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Nerve Cells and Insect Behavior—Studies on Crickets1 This Report on Nerve Cells and Insect Behavior Is Dedicated to the Memory

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Nerve Cells and Insect Behavior—Studies on Crickets1 This Report on Nerve Cells and Insect Behavior Is Dedicated to the Memory AMER. ZOOL., 30:609-627 (1990) Nerve Cells and Insect Behavior—Studies on Crickets1 FRANZ HUBER Max-Planck-Institute fur Verhaltensphysiologie, D 8130 Seewiesen, Federal Republic of Germany SYNOPSIS. Intraspecific acoustic communication during pair formation in crickets pro- vides excellent material for neuroethological research. It permits analysis of a distinct behavior at its neuronal level. This top-down approach considers first the behavior in quantitative terms, then searches for its computational rules (algorithms), and finally for neuronal implementations. Downloaded from https://academic.oup.com/icb/article/30/3/609/225053 by guest on 30 September 2021 The research described involves high resolution behavioral measurements, extra- and intracellular recordings, and marking and photoinactivation of single nerve cells. The research focuses on sound production in male and phonotactic behavior in female crickets and its underlying neuronal basis. Segmental and plurisegmental organization within the nervous system are examined as well as the validity of the single identified neuron approach. Neuroethological concepts such as central pattern generation, feedback control, command neuron, and in particular, cellular correlates for sign stimuli used in conspecific song recognition and sound source localization are discussed. Crickets are ideal insects for analyzing behavioral plasticity and the contributing nerve cells. This research continues and extends the pioneering studies of the late Kenneth David Roeder on nerve cells and insect behavior by developing new techniques in behavioral and single cell analysis. INTRODUCTION THE KIND OF APPROACH IN This report on nerve cells and insect NEUROETHOLOGY behavior is dedicated to the memory of the Neuroethology as the study of the neural late Kenneth D. Roeder, a founding father basis of behavior favors what I call the top- of neuroethology, the field of interdisci- down approach: a distinct behavioral strat- plinary research which aims to bridge the egy has to be observed and analyzed first gap between behavioral strategies and the in the field under environmental con- underlying neural substrates and mecha- straints, then quantitatively studied in the nisms. laboratory, and finally explored at its neu- Zoologists have the opportunity to select ronal and, if possible, molecular levels. This among the manifold behaviors formed by top-down approach is chosen because we evolution, and to choose those where they strongly believe that it is the behavior, think an answer is within reach when shaped and adapted by nature's abiotic and applying current technological know-how. biotic forces, which leads us to pose the Their approach is a comparative one and right questions to the nervous system. Thus, should be evolution-oriented. Zoologists neuroethologists should become familiar are interested in individual, population and with the concepts, methods, and data the species solutions, in common principles as study of behavior has to offer, as well as well as in differences. One should never with the whole scenario of modern neu- forget that a cricket differs from a frog, rosciences, including approaches at the sys- and a crayfish differs from a bird in its tem, cellular and molecular levels (Huber, demands. 1988, 1989). Neuroethologists working compara- tively have to consider two equally impor- ACOUSTIC COMMUNICATION IN CRICKETS: tant sets of questions which were formu- A FAVORABLE STRATEGY lated by T. H. Bullock (1984) (Table 1). Orthopteran and homopteran insects were among the first within the animal kingdom to have evolved hearing and 1 From the Symposium on Science as a Way of Know- sound production for intraspecific and ing—Neurobiology and Behavior organized by Edward S. Hodgson and presented at the Centennial Meeting interspecific interactions. For pair forma- of the American Society of Zoologists, 27-30 Decem- tion and reproduction, the main topics ber 1989, at Boston, Massachusetts. here, the information encoded in the send- 609 610 FRANZ HUBER TABLE 1. Aims of comparative and evolution-orientedbe considered as a releasing stimulus for veuroethology. the subsequent one (for literature see Loher 1. What are the neural correlates and causal rela- and Dambach, 1989). tionships to known behaviors and behavioral dif- ferences among animals? 2. How to improve effective calling 2. What are the behavioral correlates and causal re- and sound radiation lationships to known neural differences among an- Mole crickets have developed tactics to imals? make calling songs more efficient. They (Statements made by T. H. Bullock, 1984.) produce them in a burrow which they mod- ify to an exponential horn which amplifies sounds of the correct carrier frequency. Downloaded from https://academic.oup.com/icb/article/30/3/609/225053 by guest on 30 September 2021 er's acoustic signals must be decoded by Flying conspecifics hear such signals already the receiver. The nervous system of the at distances of several hundred meters sender (usually the male) generates sound which guide their orientation (for litera- signals which are species-specific in their ture see Bennet-Clark, 1989). frequency spectra and their temporal orga- Male tree crickets (Oecanthus burmeisteri) nization (Fig. 1) (for literature see Bennet- improve sound intensity and radiation by Clark, 1989). The nervous system of the a baffle. They cut a hole into a leaf, into receiver (usually the female) has to fulfill which they place themselves and sing (Pro- two equally important tasks: it must be able zesky-Schulze et al., 1975). to discriminate conspecific songs from abiotic and biotic noises in order to rec- 3. Satellite behaviors ognize them (song-recognition), and it must In Gryllus integer only some males call localize the sender's position in space (song- and attract female crickets (also females of localization) (for literature see Schildber- the parasitoid flies, Euphasioptery ohracea ger et al., 1989). [Cade, 1975]), whereas other males are In insects, these distinct sender-receiver silent, surround the caller and are named interactions have evolved during the course satellites. If on her way to the singing male of phylogeny; they are formed during the female meets a satellite male, he is able ontogeny and based mainly on genetically to court and to mate with her (Cade, 1980). fixed patterns of behavior. In my report I The physiological conditions responsible will concentrate on crickets and consider for calling or noncalling are still unknown. the topics listed in Table 2. Advantages and disadvantages for callers and noncallers have been discussed, but will SOME BEHAVIORAL STRATEGIES IN not be mentioned here. CRICKETS Although crickets are best known and 4. Prey-predator strategies famous for their songs and acoustically Many cricket species are nocturnally mediated behavior, they have evolved other active. Sound traps broadcasting the con- strategies which should interest us because specific song attract flying males and they point to multisensory and multimodal females from far away (Ulagaraj and conditions demonstrating that the cricket's Walker, 1973; Walker, 1982). During their world is not solely acoustic (Huber, 1988, nocturnal flights these animals can be 1989). Here are a few examples. preyed upon by echolocating and hunting bats. Teleogryllus has evolved avoidance 1. Behaviors involved in pair formation, strategies (Moiseff et al., 1978). The ani- reproduction and aggression mals hear ultrasonic sounds and process During the reproductive season adult them in distinct neurons (Moiseffand Hoy, male and female crickets display sequences 1983) which control their turning away of distinct behavioral patterns which serve from the sound source (for literature see pair formation and mating as well as indi- Pollack and Hoy, 1989). vidual spacing, aggression and territorial Acheta domestica in southern France is defence. Each single behavioral event can known as prey for a parasitic digger wasp NERVE CELLS AND INSECT BEHAVIOR 611 Calling songs Frequency spectra IHHtlHH* Gryllus campestns 2 4 6 8 1012 1416 kHz 2 0 Teleogryllvs oceanicus Downloaded from https://academic.oup.com/icb/article/30/3/609/225053 by guest on 30 September 2021 Melanogryftus desertus 2 4 6 8 10 12 14 kHz Oecanthus pellucens 12 4 6 6 10 12 14 kHz FIG. 1. Calling song patterns and frequency spectra in different species of crickets (modified from Huber, 1990). of the genus Liris. The flying wasp patrols mill while being kept in place by the coun- the cricket area then lands and approaches terrotating treadmill, we recently found a cricket on foot. In the case of no escape, that female Acheta domestica track optical the wasp stings and paralyzes the cricket. targets such as black squares (Atkins et al., The prey is then carried as food to the 1987). When given a choice between a black wasp's nest. But crickets have developed a square and a conspecific calling song (Fig. warning system, consisting of an arrange- 3), the female previously tracking a visual ment of filiform hair sensilla on their cerci. target switches to track the calling song, A flying and fast walking wasp creates air but only if its temporal pattern lies within currents strong enough to stimulate the the attractive range (Stout et al, 1987). filiform hair sensilla and to elicit activity During orientation to the sound source she which is then transmitted to different performs a zig-zag walking course which is ascending interneurons within the ventral characteristic for phonotaxis and expressed nerve cord. Their activity controls quick as a pattern of several steps interrupted by defensive and escape responses, such as short pauses. During orientation to the head stand, kicking with the hindlegs, and visual target she lacks that kind of walking running away (Gnatzy and Heusslein, 1986; mode (Weber et al, 1987). Thus, there for literature see Gnatzy and Hustert, seems to be a different interfacing between 1989). the visual and the acoustical recognition system and the walking generator. The shift 5. Combined visual and acoustical in walking modes indicates the change in cues for orientation the cricket's attention and in the modality Many crickets have well developed com- being processed.
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