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.     

Plasticity of the phonotactic selectiveness of four species of chirping crickets (Gryllidae): Implications for call recognition

Earlier studies of phonotaxis by female crickets describe this selective behavioural response as being important in the females' choices of conspecific males, leading to reproduction. In the present study, moderate (30+) to very large data sets of phonotactic behaviour by female Acheta domesticus L., Gryllus bimaculatus DeGeer, Gryllus pennsylvanicus Burmeister and Gryllus veletis Alexander demonstrate substantially greater plasticity in the behavioural choices, as made by females of each species, for the syllable periods (SP) of model calling songs (CS) than has been previously described. Phonotactic choices by each species range from the very selective (i.e. responding to only one or two SPs) to very unselective (i.e. responding to all SPs presented). Some females that do not respond to all SPs prefer a range that includes either the longest or shortest SP tested, which fall outside the range of SPs produced by conspecific males. Old female A. domesticus and G. pennsylvanicus are more likely to be unselective for SPs than are young females. Each species includes females that do not respond to a particular SP when responding to CSs with longer and shorter SPs. The results suggest that the plasticity of phonotactic behaviour collectively exhibited by the females of each species does not ensure that choices of a male's CS effectively focus the female's phonotactic responses on CSs that represent the conspecific male. The phonotactic behaviour collectively exhibited by females of each species does not readily fit any of the models for selective processing by central auditory neurones that have been proposed to underlie phonotactic choice.     

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.     

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.     

Phonotactic behaviour and vertical sound source localisation of the parasitoid fly Emblemasoma auditrix (Diptera: Sarcophagidae)

1. Acoustically guided movement in a three‐dimensional space is a complex behavioural task performed notably by birds, bats, and some insect species. The precision of acoustic orientation depends on the directionality of the hearing system as well as on auditory behaviour. 2. The fly Emblemasoma auditrix Diptera (Sarcophagidae) is a parasitoid of the cicada Okanagana rimosa Auchenorrhyncha (Cicadidae) and locates its host in the complex habitat of a forest. The phonotactic behaviour of the fly was analysed experimentally with emphasis on the vertical domain in the field. Different experimental setups allowed discriminating subsequent steps in the phonotactic behaviour of E. auditrix. 3. During the phonotactic flight, flies first landed on landmarks, which were used to re‐adjust to the elevation of the sound source. Acoustic targets were located from these resting positions. The sound source elevation was detected at the start of the flight as the longitudinal body axis was adjusted to the inclination of the target sound source. 4. Flies usually did not land directly upon the sound source, but landed nearby, and most often above the target. Within the target area, types of movement for the final approach differed in respect to target position; flies walked predominantly if the final target was located above or below, but for horizontally located targets much of the distance was covered by flight. 5. In conclusion, E. auditrix can locate the acoustic target in complex habitats and uses a flexible multi‐step approach for short‐range phonotaxis.     

Auditory pattern recognition and steering in the cricket Teleogryllus oceanicus

Male crickets Teleogryllus oceanicus (Le Guillou) produce a complex species‐specific calling song with phrases combining groups of single pulses (chirps) and groups of double‐pulses (trills) to attract females, which fly or walk towards singing males. In open‐loop trackball experiments, phonotactic steering responses to normal calling song phrases consisting of chirps and trills are strongest, suggesting that both components are necessary for maximal attractiveness. Sequences of just chirps or trills are less effective in eliciting phonotactic walking and steering. Split‐song paradigms are used to analyze the steering behaviour underlying orientation in more detail. The females' phonotactic steering reflects the alternating acoustic pattern of the split‐song paradigm. Analysis with high temporal resolution demonstrate, that even when the calling song is presented only from one side, the steering velocity and lateral deviation towards the song is modulated by steering events to single‐sound pulses. Therefore, pattern recognition, which integrates the structure of the song, appears not to be directly involved in the rapid steering response. This organization of phonotactic behaviour with a parallel processing of pattern recognition and steering is similar to other cricket species and may allow T. oceanicus females to steer transiently towards distorted song patterns as they occur in natural habitats.     

Processing of model calling songs by the prothoracic AN2 neurone and phonotaxis are significantly correlated in individual female Gryllus bimaculatus

Syllable period (SP) selective calling song processing has been demonstrated for the prothoracic, AN2 auditory neurone that correlates very well with SP‐selective phonotaxis by female cricket Gryllus bimaculatus De Geer. Both SP‐selective processing by the AN2 and the phonotactic behaviour of the female exhibit substantial plasticity. Thus, the question remains as to whether the selective responses of the AN2 neurone and the selective behaviour of the female match in an individual female. The present study is designed to answer that question. The SP‐selective phonotactic behaviour of individual females is evaluated, followed immediately by measuring the SP‐selective responses of the same female's AN2 neurone. Very significant correlations are found between the selective responses of the AN2 neurone and the same female's selective behaviour. In 208 possible comparisons (26 females, eight behavioural and neuronal tests each), 186 resulted in matches between behaviour and neuronal processing. Dividing the SP‐selective females into two groups (one group that responded phonotactically to the shortest SP tested and a second group that did not respond to this SP) resulted in significantly more selective responses to this shortest SP by the AN2 neurone in the females that responded phonotactically to the SP than for the females who did not respond to the shortest SP. The behavioural responses by these two groups to the other SPs tested are shown to be essentially identical.     

Influence of habitat structure on the phonotactic strategy of a parasitoid fly Emblemasoma auditrix

Abstract.  1. Females of the parasitoid fly Emblemasoma auditrix find their host cicadas ( Okanagana rimosa ) using the acoustic signals produced by the host. The phonotactic behaviour of the parasitoid was studied with regard to differently structured habitats.
2. Habitats were modified experimentally within a distance of 2.5 m (approximately the natural range of phonotaxis) from a loudspeaker broadcasting a model of the host calling song.
3. Video analysis showed that in an open habitat (no landmarks) more than 60% of the flies performed a direct flight towards the loudspeaker.
4. In structured habitats (with one to three landmarks) more than 90% of the flies landed on their way to the acoustic target.
5. In about 50% of the landings flies paused for several seconds indicating re-orientation during that time. Several flies included sequences of walking in their approach behaviour, whereby most walking occurred close to the loudspeaker.
6. In summary, the phonotactic approach and host finding depends on the habitat structure.     

Vibratory Communication in the Jumping Spider Phidippus clarus: Substrate‐borne Courtship Signals are Important for Male Mating Success

Recently, work has shown that multimodal communication is common throughout the animal kingdom but the function of multimodal signals is still poorly understood. Phidippus clarus are jumping spiders in which males produce multimodal (visual and vibrational) signals in both male–male (aggressive) and male–female (courtship) contexts. The P. clarus mating system is complex, with sex ratios and the level of male competition changing over the course of the breeding season. Vibrational signal components have been shown to function in male aggressive contests but their role in courtship has not been investigated. Here, we performed an experiment to test the role of vibrational signaling in courtship by observing mating success for males that were experimentally muted. We show that vibratory courtship signals, and in particular signaling rate, is an important component of mating success and potentially a target of female choice. While the ability to produce vibratory signals significantly increased mating success, some muted males were still able to successfully mate. In these trials, signaling rate also predicted mating success suggesting that redundant signal components may compensate for errors and perturbations in signal transmission or that vibratory signals function to enhance the efficacy of visual signals.     

Vibratory Communication and its Relevance to Reproductive Isolation in two Sympatric Stink Bug Species (Hemiptera: Pentatomidae: Pentatominae)

Communication is in phytophagous stink bugs of the subfamily Pentatominae related to mating behavior that among others includes location and recognition of the partner during calling and courting. Differences in temporal and frequency parameters of vibratory signals contributes to species reproductive isolation. Chinavia impicticornis and C. ubica are two green Neotropical stink bugs that live and mate on the same host plants. We tested the hypothesis that differences in temporal and spectral characteristics of both species vibratory signals enable their recognition to that extent that it interrupts further interspecific communication and copulation. To confirm or reject this hypothesis we monitored both species mating behaviour and recorded their vibratory songs on the non-resonant loudspeaker membranes and on the plant. The level of interspecific vibratory communication was tested also by playback experiments. Reproductive behavior and vibratory communication show similar patterns in both Chinavia species. Differences observed in temporal and spectral characteristics of female and male signals enable species discrimination by PCA analyses. Insects that respond to heterospecific vibratory signals do not step forward to behaviors leading to copulation. Results suggest that species isolation takes place in both investigated Chinavia species at an early stage of mating behavior reducing reproductive interference and the probability of heterospecific mating.     

Characterizing the vibratory and acoustic signals of the “purring” wolf spider,Gladicosa gulosa (Araneae: Lycosidae)

Both airborne acoustic signals and substrate-borne vibrations are prevalent modes of animal communication, particularly in arthropods. While a wide variety of animals utilize one or both of these modalities, the connection between them is still ambiguous in many species. Spiders as a group are not known for using, or even perceiving, acoustic signals, despite being well-adapted for vibratory communication. Males of the “purring” wolf spider Gladicosa gulosa are reported to produce audible signals during courtship, although the literature on this species is largely anecdotal. Using a laser Doppler vibrometer and an omnidirectional microphone in controlled conditions, we recorded and characterized the visual and mechanical (both substrate-borne and airborne) signals of this species in an attempt to provide a qualitative and quantitative overview of its signal properties. We found that the vibratory signal is composed of two primary repeating and alternating elements, consisting of pulses of stridulation and percussive strikes, as well as a less common, but repeatable, third element. We also characterized a measurable airborne component to the signal that is significantly correlated with the amplitude of the vibratory signal, which we suggest is a by-product of the strong vibration. Neither modality correlated significantly with male body size or condition. Although the exact role of the acoustic component is unclear, we speculate that the unique properties of signalling in this species may have value in answering new questions about animal communication.     

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.     

Orchestrating the score: complex multimodal courtship in the Habronattus coecatus group of Habronattus jumping spiders (Araneae: Salticidae)

Jumping spiders in the genus Habronattus use complex multimodal signals during courtship displays. In the present study, we describe multimodal displays from the Habronattus coecatus clade, comprising a diverse group of 23 described species. Habronattus coecatus group displays are made up of sex‐specific ornamentation and temporally coordinated combinations of motion displays and vibratory songs. Vibratory songs are complex, consisting of up to 20 elements organized in functional groupings (motifs) that change as courtship progresses. This temporal structuring of displays is analogous to a musical composition. Vibratory elements are associated with movement displays involving coloured and patterned ornaments on the male body. We describe general patterns of multimodal displays for 11 species including one, Habronattus borealis, which appears to have lost complex display behaviour. Habronattus coecatus group courtship is one of the most complex communication systems yet described in arthropods and this group may reveal important factors driving the evolution of complex signals. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 522–547.     

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.     

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.     

Auditory lateralization in bushcrickets: a new dichotic paradigm

Pair formation in the bushcricket Gampsocleis gratiosa is achieved through acoustic signalling by the male and phonotactic approaches of the female towards the calling song. On a walking belt in the free sound field, females tracked the position of the speaker broadcasting the male calling song with a remarkable precision, deviating by no more than 10 cm in either direction from the ideal course. Starting with stimulus angles of 6–10° the females significantly turned to the correct side, and with stimulus angles greater than 25° no incorrect turns were made. Using neurophysiological data on the directionality of the ear we calculated that with such stimulus angles the available binaural intensity difference is in the order of 1–2 dB. We developed a dichotic ear stimulation device for freely moving females with a cross-talk barrier of about 50 dB, which allowed to precisely apply small binaural intensity differences. In such a dichotic stimulation paradigm, females on average turned to the tronger stimulated side starting with a 1 dB difference between both ears. The significance of such a reliable lateralization behaviour with small interaural intensity differences for phonotactic behaviour under natural conditions is discussed.     

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.     

Vibratory signals enhance mate-guarding in a water strider (Hemiptera: Gerridae)

Mating males of the water strider Gerris remigisproduce vibratory signals when-single males grasp mating pairs. When played through live females with dead males on their backs, these signals repelled mating attempts by single males. A previous study showed that male mate-guarding enhances female foraging effectiveness in this species. Thus male mate-guarding signals also enhance female foraging effectiveness.     

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.