Chapter

Evolutionary and Phylogenetic Origins of Tympanal Hearing Organs in Insects

November 2014

November 2014

DOI:10.1007/978-3-642-40462-7_2

In book: Insect Hearing and Acoustic Communication (pp.5-26)
Chapter: Evolutionary and Phylogenetic Origins of Tympanal Hearing Organs in Insects
Publisher: Springer
Editors: Berthold Hedwig

Authors:

Johannes Strauss

Justus-Liebig-Universität Gießen

Reinhard Lakes-Harlan

Justus-Liebig-Universität Gießen

Among insects, tympanal ears evolved at least 18 times, resulting in a diversity of auditory systems. Insects use their ears in different behavioural contexts, mainly intraspecific communication for mate attraction, predator avoidance, and parasitic host localisation. Analysing the evolution of insect ears aims at revealing the phyletic origins of auditory organs, the selection pressures leading to the evolution of ears, the physiological and behavioural adaptations of hearing, and the diversification of ears in specific groups or lineages. The origin of sensory organs from preadapted proprioceptive or vibroceptive organs has now been established for different ear types. In this review, we embed research on insect hearing in a phylogenetic framework to reconstruct the ancestral sensory situation in different taxa, and the series of morphological changes during the evolution of an ear. The importance of sensory and neuroanatomical data is discussed for either mapping onto a phylogeny or as characters for phylogenetic analysis.

Motor control and directional accuracy of phonotaxis in female field crickets

Thesis

Nov 2021

Athanasios Ntelezos

This thesis addresses two aspects of the phonotactic behavior of female field crickets (Gryllus bimaculatus) as they orient towards singing males: the first one is how the auditory input is integrated into the motor activity underlying their walking responses, and the second one is how accurately they can localize a singing male in a dynamic stimulus situation. Although it has been established that the conspecific calling song is recognized via a circuit in the brain, it is not clear how pattern recognition is linked to descending motor control of phonotaxis. To analyze the auditory-induced motor responses, I recorded high-speed videos of crickets performing phonotaxis and tracked the movement of their bodies and appendages. The video analysis showed that when crickets commence phonotaxis, their body parts and appendages are activated and moved from anterior to posterior in the following order: antennae, head, prothorax, front legs, middle legs. During phonotaxis the antennae move continuously side-to-side in a rhythmic pattern, and on top of this rhythmic movement is superimposed a shift to the side the calling song is presented from. Moreover, the prothorax makes small rhythmic movements that are coupled to the stepping cycle, and on top of these rhythmic movements also steers towards the side the calling song is presented from. Following up on the results of the video analysis, I recorded the activity of the antennal muscles of the scape in crickets that performed phonotaxis. The scape contains two muscles: the adductor muscle that adducts the antenna towards the median line, and the abductor muscle that abducts it laterally. The activity of the adductor muscle is coupled to the adduction movement of the antenna during the contralateral presentation of the calling song, while the activity of the abductor muscle is coupled to the abduction movement during the ipsilateral presentation of the calling song. The antennal movement and muscular activity – especially the abduction movement and the activity of the abductor muscle – are coupled to the calling song on a chirp-to-chirp basis. The neurites of the motoneurons of the antennal muscles are located in the deutocerebrum, while the ascending auditory pathway projects into the protocerebrum. I discuss that additional auditory brain interneurons must be involved for the transfer and processing of the auditory-to-motor signal from the protocerebrum to the deutocerebrum. I also investigated the function of several thoracic muscles for potential contribution to the prothoracic movements contributing to phonotaxis. Of all the muscles tested, only the activity of pronotal muscle 56 was coupled to the prothoracic movements in crickets performing phonotaxis. Specifically, the activity of muscle 56 was coupled both to the rhythmic prothoracic movements that are coupled to the stepping cycle and to the auditory-induced steering of the prothorax. Like the antennae, the prothorax turns to the active speaker and also responds to the calling song on a chirp-to-chirp basis. I discuss that auditory input to the motoneurons of muscle 56 in the prothoracic ganglion is likely indirect via a pathway descending from the brain. Finally, I tested the accuracy of female crickets walking on a trackball as they performed phonotaxis towards a speaker oscillating constantly between 45° left and 45° right relative to their long axis. In a group of crickets, I used a drop of wax to fix the prothorax against the mesothorax and test the effect of the immobilization of the prothorax has on auditory steering. The performance of the crickets with the fixed prothorax was not statistically different from the performance of the crickets that could freely move the prothorax, however, the crickets with the fixed prothorax generally understeered towards the more lateral angles of stimulus. Overall, in this dynamic situation the angular resolution of the crickets was 6-11° in their frontal range, which is less accurate than the previously reported 1-2° for phonotaxis towards a static sound source. The results show that crickets find orientation towards a moving sound source more challenging than towards a static one. This was further corroborated with tests where the crickets steered to the correct side when two speakers positioned 5° to the left and 5° to the right alternated in the presentation of the calling song, meaning their angular resolution for static sound sources was at least 5°.

Cricket tympanal organ revisited: morphology, development and possible functions of the adult-specific chitin core beneath the anterior tympanal membrane

Article

Full-text available

Aug 2019
CELL TISSUE RES

Vertebrates and insects are phylogenetically separated by millions of years but have commonly developed tympanal membranes for efficiently converting airborne sound to mechanical oscillation in hearing. The tympanal organ of the field cricket Gryllus bimaculatus, spanning 200 μm, is one of the smallest auditory organs among animals. It indirectly links to two tympana in the prothoracic tibia via tracheal vesicles. The anterior tympanal membrane is smaller and thicker than the posterior tympanal membrane and it is thought to have minor function as a sound receiver. Using differential labeling of sensory neurons/surrounding structures and three-dimensional reconstructions, we revealed that a shell-shaped chitin mass and associated tissues are hidden behind the anterior tympanal membrane. The mass, termed the epithelial core, is progressively enlarged by discharge of cylindrical chitin from epithelial cells that start to aggregate immediately after the final molt and it reaches a plateau in size after 6 days. The core, bridging between the anterior tracheal vesicle and the fluid-filled chamber containing sensory neurons, is supported by a taut membrane, suggesting the possibility that anterior displacements of the anterior tracheal vesicle are converted into fluid motion via a lever action of the core. The epithelial core did not exist in tympanal organ homologs of meso- and metathoracic legs or of nymphal legs. Taken together, the findings suggest that the epithelial core, a potential functional homolog to mammalian ossicles, underlies fine sound frequency discrimination required for adult-specific sound communications.

Evolution of Acoustic Communication in Insects

Chapter

Full-text available

Jun 2016

Michael D Greenfield

Tympanal organs for hearing in the far field have evolved on multiple occasions among insects and are currently found in seven orders. Many, if not most, cases of insect hearing probably originated as a means for detecting and avoiding predators. In particular, sensitivity to ultrasound appears to have coevolved with echolocation signaling by insectivorous bats. However, on an overall scale, hearing is relatively rare among insects in comparison with other modalities of perception, including detection of substrate vibration. Sound signaling in insects, which typically occurs in the context of mating communication, is rarer still and is known in only five orders. Phylogenetic analyses suggest that acoustic communication in the Lepidoptera and in the suborder Caelifera (grasshoppers) of the Orthoptera originated via a “sensory bias” mechanism. Hearing was ancestral and sound signaling by males subsequently arose on multiple, independent occasions. On the other hand, acoustic communication in the Cicadidae and in the suborder Ensifera (crickets, katydids) of the Orthoptera may have originated via coevolution between female perception and male signaling. The diversity of songs among acoustic insects may reflect genetic drift and reproductive character displacement. There is little evidence, however, that insect songs are adapted to specific physical environments. In one clade of acoustic insects, the diversification of song is associated with an unusually high rate of population differentiation and speciation, which may be facilitated by a genomic co-localization of loci influencing female response/preference and male signaling. The extent to which co-localization is a general factor in speciation remains to be explored.

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

Article

Jul 2015
ECOL ENTOMOL

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.

Behavioural and neural studies of male singing and female phonotaxis behaviour in crickets

Thesis

Apr 2021

Chu-Cheng Lin

Acoustic communication in crickets is achieved by the production of calling, courtship, and rivalry songs in male crickets and the recognition of the songs by conspecifics. Male crickets sing by rhythmically opening and closing the forewings to generate sound pulses and song patterns. The central command for singing is controlled by the brain. The song structure is under control of the abdominal central pattern generator (CPG) and acts as a behavioural barrier to prevent courtship with females of closely related species. Therefore, an analysis of the song structure, the central command, and the organisation of the CPG in different cricket species could reveal how evolution shaped cricket singing behaviour. In G. bimaculatus, I recorded different song types and corresponding wing movement of individual males. I discovered a small amplitude oscillation of the forewings during courtship song that was not reported before. The similar pulse parameters and wing movements during calling and rivalry song could imply a shared neural network for the two song types in G. bimaculatus. I analysed rivalry and courtship behaviour before and after applying specific lesions to the abdominal nerve cord in G. bimaculatus. Most elements of rivalry and courtship behaviour are not affected by lesions, except for rivalry song, courtship song, and copulation. For generation of the rivalry song the central nerve cord from the brain to A4 is sufficient (same as calling song), whereas the whole nerve cord without the terminal abdominal ganglion is required for generation of courtship song. I compared the calling song before and after applying specific lesions to the abdominal nerve cord in four cricket species: G. rubens, G. assimilis, Teleogryllus oceanicus, and T. commodus. The four species show similar effects of the lesions on the generation of sound pulses besides a species-specific control of song structure, suggesting they share a conserved organisation of the CPG network for calling song. Following the discovery of the calling song command neuron in G. bimaculatus, I carried out intracellular recording in the brain of males of different species. I found the putative command neurons for calling song in G. bimaculatus, G. assimilis, and T. commodus and characterize the physiological and functional properties of these neurons. The results suggest the command neurons in the three species could be homologues by showing a similar control on generating calling song. Furthermore, based on female cricket phonotaxis preference I developed an animal acoustic selecting system, in which the females have to navigate through a complex parkour to reach the acoustic stimulus presenting speaker. I tested the system with different selecting experiments and proved the system can be applied to select females attracted to certain song pattern. Overall, these findings broaden our understanding of cricket singing in terms of neural control of different song types and evolution of singing behaviour in different species, and provide a new tool to study phonotactic behaviour.

Mapping the Auditory Space of Culex pipiens Female Mosquitoes in 3D

Article

Full-text available

Sep 2023

Simple Summary Mosquitoes possess one of the best-developed and sensitive hearing systems among insects. Their auditory Johnston’s organs located at the antennae bases include several thousand radially distributed sensory cells. Male mosquitoes use their hearing for acoustic courtship behavior, while the function of hearing in blood-sucking female mosquitoes is poorly studied. In addition to courtship behavior, hearing is presumed to be used for host detection, including the use of human voices as an attraction cue. Since mosquitoes spread dangerous diseases such as West Nile fever, understanding their hearing system is of crucial importance. We studied the auditory system of Culex pipiens female mosquitoes using behavioral and electrophysiological experiments and created a three-dimensional model of the mosquito auditory space. The in-flight position of antennae was found optimal for binaural hearing focused primarily in front of, above and below a mosquito. By varying the antennae position a mosquito can adjust the directional properties of hearing depending on behavioral context. According to our findings, the auditory system of female mosquitoes has enough resolution to estimate the direction to the sound source, while its frequency range enables detection of sounds produced by other flying mosquitoes and human hosts. Abstract The task of directional hearing faces most animals that possess ears. They approach this task in different ways, but a common trait is the use of binaural cues to find the direction to the source of sound. In insects, the task is further complicated by their small size and, hence, minute temporal and level differences between two ears. A single symmetric flagellar particle velocity receiver, such as the antenna of a mosquito, should not be able to discriminate between the two opposite directions along the vector of the sound wave. Paired antennae of mosquitoes presume the usage of binaural hearing, but its mechanisms are expected to be significantly different from the ones typical for the pressure receivers. However, the directionality of flagellar auditory organs has received little attention. Here, we measured the in-flight orientation of antennae in female Culex pipiens pipiens mosquitoes and obtained a detailed physiological mapping of the Johnston’s organ directionality at the level of individual sensory units. By combining these data, we created a three-dimensional model of the mosquito’s auditory space. The orientation of the antennae was found to be coordinated with the neuronal asymmetry of the Johnston’s organs to maintain a uniformly shaped auditory space, symmetric relative to a flying mosquito. The overlap of the directional characteristics of the left and right sensory units was found to be optimal for binaural hearing focused primarily in front of, above and below a flying mosquito.

Reconstruction of sound driven, actively amplified and spontaneous motions within the tree cricket auditory organ

Preprint

Full-text available

Nov 2021

A bstract Hearing consists of a delicate chain of events. Sound is first captured by an eardrum or similar organ which is set into vibrations, these vibrations must then be transmitted to sensory cells in a manner that opens mechanosensory channels generating an electrical signal. Studying this process is challenging. Auditory vibrations are in the nano- to picometer-scale and occur at fast temporal scales of milli to microseconds. Finally, most of this process occurs within the body of the animal where it is inaccessible to conventional measurement techniques. For instance, even in crickets, a century-old auditory model system, it is unclear how sound evoked vibrations are transmitted to sensory neurons. Here, we use optical coherence tomography (OCT) to measure how vibrations travel within the auditory organ of the western tree cricket ( Oecanthus californicus ). We also measure the reversal of this process as mechanosensory cells generate spontaneous oscillations and amplify sound-evoked vibrations. Most importantly, we found that while the mechanosensory neurons were not attached to the peripheral sound collecting structures, they were mechanically well-coupled through acoustic trachea. Thus, the acoustic trachea are not merely conduits for sound but also perform a mechanical function. Our results generate several insights into the similarities between insect and vertebrate hearing, and into the evolutionary history of auditory amplification.

Experimental river noise alters arthropod abundance

Article

Full-text available

Sep 2021

Anthropogenic noise has received considerable recent attention, but we know little about the role that sources of natural noise have on wildlife abundance and distributions. Rivers and streams represent an ancient source of natural noise that is widespread and covers much of Earth. We sought to understand the role that whitewater river noise plays on arthropod abundance in riparian habitats across a desert landscape. For two summers, we continuously broadcasted whitewater river noise and spectrally-altered river noise (shifted upwards in frequency, but maintaining the same temporal profile) to experimentally tease apart the effects of two characteristics of noise – sound levels and background spectral frequency – on arthropod abundances. We used five types of trapping methods, placed across 20 sites within the Pioneer Mountains of Idaho, USA, to collect and identify 151 992 specimens to the order level. We built Bayesian generalized linear mixed-effects models with noise characteristics and other habitat variables such as riparian vegetation, elevation, temperature, and moonlight. Of the 42 models we built (one for each order-trap type combination), 26 (62%) indicated a substantial response to at least one noise variable – sound pressure level, background spectral frequency, or an interaction between the two. Fourteen of 17 (82%) arthropod orders responded to noise in some capacity: Araneae, Coleoptera, Collembola, Dermaptera, Hemiptera, Hymenoptera, Lepidoptera, Neuroptera, Opiliones, Orthoptera, Plecoptera, Raphidioptera, Thysanoptera and Trichoptera. Only three groups appeared to be unaffected, Acari, Archaeognatha and Diptera. Results from this study suggest that the natural acoustic environment can shape arthropod abundances both directly and indirectly (via predator–prey relationships). Future work should further examine the role that the indirect effects of noise play in food webs. Natural noise should be considered an important ecological niche axis, especially as we continue to alter natural acoustic environments and replace them with anthropogenic ones.

Bridging the Gap Between Mammal and Insect Ears – A Comparative and Evolutionary View of Sound-Reception

Article

Full-text available

Jul 2021

Insects must wonder why mammals have ears only in their head and why they evolved only one common principle of ear design—the cochlea. Ears independently evolved at least 19 times in different insect groups and therefore can be found in completely different body parts. The morphologies and functional characteristics of insect ears are as wildly diverse as the ecological niches they exploit. In both, insects and mammals, hearing organs are constrained by the same biophysical principles and their respective molecular processes for mechanotransduction are thought to share a common evolutionary origin. Due to this, comparative knowledge of hearing across animal phyla provides crucial insight into fundamental processes of auditory transduction, especially at the biomechanical and molecular level. This review will start by comparing hearing between insects and mammals in an evolutionary context. It will then discuss current findings about sound reception will help to bridge the gap between both research fields.

Does the addition of a new signalling trait enhance receiver responses in diurnal geckos?

Article

Mar 2021
BEHAV PROCESS

Animal signals in multiple modalities expands the opportunity for effective communication. Among diurnal geckos of the genus Cnemaspis, chemical signalling traits preceded the evolution of visual traits. Males of all species possess chemical secreting ventral glands, but only in some species, males also express yellow gular patches. This difference in the expression of unimodal or multimodal signalling traits between closely related species provided us with an opportunity to understand the use of multimodal signals for communication. We studied receiver responses in Cnemaspis indica, a sexually monochromatic species, and in C. littoralis, a species where males possess yellow gulars. We performed behavioural trials where individuals of each species were exposed to only chemical stimuli, only visual stimuli, or both chemical and visual stimuli simultaneously from male and female conspecifics. Our results show that only chemical stimuli were necessary and sufficient to elicit responses in males and females of C. indica as well as in females of C. littoralis. However, males of the dimorphic C. littoralis required the multimodal stimulus to elicit movement-based responses. Our results suggest that the evolution of colour traits in diurnal geckos is associated with a partial shift in some receiver responses toward multimodal communication, with no addition to the behavioural repertoire.

Functional diversity of attachment and grooming leg structures is retained in all but the smallest insects

Article

Full-text available

Nov 2020
J ZOOL

Miniaturization strongly affects functional morphology. Whereas some anatomical structures are barely affected by scaling, others can fundamentally change as the body becomes ever smaller. No prior study has focused on the effect of miniaturization on grooming and attachment structures in Hymenoptera, which can be highly diverse and complex. Through comparative description of the legs of the extremely small wasps of the families Mymaridae and Trichogrammatidae, we evaluate the functional and phylogenetic patterns concerning possible functional effects of miniaturization. On the one hand, the studied species retain some features characteristic of other Chalcidoidea, while on the other, they display some parallelisms associated with miniaturization in leg structure. These observations support a two‐stage morphocline of miniaturization, wherein the first stage is characterized by the preservation of structural complexity and retention of all basic functions, as for instance in examined Megaphragma and the females of Dicopomorpha. The second stage is characterized by a significant simplification, with the loss of redundant non‐essential functions, as observed for the males of Dicopomorpha, which have grossly reduced leg structures, including total loss cleaning devices. Whether these stages are ordered or unordered should be evaluated in future study. Functional optimization of attachment in male Dicopomorpha is indicated by the highly derived mushroom‐shaped tarsi, complemented by novel grappling spurs on the hindfeet, possibly for copulation. Our observations underline adaptive trade‐offs in the expression of complex and multifunctional leg structures at extreme scales.

Adaptive Strategies in Life-History of Bushcrickets (Orthoptera) and Cicadas (Homoptera) to Parasitoids Pressure on Their Acoustic Communication Systems—A Case for Sociality?

Article

Full-text available

Aug 2019

In sexual reproduction, the search for mating partners elevates the individual’s risks of predation and parasitism. One way to increase mate search effectiveness and reduce search costs is acoustic signaling. However, acoustic orienting parasitoid flies exploit singing hosts, leading to high parasitism rates. Aggregations of males and females at mating and singing in choruses might reduce individual risks by dilution and predator saturation. This mini-review reflects on consequences for host’s acoustic signaling in choruses using the examples of cicadas and bushcrickets. It concludes that despite antagonistic selection pressure by parasitoids, singing in choruses might select for increased, not reduced signaling in males. The time joining and leaving a chorus might be crucial: once mated, a refractory period will drop males off the signaling pool, preventing parasitism. In a chorus, fast and loud singing might be highly advantageous, supporting the fittest males. Natural selection might have shaped signaling strategies in choruses, which can probably only be understood when applying individual based dynamic modeling.

Adaptive Strategies in Life-History of Bushcrickets (Orthoptera) and Cicadas (Homoptera) to Parasitoids Pressure on Their Acoustic Communication Systems—A Case for Sociality?

Article

Full-text available

Aug 2019

In sexual reproduction, the search for mating partners elevates the individual's risks of predation and parasitism. One way to increase mate search effectiveness and reduce search costs is acoustic signaling. However, acoustic orienting parasitoid flies exploit singing hosts, leading to high parasitism rates. Aggregations of males and females at mating and singing in choruses might reduce individual risks by dilution and predator saturation. This mini-review reflects on consequences for host's acoustic signaling in choruses using the examples of cicadas and bushcrickets. It concludes that despite antagonistic selection pressure by parasitoids, singing in choruses might select for increased, not reduced signaling in males. The time joining and leaving a chorus might be crucial: once mated, a refractory period will drop males off the signaling pool, preventing parasitism. In a chorus, fast and loud singing might be highly advantageous, supporting the fittest males. Natural selection might have shaped signaling strategies in choruses, which can probably only be understood when applying individual based dynamic modeling.

Implications of the Tympanal Hearing Organ and Ultrastructure of Chaetotaxy for the Higher Classification of Embioptera

Article

Jul 2019

Several slowly evolving characters are evaluated with the main objective of reinforcing the higher classiication of Embioptera. An embiopteran femoral auditory organ, described here for the irst time, exhibits diferences in shape and position that provide diagnostic criteria for higher taxonomic groups in the order. New characters on silk ejectors, bladders, and various types of leg setae are also discussed within a taxonomic framework. he utility of these new traits and their diferent conditions, for identifying monophyletic groups, was tested by a preliminary phylogenetic analysis.

Ultrasound avoidance by flying antlions (Myrmeleontidae)

Article

Full-text available

Sep 2018

The acoustic arms race between insectivorous bats and their invertebrate prey has led to the convergent evolution of ultrasound hearing in seven orders of nocturnal insects. Upon hearing the echolocation calls of an approaching bat such insects take defensive action. Here we document an unknown sense of ultrasound hearing and phonotactic flight behaviour in the neuropteran family Myrmeleontidae (antlions). The antlion Myrmeleon hyalinus was presented with sound pulses at ultrasonic frequencies used by echolocating bats and its response thresholds in tethered flight determined. Behaviours included abdominal twitches, wing-flicks, brief pauses in flight and flight cessation. Such behaviours create erratic evasive flight manoeuvres in other eared insects, particularly mantids and lacewings. Antlions responded best to ultrasound between 60-80 kHz (75 dB peSPL at 80 kHz) showing response thresholds similar to the related lacewings (Neuroptera, Chrysopidae). Yet at lower ultrasonic frequencies (20-50 kHz) antlions were far less sensitive than lacewings. Based on calculated response distances we conclude that antlions respond only after having been detected by bats rather than using early evasive flights. We argue that the high response threshold for low frequency ultrasound is adaptive for an insect that is mainly active close to and within vegetation, because a behavioural response to the lower ultrasonic frequencies used by high-flying bats would result in evasive action in the absence of actual predation risk.

Bio-inspired Visual Motion Sensing Systems for Mobile Robots

Thesis

Aug 2017

Cheng Hu

Many animals, especially flying insects are experts on reacting to approaching predators. For robots, the ability to avoiding collisions is also crucial. In locusts, a visual neuron called the Lobula Giant Movement Detector (LGMD) has been identified to be responsible for evoking collision avoidance behaviours. It has been modelled for collision avoidance on large robots or vehicles whose computational power are abundant. For micro robots, however, the limited computational capabilities on-board prevent the LGMD model to be accomplished on the robot by its own. Therefore in earlier researches, those micro robots serve only as image grabbers and motion actuators, leaving majority of the model processed on a host device connected. The unavoidable communication and consequent latency have become the bottlenecks that restrains the employment of this promising collision avoidance model in multi-agent research fields such as swarm robotics. This research focuses on the embedded modelling and realization of this bio-inspired collision sensitive model ELGMD. By carefully considering the required on-board resource, a novel micro robot Colias IV is designed to meet the requirements. Featured with the sufficient computing power, various of sensing modalities including a tiny camera, the modularized design and other specialities, this robot has become an advantageous platform to perform embedded vision tasks. The bio-inspired neural model Embedded-LGMD (ELGMD) is realized on the micro robot that can run autonomously without any off-board guidance. Optimization on the structure and timing has guaranteed its computational efficiency. The performance of the ELGMD and the effectiveness on triggering the robot’s collision avoidance behaviour are tested via systematic experiments. To achieve more precise interactive behaviours with other kinds of moving obstacles, a compound motion detection system is realized within the robot to detect various of motion patterns by integrating several neural models at a higher level, in which those LGMD-like neural models are accomplished by an unified ELGMD model with minimum reconfiguration. Experiments have been conducted to validate the improved ELGMD model and the compound motion detection system. Results of this research have demonstrated the design goals of all the proposed modules, including the hardware platform, the bio-inspired model and the compound motion detection system, indicating the practicability of implementing these bio-inspired visual motion sensing systems for further robotic studies.

Evolutionary diversification of the auditory organ sensilla in Neoconocephalus katydids (Orthoptera: Tettigoniidae) correlates with acoustic signal diversification over phylogenetic relatedness and life history

Article

Jun 2017
J EVOLUTION BIOL

Neoconocephalus tettigoniids are a model for the evolution of acoustic signals as male calls have diversified in temporal structure during the radiation of the genus. Tettigoniidae have hearing organs in the forelegs with species-specific numbers of auditory sensilla in a linear crista acustica. We investigated changes of the hearing organs during an evolutionary radiation with divergence of intraspecific acoustic signals. We compared the neuroanatomy of the crista acustica from 9 Neoconocephalus species with different temporal call features, life histories, and from different phylogenetic positions. Average numbers of auditory sensilla were species-specific, ranging between 32–35 sensilla. It is likely under sexual selection for detection of male calls and natural selection for detection of bat calls. We found statistically significant differences in sensillum numbers among species, but no relationship of crista acustica length or sensillum number with phylogenetic position or life history. Statistically significant correlations existed with call patterns: species with slow pulse rates had significantly higher numbers of auditory sensilla and a longer crista acustica. Further, species with a derived double-pulsed calls had longer cristae, and continuous callers had a higher number of auditory sensilla. Correlations with crista length were stronger than with the number of auditory sensilla. The hearing organs show considerable diversity between species despite their recent divergence and morphological and ecological similarities. Thus, they have the potential to respond to various selective pressures, including divergence of temporal and spectral signal properties. Phylogenetic constraints are unlikely to limit the evolutionary change of the auditory systems. This article is protected by copyright. All rights reserved.

Multimodal shifts in noise: Switching channels to communicate through rapid environmental change

Article

Oct 2016

Sarah Partan

A multimodal shift is the ability to switch from reliance on one sensory channel to another during communication. The shift can take place during signal production and/or perception. If environmental changes such as urbanization and climate change impair signal transmission in particular channels, it would benefit the animal to be able to switch to a relatively quieter channel. For this strategy to be successful, it requires animals to be able to send redundant information across multiple channels. I develop and explore the argument that the ability of animals to switch from a noisy channel to a relatively quiet one may be key for the animals' ability to cope with rapid anthropogenic environmental change. I review examples of multimodal shifts that occur with environmental noise as well as cases in which a predicted shift did not occur. I survey which sensory channels are used in shifts and whether the signal components are redundant or nonredundant. Most multimodal shift examples include the visual channel as one of the components. The majority of signals involved in shifts appear to be redundant, although the majority of signals involved in multimodal communication in general appear to be nonredundant, especially for chemical/visual combinations. Finally, I discuss how anthropogenic environmental changes can affect signal transmission in different channels and habitats and explain why the ability to shift channels may help animals cope with these changes. Predictions and recommendations for future work are provided.

Position-dependent hearing in three species of bushcrickets (Tettigoniidae, Orthoptera)

Article

Full-text available

Jun 2015

A primary task of auditory systems is the localization of sound sources in space. Sound source localization in azimuth is usually based on temporal or intensity differences of sounds between the bilaterally arranged ears. In mammals, localization in elevation is possible by transfer functions at the ear, especially the pinnae. Although insects are able to locate sound sources, little attention is given to the mechanisms of acoustic orientation to elevated positions. Here we comparatively analyse the peripheral hearing thresholds of three species of bushcrickets in respect to sound source positions in space. The hearing thresholds across frequencies depend on the location of a sound source in the three-dimensional hearing space in front of the animal. Thresholds differ for different azimuthal positions and for different positions in elevation. This position-dependent frequency tuning is species specific. Largest differences in thresholds between positions are found in Ancylecha fenestrata. Correspondingly, A. fenestrata has a rather complex ear morphology including cuticular folds covering the anterior tympanal membrane. The position-dependent tuning might contribute to sound source localization in the habitats. Acoustic orientation might be a selective factor for the evolution of morphological structures at the bushcricket ear and, speculatively, even for frequency fractioning in the ear.

Tempo and mode of antibat ultrasound production and sonar jamming in the diverse hawkmoth radiation

Article

May 2015

Significance Ultrasound production is one of the most sophisticated antibat strategies in nocturnal insects, yet it has never been thoroughly studied in a phylogenetic framework. We conducted high-throughput field assays using playback of echolocation attack sequences, laboratory bat–moth interaction experiments, and fossil-calibrated phylogenetic analyses to provide the first evidence that multiple unrelated hawkmoth species produce ultrasound and jam bat echolocation. Our robust tree demonstrates that sonar jamming evolved twice during the Miocene after the radiation of insectivorous bats. We provide an example of the power behind collaborative science for revealing the function and historic pattern of behavior, and predict that ultrasound production is a widespread antibat strategy in the extraordinary diversity of nocturnal insects.

Infection behavior, life history, and host parasitism rates of Emblemasoma erro (Diptera: Sarcophagidae), an acoustically hunting parasitoid of the cicada Tibicen dorsatus (Hemiptera: Cicadidae)

Article

Full-text available

Dec 2015

Brian J. Stucky

Background: 'Eavesdropping' parasitoids find their hosts by homing in on the communication signals of other insects. These parasitoids often exploit chemical communication, but at least some species of the sarcophagid genusEmblemasomaeavesdropon the acoustic communications of cicadas. Despite considerable scientific interest in acoustic parasitoids, we know remarkably little about most species of Emblemasoma. To better understand the ecology and behavioral diversity of these flies, I used a combination of field and laboratory techniques to elucidate theinfection behavior and life history of E.erro,which uses the cicada Tibicen dorsatusasa host, and I also investigated parasitoid loads and parasitism rates of T.dorsatus inmultiple host populations in the central United States. Results: Female E. erro used the acoustic signals of male T. dorsatus as the primary means of locating hosts, but they also required physical movement by the host, usually either walking or flight, to provide visual cues for the final larviposition attack. Larvae were deposited directly on the host's integument and burrowed through intersegmental membrane to enter the host's body. On average, E. erro larvae spent 88.0 h residing inside their host before leaving to pupariate, but residence time was strongly dependent on both ambient temperature and effective clutch size. Adult flies eclosed about 18 days after pupariation. Across all study sites, the mean parasitoid load of infected male T. dorsatus was 4.97 larvae/host, and the overall parasitism rate was 26.3%. Parasitism rates and parasitoid loads varied considerably amonghost population samples, and high parasitism rates were usually associated with high parasitoid loads. Conclusions: Previously, detailed information about the infection behavior, life history, and host parasitism rates of sarcophagid acoustic parasitoids was only available for one species, E. auditrix. This study reveals that the infection behavior of E. erro is quite different from that of E. auditrix and, more broadly, unlike that known for any other species of acoustic parasitoid. The life histories of these two Emblemasoma are also divergent. These differences suggest that sarcophagid acoustic parasitoids are more behaviorally and ecologically diverse than previously recognized and in need of further study.

The Tymbal: Evolution of a Complex Vibration-Producing Organ in the Tymbalia (Hemiptera excl. Sternorrhyncha)

Chapter

Full-text available

Jul 2014

The tymbal is the most complex sound- and vibration-producing organ in arthropods. The tymbal organ was first described from cicadas which use it to produce sound levels of more than 100 dB. Subsequently, it was discovered that leaf- and planthoppers, as well as true bugs and moss bugs, communicate by substrate-borne vibrations, which are also produced by tymbal-like organs. We suggest the name Tymbalia for the taxon comprising Cicadomorpha, Fulgoromorpha, and Heteropteroidea (i.e., Hemiptera exclusive of Sternorrhyncha) based on the possession of a tymbal apparatus as an autapomorphic character. While our knowledge of the hoppers’ and bugs’ ‘‘silent songs’’ is still patchy, vibrational communication is obviously used ubiquitously in the Tymbalia and we hypothesize a common origin for the vibration-producing apparatus more than 300 Mya.

Sensory evolution of hearing in tettigoniids with differing communication systems

Article

Full-text available

Jan 2014
J EVOLUTION BIOL

In Tettigoniidae (Orthoptera: Ensifera), hearing organs are essential in mate detection. Male tettigoniids usually produce calling songs by tegminal stridulation, whereas females approach the males phonotactically. This unidirectional communication system is the most common one among tettigoniids. In several tettigoniid lineages, females have evolved acoustic replies to the male calling song which constitutes a bidirectional communication system. The genus Poecilimon (Tettigoniidae: Phaneropterinae) is of special interest because the ancestral state of bidirectional communication, with calling males and responding females, has been reversed repeatedly to unidirectional communication. Acoustic communication is mediated by hearing organs that are adapted to the conspecific signals. Therefore, we analyse the auditory system in the Tettigoniidae genus Poecilimon for functional adaptations in three characteristics: (i) dimension of sound-receiving structures (tympanum and acoustic spiracle), (ii) number of auditory sensilla and (iii) hearing sensitivity. Profound differences in the auditory system correlate with uni- or bidirectional communication. Among the sound-receiving structures, the tympana scale with body size, whereas the acoustic spiracle, the major sound input structure, was drastically reduced in unidirectional communicating species. In the unidirectional P. ampliatus group, auditory sensilla are severely reduced in numbers, but not in the unidirectional P. propinquus group. Within the P. ampliatus group, the number of auditory sensilla is further reduced in P. intermedius which lost acoustic signalling due to parthenogenesis. The auditory sensitivity correlated with the size of the acoustic spiracle, as hearing sensitivity was better with larger spiracles, especially in the ultrasonic range. Our results show a significant reduction in auditory structures, shaped by the differing sex roles during mate detection.

Interaction of sound-audition traits between eared insects and arthropodophagous bats: using a DNA approach to assess diet

Article

Full-text available

May 2024

Arthropod–bat interactions are often considered as a base model for studying factors underlying predator–prey coevolutionary processes. Bats developed ultrasonic echolocation to hunt, and in response some arthropods developed defense mechanisms such as ultrasonic hearing, allowing them to elude bat predators. The present study analyzes the feeding patterns of bats, focusing on sonic-auditory sensory mechanisms in predator–prey interactions. Next-generation DNA sequence data from fecal samples were used to analyze the diet of 17 bat species from Mexico. Arthropod prey taxa were classified according to their auditory traits, and echolocation data were recompiled from literature review. We: (i) classified arthropod families according to their hearing ability; (ii) estimated arthropod taxon richness and proportion in the diet of each bat species; and (iii) used multidimensional scaling, principal component analysis, and regression to analyze prey consumption patterns in relation to their auditory traits and in relation to echolocation characteristics of bats. Finally, we analyzed the relationship between foraging time and auditory characteristics of prey. Families with hearing organs correspond to the orders Lepidoptera and Orthoptera. We registered 20 families of Lepidoptera and 5 of Orthoptera—7 and 3 with hearing organs, respectively. Of these orders, families lacking ears were recorded in the diet of a few bat species. Our results support the allotonic frequency hypothesis predicting a difference in emission frequency intervals between predator and prey. However, we found that the consumption of earless moths is less frequent and is related to diurnal and twilight activity—hence, their consumption is limited to bat species foraging early. Results indicate bats feed on arthropod prey successfully despite the ultrasonic hearing ability of the prey. These results may be due to counteradaptations that allow maintenance of an asymmetric “arms race” between bats and eared insects that favors the predator.

Polka-dotted treasures: Revising a clade of ascidian- and bivalve-associated shrimps (Caridea: Palaemonidae)

Article

Full-text available

May 2023
CONTRIB ZOOL

Most marine shrimp species of the family Palaemonidae are characterized by symbiotic associations with hosts that belong to a wide range of invertebrate phyla. One clade of related endosymbiotic species has evolved to live inside the branchial chambers of ascidians and the mantle cavities of bivalve molluscs. The phylogeny of this clade (comprising 15 bivalve-associated species in the genera Anchistus, Neoanchistus, and Paranchistus, and three species of ascidian-associated species in the genus Dasella) is the topic of the present study, which is based on both morphological and molecular data. A concatenated phylogeny reconstruction was built by using the markers coi and 16S. With the help of a total evidence approach (with a scored morphological datamatrix), species could be added for which no molecular data were available. An ancestral character state analysis was performed to detect host switches. In contrast to another endosymbiotic clade, the ancestral host state was found to be slightly in favour of bivalves. The phylogenetic relevance of morphological features is discussed with a focus on a tympanal organ located in the major chelipeds of some bivalve-associated shrimp species. This little-known anatomical structure is illustrated by sem and µCT scans. Its possible function is discussed. In the phylogeny reconstructions, both Anchistus and Paranchistus were found to be polyphyletic. They were reclassified to obtain a more natural classification: Anchistus custoides and Anchistus custos were transferred to the resurrected genus Ensiger. Paranchistus liui, P. nobilii, P. pycnodontae, and P. spondylis were transferred to Polkamenes gen. nov. Anchistus pectinis and P. ornatus were transferred to Tympanicheles gen. nov. Per genus, a key to the species is provided.

Behavioral response of Spodoptera exigua under bat echolocation call stress

Article

Apr 2023
BIOL CONTROL

Sexual selection and predation drive the repeated evolution of stridulation in Heteroptera and other arthropods

Article

Full-text available

Feb 2023

Acoustic and substrate-borne vibrations are among themost widely used signalling modalities in animals. Arthropods display a staggering diversity of vibroacoustic organs generating acoustic sound and/or substrate-borne vibrations, and are fundamental to our broader understanding of the evolution of animal signalling. The primary mechanism that arthropods use to generate vibroacoustic signals is stridulation, which involves the rubbing together of opposing body parts. Although stridulation is common, its behavioural context and evolutionary drivers are often hard to pinpoint, owing to limited synthesis of empirical observations on stridulatory species. This is exacerbated by the diversity of mechanisms involved and the sparsity of their description in the literature, which renders their documentation a challenging task. Here, we present the most comprehensive review to date on the systematic distribution and behavioural context of stridulation. We use the megadiverse heteropteran insects as a model, together with multiple arthropod outgroups (arachnids, myriapods, and selected pancrustaceans). We find that stridulatory vibroacoustic signalling has evolved independently at least 84 times and is present in roughly 20%of Heteroptera, representing a remarkable case of convergent evolution. By studying the behavioural context of stridulation across Heteroptera and 189 outgroup lineages, we find that predation pressure and sexual selection are the main behaviours associated with stridulation across arthropods, adding further evidence for their role as drivers of large-scale signalling andmorphological innovation in animals. Remarkably, the absence of tympanal ears in most Heteroptera suggests that they typically cannot detect the acoustic component of their stridulatory signals. This demonstrates that the adoption of new signalling modalities is not always correlated with the ability to perceive those signals, especially when these signals are directed towards interspecific receivers in defensive contexts. Furthermore, by mapping their morphology and systematic distribution, we show that stridulatory organs tend to evolve in specific body parts, likely originating from cleaning motions and pre-copulatory displays that are common to most arthropods. By synthesising our understanding of stridulation and stridulatory organs across major arthropod groups, we create the necessary framework for future studies to explore their systematic and behavioural significance, their potential role in sensory evolution and innovation, and the biomechanics of this mode of signalling.

Large abdominal mechanoreceptive sense organs in small plant-dwelling insects

Article

Full-text available

Apr 2022
BIOL LETTERS

The Hemiptera, with approximately 98 000 species, is one of the largest insect orders. Most species feed by sucking sap from plant tissues and are thus often vectors for economically important phytopathogens. Well known within this group are the large cicadas (Cicadomorpha: Cicadoidea: Cicadidae) because they produce extremely loud airborne sounds. Less well known are their mostly tiny relatives, the leafhoppers, spittlebugs, treehop-pers and planthoppers that communicate by silent vibrational signals. While the generation of these signals has been extensively investigated, the mechanisms of their perception are poorly understood. This study provides a complete description and three-dimensional reconstruction of a large and complex array of mechanoreceptors in the first abdominal segments of the Rhododendron leafhopper Graphocephala fennahi (Cicadomorpha: Membra-coidea: Cicadellidae). Further, we identify homologous organs in the spittlebug Philaenus spumarius (Cicadomorpha: Cercopoidea: Aphrophori-dae) and the planthopper Issus coleoptratus (Fulgoromorpha: Fulgoroidea: Issidae). Such large abdominal sensory arrays have not been found in any other insect orders studied so far. This indicates that these sense organs, together with the signal-producing tymbal organ, constitute a synapomor-phy of the Tymbalia (Hemiptera excl. Sternorrhyncha). Our results contribute to the understanding of the evolution from substrate-borne to airborne communication in insects.

Communication by substrate-borne mechanical waves in insects: From basic to applied biotremology

Chapter

Sep 2021
ADV INSECT PHYSIOL

Biotremology is a field of study focused on an ancient way of communication by ani- mals endowed with specialized organs for emission and reception of substrate-borne vibrations. Established as a scientific discipline of its own, formally separated from bio- acoustics only recently, biotremology is now rapidly spreading throughout the scientific community, offering valuable cooperation also to numerous other scientific disciplines. Insects, make significant use of substrate-borne vibrational signals and cues for inter- and intraspecific communication, to accomplish many different behaviours. In this chapter, after highlighting the main relations, and differences, between insect acoustic and vibrational communication, we provide a detailed, comprehensive overview of the knowledge and ongoing research in the field of insect biotremology. We particularly emphasise the mechanisms of sensory detection of vibrational signals and cues, and the central neural processing of the received information; the latter especially being dis- cussed in relation to insect auditory processing. In addition, we dedicate considerable attention to the behavioural and ecological aspects of insect vibrational communica- tion, to the methods and instruments of research in neurophysiology and behavioural ecology, as well as the use of acquired basic knowledge in practical applications. Whilst some topics in biotremology, such as the neuronal basis of behaviour, need highly increased research attention, the interest in applied biotremology is rising especially quickly for the high potential offered by substrate-borne vibrations as semiophysicals for pest control. Hence, insects are both the elected study model for basic biotremology research and strongly relevant for agricultural and resource management issues.

Vibrational signalling, an underappreciated mode in cricket communication

Article

Full-text available

Oct 2021
NATURWISSENSCHAFTEN

Signalling via substrate vibration represents one of the most ubiquitous and ancient modes of insect communication. In crickets (Grylloidea) and other taxa of tympanate Ensifera, production and detection of acoustic and vibrational signals are closely linked functionally and evolutionarily. Male stridulation produces both acoustic and vibrational signal components, the joint perception of which improves song recognition and female orientation towards the signaller. In addition to stridulation, vibrational signalling mainly through body tremulation and/or drumming with body parts on the substrate has long been known to be part of crickets' close-range communication, including courtship, mate guarding and aggression. Such signalling is typically exhibited by males, independently or in conjunction with stridulation, and occurs literally in all cricket lineages and species studied. It is further also part of the aggressive behaviour of females, and in a few cricket groups, females respond vibrationally to acoustic and/or vibrational signals from males. The characteristics and function of these signals have remained largely unexplored despite their prevalence. Moreover, the communication potential and also ubiquity of cricket vibrational signals are underappreciated, limiting our understanding of the function and evolution of the cricket signalling systems. By providing a concise review of the existing knowledge of cricket perception of vibrations and vibrational signalling behaviour, we critically comment on these views, discuss the communication value of the emitted signals and give some methodological advice respecting their registration and control. The review aims to increase awareness, understanding and research interest in this ancient and widespread signalling mode in cricket communication.

Phylogenomic analysis sheds light on the evolutionary pathways towards acoustic communication in Orthoptera

Article

Full-text available

Oct 2020

Acoustic communication is enabled by the evolution of specialised hearing and sound producing organs. In this study, we performed a large-scale macroevolutionary study to understand how both hearing and sound production evolved and affected diversification in the insect order Orthoptera, which includes many familiar singing insects, such as crickets, katydids, and grasshoppers. Using phylogenomic data, we firmly establish phylogenetic relationships among the major lineages and divergence time estimates within Orthoptera, as well as the lineage-specific and dynamic patterns of evolution for hearing and sound producing organs. In the suborder Ensifera, we infer that forewing-based stridulation and tibial tympanal ears co-evolved, but in the suborder Caelifera, abdominal tympanal ears first evolved in a non-sexual context, and later co-opted for sexual signalling when sound producing organs evolved. However, we find little evidence that the evolution of hearing and sound producing organs increased diversification rates in those lineages with known acoustic communication.

Beyond aerodynamics: The critical roles of the circulatory and tracheal systems in maintaining insect wing functionality

Article

Full-text available

Sep 2018

Günther Pass

beyond aerodynamics

Article

Aug 2018
ARTHROPOD STRUCT DEV

Günther Pass

Involvement of Mechanosensory Complex Structures of the Cricket Gryllus bimaculatus Larvae (Orthoptera, Gryllidae) in Triggering of Motor Responses to Sound

Article

Mar 2018

Using an ethological approach, we studied the possibility of sound perception as well as probable contribution of diverse mechanosensory systems composing the mechanosensory complex to triggering of motor responses to sound stimulation in the cricket Gryllus bimaculatus larvae. It was shown that larvae can perceive sounds and respond to them by a locomotor reaction in a relatively broad frequency range, which becomes narrower as sound intensity decreases [0.1–6.6 kHz (111 ± 3 dB SPL), 0.1–1.4 kHz (101 ± 3 dB SPL), 0.1–0.8 kHz (91 ± 3 dB SPL]. Sound perception and triggering of motor responses appear to involve the cercal organs (CO), subgenual organs (SO) and, probably, other distant mechanosensory organs (DMO). Normal functioning of CO is essential for triggering locomotor responses to sound within the ranges of 1–1.4 kHz (101 ± 3 dB SPL) and 0.1–0.8 kHz (91 ± 3 dB SPL). CO are not necessary for triggering of motor responses to cues with an intensity of 111 ± 3 dB. SO and, probably, other DMO provide locomotor responses to sound within the ranges of 0.1–6.6 kHz (111 ± 3 dB SPL), 0.1–0.9 kHz (101 ± 3 dB SPL), and 0.1–0.3 kHz (91 ± 3 dB SPL). Thus, last instar larvae of G. bimaculatus lacking the tympanal organs can perceive sounds using CO, SO and, probably, other DMO, which (as in cricket imagoes) are likely to compose an integrated mechanosensory complex providing adequate acoustic behavior of this cricket species. Performance efficiency and sensitivity of the mechanosensory complex (specifically, CO) rely on the thoroughness of grooming. After self-cleaning of CO, the level of larval motor activity in response to cue presentation returned to the baseline and sometimes even increased. We assume that under normal conditions the mechanosensory complex, which triggers motor responses to a sound, is involved in the defensive escape response aimed at rescuing from predators.

Maintaining insect wing functionality - A review of the role played by the circulatory and tracheal systems

Article

Full-text available

May 2018

Günther Pass

Insect wings consist almost entirely of lifeless cuticle; yet their veins host a complex multimodal sensory apparatus and other tissues that require a continuous supply of water, nutrients and oxygen. This review provides a survey of the various living components in insect wings, as well as the specific contribution of the circulatory and tracheal systems to provide all essential substances. In most insects, hemolymph circulates through the veinal network in a loop flow caused by the contraction of accessory pulsatile organs in the thorax. In other insects, hemolymph oscillates into and out of the wings due to the complex interaction of several factors, such as heartbeat reversal, intermittent pumping of the accessory pulsatile organs in the thorax, and the elasticity of the wall of a special type of tracheae. A practically unexplored subject is the need for continuous hydration of the wing cuticle to retain its flexibility and toughness, including the associated problem of water loss due to evaporation. Also, widely neglected is the influence of the hemolymph mass and the circulating flow in the veins on the aerodynamic properties of insect wings during flight. Ventilation of the extraordinarily long wing tracheae is probably accomplished by intricate interactions with the circulatory system, and by the exchange of oxygen via cutaneous respiration.

Involvement of the mechanosensory complex structures of the cricket Phaeophilacris bredoides in triggering of motor responses to sound

Article

Nov 2017

Using an ethological approach, we studied the possibility of sound perception as well as probable contribution of diverse mechanosensory systems composing the mechanosensory complex to triggering of motor responses to sound stimulation in imaginal crickets Phaeophilacris bredoides lacking the tympanal organs (“deaf”). It was shown that Ph. bredoides imagoes are able to perceive sounds and respond to sound cues by a locomotor reaction in a relatively broad frequency range which becomes narrower as sound intensity decreases [0.1–6.0 kHz (111 ± 3 dB SPL), 0.1–1.5 kHz (101 ± 3 dB SPL), 0.1–1.3 kHz (91 ± 3 dB SPL), 0.1–0.6 kHz (81 ± 3 dB SPL), and 0.1 kHz (71 ± 3 dB SPL)]. Sound perception and triggering ofmotor responses appear to involve the cercal organs (CO), subgenual organs (SO) and, probably, other distant mechanosensory organs (DMO). CO are essential for triggering of locomotor responses to sound within the ranges of 1.6–6.0 kHz (111 ± 3 dB SPL), 1–1.5 kHz (101 ± 3 dB SPL), 0.9–1.3 kHz (91 ± 3 dB SPL), and 0.5–0.6 kHz (81 ± 3 dB SPL). SO and, probably, other DMO provide locomotor responses to sound within the ranges of 0.1–6.0 kHz (111 ± 3 dB SPL), 0.1–0.8 kHz (101 ± 3 dB SPL), 0.1–0.4 kHz (91 ± 3 dB SPL), and 0.1–0.4 kHz (81 ± 3 dB SPL). From this, it follows that “deaf” (nonsinging) Ph. bredoides can perceive sounds using CO, SO and, probably, other DMO, which (as in singing crickets) are likely to compose an integrated mechanosensory complex providing adequate acoustic behavior of this cricket species. Performance efficiency and sensitivity of the mechanosensory complex (specifically, of CO) rely on the thoroughness of grooming. Following self-cleaning of CO, the level of cricket motor activity in response to cue presentation returned to the baseline and sometimes even increased. Whether or not crickets of this species communicate acoustically is yet to be found out, however, we suggest that the mechanosensory complex, which triggers motor responses to a sound, is normally involved in the defensive escape response aimed at rescuing from predators.

Phonotactic flight of the parasitoid fly Emblemasoma auditrix (Diptera: Sarcophagidae)

Article

Full-text available

Jan 2017
J COMP PHYSIOL A

The parasitoid fly Emblemasoma auditrix locates its hosts using acoustic cues from sound producing males of the cicada Okanagana rimosa. Here, we experimentally analysed the flight path of the phonotaxis from a landmark to the target, a hidden loudspeaker in the field. During flight, the fly showed only small lateral deviations. The vertical flight direction angles were initially negative (directed downwards relative to starting position), grew positive (directed upwards) in the second half of the flight, and finally flattened (directed horizontally or slightly upwards), typically resulting in a landing above the loudspeaker. This phonotactic flight pattern was largely independent from sound pressure level or target distance, but depended on the elevation of the sound source. The flight velocity was partially influenced by sound pressure level and distance, but also by elevation. The more elevated the target, the lower was the speed. The accuracy of flight increased with elevation of the target as well as the landing precision. The minimal vertical angle difference eliciting differences in behaviour was 10°. By changing the elevation of the acoustic target after take-off, we showed that the fly is able to orientate acoustically while flying.

The Auditory System of the Dipteran Parasitoid Emblemasoma auditrix (Sarcophagidae)

Article

Full-text available

Aug 2016
J INSECT SCI

Several taxa of insects evolved a tympanate ear at different body positions, whereby the ear is composed of common parts: a scolopidial sense organ, a tracheal air space, and a tympanal membrane. Here, we analyzed the anatomy and physiology of the ear at the ventral prothorax of the sarcophagid fly, Emblemasoma auditrix (Soper). We used micro-computed tomography to analyze the ear and its tracheal air space in relation to the body morphology. Both tympana are separated by a small cuticular bridge, face in the same frontal direction, and are backed by a single tracheal enlargement. This enlargement is connected to the anterior spiracles at the dorsofrontal thorax and is continuous with the tracheal network in the thorax and in the abdomen. Analyses of responses of auditory afferents and interneurons show that the ear is broadly tuned, with a sensitivity peak at 5 kHz. Single-cell recordings of auditory interneurons indicate a frequency- and intensity-dependent tuning, whereby some neurons react best to 9 kHz, the peak frequency of the host’s calling song. The results are compared to the convergently evolved ear in Tachinidae (Diptera).

Vibrational Signaling

Chapter

Jun 2016

Jayne E. Yack

Vibrational communication is widespread in insects, yet scientists are only beginning to appreciate the importance and complexity of this communication channel. Substrate vibrations are widely available to insects living on plants, sand, soil, leaf litter, or fabricated materials such as beehives, termite mounds, or silk. Sources of vibrations important to insects may be abiotic (e.g., wind, rain) or biotic (e.g., signals or cues arising from conspecifics, predators, and even plants). This chapter focuses primarily on insects and specifically on adults that exploit plant-borne vibrations, reflecting most of the research to date. Some consideration is paid to other invertebrates such as spiders and scorpions, as well as juvenile stages such as eggs, larvae, and pupae. Topics covered include the diversity of taxa exploiting substrate-borne vibrations, the complexity of their vibratory environments, and the multitude of ways that vibrations are generated and used in social communication, finding food, avoiding predators, and monitoring the environment. Vibratory sense organs, including subgenual organs, lyriform organs, and Johnston’s organs and their constituent mechanosensilla are described. The vibratory landscape of insects and other invertebrates is poorly documented for most taxa, and all lines of investigation, from “identifying the players” to understanding how complex vibratory signals are detected and processed to recognize and localize sources, are unchartered territories ripe for further investigation.

Central Neural Processing of Sound Signals in Insects

Chapter

Jun 2016

The sense of hearing contributes importantly to an animal’s fitness. It allows detection of predators and prey and communication with conspecifics even in the dark and over large distances. Hearing organs evolved in about 20 groups of insects. Hearing is used by moths and other insects for avoiding predatory bats; by cicada, crickets/bushcrickets, moths, and grasshoppers for intraspecific communication; and by parasitic flies to locate singing hosts. Despite the variety of these insect groups, the neural processing of sound signals faces very similar fundamental challenges related to signal detection, directional processing, frequency discrimination, pattern recognition, and coping with self-generated noise. Solutions to these problems are implemented by specific network, cellular, and synaptic properties of neural circuits. Owing to their rather simple organization, insect auditory pathways can be explored and analyzed at the level of identified neurons to reveal fundamental mechanisms of auditory processing.

Parasitoid flies exploiting acoustic communication of insects— comparative aspects of independent functional adaptations

Article

Full-text available

Nov 2014

Two taxa of parasitoid Diptera have independently evolved tympanal hearing organs to locate sound producing host insects. Here we review and compare functional adaptations in both groups of parasitoids, Ormiini and Emblemasomatini. Tympanal organs in both groups originate from a common precursor organ and are somewhat similar in morphology and physiology. In terms of functional adaptations, the hearing thresholds are largely adapted to the frequency spectra of the calling song of the hosts. The large host ranges of some parasitoids indicate that their neuronal filter for the temporal patterns of the calling songs are broader than those found in intraspecific communication. For host localization the night active Ormia ochracea and the day active E. auditrix are able to locate a sound source precisely in space. For phonotaxis flight and walking phases are used, whereby O. ochracea approaches hosts during flight while E. auditrix employs intermediate landings and re-orientation, apparently separating azimuthal and vertical angles. The consequences of the parasitoid pressure are discussed for signal evolution and intraspecific communication of the host species. This natural selection pressure might have led to different avoidance strategies in the hosts: silent males in crickets, shorter signals in tettigoniids and fluctuating population abundances in cicadas.

Selective forces on origin, adaptation and reduction of tympanal ears in insects

Article

Full-text available

Nov 2014

Insect ears evolved many times independently. As a consequence, a striking diversity exists in the location, construction and behavioural implementation of ears. In this review, we first summarise what is known about the evolutionary origin of ears and the presumed precursor organs in the various insect groups. Thereafter, we focus on selective forces for making and keeping an ear: we discuss detecting and localising predators and conspecifics, including establishing new "private" channels for intraspecific communication. More advanced aspects involve judging the distance of conspecifics, or assessing individual quality from songs which makes auditory processing a means for exerting sexual selection on mating partners. We try to identify negative selective forces, mainly in the context of energy expenditure for developing and keeping an ear, but also in conjunction with acoustic communication, which incorporates risks like eavesdropping by predators and parasitoids. We then discuss balancing pressures, which might oppose optimising an ear for a specific task (when it serves different functions, for example). Subsequently, we describe various scenarios that might have led to a reduction or complete loss of ears in evolution. Finally, we describe cases of sex differences in ears and potential reasons for their appearance.

Computational principles underlying recognition of acoustic signals in grasshoppers and crickets

Article

Full-text available

Sep 2014

Grasshoppers and crickets independently evolved hearing organs and acoustic communication. They differ considerably in the organization of their auditory pathways, and the complexity of their songs, which are essential for mate attraction. Recent approaches aimed at describing the behavioral preference functions of females in both taxa by a simple modeling framework. The basic structure of the model consists of three processing steps: (1) feature extraction with a bank of 'LN models'-each containing a linear filter followed by a nonlinearity, (2) temporal integration, and (3) linear combination. The specific properties of the filters and nonlinearities were determined using a genetic learning algorithm trained on a large set of different song features and the corresponding behavioral response scores. The model showed an excellent prediction of the behavioral responses to the tested songs. Most remarkably, in both taxa the genetic algorithm found Gabor-like functions as the optimal filter shapes. By slight modifications of Gabor filters several types of preference functions could be modeled, which are observed in different cricket species. Furthermore, this model was able to explain several so far enigmatic results in grasshoppers. The computational approach offered a remarkably simple framework that can account for phenotypically rather different preference functions across several taxa.

The Phylogeny of the Extant Hexapod Orders

Article

Full-text available

Jun 2001
CLADISTICS

Morphological and molecular data are marshalled to address the question of hexapod ordinal relationships. The combination of 275 morphological variables, 1000 bases of the small subunit nuclear rDNA (18S), and 350 bases of the large subunit nuclear rDNA (28S) are subjected to a variety of analysis parameters (indel and transversion costs). Representatives of each hexapod order are included with most orders represented multiply. Those parameters that minimize character incongruence (ILD of Mickevich and Farris, 1981, Syst. Zool. 30, 351-370), among the morphological and molecular data sets are chosen to generate the best supported cladogram. A well-resolved and robust cladogram of ordinal relationships is produced with the topology (Crustacea ((Chilopoda Diplopoda) ((Collembola Protura) ((Japygina Campodeina) (Archaeognatha (Zygentoma (Ephemerida (Odonata ((((Mantodea Blattaria) Isoptera) Zoraptera) ((Plecoptera Embiidina) (((Orthoptera Phasmida) (Grylloblattaria Dermaptera)) ((((Psocoptera Phthiraptera) Thysanoptera) Hemiptera) ((Neuropteroidea Coleoptera) (((((Strepsiptera Diptera) Mecoptera) Siphonaptera) (Trichoptera Lepidoptera)) Hymenoptera)))))))))))))).

Communication and reproductive behaviour in North American Jerusalem crickets (Stenopelmatus) (Orthoptera: Stenopelmatidae).

Chapter

Full-text available

Mar 2001

David B. Weissman

Wetas are native to New Zealand and in evolutionary terms are insect 'dinosaurs' within the Orthoptera. Related species occur in South Africa, Australia, North America and to a lesser extent, Europe. This book brings together all known information on these groups (mostly in superfamilies Stenopelmatoidea and Gryllacridoidea) to form a compendium of existing scientific knowledge for future biological investigation and conservation. It is particularly useful for those working and researching in the areas of entomology, ecology and evolution, and contains 26 chapters by various authors in sections on: Systematics and biogeography (7 chapters); Morphology and anatomy (4 chapters); Ecology (3 chapters); Behaviour (5 chapters); Reproduction and development (2 chapters); Physiology (4 chapters); and Conservation of endangered species (1 chapter). A review of the Gryllacrididae is included, because of confusion over common names. A list of contributors and an index are also provided.

Signalers and Receivers : Mechanisms and Evolution of Arthropod Communication

Book

Full-text available

Mar 2002

Michael D Greenfield

In most terrestrial and aquatic habitats, the vast majority of animals transmitting and receiving communicative signals are arthropods. This book presents the story of how this important group of animals use pheromones, sound, vibration, and light for sexual and social communication. Because of their small to minute body size most arthropods have problems sending and receiving acoustic and optical information, each of which have their own severe constraints. Because of these restraints they have developed chemical signaling which is not similarly limited by scale. Presenting the latest theoretical and experimental findings from studies of signaling, it suggests that close parallels between arthropods and vertebrates reflect a very limited number of solutions to problems in behavior that are available within the confines of physical laws.

Substrate-transmitted acoustic signals of the primitive cicada, Tettigarcta crinita Distant (Hemiptera Cicadoidea, Tettigarctidae)

Article

Full-text available

Dec 1999

Male cicadas are familiar for their unique loud airborne calls used in courtship and mate recognition. Extant Tettigarcta species in Australia are little-known relict survivors of a primitive Mesozoic cicada radiation which do not make loud calls and lack either the apparatus to produce them or the auditory organs to detect them. Field studies on live insects in New South Wales for the first time show that Tettigarcta produce low-intensity, substrate-transmitted acoustic signals in courtship. This habit seems to be a primitive (plesiomorphic) feature.

How cicadas interpret acoustic signals

Article

Full-text available

May 2000

The vertebrate ear can analyse the frequency components of sound with high resolution, recognizing complex acoustic signals even against a noisy background

Chordotonal Organs of Insects

Article

Full-text available

Dec 1998
ADV INSECT PHYSIOL

Chordotonal organs are generally found in Insecta and Crustacea. In insects, chordotonal organs occur in great morphological diversity, and are found at nearly every exoskeletal joint and between joints within limb and body segments. Morphologically, a chordotonal organ is a cluster of sensilla connected to movable parts of skeletal cuticle or to the tracheal system, or sometimes inserting into a connective tissue strand. It is noted within some chordotonal organs, neurons are clustered into one or two groups, termed scoloparia that can be morphologically separated from each other. Chordotonal organs are not normally associated with external cuticular structures, such as hairs, bristles, or campaniform sensilla. The chapter describes the histological methods, diversity in distribution, structure and function, ultrastructure, mechanics of the scolopidium, physiological responses of chordotonal organs, processing of information and development of chordotonal organs, and evolution and homology. Combining the technologies of neurophysiology with those of genetics, electron microscopy, membrane biochemistry, and biophysics can elucidate the mechanisms that provide chordotonal sensilla with their different physiological properties.

A Comparative Study of Mating Behaviour in Some Neotropical Grasshoppers (Acridoidea)

Article

Full-text available

Apr 1987
ETHOLOGY

Klaus Riede

Aspects of premating and mating behaviour in several South American grasshopppers (Acridoidea) are described and compared. Examples of communication by acoustical, visual and chemical means are given. Acoustic signals are emitted only by species of the subfamilies Gomphocerinae, Acridinae, Romaleinae and Copiocerinae. Each subfamily has distinct sound-producing mechanisms, and the songs occur in different behavioural contexts. In Gomphocerinae and Acridinae the sexes recognize and attract each other by species-specific songs produced by a femuro-tegminal stridulatory mechanism. In contrast, Romaleinae produce a simple song by rubbing the hindwings against the forewings. These songs are similar in different species and no attraction of females could be demonstrated, but the behaviour may function in male-male interaction and during copulation. Sexual pheromones also play a role in this subfamily. Acoustic activity during copulation has been observed in Aleuasini (Copiocerinae), but its function is still unclear. No sound production at all exists in the Leptysminae, Rhytidochrotinae, Ommatolampinae, Melanoplinae, Proctolabinae and Bactrophorinae, but conspicuous movements of hindlegs (kneewaving) and antennae were observed. In some species these form part of a soundless courtship display. Ecological constraints have little influence on the basic mating strategies: romaleine, gomphocerine and melanopline grasshoppers often coexist in various habitats, but show the divergent behaviour patterns characteristic of their respective subfamilies. Intrinsic factors of female reproductive physiology seem to be more important: a hormonally controlled reproductive cycle in gomphocerine females provides for only few short copulations, while romaleine females copulate frequently and longer. In Gomphocerinae and Acridinae, receptive females are rare (male-biased operational sex ratio) which leads to intense competition among males. It is hypothesized that this could be responsible for the high diversification of song and courtship patterns in these subfamilies.

Exceptionally Preserved Fossil Insect Ears from the Eocene Green River Formation of Colorado

Article

Full-text available

Jan 2012
J Paleontol

Tympanal ears in insects are important for both intraspecific communication and for the detection of nocturnal predators. Ears are thought, based on modern forms, to have originated independently multiple times within insects and can be found on multiple regions of the body. Here we describe and document the exceptionally well preserved tympanal ears found in crickets and katydids from the Eocene Green River Formation of Colorado, which are virtually identical to those seen in modern representatives of these groups. These specimens are among the best preserved insect ears in the fossil record and establish the presence of ears in two major clades of Orthoptera 50 million years ago. Also discussed and evaluated are previously described insect ears from the Mesozoic and the implications of the findings of the present study for studying the evolution of ears within insects.

Evolutionary transition from stretch to hearing in ancient grasshoppers

Article

Full-text available

Aug 1998

Ears of modern insects occur on a wide variety of body parts and are thought to have evolved from ubiquitous stretch or vibration receptors. This relationship, based on comparative anatomy and similarities in the embryological development of ears in divergent taxa, has led to the widespread assumption of homology of these structures in insects, although this has not been tested rigorously. Here we report on the hearing organs of a relatively ancient, atympanate bladder grasshopper (Bullacris membracioides), which is capable of signalling acoustically over ~2km. We show that, within single individuals of this species, serially repeated abdominal ears show functional continuity from simple to more complex forms. All 12 morphologically differentiated organs respond to sound frequencies and intensities that are biologically significant, and mediate adaptive behavioural responses. By linking observations at the anatomical, physiological and behavioural level, our experiments provide evidence for the transition in function and selective advantage during the evolutionary development of this complex structure,. It is possible that ancestral insects with only simple pleural receptors had auditory capability covering distances substantially greater than contemporary insects with tympanate ears.

Sexual dimorphism of auditory function and structure in praying mantises (Mantodea; Dictyoptera)

Article

Full-text available

Mar 1990
J ZOOL

David Yager

Sexual dimorphism of tympanate auditory systems in insects has bees described in only a few taxonomically isolated cases. However, widespread sexual dimorphism occurs in the ultrasound‐sensitive, midline ear of the praying mantis. In dimorphic species, it is always the female mantis that shows a reduction in ultrasonic hearing. The dimorphism may be mild—a difference in tuning and small reduction in sensitivity—or extreme with no evidence of audition in the female. In all but the mildest cases, the reduction in hearing is accompanied by significant anatomical divergence from the male ear structure. Two distinct metathoracic groove (‘ear’) types are linked to hearing reduction in the females. Anatomical evidence of auditory sexual dimorphism appears in 34% of the 183 mantis genera examined. The dimorphic genera are widely but non‐uniformly distributed within three of the four largest mantis families. Auditory sexual dimorphism is closely correlated with dimorphism in wing length. In general, mantises with functional wings have sensitive ultrasonic hearing while those with short wings do not. These findings support the hypothesis that ultrasonic hearing in mantises is part of a defensive system against attack by echolocating bats.

Molecular phylogeny of the Calyptratae (Diptera: Cyclorrhapha) with an emphasis on the superfamily Oestroidea and the position of Mystacinobiidae and McAlpine's fly

Article

Full-text available

Aug 2010
SYST ENTOMOL

The dipteran clade Calyptratae is comprised of approximately 18 000 described species (12% of the known dipteran diversity) and includes well-known taxa such as houseflies, tsetse flies, blowflies and botflies, which have a close association with humans. However, the phylogenetic relationships within this insect radiation are very poorly understood and controversial. Here we propose a higher-level phylogenetic hypothesis for the Calyptratae based on an extensive DNA sequence dataset for 11 noncalyptrate outgroups and 247 calyptrate species representing all commonly accepted families in the Oestroidea and Hippoboscoidea, as well as those of the muscoid grade. DNA sequences for genes in the mitochondrial (12S, 16S, cytochrome c oxidase subunit I and cytochrome b) and nuclear genome [18S, 28S, the carbamoyl phosphate synthetase region of CAD (rudimentary), Elongation factor one alpha] were used to reconstruct the relationships. We discuss problems relating to the alignment and analysis of large datasets and emphasize the advantages of utilizing a guide tree-based approach for the alignment of the DNA sequences and using the leaf stability index to identify ‘wildcard’ taxa whose excessive instability obscures the phylogenetic signal. Our analyses support the monophyly of the Calyptratae and demonstrate that the superfamily Oestroidea is nested within the muscoid grade. We confirm that the monotypic family Mystacinobiidae is an oestroid and further revise the composition of the Oestroidea by demonstrating that the previously unplaced and still undescribed ‘McAlpine’s fly’ is nested within this superfamily as a probable sister group to Mystacinobiidae. Within the Oestroidea we confirm with molecular data that the Calliphoridae are a paraphyletic grade of lineages. The families Sarcophagidae and Rhiniidae are monophyletic, but support for the monophyly of Tachinidae and Rhinophoridae depends on analytical technique (e.g. parsimony or maximum likelihood). The superfamilies Hippoboscoidea and Oestroidea are consistently found to be monophyletic, and the paraphyly of the muscoid grade is confirmed. In the overall relationships for the calyptrates, the Hippoboscoidea are sister group to the remaining Calyptratae, and the Fanniidae are sister group to the nonhippoboscoid calyptrates, whose relationships can be summarized as (Muscidae (Oestroidea (Scathophagidae, Anthomyiidae))).

Spatial Organization of Tettigoniid Auditory Receptors: Insights From Neuronal Tracing

Article

Full-text available

Nov 2012
J MORPHOL

The auditory sense organ of Tettigoniidae (Insecta, Orthoptera) is located in the foreleg tibia and consists of scolopidial sensilla which form a row termed crista acustica. The crista acustica is associated with the tympana and the auditory trachea. This ear is a highly ordered, tonotopic sensory system. As the neuroanatomy of the crista acustica has been documented for several species, the most distal somata and dendrites of receptor neurons have occasionally been described as forming an alternating or double row. We investigate the spatial arrangement of receptor cell bodies and dendrites by retrograde tracing with cobalt chloride solution. In six tettigoniid species studied, distal receptor neurons are consistently arranged in double-rows of somata rather than a linear sequence. This arrangement of neurons is shown to affect 30-50% of the overall auditory receptors. No strict correlation of somata positions between the anterio-posterior and dorso-ventral axis was evident within the distal crista acustica. Dendrites of distal receptors occasionally also occur in a double row or are even massed without clear order. Thus, a substantial part of auditory receptors can deviate from a strictly straight organization into a more complex morphology. The linear organization of dendrites is not a morphological criterion that allows hearing organs to be distinguished from nonhearing sense organs serially homologous to ears in all species. Both the crowded arrangement of receptor somata and dendrites may result from functional constraints relating to frequency discrimination, or from developmental constraints of auditory morphogenesis in postembryonic development. J. Morphol. © 2012 Wiley Periodicals, Inc.

Patterns of praying mantis auditory system evolution based on morphological, molecular, neurophysiological, and behavioural data

Article

Full-text available

Jul 2008
BIOL J LINN SOC

Some praying mantids have sensitive ultrasonic hearing arising from a unique ‘cyclopean’ ear located in the ventral metathorax. The present study explores the evolutionary history of the mantis auditory system by integrating large anatomical, neurophysiological, behavioural, and molecular databases. Using an ‘auditory phylogeny’ based on 13 morphological characters, we identified a primitively earless form of metathoracic anatomy in several extant taxa. In addition, there are five distinct mantis auditory systems. Three of these can be identified anatomically, and the other two can only be detected neurophysiologically. Superimposing these results onto a phylogenetic tree derived from molecular data from seven genes shows that the cyclopean mantis ear evolved once approximately 120 Mya. All the other auditory system types are either varying degrees of secondary loss, or are recent innovations that each occurred independently multiple times. The neurophysiological response to ultrasound is remarkably consistent across all taxa tested, as is the multicomponent, in-flight behaviour triggered by ultrasound. Thus, mantids have an ancient, highly conserved auditory neural–behavioural system. Although ultrasonic hearing in several insect groups evolved in response to bat predation, mantis hearing predates the appearance of bats (approximately 63 Mya) and must originally have functioned in communication, prey detection, or avoidance of nonbat predators. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94, 541–568.

Comparison of auditory sense organs in parasitoid Tachinidae (Diptera) hosted by Tettigoniidae (Orthoptera) and homologous structures in a non-hearing Phoridae (Diptera)

Article

Full-text available

Nov 2007

The dipteran parasitoids Therobia leonidei and Homotrixa alleni (Tachinidae) use acoustic cues to locate their calling tettigoniid (Ensifera, Orthoptera) hosts. The sexually dimorphic tympanal organs of both fly species are located at the prosternum. For comparison a homologous chordotonal organ in the non-hearing fly Phormia regina, Meigen (Phoridae) is also described. The scolopidial sense organs of the ears have approximately 180 sensory cells in Th. leonidei and 250 cells in H. alleni. Interspecific analysis indicates that the cell number and arrangement might be genus specific in Tachinidae. The mononematic scolopidia, each with one sensory cell, are of different sizes and insert at the tympanal membrane. Large scolopidial units (diameter of sensory cells up to 50μm) extend longitudinally from the centre of the sensory organ towards the ligament, whereas small units (sensory cell diameter up to 10μm) are arranged sequentially within the sensory organ. This arrangement is discussed to be a possible basis for frequency discrimination. The ultrastructure of the scolopidia is similar in the hearing and non-hearing flies. In both groups, the majority of scolopales has a diameter from 2 to 2.9μm, although hearing species have additionally wider scolopales. The homologous chordotonal organ of Ph. regina consists of approximately 55 sensory cells of uniform direction. The data are discussed in comparison to the ears of other Diptera.

The Phylogeny of the Extant Hexapod Orders

Article

Full-text available

Jun 2001

Morphological and molecular data are marshalled to address the question of hexapod ordinal relationships. The combination of 275 morphological variables, 1000 bases of the small subunit nuclear rDNA (18S), and 350 bases of the large subunit nuclear rDNA (28S) are subjected to a variety of analysis parameters (indel and transversion costs). Representatives of each hexapod order are included with most orders represented multiply. Those parameters that minimize character incongruence (ILD of Mickevich and Farris, 1981, Syst. Zool. 30, 351–370), among the morphological and molecular data sets are chosen to generate the best supported cladogram. A well-resolved and robust cladogram of ordinal relationships is produced with the topology (Crustacea ((Chilopoda Diplopoda) ((Collembola Protura) ((Japygina Campodeina) (Archaeognatha (Zygentoma (Ephemerida (Odonata ((((Mantodea Blattaria) Isoptera) Zoraptera) ((Plecoptera Embiidina) (((Orthoptera Phasmida) (Grylloblattaria Dermaptera)) ((((Psocoptera Phthiraptera) Thysanoptera) Hemiptera) ((Neuropteroidea Coleoptera) (((((Strepsiptera Diptera) Mecoptera) Siphonaptera) (Trichoptera Lepidoptera)) Hymenoptera)))))))))))))).

On the Functional Morphology of the Auditory System in Bush Crickets (Orthoptera: Tettigonioidea)

Article

Sep 1979
ENTOMOL GEN

Rolf Schumacher

The Evolutionary Biology of Hearing

Book

Jan 1992

To develop a science of hearing that is intellectu The five-day conference was held at the Mote ally satisfying we must first integrate the diverse, Marine Laboratory in Sarasota, Florida, May - extensive body of comparative research into an 24, 1990. The invited participants came from the evolutionary context. The need for this integra fields of comparative anatomy, physiology, biophys tion, and a conceptual framework in which it could ics, animal behavior, psychophysics, evolutionary be structured, were demonstrated in landmark biology, ontogeny, and paleontology. Before the papers by van Bergeijk in 1967 and Wever in 1974. conference, preliminary manuscripts of the invited However, not since 1965, when the American papers were distributed to all participants. This facilitated - even encouraged - discussions through Society of Zoologists sponsored an evolutionary conference entitled ''The Vertebrate Ear;' has there out the conference which could be called, among other things, "lively. " The preview of papers, along been a group effort to assemble and organize our current knowledge on the evolutionary-as with the free exchange of information and opinion, opposed to comparative-biology of hearing. also helped improve the quality and consistency of In the quarter century since that conference the final manuscripts included in this volume. there have been major changes in evolutionary In addition to the invited papers, several studies concepts (e. g. , punctuated equilibrium), in sys were presented as posters during evening sessions.

Hearing

Article

Dec 2009

This chapter discusses sense of hearing among insects. Using sound, vertebrates and insects are often capable of sensing, identifying, and locating their predators, prey, conspecific rivals, and mates by hearing their intentional or unintentional acoustic signals. Natural selection has shaped the form and function of hearing organs (ears) in insects over evolutionary time. In this respect, the ears of insects show much greater diversity than those of vertebrates, for reasons that will be apparent in our discussion. There is tremendous morphological diversity of insect ears. The multitude of different ear designs and locations reflects the unique physical and behavioral challenges faced by each insect. Yet despite their many differences, most ears follow a similar morphological plan. Each typically consists of three identifiable substructures: a tympanal membrane, a tracheal air chamber, and a chordotonal sensory organ. Ears of many nocturnal Lepidoptera, for example, are so thin that they are transparent. Such fragile membranes are typically protected within body cavities or by external flaps of cuticle. In contrast, the thicker, opaque tympanal membranes of some diurnal butterflies or grasshoppers are conspicuously positioned on the outer surface of the body.

Zur funktionellen Morphologie des auditorischen Systems der Laubheuschrecken

Article

Jan 1979

R. Schumacher

Evolutionary pathways of truncal tympanal organs in Lepidoptera (Insecta: Holometabola)

Article

May 2000
ZOOL ANZ

Ivar Hasenfuss

The structure of the truncal tympanal organs of 111 species representing diverse lepidopteran groups was examined from an acoustic point of view. Fundamental differences in organization indicate the independent evolution of the organs. Secondary similarities exhibited by acoustically important parts must then be regarded as analogies based on the same functional needs. Discussion of the analogies led to the following hypotheses about the role of the structures in question. (1) The "accessory tympana" are means by which the disturbing influences of muscle contractions are minimized. (2) Bipartite tympana, i.e. tympana proper with adjacent conjunctivae, are responsible for increased sensitivity to higher frequencies. (3) External cup- or hood-like projections and changes in the volume of tympanal air cavities are means of tuning the maximal sensitivity to sound frequencies. The results, in connection with a plausible scenario, made it possible to discuss possible pathways in the evolution of the hearing organs. Functional and evolutionary aspects of the tympanal organs of Dudgeoneidae, Pyraloidea, Geometridae, Uraniidae, Drepanidae and Noctuoidea are discussed. The unusual structure of the tympanal scolopal organs in Crambidae suggest that they are sensitive to movements in length and width. Differences in notodontid and non-notodontid Noctuoidea are discussed as possible results of a cladistic furcation during an early evolutionary stage of the hearing organs.

The Evolutionary Biology of Hearing

Chapter

Jan 1992

Ron Hoy

In a volume devoted to the evolutionary biology of hearing it is worth emphasizing that among terrestrial animals, only the vertebrates and insects have evolved specialized receptor systems for hearing. Like other sensory modalities hearing subserves survival behavior of which two stand out: reproductive behavior and predator detection. Hearing mediates both behaviors in a wide variety of vertebrates and insects, and especially among nocturnally active species in both. I will briefly touch on the well-known role of hearing in the reproductive hearing of insects since it is the subject of other chapters in this volume (Michelsen, Chapter 5; Romer, Chapter 6; Lewis, Chapter 7), and I will devote most of this chapter to the evolution of insect hearing in relation to predators.

Das H�rverm�gen vonNepa cinerea L.

Article

Mar 1975

Brigitte Arntz

The morphology and innervation of the pterothoracic scolopal organs ofNepa cinerea were studied using stereoscan and methylene blue staining. The behavior ofNepa cinerea when excited by sounds was observed and analyzed. When the animals are exposed to sound they assume a thanatosis, whose duration and habituation are dealt with in this study. Through exstirpation experiments it was possible to prove that the thoracic scolopal organs are the sound receivers that evoke death feigning. By extracellular recording from the nerve of the scolopal organs it was directly confirmed that they are sound receivers. The threshold curves of the organs were determined. One sensory cell is more sensitive than the other to the extent of 12,5 dB. Both have a logarithmic intensity characteristic, although the rate of incline however differs. With longer stimuli the spike activity of both units decreases in a phasic-tonic way.

Molecular Phylogenetic Analysis of the Pneumoroidea (Orthoptera, Caelifera): Molecular Data Resolve …

Article

Jul 2000

Molecular Phylogenetic Analysis of the Pneumoroidea (Orthoptera, PK Flook, 1 S. Klee, and CHF Rowell Zoology Institute, University of Basel, Basel 4051, Switzerland A key transition in the evolution of the insect

The Relation Between Hearing And Flying In Crickets

Article

Jan 1990

Daniel Otte

Molecular phylogenies, morphological homologies and the evolution of moth ‘ears’

Article

Apr 2012

Niels P. Kristensen

The recent suggestion that complex hearing organs (‘ears’) may have been evolved just once in the stem lineage of a clade of ditrysian moths including the pyraloids and ‘Macroheterocera’ is discussed. It is argued that homology between ears situated in different segments and in different morphological territories (dorsal or ventral) of the same segment must be ruled out, and that therefore the number of independent origins of ears in the said clade is three at the very least. Mechanical protection of the ventral abdominal base by the backwards slanting metacoxae permits an attenuation of the body wall which would facilitate multiple independent origins of ears exactly in this region.

Structure of atympanate tibial organs in legs of the cave-living Ensifera, Troglophilus neglectus (Gryllacridoidea, Raphidophoridae)

Article

Jan 1995
J MORPHOL

Troglophilus neglectus (Gryllacridoidea, Raphidophoridae) is a nocturnal Ensifera which can be found in caves of Slovenia. The anatomy of the tibial organs in the fore-, mid-, and hindlegs, as well as the external morphology of the proximal fore-tibia and the prothoracic tracheal system, is described comparatively. In the prothorax and in the forelegs, no sound-conducting structures such as an acoustic trachea, enlarged spiracles, or tympana are developed. A group of 8-10 campaniform sensillae is located in the dorsal cuticle of the proximal tibia. In each leg, the tibial organ complex is built up by two scolopale organs, the subgenual organ and the intermediate organ; the structure and the number of scolopidia is similar in each leg. No structure resembling the crista acoustica is found. The subgenual organ contains around 30 scolopidia; the intermediate organ is subdivided into a proximal part containing 8-9 scolopidia and a distal part with 5-6 scolopidia. The two groups of scolopidia are not directly connected to the tracheal system. The tibial organs in the forelegs are insensitive to airborne sound, and they appear to be more primitive compared to those found in members of the Tettigoniidae and the Gwllidae. The results indicate that the complex tibial organs in all legs of T. neglectus are primarily vibrosensitive.

Hearing in Notodontid Moths: A Tympanic Organ with a Single Auditory Neurone

Article

Nov 1984

Byannemarie Surlykke

SUMMARY 1. Notodontid moths possess paired tympanic organs basically similar to the ears in other noctuoid families, but with a single auditory .A cell. The A cell and the non-auditory B cell were studied anatomically by infusion of C0CI2 and physiologically by recordings from the tympanic nerve. 2. The response of the A cell is determined by intensity parameters and temporal parameters of an ultrasonic stimulus. The notodontid ear is as sensitive as the ears of sympatric noctuids. The directional sensitivity is approximately the same as in noctuids of comparable size (maximal interaural intensity difference of 10-15 dB). The dynamic range of the A cell is about 20-25 dB. Sound levels exceeding the threshold by 30-40dB will saturate the A cells in both ears. Stimuli with different pulse lengths (from 5 to 200 ms, corresponding to pulse repetition rates (PRR) from 100—2-5 Hz), but equal duty cycles (50%) gave a maximum response for pulse lengths lying between 30 and 50 ms. The receptor cell followed the sound pulses in a one-to-one manner even at a PRR of 200 Hz. 3. Notodontid moths seem to show the same 'bimodal' evasive behaviour as noctuids. This behaviour can be explained on the basis of intensity parameters, since only low intensity stimuli will give the notodontid direc- tional information. Hence, directional evasive behaviour is expected at low sound pressure levels (SPL), while high SPL (saturating both A cells) should elicit a non-directional evasive behaviour. However, the evasive behaviour could also be explained in terms of time parameters. Hunting bats increase the PRR of their cries when closing in on a prey and the moths may be able to use these time cues for changing their behaviour.

Complex tibial organs in the forelegs, midlegs, and hindlegs of the bushcricket Gampsocleis gratiosa (Tettigoniidae): Comparison of the physiology of the organs

Article

Oct 1994

Complex tibial organs are found in all three pairs of legs of tettigoniids and consist of the subgenual organ, the intermediate organ, and the crista acoustica. In the forelegs of most tettigoniids, the tibial organs in association with tympanic membrane, tracheal tube, and spiracle are highly developed sound transmitting structures (tympanal organs), but not so in the mid and hind pairs of legs (atympanal organs). We have studied the electrophysiology of the atympanal organs and in particular of the intermediate organ and the crista acoustica using extracellular recordings to obtain summed responses to vibratory and acoustic stimuli and single cell recordings from the different receptor cells. Significant differences in the responses of the receptor cells of the tympanal and atympanal organs were found predominantly in the case of sound stimulation. Whereas the crista acoustica and the distal part of the intermediate organ of the foreleg are very sensitive auditory receptor organs, the same organs in the mid‐and hindlegs appear to respond not at all or only unspecifically to airborne sound stimuli. By contrast, the responses to vibratory stimuli are similar if not identical. The functions of the subgenual organs in all six legs are basically identical, but the function of the middle and distal parts of the crista acoustica in the mid‐and hindlegs remains to be characterized.© 1994 wiley‐lines, Inc.

The Organization of the Auditory Organ of the Bladder Cicada, Cystosoma Saundersii

Article

Apr 1981
PHILOS T R SOC B

The auditory organ of Cystosoma saundersii consists of 2000-2200 scolopidia arranged in two groups, a dorsal and a ventral group. The dorsal group contains scolopidia orientated along the longitudinal axis of the organ while the ventral group contains scolopidia aligned at right angles to these. On the basis of current theories of sensory transduction, it is possible that these groups may have different intensity characteristics. The cellular composition of an individual scolopidium was described at the electron microscope level and was found to be similar to that occurring in most other chordotonal organs. Slight differences in fine structure were observed in the structure of the scolopale, the mass and position of the ciliary dilatation and the ciliary root. Differences in these parameters may influence the adequate stimulus needed for a chordotonal organ. The fine structure of proximal and distal attachments of the scolopidia to the cuticle is similar to that of muscle attachments observed in insects, crustaceans and arachnids. The central projections of the auditory nerve within the thoracic ganglia are similar to those described for the periodical cicadas.

Nerve Cells and Insect Behavior

Article

Jan 1967

K. D. Roeder

Singing and hearing in a Tertiary bushcricket

Article

Jun 1999
NATURE

Communication organs are poorly represented in the fossil record, so their evolution is usually reconstructed by comparison of extant species using a phylogenetic approach. We have analysed some extremely well preserved stridulatory and hearing organs of the oldest known bushcrickets from the lowermost Tertiary sediments of Denmark (55 million years old). These fossils indicate that males sang with a broadband frequency spectrum, and it is likely that both sexes could hear ultrasound. The fossil wings have lower asymmetry than extant species, indicating that bushcrickets may have evolved from a bilaterally symmetrical ancestor.

The auditory‐vibratory sensory system of Polysarcus denticauda (Phaneropterinae, Tettigoniidae): III. Physiology of the ventral cord neurons ascending to the head ganglia

Article

Sep 1997
J Exp Zool

In Polysarcus denticauda, a phaneropterine bushcricket with extremely thick uncovered tympana and an aberrant morphology of the cristae acusticae of the complex tibial organs, the electrophysiology of the auditory-vibratory ventral cord neurons ascending to the brain was investigated. Although the receptor organs in this species have some extraordinary response properties, the central auditory-vibratory neurons could be basically classified into the same functional types of S-, V-, and VS- neurons previously described for other bushcricket species. However, in some details the responses of most of the S- and VS- neurons are different. The S-neurons are generally more tonic and the VS-neurons give smaller responses to airborne sound stimulation than do the neurons belonging to the same functional types in most other bushcricket species.

Sound production in primitive Orthoptera from Western Australia: Sounds used in defence and social communication in Ametrus sp. and Hadrogryllacris sp. (Gryllacrididae: Orthoptera)

Article

Jul 1997

Sound production in two undescribed species of Gryllacrididae belonging to the genus Ametrus sp. and Hadrogryllacris sp. takes the form of defensive stridulation and intra-specific signalling by drumming on the substrate. Defensive stridulation is produced as part of an elaborate visual display, by femoro-tergal stridulation. Two rows of spines on abdominal tergites II and III of both species are rubbed by an elongate area of tubercules on the inner femoral surface of the hind legs. Analysis showed that the motion of the leg relative to the abdomen involves a complex counter-rotation of the leg between leg and abdomen. The defensive display may be performed in day light. Social signalling in both species occurs after dark, and involves drumming on the substrate by both hind legs in loose synchrony. Drumming is rhythmic and species' specific. Males respond to playback calls and females duet with males. The evolution of this calling behaviour is discussed and comparisons are made with the other primitive ensiferan family known to produce both tergo-abdominal defensive stridulation and femoral drumming behaviour, the Stenopelmatidae.

Das Hörvermögen von Nepa cinerea L

Article

Jan 1975

The morphology and innervation of the pterothoracic scolopal organs ofNepa cinerea were studied using stereoscan and methylene blue staining.

Reproductive Behavior of Ground Weta (Orthoptera: Anostostomatidae): Drumming Behavior, Nuptial Feeding, Post-copulatory Guarding and Maternal Care

Article

Jan 2009

Darryl T. Gwynne

Compared to other ensiferan Orthoptera such as true crickets (Gryllidae) and katydids (Tettigoniidae) relatively little is known about the reproductive behavior of Anostostomatidae (formerly Stenopelmatidae), the king crickets, weta and allies. Moreover, although the New Zealand species (the weta) are best known, there is little knowledge of the biology of ground weta (Hemiandrus species), a variable genus especially with regard to ovipositor length. This paper presents observations of mating and post-mating behavior of several Hemiandrus species with short ovipositors. Sexually active males and females drum their abdomens on the substrate, apparently as local signals for mate attraction (pheromones may be involved in long distance communication). After mating there is both maternal and paternal investment. Females provide care to eggs and young larvae and males provide a spermatophylax to the female, a mating meal that, in other ensiferan Orthoptera can be an important source of nutrition. In contrast to other ensiferans, however, the spermatophylax of Hemiandrus species with short ovipositors is deposited on the female's abdomen, a separate location from the sperm ampulla. The spermatophylax is deposited while the male is attached to the female's underside, apparently to her modified 6th abdominal sternite. Also, in contrast to related taxa, males remain with their mates while the mating meal is eaten. These observations indicate that ground weta are excellent systems for examining behavioral and ecological questions about the evolution of complex signals, as well as the evolution of maternal and paternal investment.

Structure of atympanate tibial organs in legs of the cave-living ensifera, Troglophilus neglectus (Gryllacridoidea, Raphidophoridae)

Article

Feb 2005
J MORPHOL

Troglophilus neglectus (Gryllacridoidea, Raphidophoridae) is a nocturnal Ensifera which can be found in caves of Slovenia. The anatomy of the tibial organs in the fore-, mid-, and hindlegs, as well as the external morphology of the proximal fore-tibia and the prothoracic tracheal system, is described comparatively. In the prothorax and in the forelegs, no sound-conducting structures such as an acoustic trachea, enlarged spiracles, or tympana are developed. A group of 8–10 campaniform sensillae is located in the dorsal cuticle of the proximal tibia. In each leg, the tibial organ complex is built up by two scolopale organs, the subgenual organ and the intermediate organ; the structure and the number of scolopidia is similar in each leg. No structure resembling the crista acoustica is found. The subgenual organ contains around 30 scolopidia; the intermediate organ is subdivided into a proximal part containing 8-9 scolopidia and a distal part with 5–6 scolopidia. The two groups of scolopidia are not directly connected to the tracheal system. The tibial organs in the forelegs are insensitive to airborne sound, and they appear to be more primitive compared to those found in members of the Tettigoniidae and the Gwllidae. The results indicate that the complex tibial organs in all legs of T. neglectus are primarily vibrosensitive. © 1995 Wiley-Liss, Inc.

Structure of the green lacewing tympanal organ (Chrysopa carnea, Neuroptera)

Article

Aug 1970
J MORPHOL

Lee A Miller

Small swellings near the base of the radial vein in each fore wing of the green lacewing, Chrysopa carnea, resemble typical insect tympanal organs, but some important differences are apparent. The swellings are bounded dorsally and laterally by thick cuticle and ventrally by thin, membranous cuticle. The ventral membrane is formed by a single, thin sheet of exocuticle with flattened hypodermis internally, but lacks the tracheal component that forms part of the tympanum in the typical insect tympanal organ. The portion of the membrane beneath each swelling is rippled while proximally it is smooth. In contrast to typical insect tympanal organs, the swellings in C. carnea are largely fluid-filled since an unexpanded trachea runs through each organ. A distal and a proximal chordotonal organ composed of typical chordotonal sensory units are associated with each swelling. The distal organ contains from five to seven units while the proximal organ is composed of from 18 to 20 units. Each sensory unit is composed of three readily identifiable cells. Distally, an attachment cell unites with the membrane and is contiguous with the scolopale cell, which surrounds the dendrite of the bipolar neuron. On the basis of the morphological evidence, one would not expect these swellings to function as sound receptors. However, the results of physiological and behavioral experiments, presented elsewhere, show that these organs are receptors for ultrasound.

Auditory characteristics and sexual dimorphism in the gypsy moth

Article

Mar 2008
PHYSIOL ENTOMOL

The auditory characteristics of two populations (laboratory reared and wild) of North American gypsy moths (Lymantriidae: Lymantria dispar L.) were sampled and the neurally derived thresholds of wild males and females to frequencies from 5 to 150 kHz compared. The noctuoid auditory receptors, Al and A2-cell, and putative proprioceptor, B-cell, were identified. Both sexes possess neurally responsive ears but females exhibit median best frequencies significantly lower than those of males. Audiogram comparisons reveal significantly different thresholds at 5–15 kHz, 30–120 kHz and 130–140 kHz, with females less sensitive to all but the lowest frequencies. Wild male populations reveal less audiogram variability than laboratory-reared individuals, while females' tuning curves appear more similar. The high variability present in colony moths warrants caution in the use of laboratory-reared insects for studies that assume natural levels of selection pressure. We suggest that male L. dispar possess adaptively functional ears tuned to the frequencies in the echo-location signals of bats but that the flightless females of this species are not exposed to bat predation and therefore possess ears in a state of evolutionary degeneration.

Morphological and physiological differences of the auditory system in three related bushcrickets (Orthoptera: Phaneropteridae, Poecilimon)

Article

Mar 1992
PHYSIOL ENTOMOL

The auditory system of three closely related bushcrickets was investigated with respect to morphological and physiological differences. The size of the acoustic vesicle in the prothorax cavity and the size of the acoustic spiracle were compared to differences in auditory tuning of the tympanic nerve and differences in the directionality. The results indicate that a small auditory vesicle and auditory spiracle provide reduced sensitivity in the high frequency range (above 10—15 kHz), but increase sensitivity at low frequencies (below 10 kHz). The directionality of the hearing system deteriorates at frequencies between 10 and 25 kHz in species with a small spiracle and trachea. The evolutionary implications of these differences of the auditory systems are discussed. They are considered to be influenced more by ecological factors than bioacoustical ones.

One hundred years of instability in ensiferan relationships

Article

Jul 2010
SYST ENTOMOL

Although Ensifera is a major insect model group, its phylogenetic relationships have been understudied so far. Few phylogenetic hypotheses have been proposed, either with morphological or molecular data. The largest dataset ever used for phylogeny reconstruction on this group is molecular (16S rRNA, 18S rRNA and 28S rRNA sequences for 51 ensiferan species), which has been used twice with different resultant topologies. However, only one of these hypotheses has been adopted commonly as a reference classification. Here we re-analyse this molecular dataset with different methods and parameters to test the robustness and the stability of the adopted phylogeny. Our study reveals the instability of phylogenetic relationships derived from this dataset, especially for the deepest nodes of the group, and suggests some guidelines for future studies. The comparison between the different classifications proposed in the past 70 years for Ensifera and our results allows the identification of potential monophyletic clades (katydids, mole crickets, scaly crickets + Malgasia, true crickets, leaf roller crickets, cave crickets) and the remaining unresolved clades (wetas, Jerusalem crickets and most of the highest rank clades) in Ensifera phylogeny.

Convergence and parallelism: Is a new life ahead of old concepts?

Article

Feb 2005
CLADISTICS

In comparative biology, character observations initially separate similar and dissimilar characters. Only similar characters are considered for phylogeny reconstruction; their homology is attested in a two-step process, firstly a priori of phylogeny reconstruction by accurate similarity statements, and secondly a posteriori of phylogeny analysis by congruence with other characters. Any pattern of non-homology is then a homoplasy, commonly, but vaguely, associated with “convergence”. In this logical scheme, there is no way to analyze characters which look similar, but cannot meet usual criteria for homology statements, i.e., false similarity detected a priori of phylogenetic analysis, even though such characters may represent evolutionarily significant patterns of character transformations. Because phylogenies are not only patterns of taxa relationships but also references for evolutionary studies, we propose to redefine the traditional concepts of parallelism and convergence to associate patterns of non-homology with explicit theoretical contexts: homoplasy is restricted to non-similarity detected a posteriori of phylogeny analysis and related to parallelism; non-similarity detected a priori of phylogenetic analysis and necessarily described by different characters would then correspond to a convergence event s. str. We propose to characterize these characters as heterologous (heterology). Heterology and homoplasy correspond to different non-similarity patterns and processes; they are also associated with different patterns of taxa relationships: homoplasy can occur only in non-sister group taxa; no such limit exists for heterology. The usefulness of these terms and concepts is illustrated with patterns of acoustic evolution in ensiferan insects. © The Willi Hennig Society 2005.

Desutter-Grandcolas L. Phylogeny and the evolution in extant Ensifera (Insecta, Orthoptera). Zoologica Scripta

Article

Nov 2003
ZOOL SCR

Laure Desutter-Grandcolas

Ensifera present an appropriate and interesting model for the study of acoustic communication, because of their diverse signal and communication modalities, and due to their accessibility for field and laboratory studies. Several hypotheses have been proposed to explain the acoustic evolution of Ensifera, but they were elaborated without any reference to a falsifiable phylogeny, and were consequently highly speculative. Similarly, phylogenetic relationships between ensiferan clades have not hitherto been studied using modern standard methodology, and the sole cladistic analysis by Gwynne in 1995 was methodologically flawed. No sound hypothesis therefore currently exists for ensiferan phylogeny, which precludes historical analysis of their communication modalities. In the present paper, the phylogeny is established on the basis of morpho-anatomical characters and used to analyse the evolution of acoustic communication in this clade by mapping the characters related to auditory and stridulatory structures onto the resultant trees. Cladistic analyses resulted in two equi-parsimonious cladograms (length 154, C 64, CI 58, RI 61) with the following topologies: (1) [(Grylloidea–Gryllotalpidae) (Rhaphidophoridae (Schizodactylidae (Gryllacrididae ((Stenopelmatidae–Cooloola) (Anostostomatidae (Prophalangopsis (Cyphoderris (Tettigoniidae–Lezina))))))))] (2) [(Grylloidea–Gryllotalpidae)(Rhaphidophoridae (Schizodactylidae (Gryllacrididae–Cooloola–(Stenopelmatidae (Anostostomatidae (Prophalangopsis (Cyphoderris (Tettigoniidae–Lezina))))))))]. According to these topologies, Ensifera were ancestrally devoid of acoustic and hearing systems. An acoustic (tegminal or femoro-abdominal) apparatus appeared a number of times independently with convergent structures. Similarly, tibial tympana developed several times independently. Moreover, four hypotheses (each according to a definite pattern of character transformation) can be proposed to explain the evolution of acoustic communication in the different ensiferan clades and relate it to a definite communicatory context. These hypotheses do not apply equally to ensiferan subclades. Grylloidea and Gryllotalpoidea could have experienced convergently a direct development of an intraspecific acoustic communication. Acoustic communication in Tettigoniidea has evolved more ambiguously, and may either have resulted from a direct evolution analogous to that having occurred in Gryllidea, or have developed in a completely different behavioural context. Future studies of acoustic communication in the different ensiferan clades will have to take into account the fact that the involved structures most often are not homologous and that their evolution may not have taken place in similar conditions. Different hypotheses of acoustic communication evolution may apply to different clades, and there may be no single explanation for acoustic communication in Ensifera.

Physical and physiological properties of the tettigoniid (“grasshopper”) ear

Article

Jan 1975

Harald Nocke

1. The hearing threshold for test sound frequencies above 2 kHz and the directional properties of the intact tettigoniid ear (8 kHz test sound) remain unchanged if sound is prevented from acting on theouter surface of the tympana (Figs. 6, 14). This cannot readily be understood from present theories on tettigoniid hearing. 2. No changes of the hearing threshold above 0.5 kHz or the directionality at 8 kHz can be observed if onlyone tympanum, anterior or posterior, is damped. The hearing threshold shows an increase only afterboth tympana have been damped (Figs. 7, 17). 3. The ear becomes very insensitive to sound and looses the directional properties (8 kHz test sound), characteristic of the intact ear, if the tympanal trachea is blocked at the spiracle on the thorax (Figs. 5, 16). This demonstrates the importance of the sound pathway via the tympanal trachea. 4. The directional sensitivity, i.e. the hearing threshold for a given sound frequency, depends on the relative position between the direction of sound incidence and the tympanal spiracle on the thorax (Figs. 12, 13). The symmetry axis of the directivity pattern (8 kHz test sound) is fixed in relation to the longitudinal axis of the body and does not change if the foreleg is moved into different walking positions (Fig. 15). 5. The optimum frequency of hearing of the tettigoniid ear is changed by altering the length of the tympanal trachea (Figs. 9, 19). 6. Two theories, namely the horn and the resonator theory, relating to the acoustical function of the tympanal trachea are discussed.

Functional morphology and development of tibial organs in the legs I, II and III of the bushcricketEphippiger ephippiger (Insecta, Ensifera)

Article

Sep 1992

Wolfgang Rössler

The anatomy of the complex tibial organs in the pro-, meso- and metathoracic legs of adults and larvae of the bushcricketEphippiger ephippiger is described comparatively. The subgenual organ and the intermediate organ are differentiated in the same way in legs I, II and III; the anatomy of the crista acustica and the tracheal morphology are significantly different. The final number of scolopidia in the tibial organ of each leg is present at the time of hatching. In the subgenual organ, the number of scolopidia is the same in all legs; in the intermediate organ, and especially in the crista acustica, the number of scolopidia decreases from leg I to legs II and III. In the first larval instar, the morphology of the tibia, the course of the trachea and the anatomy of accessory structures are developed in the same way in each leg. The specific differentiations forming the auditory receptor organ in leg I, such as the acoustic trachea, the tympana and tympanal cavities, develop step by step in subsequent instars. The auditory threshold recorded from the tympanal nerve in the prothoracic leg of adults is remarkably lower than in the meso- and metathoracic legs. Morphometrical analyses of structures that are suggested to play a role in stimulus transduction on scolopidia of the crista acustica reveal significant differences in the three legs.

Ultrasound-sensitive ears in a parasitoid fly

Article

Apr 1992

Evolution of the metathoracic tympanal ear and its mesothoracic homologue in the Macrolepidoptera (Insecta)

Article

Oct 1999

Two independent methods of comparison, serial homology and phylogenetic character mapping, are employed to investigate the evolutionary origin of the noctuoid moth (Noctuoidea) ear sensory organ. First, neurobiotin and Janus green B staining techniques are used to describe a novel mesothoracic chordotonal organ in the hawkmoth, Manduca sexta, which is shown to be serially homologous to the noctuoid metathoracic tympanal organ. This chordotonal organ comprises a proximal scolopidial region with three bipolar sensory cells, and a long flexible strand (composed of attachment cells) that connects peripherally to an unspecialized membrane ventral to the axillary cord of the fore-wing. Homology to the tympanal chordotonal organ in the Noctuoidea is proposed from anatomical comparisons of the meso- and metathoracic nerve branches and their corresponding peripheral attachment sites. Second, the general structure (noting sensory cell numbers, gross anatomy, and location of peripheral attachment sites) of both meso- and metathoracic organs is surveyed in 23 species representing seven superfamilies of the Lepidoptera. The structure of the wing-hinge chordotonal organ in both thoracic segments was found to be remarkably conserved in all superfamilies of the Macrolepidoptera examined except the Noctuoidea, where fewer than three cells occur in the metathoracic ear (one cell in representatives of the Notodontidae and two cells in those of other families examined), and at the mesothoracic wing-hinge (two cells) in the Notodontidae only. By mapping cell numbers onto current phylogenies of the Macrolepidoptera, we demonstrate that the three-celled wing-hinge chordotonal organ, believed to be a wing proprioceptor, represents the plesiomorphic state from which the tympanal organ in the Noctuoidea evolved. This ’trend toward simplicity’ in the noctuoid ear contrasts an apparent ’trend toward complexity’ in several other insect hearing organs where atympanate homologues have been studied. The advantages to having fewer rather than more cells in the moth ear, which functions primarily to detect the echolocation calls of bats, is discussed.

Das mesothorakale Tympanalorgan von Corixa Punctata Ill. (Heteroptera. Corixidae)

Article

Jan 1976

Joachim Prager

1. Action potentials of the mesothoracic tympanic organ's two receptor units (Al and A2) were recorded extracellularly. The impulse activity of both receptor units rises beyond resting activity when stimulated by airborne sound. 2. The time course of the excitation of both receptor units appears to be phasic-tonic (Fig. 4). 3. The influence of stimulus intensity and its time course on the excitation of both receptor units was studied (Figs. 5–8). 4. The threshold curves of the receptor units Al and A2 for airborne sound were determined in the frequency range between 0.3 to 20 kHz. The two receptor units differ. Receptor unit Al shows a distinct threshold minimum, whereas the threshold curve of the less sensitive receptor units A2 appears more flat (Fig. 9). 5. The threshold curves of the receptor units on the left body side differ from those on the right. The threshold minimum of unit Al left is absolutely lower than that of Al right and lies at higher frequencies (Fig. 10). 6. As observed under the light microscope, vibrations of the organ's base and bulb differ from one side of the body to the other (Fig. 11). 7. Removing the bulb influences the mode of oscillation of the base as well as the threshold curves of the receptor units. 8. A hypothesis is proposed regarding the function of integumentary structures on the membrane in stimulus transformation.

Precursor structures and evolution of Tympanal organs in Lepidoptera (Insecta, Pterygota)

Article

Oct 1997

Ivar Hasenfuss

The patterns of scolopal organs and their innervation were studied by the methylene blue method in larvae, pupae and adults of an Yponomeuta species (Yponomeutidae) and of tympanate adult representatives of the Noctuoidea, Geometridae, Drepanidae and Pyraloidea. The studies were focused mainly on the mesothorax, the metathorax and some anterior abdominal segments. In the abdominal tympanal organs of Geometridae, Drepanidae and Pyraloidea, the auditory scolopidia are homologous with the lateral scolopal organs of the first abdominal segment; however, the hearing organs as such evolved independently in the three taxa. The studies confirm that the tympanal organ in the Noctuoidea is derived from the caudal dorsolateral region of the metathorax including its dorsal scolopal organ and the B-cell. The adult scolopal organs are present already in the larvae and are maintained nearly unchanged during metamorphosis to the adult. Only in the Noctuoidea are the three sensory cells of the larval scolopal organs, which become part of the tympanal organs, reduced to one (in Notodontidae) or two (in other Noctuoidea) during metamorphosis. A hypothetical scenario of the evolution of the tympanal organs is outlined.

The coding of airbone-sound and vibration signals in bimodal ventral-cord neurons of the grasshopper Tettigonia cantans

Article

Jan 1980

In grasshoppers, the auditory and vibrational senses converge on the same ventral-cord neurons. All neurons in the ventral cord that discharge impulses in response to either airborne-sound or vibration stimuli also receive synaptic inputs from the other sensory system. The latter elicit either subthreshold excitation or inhibition. The coding of the conspecific song in the responses of most ventral-cord neurons ofTettigonia cantans is considerably improved when the stimulus consists not of simulated natural sounds alone, but of such sounds together with either maintained vibration or vibration matched to the temporal structure of the song. Stridulating tettigoniids produce both airborne and substrate-conducted sound. Thus the perception of airborne sound and vibration, and their simultaneous processing in individual ventral-cord neurons, may be of fundamental importance — not only in localizing a nearby sound source, but also in facilitating the recognition of conspecific signals.

The auditory system of silent grasshoppers, differing in regression of their tympanal ears (Melanoplinae: Podismini)

Article

Jan 2010

Reduction of tympanal hearing organs is repeatedly found amongst insects and is associated with weakened selection for hearing. There is also an associated wing reduction, since flight is no longer required to evade bats. Wing reduction may also affect sound production. Here, the auditory system in four silent grasshopper species belonging to the Podismini is investigated. In this group, tympanal ears occur but sound signalling does not. The tympanal organs range from fully developed to remarkably reduced tympana. To evaluate the effects of tympanal regression on neuronal organisation and auditory sensitivity , the size of wings and tympana, sensory thresholds and sensory central projections are compared. Reduced tympanal size correlates with a higher auditory threshold. The threshold curves of all four species are tuned to low frequencies with a maximal sensitivity at 3–5 kHz. Central projections of the tympanal nerve show characteristics known from fully tympanate acridid species, so neural elements for tympanal hearing have been strongly conserved across these species. The results also confirm the correlation between reduction in auditory sensitivity and wing reduction. It is concluded that the auditory sensitivity of all four species may be maintained by stabilising selective forces, such as predation.

Evolutionary and Phylogenetic Origins of Tympanal Hearing Organs in Insects

Abstract

No full-text available

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