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Sensillum structure via electron microscopy. a: Longitudinal section of the scolopale (compare with Fig. 2c). The inset shows a longitudinal section of the basal body, where the ciliary root ends and the sensory cilium begins. b: Cross section of the scolopale cap, connected to the attachment cell by desmosomes. c: Cross section of attachment cells with connections by desmosomes. The inset shows another kind of connection between two attachment cells. d: Cross section of the scolopale in the area where the scolopale rods are connected to form a cylinder. at, attachment cell; c, cilium; crt, ciliary root; d, desmosome; ex, extracellular space; gm, granular material; mt, microtubuli; sc, scolopale cap; scc, scolopale cell; sr, scolopale rod. Scale bars 1.7 m in a; 0.25 m in a (inset); 0.6 m in b; 2.5 m in c; 0.4 m in d.
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In different insect taxa, ears can be found on virtually any part of the body. Comparative anatomy and similarities in the embryological development of ears in divergent taxa suggest that they have evolved multiple times from ubiquitous stretch or vibration receptors, but the homology of these structures has not yet been rigorously tested. Here we...
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Context 1
... scolopale cell (Figs. 3, 4a). In the middle of this extracellular space is an area of granular material. The canal is maintained by the scolopale rods situated in the scolopale cell. Five to seven rods are separated from each other in the middle of the scolopale, but at the scolopale edges the rods are connected to each other, forming a cylinder (Fig. 4d). The scolopale rods have an electron-dense appearance. The cilium protrudes to the scolopale cap at the tip of the scolopale ...
Context 2
... entering the scolopale cap, the sensory cilium dilates and the 9 pairs of microtubuli surround a cylinder of electron-dense material. The scolopale cap is an extra- cellular structure consisting of electron-dense material penetrated by holes and cavities (Fig. 4a,b). The attach- ment cell constitutes the final cell of the sensillum. It surrounds the scolopale cap and is tightly attached to it by desmosomes. Attachment cells are extremely long (up to 1.4 mm), have very long nuclei, contain densely packed microtubuli, and are interconnected by desmosomes ( ...
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Citations
... These organs are present in all parts of the insect body [1,3,4]. Chordotonal organs consist of a Insects 2024, 15, 392 2 of 12 highly variable number of scolopidial sensilla that can range from a single sensillum to several thousand sensilla [5][6][7][8][9][10][11][12][13]. Scolopidial sensilla detect mechanical forces acting on the dendrite of the sensory neurons [3,14,15]. ...
The subgenual organ complex of stick insects has a unique neuroanatomical organisation with two elaborate chordotonal organs, the subgenual organ and the distal organ. These organs are present in all leg pairs and are already developed in newly hatched stick insects. The present study analyses for the first time the morphology of sensory organs in the subgenual organ complex for a membrane connecting the two sensory organs in newly hatched insects (Sipyloidea chlorotica (Audinet-Serville 1838)). The stick insect legs were analysed following hatching by axonal tracing and light microscopy. The subgenual organ complex in first juvenile instars shows the sensory organs and a thin membrane connecting the sensory organs resembling the morphology of adult animals. Rarely was this membrane not detected, where it is assumed as not developed during embryogenesis. The connection appears to influence the shape of the subgenual organ, with one end extending towards the distal organ as under tension. These findings are discussed for the following functional implications: (1) the physiological responses of the subgenual organ complex to mechanical stimuli after hatching, (2) the influence of the membrane on the displacement of the sensory organs, and (3) the connection between the subgenual organ and distal organ as a possible functional coupling.
... In bladder grasshoppers, acoustic communication plays a major role in mate location (van Staaden and Römer 1997;Römer and Bailey 1998;van Staaden et al. 2003;van Staaden 2004, 2006). To attract females, males produce a loud advertisement call by rubbing a line of ridges on their hind-femur against a crescent-shaped ridge on the side of the inflated abdominal bladder, functioning as an acoustic resonator. ...
Acoustic communication in animals relies upon specific contexts and environments for effective signal transmission. Increasing anthropogenic noise pollution and different weather conditions can disrupt acoustic communication. In this study, we investigated call parameter differences in the bladder grasshopper Bullacris unicolor inhabiting two sites in close proximity to each other that differed in their noise levels. Calling activity was monitored via passive acoustic recorders. Weather conditions, including wind speed, temperature and humidity, were also recorded. We found that the interval between successive calls increased with higher noise levels at both sites, and the peak frequency became lower. The total number of calls detected also decreased with anthropogenic noise, but this relationship was only evident at the noisier site. In addition, grasshoppers shifted the timing of their calls to later in the night at the noisier site, possibly to take advantage of relatively lower noise levels. We also found that weather conditions, particularly temperature, had a significant influence on call parameters. Further studies are thus needed to disentangle the effects of anthropogenic noise and environmental variables on calling activity in this species. Our results lend support to the growing concern regarding the effects of noise pollution on animal acoustic signalling systems and also highlight the complexity of factors which affect sound signalling in natural environments.
... The example of the atympanate bladder grasshopper Bullacris membracioides 248 with no less than six pairs of ears demonstrates that responses to biologically 249 significant sound may not depend on sender–receiver matching, given that some 250 conditions are met (van Staaden and R€ omer 1998; vanStaaden et al. 2003). These 251 insects possess six pairs of ears: one in abdominal segment 1, homologous to the 252 single pair of tympanate ears found in " modern " grasshoppers, and in addition, five 253 posterior pairs of ears in abdominal segments 2–6, resembling pleural chordotonal 254 organs (plCOs) in other grasshoppers. ...
... All six pairs of plCOs respond to acoustic 255 stimulation within a biologically meaningful intensity and frequency range, 256 although only the organs in the posterior segments matched with their tuning to 257 the male call at 1.7 kHz. By contrast, the organ in the first abdominal segment is 258 tuned to 4 kHz, but since it is extremely sensitive (absolute threshold 13 dB SPL), 259 the active range of the signal achieved with this " mismatched organ " is much higher 260 than the corresponding value of the matched pairs of ears (vanStaaden et al. 2003). ...
The sense of hearing evolved in insects many times independently, and different groups use sound for intraspecific communication, predator detection, and host finding. Although it can be generally assumed that ears and associated auditory pathways are matched to the relevant properties of acoustic signals and cues, the behavioral contexts, environmental conditions, and selection pressures for hearing may differ strongly between insects. Given the diversity in ear structure, active range of hearing, and the behavioral and ecological context under which hearing evolved, it is probably not surprising to find cases of sensory systems apparently mismatched to relevant parameters of the physical world. Indeed, such cases may be equally instructive for the principle of matching as the perfectly matched ones, since they may tell us something about the conflicting selection pressures and trade-offs associated with a given solution. The examples I have chosen cover the most traditional aspect of matching in the acoustic domain, namely, how the carrier frequency of the relevant sound is matched to the tuning of receivers and how central nervous processing allows species-specific responses to the temporal parameters of song. However, economical filtering also occurs in the intensity domain, starting as early as in the receptors and continuing at the first synapse of central processing. All examples serve to illustrate the similarities and differences between the sensory systems; both may help to define the conditions under which matching operates and may have evolved.
... Indeed, when we consider the number of auditory afferents across bat-detecting insects ( Table 1), those that use their ears solely to detect bats have fewer afferents (1-32) than those that also use their ears for other purposes (60-150). The number of afferents is even greater for insects that only use their ears for communication, such as cicadas (∼1500; Wohlers et al., 1979) and bladder grasshoppers (∼2000; Van Staaden et al., 2003). In addition to rapid information processing, evolutionary history and physical and energetic constraints probably contributed to the simplicity of bat-detecting ears (Hasenfuss, 1997;Dusenbury, 2001;Smith and Lewicki, 2006;Niven and Laughlin, 2008). ...
Echolocation in bats and high-frequency hearing in their insect prey make bats and insects an ideal system for studying the sensory ecology and neuroethology of predator-prey interactions. Here, we review the evolutionary history of bats and eared insects, focusing on the insect order Lepidoptera, and consider the evidence for antipredator adaptations and predator counter-adaptations. Ears evolved in a remarkable number of body locations across insects, with the original selection pressure for ears differing between groups. Although cause and effect are difficult to determine, correlations between hearing and life history strategies in moths provide evidence for how these two variables influence each other. We consider life history variables such as size, sex, circadian and seasonal activity patterns, geographic range and the composition of sympatric bat communities.We also review hypotheses on the neural basis for antipredator behaviours (such as evasive flight and sound production) in moths. It is assumed that these prey adaptations would select for counter-adaptations in predatory bats. We suggest two levels of support for classifying bat traits as counter-adaptations: traits that allow bats to eat more eared prey than expected based on their availability in the environment provide a low level of support for counter-adaptations, whereas traits that have no other plausible explanation for their origination and maintenance than capturing defended prey constitute a high level of support. Specific predator counter-adaptations include calling at frequencies outside the sensitivity range of most eared prey, changing the pattern and frequency of echolocation calls during prey pursuit, and quiet, or 'stealth', echolocation.
... Given the detailed duetting behavior and the sophisticated use of atmospheric conditions at night for maximizing the active range of the signal, it is a surprise to note the absence of tympana in the abdominal hearing organs, which are typical for ears of modern grasshoppers. In order to determine the neural basis underlying pair formation behavior in B. membracioides, van Staaden and Römer (1998) and van Staaden et al. (2003) used anatomical, neurophysiological, and behavioral analyses to define the extent to which this species possesses functional ears despite the lack of tympana. At the same position, laterally in the first abdominal segment where in modern grasshoppers a pair of tympanal ears is located, the bladder grasshopper lacks a thinned tympanic membrane, but nevertheless, there is a pear-shaped pleural chordotonal organ (plCO1) in a corresponding location as the Müller's organ (Fig. 3.1a). ...
... In at least three species of pneumorid, there are alternate males which are incapable of flight and sound production because they lack macropterous wings and the inflated abdomen, but retain the strong host-plant philopatry of nymphal stages and can be found in the field in copula with females (Alexander and van Staaden 1989; Fig. 3.1 ). Despite the fact that inflated and alternate morphs follow distinctly different developmental trajectories in attaining their final forms (Donelson and van Staaden 2005), tuning and sensitivity of their hearing organs is identical (van Staaden et al. 2003). Costs and benefits for polyphenic males differ strongly though, with adult longevity of small, uninflated males twice that of the larger inflated ones (Donelson et al. 2008 ). ...
Bladder grasshoppers are a small family of Orthoptera, with ear morphology and physiology, behavior, and sensory ecological features outstanding among acoustic insects. Acoustic communication is characterized by male and female duetting and male phonotaxis. The detection distance of the male signal is exceptional at about 2 km, achieved via stridulation against air-filled abdominal resonators, and exploitation of weather conditions ideal for sound transmission. In at least three species, alternate male morphs occur which are incapable of flight and sound production but copulate with females. Such alternative mating tactics constitute profound selective pressures for sexual competition and the evolution of the communication system. Auditory sensitivity is mediated by an array of six pairs of atympanate ears in abdominal segments A1–A6. The auditory organ, a pleural chordotonal organ, in A1 comprises about 2,000 sensilla, whereas ears in segments A2–A6 are less developed, making pneumorids a unique system for studying the evolution of complex ears from simple precursors.
... Long-distance acoustic signaling and hearing is used by the ancient bladder grasshopper Bullacris membracioides (van Staaden, M. J. and Römer, H., 1997;van Staaden, M. J. et al., 2003). Auditory organs in males and females may represent an early evolutionary stage. ...
Invertebrate auditory pathways are used for processing of species-specific signals and predator sounds. Although many invertebrates have sensory structures that can respond to sound, hearing is well developed and widely used only in insects, which form the subject of this chapter. Primary auditory afferents respond to sound pressure-induced mechanical oscillations of a tympanic membrane. The afferents forward their spike activity to an auditory neuropil in the central nervous system. Here, the first steps of signal processing are performed by local and ascending auditory neurons. Information on intensity, frequency, or direction is refined and sent to the brain via ascending axons. In the brain, a more complex processing takes place; based on the specific pattern of sound signals, different behavioral responses may be initiated. Although hearing has evolved in different groups of insects, the functional organization of the auditory pathway appears to be similar across the taxa. A brief overview presents the different hearing organs that have evolved in insects. Then the spatial organization of afferents in the auditory organs and the arrangement of their central projection patterns are compared with their functional properties. This demonstrates a highly structured organization of the auditory pathways already at the first stages of neural processing. The central auditory pathways of different groups of insects are described with particular emphasis on functional properties such as frequency analysis, temporal processing, pattern recognition, and the processing of directional acoustic information. Neural mechanisms are analyzed and the contribution of single neurons to behavior is highlighted. Finally we describe the impact of motor activity on hearing and what mechanisms may be employed to maintain auditory sensitivity during sound production.
... Given the conservative nature of nervous systems (Dumont & Robertson, 1986;Edwards & Palka, 1991;Paul, 1991;Tierney, 1995), the key changes are most likely biomechanical, such as broadening of thinned cuticular areas and apposition of enlarged tracheal sacs to that cuticle. As graphically demonstrated in pneumorid grasshoppers (van Staaden & Römer, 1998;van Staaden et al., 2003), serially homologous regions can have a shared potential for transformation to an auditory organ. Although independently evolved, such segmental ears are actually the same in an evolutionary-developmental sense (Raff, 1996;Yager, 1999a). ...
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.
... Long-distance acoustic signaling and hearing is used by the ancient bladder grasshopper Bullacris membracioides (van Staaden, M. J. and Römer, H., 1997;van Staaden, M. J. et al., 2003). Auditory organs in males and females may represent an early evolutionary stage. ...
... In these insects, the single attachment renders the ear 'tone deaf', but multiple scolopidia within the single chordotonal organ extend the range of sound intensities detectable by the insect. In grasshoppers (Acrididae), multiple chordotonal organ attachment sites enable the insect to discriminate frequencies, since diVerent regions of the tympanal membrane to which the receptors attach diVer in their resonant properties (Michelsen 1971a, b; Jacobs et al. 1999; Van Staaden et al. 2003). In hedylids, the three chordotonal organs may indeed respond to diVerent frequencies due to the resonant properties of the tympanal membrane. ...
Nocturnal Hedyloidea butterflies possess ultrasound-sensitive ears that mediate evasive flight maneuvers. Tympanal ear morphology, auditory physiology and behavioural responses to ultrasound are described for Macrosoma heliconiaria, and evidence for hearing is described for eight other hedylid species. The ear is formed by modifications of the cubital and subcostal veins at the forewing base, where the thin (1-3 microm), ovoid (520 x 220 microm) tympanal membrane occurs in a cavity. The ear is innervated by nerve IIN1c, with three chordotonal organs attaching to separate regions of the tympanal membrane. Extracellular recordings from IIN1c reveal sensory responses to ultrasonic (>20 kHz), but not low frequency (<10 kHz) sounds. Hearing is broadly tuned to frequencies between 40 and 80 kHz, with best thresholds around 60 dB SPL. Free flying butterflies exposed to ultrasound exhibit a variety of evasive maneuvers, characterized by sudden and unpredictable changes in direction, increased velocity, and durations of approximately 500 ms. Hedylid hearing is compared to that of several other insects that have independently evolved ears for the same purpose-bat detection. Hedylid hearing may also represent an interesting example of evolutionary divergence, since we demonstrate that the ears are homologous to low frequency ears in some diurnal Nymphalidae butterflies.
... This intensity is well above the female behavioural response threshold of ca. 65 dB SPL, but below that at which receptor response is saturated (van Staaden et al., 2003). ...
Male acoustic signals and the information they convey are often critical determinants of fe-male mate choice. Bladder grasshoppers are one of numerous orthopteran taxa utilizing sound as the basis of courtship and ultimately mating. However, despite the extreme specializations for long-distance acoustic communication in this family, female mating preferences for male calls have not been previously investigated. Here we examine female acoustic responses to playbacks of male calls in Bullacris membracioides. Females were tested in three separate contexts, viz. response to conspecific calls of different individuals, response to degraded con-specific calls, and response to the calls of two heterospecifics. Female response was sig-nificantly correlated with seven of eight measured call features within B. membracioides, indicating sexual selection to be operating in this species. Females also responded to con-specific calls with degradation levels equivalent to a male calling 150 m away, but intensity equivalent to one at 25 m, identifying call amplitude rather than degradation as the factor limiting female response. However, as response decreased with increasing call degradation, signal quality remains a factor in female preference. Calls of the sister taxon B. interme-dia were equally attractive to B. membracioides females as were conspecific calls, while the more distinct calls of B. serrata were less preferred than those of both B. membracioides and B. intermedia. This indicates a lack of discriminatory ability against a similar sounding heterospecific.
