute major components of the soybean pest complex in Brazil. During mating, they communicate with species and sex-specific vibratory signals whose spectral properties are characteristic of the subfamily Pentatominae. Songs differ between species in the time structure and amplitude modulation of their units. The repertoire of A. impicticorne, E. heros and T. perditor fits into the scheme described for most investigated stink bugs: females call with a sequence of pulses that differ between species in their duration and repetition rate, and males respond with courtship songs of species-specific temporal structure and amplitude modulation of complex pulse trains. Female calling and male courtship songs are the main constituents of vibratory communication between sexes in the mating period. The other vibratory emissions appear to represent either transitional songs, support recognition during close-range courtship, or are involved in male rivalry. The first recorded vibratory emissions of P. guildinii confirm that the genus Piezodorus represents an exception within the Pentatominae. Irregularly repeated female vibratory signals of P. guildinii do not trigger typical male courtship responses as they would in the small stink bugs Holcostethus strictus and Murgantia histrionica. On the other hand, complex rivalry with extensive frequency modulation of pulses, as also described in Piezodorus lituratus, opens a new insight into the role of vibratory communication in stink bugs.     

Vibrational directionality in the southern green stink bug, Nezara viridula (L.), is mediated by female song

We tested the hypothesis that male southern green stink bugs, Nezara viridula (L.), use substrate-borne songs to locate females. We recorded the responses of bugs on plants to the vibrations caused by a prerecorded female song and by an artificial sound. The female song caused males to walk, to respond with the calling and courtship songs and to approach the source of the song with characteristic search behaviour at junctions between branches on the plants. At a junction, a searching male stopped, stretched his legs and antennae and compared the vibratory signals on the two branches, with different combinations of legs and antennae. The males then left the junction and approached the source of the vibration. Males located the loudspeaker significantly more frequently in the presence than in the absence of vibratory stimuli on cyperus, Cyperus alternifolius L., and beans, Phaseolus vulgaris L. Vibrational directionality was also elicited by artificial pure tones whose spectral and temporal parameters were similar to those of natural female song. Females showed no reaction to vibratory stimulation and no vibrational directionality. We discuss possible mechanisms underlying vibrational directionality in the light of expected signal changes during transmission through plants. Copyright 1999 The Association for the Study of Animal Behaviour.     

Acoustic defence in an insect: characteristics of defensive stridulation and differences between the sexes in the tettigoniid Poecilimon ornatus (Schmidt 1850)

Many insects exhibit secondary defence mechanisms upon contact with a predator, such as defensive sound production or regurgitation of gut contents. In the tettigoniid Poecilimon ornatus, both males and females are capable of sound production and of regurgitation. However, wing stridulatory structures for intraspecific acoustic communication evolved independently in males and females, and may result in different defence sounds. Here we investigate in P. ornatus whether secondary defence behaviours, in particular defence sounds, show sex-specific differences. The male defence sound differs significantly from the male calling song in that it has a longer syllable duration and a higher number of impulses per syllable. In females, the defence sound syllables are also significantly longer than the syllables of their response song to the male calling song. In addition, the acoustic disturbance stridulation differs notably between females and males as both sexes exhibit different temporal patterns of the defence sound. Furthermore, males use defence sounds more often than females. The higher proportion of male disturbance stridulation is consistent with a male-biased predation risk during calling and phonotactic behaviour. The temporal structures of the female and male defence sounds support a deimatic function of the startling sound in both females and males, rather than an adaptation for a particular temporal pattern. Independently of the clear differences in sound defence, no difference in regurgitation of gut content occurs between the sexes.