Reproductive behaviour and vibratory communication of the neotropical predatory stink bug Podisus nigrispinus

Vibratory communication during reproductive behaviour is less well described in predatory (Asopinae) than in phytophagous (Pentatominae) stink bugs. Different steps in the mating behaviour of the predatory stink bug Podisus nigrispinus (Dallas) (Hemiptera: Pentatomidae; Asopinae) are described in the present study, together with vibratory signals emitted on artificial and natural substrate during courtship and copulation. Vibratory signals in Podisus nigrispinus have a decisive role in copulation success and are produced in both sexes by abdominal vibration and tremulation. In P. nigrispinus, one species‐specific female and two male songs, which do not show the calling function typically found in phytophagous stink bugs, are produced by abdominal vibration and are emitted during reproductive behaviour. Additionally, P. nigrispinus produces tremulatory signals that have no species or sex specificity. Tremulatory signals emitted spontaneously on a plant as a sequence of readily repeated pulses are similar to the calling songs of the Pentatominae stink bug. These signals may carry information on the presence of a mate; however, in other behavioural contexts, they may have a different function, such as advertisement or even alarm signals. Plants transmit vibratory signals produced by both mechanisms as a low‐pass filter, increasing the amount of low‐frequency components. The results of the present study raise important questions about the interaction between chemical and vibratory signals in the mating behaviour of predatory stink bugs.     

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.     

The effect of vibratory disturbance on sexual behaviour of the southern green stink bug Nezara viridula (Heteroptera, Pentatomidae)

The effect of vibratory disturbance on sexual behaviour and substrate-borne sound communication of the southern green stink bug, Nezara viridula L. was studied. Disturbance signals do not change the time N. viridula males need to locate the source of vibratory signals, but decrease the number of males responding with the calling and courtship song to calling females. Female N. viridula proceed calling during stimulation with disturbance signals but some of them change the song rhythm by skipping one or more signal intervals or emitting the repelling signals. The number of females which change the dominant frequency of the calling song decreases proportionally with increasing differences between the dominant frequency of the disturbance signals and the emitted female calling song. Variation of the song dominant frequency probably serves females to avoid interference by increasing the signal to noise ratio. Signal duration and repetition rate do not change significantly when the female is stimulated with the disturbance signals. This indicates that frequency shift by calling females is the main strategy for reducing interference by competitive signalers in N. viridula vibrational communication.     

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.     

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 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.     

Stink bug interaction with host plants during communication

In solitary plant-dwelling stink bug species, success depends crucially on efficient mate location and recognition, mediated by signals transmitted through the plant. All stink bugs investigated so far communicate with species and sex-specific narrow-band calling and courtship song signals produced by abdomen vibration. Calling songs of lower specificity are characterized by readily repeated units emitted with regular repetition rate from the same place on a plant, while courtship songs take place at shorter distances in the process of species and sex recognition, together with signals of other modalities. Signal spectra with about 100Hz fundamental frequency and harmonics below 1000Hz are tuned to the resonant properties of their green host plants. The majority of the identified leg vibratory receptor cells and the underlying ventral cord interneurons respond best in the frequency range below 500Hz. Green plants with low pass filtering properties transmit optimally signals with a dominant frequency around 100Hz and strongly attenuate vibrations above 600Hz. Accurate tuning of signal spectral properties with the plant's mechanical characteristics enables communication over several meter distances, with dispersive bending waves running through the plant's rod-like structures under standing wave conditions.     

Mechanism of mate detection in parasitoid wasps: sound and vibratory cues change with the developmental progress of future mates inside host pupal cases

Insects including parasitoid wasps use acoustic and vibratory signals in the context of sexual communication, mate recognition, courtship and mating. Males of the parasitoid wasp Pimpla disparis Viereck (Hymenoptera: Ichneumonidae) detect insect host pupae parasitized by a conspecific female, learn their location, visit them repeatedly and remain on or near them when the prospective mate nears emergence. In the present study, the acoustic and vibratory cues that males exploit to detect the presence and track the developmental progress of a future mate inside a host pupal case are investigated. Responses are acquired from developing parasitoids (DePa) by airborne sound and laser Doppler vibrometer recordings, after gently stimulating each of 20 wax moth host pupae with a paintbrush on days 1–23 post parasitism. Sound and vibratory cues produced by DePa are detectable from day 7 onward and relate mostly to spinning movements. Parameters of sound and vibratory cues (amplitude, dominant frequency, upper limit of frequency band) change significantly over time and thus could ‘inform’ a visiting adult male about the stage of development of DePa. Adult males antennating a parasitized pupa and flying around it also induce vibrations, which in turn may inform DePa about the presence of a male. There is no experimental evidence for true signalling and rapid information exchange between DePa and adult males. Delaying reply signals may help DePa avoid attacks by illicit receivers of such signals, including female (hyper)parasitoids and invertebrate predators.     

Transmission of Podisus maculiventris tremulatory signals through plants

Males of the predaceous stink bug Podisus maculiventris (Say) (Heteroptera: Pentatomidae: Asopinae) emit low frequency tremulatory signals. Laser vibrometry was used to record and analyze naturally emitted signals, focusing on variation in signal velocity and frequency during transmission through plants (Phaseolus vulgaris L. and Plumbago auriculata Lam.) as a function of distance from the vibrational source. Signal velocity varied individually between 2 and 15 mm/s recorded on a plant close to the calling male and decreased by 0.3 to 1.5 dB/cm on bean and 0.3 to 0.9 dB/cm on plumbago. The dominant frequency of signals was variable at frequencies below 50 Hz. On bean frequencies centered around 10 Hz or 20 Hz were dominant for signals recorded at the source. Transmission through bean resulted in an increase in the 20 Hz peak relative to other frequencies in the signal. Variation of the dominant frequencies of signals transmitted through plumbago stems were more predictable, showing typical changes in amplitude relative to the distance from the source. The regular variation of the dominant frequency along the stem with linear increase of signal velocity at decreasing distance from the source may provide plant-dwelling insects with information about the distance to the calling individual.     

Tremulatory and Abdomen Vibration Signals Enable Communication through Air in the Stink Bug Euschistus heros

Communication by substrate-borne mechanical signals is widespread among animals but remains one of their least understood communication channels. Past studies of vibrational communication in insects have been oriented predominantly to communication during mating, showing that species- and sex-specific vibrational signals enable recognition and localization of potential mates on continuous solid substrates. No special attention has been paid to vibrational signals with less obvious specificity as well as to the possibility of vibrational communication across substrates that are not in physical contact. We aimed to reinvestigate emission of the aforementioned vibrational signals transmitted through a plant in the stink bug Euschistus heros (Pentatomidae: Pentatominae) and to check whether individuals are able to communicate across adjecent, physically separated substrates. We used laser vibrometry for registration of substrate-borne vibrational signals on a bean plant. Using two bean plants separated for 3 to 7 cm between two most adjacent leaves, we investigated the possibility of transmission of these signals through air. Our study showed that males and females of E. heros communicate using tremulatory, percussion and buzzing signals in addition to the previously described signals produced by vibrations of the abdomen. Contrary to the latter, the first three signal types did not differ between sexes or between pentatomid species. Experiments with two physically separated plants showed significant searching behaviour and localization of vibrational signals of an E. heros male or a female, in response to abdominal vibration produced signals of a pair duetting on the neighbouring plant, in comparison to control where no animals were on the neighbouring plant. We also confirmed that transmission through air causes amplitude and frequency decay of vibrational signals, which suggests high-amplitude, low-frequency tremulatory signals of these stink bugs their most plausible way of communication across discontinuous substrates.     

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.     

Songs of Holcostethus strictus (Fabricius): a different repertoire among landbugs (Heteroptera: Pentatomidae)

Songs emitted during mating by male and female Holcostethus strictus were recorded as substrate vibrations. Spectra of the vibrational signals have a dominant frequency peak between 100 and 260 Hz and in this respect reflect the general characteristic of the family Pentatomidae. Songs of H. strictus differ from the song repertoire of the southern green stink bug Nezara viridula (L.) (Pentatomidae) in many respects. The female calling and courtship songs differ in echeme and phrase duration. The male calling song is composed of spectrally different subunits. The male courtship song is characterised by three types of spectrally and temporally different echemes. The male copulatory song is composed of echemes of two types, which constitute a phrase of less regular temporal structure. In H. strictus, males start to sing first and female songs are less complex than in N. viridula. The female calling song is evoked by male calling and does not trigger male response. The female and male courtship song phrases are superimposed on one another and we have not observed any obvious regularity in their exchange. The possible role of different songs in H. strictus is discussed and compared with that in other pentatomide landbug species.     

Vibratory courtship in a web-building spider: signalling quality or stimulating the female?

Courtship behaviour in spiders in the form of premating vibrations by males may function (1) as a male identity signal used for species recognition, (2) in suppression of female aggressiveness, (3) to stimulate female mating behaviour, or (4) as a quality signal used in female choice. We investigated the function of web vibration by male Stegodyphus lineatus in a series of experiments. Regardless of vibratory performance, all males mated successfully with virgin females but only 56.4% of males mated with nonvirgin females. Vibratory performance did not influence male mating success, but heavier males had a higher probability of mating with mated females. Males vibrated less often and produced fewer vibrations when introduced on the web of a mated female. Males that vibrated webs of virgin females mated faster than nonvibrating males, but there was no effect of vibration rate or body mass. There was no effect of male vibratory effort or vibration rate on female reproductive success measured as time to egg laying, clutch size, number of hatched young, number of dispersed young and offspring body mass after a single mating. Males vibrated on abandoned virgin female webs but the response decreased with increasing duration of female absence, suggesting that females produce a web-borne pheromone, which elicits male vibrating behaviour. Mated females were less receptive and not stimulated by male vibrating behaviour. We conclude that male premating vibrations in S. lineatus do not function as a male quality signal selected via female choice. Rather, the primary function of this behaviour may be to stimulate a receptive female to mate. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Male Competition in a Wandering Spider (Cupiennius getazi,Ctenidae)

We describe male-male competition in a wandering spider living on plants (Cupiennius getazi, Ctenidae) and discuss it within the general context of the mating system. 1. Males produce vibratory courtship signals (duration about 20 s) and competition signals (2 s). Upon exposure to female silk, males produce almost exclusively courtship signals (98%) if alone or in the presence of a female. In the presence of a rival alone, an average of 25% of a male's vibratory signals are courtship signals and 75% competition signals. In the presence of both a rival and a female, an average of 50% are courtship and 50% competition signals. Females respond to both male courtship and/or competition signals with vibratory courtship whereas males react by vibratory competition. The intensity of the reaction of both males and females is independent of the signal type. 2. Males displaying vibratory signals move slowly over the plant and repel attacks from rivals and females with extended front legs. Pairs of males interact in three ways. (i) Both males produce vibratory signals; one of them leaves the plant (53% of 90 trials). (ii) Both males vibrate, approach and touch (20%) or pounce on each other (20%). (iii) A male approaches the signalling opponent without producing vibrations and attacks him (7%). This is a conditional vibrocryptic tactic. The presence of a female incites male competition. Males do not interact with the female but approach each other (in 24% of the 26 trials “vibrocryptically”) and escalate more often (88%) and more quickly to overt fight than in the absence of a female. The male remaining on the plant approaches the female. 3. Male-male fights are ritualized. During 64 bodily contacts no male was injured. Males exposed to female silk and males using the vibrocryptic tactic were more often the winners of an interaction than males not exposed to female silk and than males vibrating while approaching their rival. The outcome of fights is not correlated with age, leg length, body weight and rate of signalling when no female is present. In contrast, body weight and leg length determine the outcome when a responding female is present, the larger male being the winner. 4. Intrasexual and intersexual interactions suggest that both male competition and female choice mechanisms may regulate sexual selection in this species.     

Sound is involved in multimodal communication of Loxosceles intermedia Mello-Leitão, 1934 (Araneae; Sicariidae)

Signals of different modalities are involved during courtship of the brown spider Loxosceles intermedia. A spine on the pedipalp is rubbed against the grooves on the retrolateral region of the chelicerae producing stridulatory signals, which have a dominant frequency of the airborne component range around 770 Hz for females and around 170 Hz for males. These values are significantly lower for the substrate-borne component. The sound pressure level of stridulatory signals lies below 50 dB and the velocity values below 1 mm/s. The copulation frequency does not depend on the presence of pedipalps in females; however, in males the removal of pedipalps decreases the courtship frequency. During courtship, females vibrate their abdomens after being touched by the courting male, producing tremulatory signals with the dominant frequency below 100 Hz, sound pressure level below 60 dB and velocity below 3 mm/s. This vibration may function as a sign of the akinesia state since it precedes the introduction of the embolus. Cuticular compounds probably determine the recognition of the male by the female. Data from the present study corroborate the generalist nature of L. intermedia in which signals of different modalities are used during courtship.     

Host location by a parasitoid using leafminer vibrations: characterizing the vibrational signals produced by the leafmining host

Abstract. The aim of this study was to characterize the vibrations produced by the apple tentiform leafminer Phyllonorycter malella (Ger.) (Lepidoptera, Gracillariidae). Host location using vibrations by one of its parasitoids Sympiesis sericeicornis Nees (Hymenoptera, Eulophidae) was postulated by Casas (1989) on the basis of detailed quantitative behavioural observations and has also been suggested by other authors on similar systems. Both host and parasitoid send and may receive vibratory signals; consequently we first attempted to characterize and classify the signals, one of the first steps required in the design of an adequate vibrational biotest. In this respect, our approach differs fundamentally from the familiar setting of host location via semiochemicals and is best framed within the context of vibratory communication. Vibrational signals produced by a moving larva and pupa were measured on several spots on the leaf using a laser vibrometer. The emitted signals were characterized by their temporal patterns of change in amplitude and frequency spectra. The vibrational patterns released by a moving larva were different from those released by a wriggling larva and a wriggling pupa in the time as well as in the frequency domains. Wriggling larvae and wriggling pupae triggered vibrations that were similar in frequency, but differed in their temporal pattern. Frequencies up to 15 kHz could be identified. The amplitudes and frequencies of the signals both decreased significantly from the tip to the base of the leaf. A wriggling pupa and a wriggling larva produced stronger signals than a foraging larva. All calculated parameters (displacement, velocity, acceleration, and duration of the signal components) of the vibrational signals were found to be in a range comparable with others used for well-known arthropod communication systems. The vibrations produced by the host displayed distinct characteristics: they could usually be distinguished easily from background noise; could be perceived anywhere on the leaf; and were specific for a certain host stage and activity. Our findings support the hypothesis that vibration signals represent a reliable source of information to foraging parasitoids and, therefore, explain certain behavioural patterns observed in a population of S. sericeicornis females foraging in the field.     

Male–male interactions and male mating success in the leafhopper Aphrodes makarovi

In mating systems based on substrate‐borne vibrations, sexual communication often involves a reciprocal exchange of species‐ and sex‐specific vibrational signals and male is searching for a stationary female. In the leafhopper Aphrodes makarovi, female reply is essential for successful location of the female and its variable duration directly affects male's costs associated with signalling and searching. We studied male and female behaviour in a trio situation (two males and one female), and our results show that male–male competition had important effects on male mating success. Females replied equally to advertisement calls emitted by the winning and losing males and mated with the first male that located them, regardless of his investment in calling effort. Males eavesdropped to male–female duet maintained by the rival, and the winners were better at exploiting female replies to the rival's advertisement calls by silently approaching the female. To interfere with the ongoing male–female duet, males also emitted masking signals overlapping the latter part of the female reply. More overlapped female replies were registered in response to the losers and masking signals most likely delay the rival in reaching the female. Our study shows that a comprehensive understanding of male mating success and female preferences in vibrational duetting systems requires also investigations in more complex settings that more realistically represent the situation in nature.     

Vibratory signals of the harlequin bug and their transmission through plants

Abstract. Males of the harlequin bug, Murgantia histrionica (Hahn), produce five different vibrational songs, whereas females produce one song. Songs differ from those of other stink bugs primarily in their species‐specific temporal characteristics. The broad band male courtship songs of M. histrionica are achieved by a combination of different frequency modulated and/or narrow band subunits, with several higher harmonic frequencies. Males rather than females initiate substrate‐borne vibrational communication, and the longer‐range calling songs found typically in other pentatomid species are lacking. Interindividual differences in song temporal and spectral characteristics are discussed. Transmission of vibrational songs through a cabbage head is more efficient along veins than along lamina. Attenuation of signals transmitted through veins is low and similar to that reported previously for plant stalks. On the leaf vein, distances between peak amplitude minima and maxima are different for the dominant and subdominant frequencies. At any distance from the vibration source, a different relationship between spectral peak amplitudes can be recorded. Resolution of these differences, together with velocity differences between signals recorded on the vein and lamina, may help small stink bugs to estimate distance and to locate each other on a plant.     

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.