Andreas Stumpner

Evolution and function of auditory systems in insects.

Abstract. While the sensing of substrate vibrations is common among arthropods, the reception of sound pressure waves is an adaptation restricted to insects, which has arisen independently several times in different orders. Wherever studied, tympanal organs were shown to derive from chordotonal precursors, which were modified such that mechanosensitive scolopidia became attached to thin cuticular membranes backed by air-filled tracheal cavities (except in lacewings). The behavioural context in which hearing has evolved has strongly determined the design and properties of the auditory system. Hearing organs which have evolved in the context of predator avoidance are highly sensitive, preferentially in a broad range of ultrasound frequencies, which release rapid escape manoeuvres. Hearing in the context of communication does not only require recognition and discrimination of highly specific song patterns but also their localisation. Typically, the spectrum of the conspecific signals matches the best sensitivity of the receiver. Directionality is achieved by means of sophisticated peripheral structures and is further enhanced by neuronal processing. Side-specific gain control typically allows the insect to encode the loudest signal on each side. The filtered information is transmitted to the brain, where the final steps of pattern recognition and localisation occur. The outputs of such filter networks, modulated or gated by further processes (subsumed by the term motivation), trigger command neurones for specific behaviours. Altogether, the many improvements opportunistically evolved at any stage of acoustic information-processing ultimately allow insects to come up with astonishing acoustic performances similar to those achieved by vertebrates.

Convergent evolution of insect hearing organs from a preadaptive structure

Flies of the taxon Emblemasomatini (Sarcophagidae: Diptera) independently evolved an ear with the same anatomy and location as the Ormiini (Tachinidae: Diptera). Both ears represent a first case of convergent evolution of homologous insect ears, which raises the question for a preadaptation. Physiological and anatomical data indicate a preadaptive–sound–insensitive, but vibration–sensitive scolopidial chordotonal organ in non–hearing flies. As selective pressure for the evolutionary transformation from a vibration receiver into a sound receiver, fast and precise cues for the localization and detection of the sound producing hosts can be presumed.

A new biophysical method to determine the gain of the acoustic trachea in bushcrickets.

A method is described for measuring the gain (i.e., the change of amplitude and phase angle) for sounds that propagate to the internal surface of the tympana in ears working as pressure difference receivers. The gain of the acoustic trachea has been measured in two similarly sized and closely related species of bushcrickets, in which the acoustic spiracles and tracheae differ markedly in size. The amplitude part of the gain is much larger in the species with the larger acoustic spiracle, whereas the phase part is very similar in the two species. The method is compared with other methods, which in the past have been used for estimating the gain of sound pathways inside animal bodies.

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

Abstract. 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.

Evolutionarily conserved coding properties of auditory neurons across grasshopper species

We investigated encoding properties of identified auditory interneurons in two not closely related grasshopper species (Acrididae). The neurons can be homologized on the basis of their similar morphologies and physiologies. As test stimuli, we used the species-specific stridulation signals of Chorthippus biguttulus, which evidently are not relevant for the other species, Locusta migratoria. We recorded spike trains produced in response to these signals from several neuron types at the first levels of the auditory pathway in both species. Using a spike train metric to quantify differences between neuronal responses, we found a high similarity in the responses of homologous neurons: interspecific differences between the responses of homologous neurons in the two species were not significantly larger than intraspecific differences (between several specimens of a neuron in one species). These results suggest that the elements of the thoracic auditory pathway have been strongly conserved during the evolutionary divergence of these species. According to the ‘efficient coding’ hypothesis, an adaptation of the thoracic auditory pathway to the specific needs of acoustic communication could be expected. We conclude that there must have been stabilizing selective forces at work that conserved coding characteristics and prevented such an adaptation.

SONG PRODUCTION AND SONG RECOGNITION IN A GROUP OF SIBLING GRASSHOPPER SPECIES (CHORTHIPPUS DORSATUS, CH. DICHROUS AND CH. LORATUS: ORTHOPTERA, ACRIDIDAE)

ABSTRACT 1. Chorthippus dorsatus, Ch. dichrous and Ch. loratus are closely related, sympatric grasshopper species (subfam. Gomphocerinae) with few morphological differences. 2. Songs of males contain two elements: pulsed syllables produced during synchronous movements of the hindlegs (part A) and ongoing noise produced during alternating movements of the hindlegs (part B). Part A predominates in songs of Ch. loratus and part B in songs of Ch. dichrous. In Ch. dorsatus both parts contribute nearly equally to the songs. 3. Ch. dichrous and Ch. loratus are Eastern species, while Ch. dorsatus occurs all over Europe including Spain and Italy. The songs of different populations of Ch. dorsatus in Europe are compared. 4. Female stridulation of the three species is similar to male stridulation. 5. Females prefer—expressed by their response songs—the conspecific signals over heterospecific ones. Discrimination, however, is not perfect. 6. Tested with artificial song models, females of the different species differ ...

Songs and the Function of Song Elements in Four Duetting Bushcricket Species (Ensifera, Phaneropteridae, Barbitistes)

The structure of male songs and the timing of female replies with respect to the male songs are described for four species of the palaearctic bushcricket genus Barbitistes (B. constrictus, B. ocskayi, B. serricauda, B. yersini). In a male song, 3 to 16 syllables form a chirp followed by a “trigger syllable” after a longer interval. The trigger syllable releases a female reply with a latency of 30 to 50 ms in all four species. In B. serricauda songs, there is no clearly separated trigger syllable. Instead, the first syllable of a chirp functions as a trigger syllable. Some B. serricauda males may produce a short female-type syllable just at the moment, when a female would reply. The possible function of such a syllable is acoustical mimicry. When comparing at least two song parameters, each species occupies a specific combination of values. According to the overlap of parameters a close phylogenetic relationship between B. constrictus and B. serricauda and between B. ocskayi and B. yersini is assumed. This interpretation is compared with a hypothesis based on morphological investigations.

Diversity of intersegmental auditory neurons in a bush cricket

Various auditory interneurons of the duetting bush cricket Ancistrura nigrovittata with axons ascending to the brain are presented. In this species, more intersegmental sound-activated neurons have been identified than in any other bush cricket so far, among them a new type of ascending neuron with posterior soma in the prothoracic ganglion (AN4). These interneurons show not only morphological differences in the prothoracic ganglion and the brain, but also respond differently to carrier frequencies, intensity and direction. As a set of neurons, they show graded differences for all of these parameters. A response type not described among intersegmental neurons of crickets and other bush crickets so far is found in the AN3 neuron with a tonic response, broad frequency tuning and little directional dependence. All neurons, with the exception of AN3, respond in a relatively similar manner to the temporal patterns of the male song: phasically to high syllable repetitions and rhythmically to low syllable repetitions. The strongest coupling to the temporal pattern is found in TN1. In contrast to behavior the neuronal responses depend little on syllable duration. AN4, AN5 and TN1 respond well to the female song. AN4 (at higher intensities) and TN1 respond well to a complete duet.

Auditory interneurons in a hearing fly (Therobia leonidei, Ormiini, Tachinidae, Diptera)

The physiology and morphology of auditory interneurons of a fly, the parasitoid Therobia leonidei, are described for the first time. 1. The hearing threshold has been determined with summed recordings of the neck connective. Females are most sensitive in a frequency range from 16 to 40 kHz (thresholds: around 45 dB SPL). This broad hearing range matches with the peak frequencies of the song spectra of host bushcricket species. Male flies are 10–20 dB less sensitive than females. 2. The sensory cells of the prosternal tympanal organ of T. leonidei project into the thoracico-abdominal ganglion complex with arborizations in all three thoracic neuromeres. 3. Three types of ascending auditory interneurons were identified by their morphology and response properties. These have arborizations in all three thoracic neuromeres and terminate soma-contralaterally in the brain. At least three other neuron types were also identified according to response properties alone. The neurons show similar spectral tuning but different sensitivities.

A species-specific frequency filter through specific inhibition, not specific excitation

Abstract. Many bushcrickets produce specific song spectra for acoustic communication. Song detection and/ or recognition may make use of such specificity. Where in the nervous system are the filters for song frequency situated? A peripheral tuning for song frequency typically does not exist. Auditory receptor cells of bushcrickets connect to local and ascending neurons in the prothoracic ganglion. One of the ascending neurons (1) may function as a frequency filter in a group of four related bushcrickets (genera Ancistrura, Barbitistes). The frequency response of ascending neuron 1 is species-specific roughly corresponding to the frequency of the conspecific male song. The species-specific tuning of the neuron is not brought about by specific excitation, but by specific inhibition. By eliminating this frequency-dependent and species-specific inhibition the former filter neuron is transformed into an unspecific broad-band neuron in all four species. Its tuning then does not differ from omega neuron 1, a local neuron which is rather unspecific for frequency. Also, the supra-threshold responses of ascending neuron 1, which are different in intact animals, are similar to each other and similar to omega neuron 1 following elimination of inhibition. Only ascending neuron 1 of Ancistrura retains some species-specific features at low frequencies. In conclusion, evolution changed inhibition, not excitation of a species-specific neuron.