Consistency of females’ stridulatory behaviour during inter‐sexual interactions in spiders

In a sexual context, it is expected that females base their choice of mate on the behaviours that males perform during courtship, as such behaviours are associated with the male's mate quality. Stridulation is one form of female communication in arthropods, for example, spiders. In spiders, stridulation during sexual interactions is relatively common in some groups but mainly restricted to males. In the pholcid spider Holocnemus pluchei (Pholcidae), both sexes have stridulatory organs. The aims of the present work were to: (a) determine possible differences in the frequency of occurrence of stridulation between females during inter‐sexual interactions, (b) establish female consistency in stridulation along repeated interactions and (c) analyse if female stridulation is associated with certain male behaviours during pre‐copulatory courtship and with male size. Female H. pluchei showed highly repeatable differences in their frequency of stridulation across consecutive encounters with males (ICC = 0.64). However, only a modest level of repeatability was detected in total time females spent stridulating across trials (ICC = 0.19). Females’ mean stridulatory behaviour did not change across ten consecutive trials spread across 20 days, and their behaviour was apparently unaffected by male persistence of copulatory attempted and/or size. These results imply that the frequency of female stridulatory behaviour is a trait that is highly characteristic of each individual. Finally, our work opens the door to determine whether behavioural consistency manifests in other ecological contexts and their functional implications.     

Intracolony vibroacoustic communication in social insects

Vibrations and sounds, collectively called vibroacoustics, play significant roles in intracolony communication in termites, social wasps, ants, and social bees. Modalities of vibroacoustic signal production include stridulation, gross body movements, wing movements, high-frequency muscle contractions without wing movements, and scraping mandibles or tapping body parts on resonant substrates. Vibroacoustic signals are perceived primarily via Johnston’s organs in the antennae and subgenual organs in the legs. Substrate vibrations predominate as vibroacoustic modalities, with only honey bees having been shown to be able to hear airborne sound. Vibroacoustic messages include alarm, recruitment, colony activation, larval provisioning cues, and food resource assessment. This review describes the modalities and their behavioral contexts rather than electrophysiological aspects, therefore placing emphasis on the adaptive roles of vibroacoustic communication. Although much vibroacoustics research has been done, numerous opportunities exist for continuations and new directions in vibroacoustics research.     

Colony Wide Behavioral Contexts of Stridulation in Imported Fire Ants (Solenopsis invicta Buren)

Red imported fire ants, Solenopsis invicta, possess stridulatory organs and stridulate in a variety of contexts. We used a stethoscope mounted microphone to study stridulation at the colony level in the context of emigration, disturbance, and excavation. In conjunction with preliminary observations of nest and foraging activities, our results suggest stridulation serves multiple functions in S. invicta. Stridulation was not significantly increased in colonies during responses to disturbance, and only marginally during colony emigration. Colonies involved in excavation, however, exhibited a significant increase in stridulatory activity. Four possible explanations for the function of stridulation in this context are discussed in relation to the stridulatory behavior of individuals, solitary wasps, and published literature on formicid stridulation.     

Unusual abdomino-alary,defensive stridulatory mechanism in the bushcricket Pantecphylus cerambycinus (Orthoptera,Tettigonioidea, Pseudophyllidae)

The bushcricket Pantecphylus cerambycinus has two types of stridulatory mechanisms and acoustical signals. The elytro-elytral mechanism typical for tettigonioid bushcrickets is used to produce a narrow-band calling song (peak frequency 15 kHz). An abdomino-alary mechanism is used for disturbance stridulation. Its stridulatory file is situated on the hind edge of the abdominal tergites and consists of 50-70 parallel ridges, covering the whole width of the tergite. The broad-band sound (peak frequency 10 kHz) is produced by the contact between the file and ribs situated on the upper side of the hindwings which are folded in such a way that their upper side is directed toward the tergites. Defensive stridulation in bushcrickets is reviewed here, and its function and evolution discussed in the context of predator avoidance strategies. © 1996 Wiley-Liss, Inc.     

Signalling and Sexual Conflict: Female Spiders Use Stridulation to Inform Males of Sexual Receptivity

The use of acoustic signals by males during courtship and mating is well known. Nevertheless, their association with female unwillingness to mate is much less studied. In spiders, stridulation during sexual interactions is relatively common in some groups, but mainly restricted to males. In the pholcid spider Holocnemus pluchei, both sexes have stridulatory organs. The aims of the present work were (1) to establish whether female stridulation occurs during intra‐ and inter‐sexual interactions, (2) to determine whether female reproductive status affects the likelihood that she will stridulate and (3) to determine whether female stridulation is influenced by male sexual behaviour. We found that female stridulation usually occurs both during intrasexual interactions and, most frequently, during intersexual interactions. Females with more previous matings stridulated more frequently. Stridulation intensity was higher in females that did not accept new copulations compared with those that copulated. Female stridulation did not vary in elaborated and non‐elaborated courtship. Thus, females use stridulation to communicate levels of sexual receptivity. It is also possible that females use stridulation to indirectly assess male ability to persist and persuade.     

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.     

Pharmacological brain stimulation releases elaborate stridulatory behaviour in gomphocerine grasshoppers – conclusions for the organization of the central nervous control

Grasshoppers produce a variety of sounds generated by complex movements of the hindlegs. Stridulation, performed in the context of partner finding, mating and rivalry, can be released by pressure injection of cholinergic agonists into the protocerebrum. Particularly stimulation with muscarinic agonists induced long-lasting stridulation that resembled the natural behaviour to an astonishing degree, not only with respect to their temporal structure and right/left coordination, but also to changes in the song sequences according to the progress of courtship stridulation, even including accessory movements of other parts of the body. According to the complexity of their stridulatory behaviour ten gomphocerine species were chosen for this comparative study. The results indicate that the protocerebrum fulfils two important tasks in the control of stridulation: (1) it integrates sensory input relevant to stridulation that represents a certain behavioural situation and internal state of arousal, and (2) it selectively activates and deactivates the thoracic networks that generate the appropriate movement and sound patterns. With the knowledge of the natural behaviour and the accessibility to pharmacological and electrophysiological studies, the cephalic control system for stridulation in grasshoppers appears to be a suitable model for how the brain selects and controls appropriate behaviours for a given situation.     

SOUND PRODUCTION BY AQUATIC INSECTS

1. Sound production by aquatic insects is found in four orders — Trichoptera, Odonata, Heteroptera and Coleoptera. 2. Immature aquatic insects that produce sound are rare, stridulation being present in one family of Trichoptera (Hydropsychidae) and one genus and species in a relic suborder of Odonata (Anisozygoptera) - Epiophlebia superstes. Hydropsychid larvae produce sound with a head/fore femur mechanism and use sound as part of aggressive behaviour for defence of feeding nets. Larval E. superstes use a hind femur/abdominal mechanism to dissuade predators. 3. Sound production has been documented in adults of all families of aquatic Heteroptera except Helotrephidae. In corixids and notonectids, acoustic signals play a role in mating. Members of the genus Buenoa (Notonectidae) are unique in having two stridulatory mechanisms in the same individual. Sound production has been most intensively studied in the Corixidae. Although sounds are used in mating by all singing corixids, their use seems to be facultative in some species and obligatory in others. Recent experiments by Theiss (1982) have shown that the air stores carried by corixids are used for both sound radiation and reception. 4. The adephagan beetle families Hygrobiidae, Dytiscidae and Haliplidae have all been shown to produce sound. Mechanisms of sound production have been established for haliplids and hygrobiids but have yet to be for most dytiscids. Sound production is used by beetles as part of sequences of aggressive/defensive and reproductive behaviour. 5. Sound production is especially well documented in the Hydrophilidae (Polyphaga). Hydrophilids use an abdominal/elytral mechanism and sound appears to be used in the same contexts as in adephagans. 6. Insects that produce sound under water must contend with the physical problems of sound transmission in a relatively dense, viscous medium with sharp boundaries. Because of potential distortion of the frequency components in a signal by reflection from the air/water interface in very shallow water, frequency is unreliable for encoding information. Aquatic insects use instead amplitude modulation and temporal patterning of signals. 7. For aquatic invertebrates, sound fields are different than those in air because the extent of the near field is approximately four times greater in water. This near field, a region in which displacement waves are predominant over pressure waves, extends to a greater distance than most aquatic insects communicate over. Such displacement waves could have important but as yet unconsidered effects. 8. The mass and viscosity of the water dictates that sound producing structures of aquatic insects should be heavier and more massive than those of terrestrial insects. A survey of stridulatory organs of aquatic insects reveals this to be true and reveals that the relatively fragile, membranous stridulatory organs of some terrestrial insects (especially Orthoptera) are absent. 9. The elaboration of sound producing structures in aquatic insects probably occurred at the family or subfamily level and for Heteroptera, Trichoptera and Odonata evolved after the invasion of the water. Acoustic signals used reproductively would probably be more closely associated with the emergence of new taxa. 10. Stridulatory structures have been derived from either structures devoted to some other function or from structures involved in the behaviour currently enhanced by sound production.     

Sexual selection and the evolution of exclusive paternal care in arthropods

Internal fertilization and anisogamy are thought to impede the evolution of exclusive paternal care by reducing paternity assurance and increasing male promiscuity. The potential role of sexual selection in easing these constraints is currently being examined in vertebrates but has not been seriously studied in most arthropods. To distinguish the effects of sexual from natural selection on the evolution of arthropod paternal care, I tested predictions of the state of several life history and behavioural traits under both forms of selection across all known taxa with exclusive paternal care. The results suggest parallels between prezygotic nuptial gifts and exclusive postzygotic paternal care and support the hypothesis that, in arthropods, male behaviours that enhance female reproductive success either directly by releasing females from the fecundity constraints of maternal care (enhanced fecundity hypothesis) or indirectly by identifying mates with superior genes (handicap principle) are traits on which sexual selection has acted. Under such conditions males willing to guard young become preferred mates for gravid females and enjoy greater promiscuity than males unable or unwilling to guard. Females use nest construction or the act of guarding another female's eggs as honest signals of paternal intent and quality. Copyright 2000 The Association for the Study of Animal Behaviour.     

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.     

Auditory information processing in stridulating grasshoppers: tympanic membrane vibrations and neurophysiology

During stridulation in the gomphocerine grasshopper Omocestus viridulus the leg movements, sound pattern and either summed auditory nerve activity or single interneuron activity were recorded. Simultaneous laser interferometric and vibrometric measurements of the displacement and velocity of the tympanic membrane were performed at the pyriform vesicle (d-receptor group). Slow displacements of the tympanic membrane occur in phase with the ventilatory and stridulatory rhythm and reach 10 m_peak-peak and 1–3 m_peak-peak in amplitude, respectively. Additionally, the tympanic membrane oscillates maximally in the range 5–10 kHz. These high-frequency oscillations are due to sound production and motor activity and correspond in amplitude to oscillations evoked by sound pressures of 90-dB SPL. They activate the auditory receptors during most of the stridulatory cycle even during mute stridulation. Only at the lower reversal point of the leg movement are membrane vibrations and receptor activity at a minimum. As a consequence the response of receptors and interneurons to auditory stimuli are generally impaired and an auditory response of receptors and interneurons can be elicited only during a short period at the lower reversal point. Although in this phase of the stridulatory cycle auditory sensitivity is present, males do not show phonotactic responses towards female songs during ongoing own stridulation.     

Phylogenetic analysis of the Wnt gene family and discovery of an arthropod wnt-10 orthologue

Wnt genes encode a conserved family of secreted signaling proteins that play many roles in arthropod and vertebrate development. We have investigated both the phylogenetic history and molecular evolution of this gene family. We have identified a novel Wnt gene in a diversity of arthropods that it is likely an orthologue of the vertebrate Wnt-10 group. Wnt-10 is one of only two cases in which orthology between protostome and deuterostome genes could be consistently assigned based on our analyses. Despite difficulties in assessing orthologies, all of our trees suggest that the most recent common ancestor of protostomes and deuterostomes possessed more than the five Wnt genes known from either arthropods or nematodes. This suggests that Wnt gene loss has occurred during protostome evolution. In addition, we examined the rate of amino acid evolution in the two arthropod/deuterostome orthology groups we identified. We found little rate variation across taxa, with the exception that Drosophila Wnt-1 is evolving more rapidly than all vertebrate and most arthropod orthologues.     

Reverse stridulatory wing motion produces highly resonant calls in a neotropical katydid (Orthoptera: Tettigoniidae: Pseudophyllinae)

This paper describes the biomechanics of an unusual form of wing stridulation in katydids, termed here 'reverse stridulation'. Male crickets and katydids produced sound to attract females by rubbing their forewings together. One of the wings bears a vein ventrally modified with teeth (a file), while the other harbours a scraper on its anal edge. The wings open and close in rhythmic cycles, but sound is usually produced during the closing phase as the scraper moves along the file. Scraper-tooth strikes create vibrations that are subsequently amplified by wing cells specialised in sound radiation. The sound produced is either resonant (pure tone) or non-resonant (broadband); these two forms vary across species, but resonant requires complex wing mechanics. Using a sensitive optical diode and high-speed video to examine wing motion, and Laser Doppler Vibrometry (LDV) to study wing resonances, I describe the mechanics of stridulation used by males of the neotropical katydid Ischnomela gracilis (Pseudophyllinae). Males sing with a pure tone at ca.15 kHz and, in contrast to most Ensifera using wing stridulation, produce sound during the opening phase of the wings. The stridulatory file exhibits evident adaptations for such reverse scraper motion. LDV recordings show that the wing cells resonate sharply at ca. 15 kHz. Recordings of wing motion suggest that during the opening phase, the scraper strikes nearly 15,000 teeth/s. Therefore, the song of this species is produced by resonance. The implications of such adaptations (reverse motion, file morphology, and wing resonance) are discussed.     

Historical use of substrate-borne acoustic production within the Hemiptera: first record for an Australian Lophopid (Hemiptera, Lophopidae)

Abstract  Here the first record of communication through substrate-borne vibrations for the Lophopidae family is reported. The signals from Magia subocellata that the authors recorded were short calls with a decreasing frequency modulation. Acoustic vibrations have been observed for other families within the Hemiptera and a scenario concerning the historical use of vibrational communication within the Hemiptera is tested using a phylogenetic inference. The most parsimonious hypothesis suggests that substrate-borne communication is ancestral for the hemipteran order and highlights the groups for which future acoustic research should be undertaken.     

Analysis of the Stridulation in Solifuges (Arachnida: Solifugae)

Stridulation in solifuges has not been investigated yet. We performed a comparative analysis of the stridulatory organs and sounds produced by juveniles of various developmental stages and adults (both sexes) of Galeodes caspius subfuscus Birula. The stridulatory organ is of similar morphology in all developmental stages. The sound that they produced was a broad frequency hissing, composed of one or two chirps with maximum at 2.4 kHz. The intensity of the sound was found to increase with body size. Otherwise, no differences were observed between stridulation in juvenile, male and female individuals. Therefore, we suggest that the stridulation in solifuges has primarily a defensive role. As solifuges are neither venomous nor unpalatable, they might imitate an accoustically aposematic organism that shares the same habitat and has similar circadian activity, e.g. vipers. It may also have an intraspecific function in reduction of cannibalistic tendencies.     

A unique form of light reflector and the evolution of signalling in Ovalipes (Crustacea: Decapoda: Portunidae)

The first demonstration, to our knowledge, of an evolutionary shift in communication mode in animals is presented. Some species of Ovalipes display spectacular iridescence resulting from multilayer reflectors in the cuticle. This reflector is unique in animals because each layer is corrugated and slightly out of phase with adjacent layers. Solid layers are separated from fluid layers in the reflector by side branches acting as support struts. An effect of this reflector is that blue light is reflected over a ''broad'' angle around a plane parallel to the sea floor when the host crab is resting. Species of Ovalipes all possess stridulatory structures. The shallow-water species with the best developed stridulatory structures are non-iridescent and use sound as a signal. Deep-water species possess poorly developed stridulatory structures and display iridescence from most regions of the body. In deep water, where incident light is blue, light display is highly directional in contrast to sound produced via stridulation. Sound and light display probably perform the same function of sexual signalling in Ovalipes, although the directional signal is less likely to attract predators. Deep-water species of Ovalipes appear to have evolved towards using light in conspecific signalling. This change from using sound to using light reflects the change in habitat light properties, perhaps the hunting mechanisms of cohabitees, and its progression is an indicator of phylogeny. The changes in sexual signalling mechanisms, following spatial–geographical isolation, may have promoted speciation in Ovalipes.     

Stridulatory behaviour in a New Zealand weta, Hemideina crassidens

Using a femoral-abdominal stridulatory mechanism, wetas produce the following stridulatory behaviours: aggression, mating, calling, defence and disturbance. Syllable period, rather than number of syllables/echeme or syllable duration, was the most stereotyped temporal parameter for aggression, mating and calling stridulation. Coefficients of variation of the above parameters were large and overlapped considerably for aggression and mating stridulation. We concluded that, for these two behaviours, a basic sound pattern is used to convey different messages to female and male receiver wetas, respectively, but the syllable period of the pattern decreases with increased excitation of males in aggressive encounters. In adult male combat, winners stridulated last in a bout, and produced significantly more aggression sounds than losers.     

Vibrational signalling in a Gondwanan relict insect (Hemiptera: Coleorrhyncha: Peloridiidae)

Ancient, long-extinct floras and faunas can be reassembled through fossils and phylogenetics, and even palaeo-environments can be reconstructed with the aid of palaeoclimatology. However, very little is known about the sound-scape of the past. Of what kind were the first biologically meaningful sounds and vibrations ever emitted and perceived? The earliest signals in the history of life were probably produced by arthropods making use of the mechanical properties of their exoskeleton. Here, we report an observation of vibrational signalling in the coleorrhynchan Hackeriella veitchi, a representative of a Gondwanan relict insect lineage which is still extant in the Queensland rainforest. Our finding suggests that vibrational signalling by tymbal organs is ancestral for the Hemiptera (exclusive of Sternorrhyncha)--the song of the Coleorrhyncha was a likely element of the acoustic environment in the Permian moss forests and had possibly changed little since.     

Stridulatory pattern generation in acridid grasshoppers: metathoracic interneurons in Stenobothrus rubicundus (Germar 1817)

Stridulation was elicited in tethered gomphocerine grasshoppers of the species Stenobothrus rubicundus in order to identify interneurons of the stridulation pattern generator, and describe their morphological and physiological properties. Nine types of such neurons could be found and characterized; eight of those could additionally be compared to corresponding neuron types previously known from other species. As shown in detail for one selected type, the neurons of the stridulation pattern generator are very similar in their anatomical appearance, and possess similar physiological qualities at least in two species with similar stridulation patterns. Stridulation interneurons of species with largely different stridulatory motor patterns have a similar morphology, but show a different activation timing throughout the stridulation. Nevertheless, special properties such as resetting or initiation capability of certain stridulation interneurons seem to be conserved throughout the species. The results suggest that the stridulation pattern generator of different species consists of a uniform set of interneurons that change their activity pattern to produce species-specific song movements.     

Substrate Vibrations during Courtship in Three Drosophila species

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