Animal signals and communication 2: animal communication and noise

Abstract

Research on insect hearing and acoustic communication has made enormous progress in the twentieth century. Following the first descriptions of auditory organs behavioural studies pointed to the importance of insect hearing for intraspecific acoustic communication, predator avoidance and prey detection. Analysing the neural mechanisms underlying auditory processing and the motor activity for acoustic signalling in a variety of species has provided us with a deep functional understanding of this insect behaviour. As questions of central biological importance are exemplified in Insect Hearing and Acoustic Communication these will drive the current and future research. The sounds of singing and chirping insects are a salient feature of summer meadows, Mediterranean olive groves or tropical rain forests and have always caught the attention of naturalists and scientists. The evolution of insect ears has been driven by sexual and by natural selection in the context of intraspecific communication and by predator avoidance and prey detection. Ears have evolved in a variety of body regions, and evolved many times in parallel. The functional significance of insect acoustic signals and hearing organs, however, has only become evident over time. When Pumphrey (1940) wrote the first comprehensive review on “Hearing in Insects”, he began his conclusions with “The present time is perhaps a happy one for reviewing the experimental findings on the physiology of audition in insects in relation to their behaviour”. For Pumphrey, due to the earlier first detailed anatomical descriptions of hearing organs in different groups of insects, for example by Schwabe (1906) and Eggers (1911), and the demonstration that female crickets are attracted to the acoustic signals of a male calling song broadcast by a telephone receiver (Regen 1913), it became obvious that sound production and the sense of hearing played a crucial role in insect behaviour. The development of suitable electronic equipment allowed the field to progress rapidly, as indicated by the following key papers: The first electrophysiological recordings of auditory nerve activity in crickets and bushcrickets were obtained by Weever and Bray (1933) and gave an indication of the frequency range of the auditory responses. The biophysics of tympanal organs was analysed by Autrum (1941) and was related to a general theory of insect hearing. Roeder took his moth preparations to the field and demonstrated both the ultrasound sensitivity of moth ears and the afferent responses to sonar calls of hunting bats passing by (Roeder and Treat 1957). In 1961, the first recordings of thoracic auditory neurons in Tettigoniids were reported by Suga and Katsuki (1961) addressing frequency analysis, directional sensitivity and central inhibition. Questions about the higher central mechanisms of acoustic communication remained open for some time until Huber (1960) elicited singing behaviour in crickets by means of electrical brain stimulation and Roeder (1969) carried out the first recordings of auditory brain neurons in moths. Then developments were fast: The advent of neural tracing techniques and intracellular recordings in insects allowed such advances as a systematic study of auditory pathways at the level of identified neurons, their structure and response properties (e.g. Rehbein et al. 1974; Casaday and Hoy 1977; Wohlers and Huber 1978) and a cellular approach to the neuronal control of singing behaviour (Bentley 1969). The increase in the inventory of scientific tools over the last decades with advances in behavioural and neural recording methods, in microscopy, and in molecular and genetic methods now allows tackling fundamental problems of insect hearing and acoustic communication at all levels from ecology to molecular mechanisms. 1.1 Central Research Questions The variety of signalling behaviours and hearing organs makes insects highly suitable animals to explore and analyse signal generation and auditory processing. The fascinating progress that has been made is still related to a set of central questions characterising the focus of past, current and future research: How did hearing and acoustic communication behaviour evolve in insects and what is the neural and developmental origin of the auditory organs? What are the functional properties of hearing organs in respect of intensity, frequency and directional sensitivity and how are these achieved at a molecular, biophysical and neural level? How are hearing and sound production embedded in the natural lifestyle of the animals allowing intraspecific communication and also predator avoidance and even predation? How is phonotactic behaviour tuned to the communication signals of conspecifics? What are the neural mechanisms of peripheral and central auditory processing that allow the recognition of species-specific sounds and lead to adapted motor responses? What are the biophysical and neural mechanisms underlying signal generation? How are central pattern generators organised that drive the species-specific motor activity and how is their activity controlled by the brain? Finally: What is the genetic basis of acoustic communication behaviour that leads to species-specific signal generation and pattern recognition and even speciation? The subsequent chapters of this book will cover and address these questions to different degrees. The answers to these questions provide us with profound and fundamental understanding of a conspicuous and crucial insect behaviour. The final story will emerge by our ongoing research activity, closing again with Pumphrey (1940): “It will be obvious that much remains to be done”. Contents 1 Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 Berthold Hedwig 2 Evolutionary and Phylogenetic Origins of Tympanal Hearing Organs in Insects. . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Johannes Strauß and Reinhard Lakes-Harlan 3 Hearing and Sensory Ecology of Acoustic Communication in Bladder Grasshoppers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27 Heiner Römer, Adam R. Smith and Moira van Staaden 4 Auditory Parasitoid Flies Exploiting Acoustic Communication of Insects . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45 Berthold Hedwig and Daniel Robert 5 Adaptive Sounds and Silences: Acoustic Anti-Predator Strategies in Insects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 William E. Conner 6 Acoustic Communication in the Nocturnal Lepidoptera . . . . . . . . . . . 81 Michael D. Greenfield 7 Cicada Acoustic Communication. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101 Paulo J. Fonseca 8 Towards an Understanding of the Neural Basis of Acoustic Communication in Crickets. . . . . . . . . . . . . . . . . . . . . . . . . . . 123 Berthold Hedwig 9 Neural Processing in the Bush-Cricket Auditory Pathway. . . . . . . . . . 143 Andreas Stumpner and Manuela Nowotny viii Contents 10 Evolution of Call Patterns and Pattern Recognition Mechanisms in Neoconocephalus Katydids . . . . . . . . . . . . . . . . . . . . . 167 Johannes Schul, Sarah L. Bush and Katy H. Frederick 11 Processing of Species-Specific Signals in the Auditory Pathway of Grasshoppers. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185 Bernhard Ronacher 12 Sound Communication in Drosophila. . . . . . . . . . . . . . . . . . . . . . . . . . 205 Damiano Zanini, Bart Geurten, Christian Spalthoff and Martin C. Göpfert Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 219