Theo Weber

Auditory behavior of the cricket: II. Simplicity of calling-song recognition inGryllus, and anomalous phonotaxis at abnormal carrier frequencies

Summary1.Essential and nonessential features of the male field-cricket (Gryllus campestris L.) calling song have been identified by varying acoustic parameters while testing for phonotactic tracking by females walking on the Kramer spherical treadmill.2.In the natural calling song, a 5-kHz carrier is modulated into 4-syllable chirps, repeated 2–4 times per second; the syllable rate within each chirp is near 30 Hz. Surprisingly, however, the majority of females that are ‘good trackers’ of calling song also track pure ‘trill’ — continuous 30-Hz trains of syllables having no chirp structure — for many minutes. Trill having identical sound power but the wrong syllable rate is not tracked.3.The ratio of syllable duration to syllable repetition interval — that is, the ‘duty cycle’, which is near 50% in nature — can be increased to as much as ca. 90% (intersyllable pauses as brief as 4–5 ms) without degrading tracking performance, as long as syllable repetition rate is near 30 Hz. Similarly, very short duty cycles — in the extreme case songs with syllables consisting of 200-μs ‘clicks’ — can elicit tracking of the sound source by the female.4.Fine details of the temporal structure of the syllables evidently do not convey information in our conditions, because (i)G. campestris females track both the maleG. campestris and the somewhat similar maleG. bimaculatus calling song, and (ii) tracking ofcampestris calling song is indistinguishable from tracking of the same song played backward.5.All the above results are compatible with the view that repetitive modulation near 30 Hz is the chief — and in some cases both necessary and sufficient — parameter of songs that trigger the neuronal ‘recognition’ of male song. Properties of alternative candidate mechanisms for such a process are described.6.As one test that may distinguish among such mechanisms, the range of syllable rates over which recognition is elicited is measured by a paradigm that keeps chirp duration, chirp rate and chirp energy approximately constant. At 80 dB, tracking is observed reliably in the range 20–40 Hz, whereas syllable rates below 15 Hz and above 50 Hz are largely rejected. Multiple-peak structure within this response spectrum, predicted by certain of the recognition mechanisms considered, is — if present — not resolved by our methods.7.Variation of the song parameter ‘carrier frequency’ to values above the natural ca. 5 kHz results in a striking phenomenon at high sound intensities. Maintained ‘tracking’ is observed, but at characteristic, erroneous angles with respect to the sound source. To compare this ‘anomalous phonotaxis’ with the negative phonotaxis reported in other gryllids during flight, we repeat Moiseff et al.s (1978) ‘one-eared circling’ experiments on the Kramer treadmill, in three species of gryllids. InTeleogryllus, walking shows parallels to flight (reversal of one-eared circling in comparisons of 5 and 15 kHz) with respect to the carrier-frequency dependence of phonotaxis. WalkingGryllus andTeleogryllus evidently differ in this respect;Gryllus rarely exhibits negative phonotaxis (by one-ear criteria) at frequencies eliciting anomalous phonotaxis.Finally, we show that simple pressure-gradient effects associated with the ipsilateral spiracular pathways could in principle account for the directional hearing observed inGryllus, and that the same formulation predicts anomalous directions of tracking, qualitatively like those measured, at elevated carrier frequencies. Such trial explanations evidently require drastic modification, however, if they are to account for the behavioral effects of blocking single tympanal and spiracular inputs.

Auditory behavior of the cricket. III: Tracking of male calling song by surgically and developmentally one-eared females, and the curious role of the anterior tympanum

Summary1.Many one-eared female crickets (Gryllus campestris andGryllus bimaculatus), whether the loss is due to surgery or to developmental accident, can maintain characteristic, stable courses with respect to the direction of male calling song, when tested on the Kramer spherical tread-mill. The error angles are usually less than 90°, so that Regens (1924) remark about the success of such females in finding singing males is supported.2.Some females with developmental unilateral hearing deficit, confirmed both histologically and by sparing of tracking after removal of the suspect leg, track nearly as accurately as normal animals with two ears.3.Experiments in which tympana were immobilized with wax, whether tracking behavior or interneuron responses were monitored, show that the anterior tympanum — considered for some time to be irrelevant to hearing — mediates appreciable sound input to the auditory receptors, at least when the posterior tympana are blocked.4.The above results resolve two current paradoxes regarding comparison of tympanum immobilization in behavior with the mechanics of receptor excitation:First, because even unambiguously one-eared animals can maintain stable sound-oriented courses, such tracking performance with waxed tympana does not argue that total tympanal immobilization spares some auditory function of that ear (cf. Schmitz et al. 1983). The argument assumes that tracking would not be expected if one ear were silenced; the assumption is evidently false.Second, it has been unclear why waxing of both posterior tympana raises tracking threshold only ca. 20 dB (Schmitz 1983) whereas the tympanalmechanics studies of Kleindienst et al. (1983) have suggested a much greater deficit. Our finding that one must wax the anterior tympana as well, in order to produce deficit greater than ca. 20 dB, clarifies the situation. That is, in the biophysical experiments both tympana of the leg were immobilized by the procedures used (pressure matching and water immersion), whereas in most current behavioral tympanum-waxing experiments (but not in those of Bailey and Thomson 1977) the anterior tympana have been ignored.5.A novel behavioral effect was observed with all four tympana blocked. Thresholds for orientation were ca. 90–100 dB, but in every case the animals tended to walk away from the loudspeaker.6.The search for an explanation of one-eared tracking leads us to analogies with the recovery from imbalance following such surgery as hemilabyrinthectomy in vertebrates. A ‘phantom tympanum’, on the side with deficit, could in principle participate in corrective tracking, by the usual notions of bilateral comparison.

Auditory behavior of the cricket. I: Dynamics of compensated walking and discrimination paradigms on the Kramer treadmill

Summary1.In applying the recently developed methods of compensated walking to the study of cricket phonotaxis, we have first asked how such devices alter the dynamic body-substrate situation from that experienced in natural walking on a fixed substrate. Because a quantitative treatment has not been available, we derive certain general mechanical requirements of such compensation systems, and show in this context just what the Kramer treadmill accomplishes.2.Mathematical predictions of the above analysis were confirmed by frame-by-frame TV analysis of crickets during natural walking and compensated walking on the Kramer treadmill. These are as follows. Body-substrate inertial effects can be made to resemble those occurring during fixed-substrate walking as long as the animal walks continuously and the compensation is highly damped. During starts and stops, however, body-substrate acceleration, and hence the associated leg forces, differ severely from those experienced in walking on a fixed substrate.3.Despite the above effects, the presence of some bearing noise, and the elimination of all visual guidance, we show that a useful form of ‘blind auditory tracking’ can be obtained regularly. Loudspeakers playing the male calling song are accurately tracked by females, with meandering of direction about the target direction, via several characteristic modes of start-stop behavior. The tracking mode adopted at any instant can depend upon song attractiveness, song intensity, the history of stimuli presented, the individual, and factors unknown to us. The mode adopted also affects the nature of the meandering seen in the direction record.4.Depending upon the season and the source of the crickets, one-quarter to one-half of adult females older than 3 to 4 weeks turn out to be ‘good trackers’ in our conditions, and to remain so for some weeks. Sound intensity has little effect upon tracking accuracy in the range 70–90 dB, as long as the song is an attractive one.5.We have developed experimental paradigms which test for discrimination by the female between male calling song and various ‘wrong songs’. These employ two alternating loudspeakers to control against directional clues available from the apparatus, and allow comparison of response to different songs both sequentially and simultaneously (the choice situation). We show that in both kinds of presentation females can clearly and reproducibly discriminate between calling song and wrong songs having no syllable structure or the wrong syllable repetition rate.6.If during the tracking of calling song the song is turned off, the female stops within a few seconds. If, instead, one replaces the calling song suddenly with a wrong song (rejected when presented alone), the wrong song is ‘tracked’ for 10 to 20 s or more. These effects have implications regarding operational definitions of ‘motivation’ and ‘context setting’; they may also lead to ways of distinguishing between the recognition and tracking processes.7.Contrary to expectation based on earlier work withGryllus campestris, we find that increasing the number of syllables per chirp in the range 4–8 (with repetition interval 30 ms) increases, rather than decreases, attractiveness of the song in both our sequential and our choice tests.8.The finding that attractiveness of a song increases with number of syllables suggests that inGryllus the key feature of sound signals that elicit ‘recognition and pursuit’ may be modulation power near 30 Hz, associated with the syllable repetition rate.This hypothesis predicts that natural ‘rivalry song’ (with chirps of 20 or more syllables near the 30-Hz rate) ought to be very attractive; we find that it is, and suggest a reinterpretation of its role in nature.9.In a separate set of experiments, the callingsong sound was gated by the walking-velocity signal so that sound could be heard either (i) only during walking or (ii) only during stops. Only our two best trackers succeeded in our tracking tests if sound was presented strictly during walking; 8 good trackers failed. With sound available only during stops, many succeeded if they happened to employ a suitable tracking mode. Our impression is that ‘stopping to listen’ (or even to look) is ordinarily a significant part of the search behavior.

Filtering of temporal parameters of the calling song by cricket females of two closely related species: a behavioral analysis

Abstract The phonotactic response of cricket females was investigated on a locomotion compensator to determine the temporal parameters of the males calling song which are important for species recognition. Two sympatric species (Teleogryllus commodus, T. oceanicus) that show different syllable periods in the chirp and trill parts of their calling songs were used. By their responses T. commodus females exhibited two temporal filters for syllable periods, which were tuned to the species-specific syllable periods occurring during chirp and trill. For song recognition both filters had to be activated and for both a minimum number of three to five consecutive syllable periods was necessary. In contrast, T. oceanicus females showed only one sharply tuned filter corresponding to the chirp part of the males calling song. This filter was sufficient for calling song recognition. Syllable periods of the trill part also influenced calling song recognition, but these played only a minor role. Carrier frequency was also important for positive phonotaxis. Calling song recognition by T. commodus females is largely based on central nervous processing, while for T. oceanicus both peripheral frequency filtering and central temporal filtering is important.

Frequency and temporal pattern-dependent phonotaxis of crickets (Teleogryllus oceanicus) during tethered flight and compensated walking

SummaryPhonotactic responses ofTeleogryllus oceanicus were studied with two methods. Tethered crickets were stimulated with sound while they performed stationary flight, and steering responses were indicated by abdominal movements. Walking crickets tracked a sound source while their translational movements were compensated by a spherical treadmill, and their walking direction and velocity were recorded.During both flight and walking, crickets attempted to locomote towards the sound source when a song model with 5 kHz carrier frequency was broadcast (positive phonotactic response) and away from the source when a song model with 33 kHz carrier frequency was used (negative phonotactic response) (Figs. 2, 4).One-eared crickets attempted, while flying, to steer towards the side of the remaining ear when stimulated with the 5 kHz model, and away from that side in response to the 33 kHz model (Fig. 3). While walking, one-eared crickets circled towards and away from the intact side in response to the 5 kHz and 33 kHz models, respectively (Fig. 6).Positive and negative responses differed in their temporal pattern requirements. Phonotactic responses were not elicited when a non-calling song pattern (2 pulses/s) was played with a carrier frequency appropriate for positive phonotactic responses (5 kHz), but this pattern did elicit negative responses with 33 kHz carrier frequency (Figs. 7–10). When an intermediate carrier frequency, 15 kHz, was used, the response type (positive or negative) depended on the stimulus temporal pattern; the calling song pattern elicited primarily positive responses, while the non-calling song pattern elicited negative responses (Figs. 11, 12, 14, 15). A curious phenomenon was often observed in the flight steering responses; while most responses to 15 kHz song pattern were primarily positive, they often had an initial negative component which was supplanted by the positive component of the response after approximately 2–5 s (Figs. 11, 12).In recent experiments onGryllus campestris, Thorson et al. (1982) described frequency-dependent errors in phonotactic direction (anomalous phonotaxis) and showed how such errors might arise from the frequency-dependent directional properties of the crickets auditory apparatus. Our findings, particularly the dependence of response type on temporal pattern when 15 kHz carrier frequency was used, argue that frequency-dependent directional properties alone cannot account for positive and negative phonotaxis inT. oceanicus. Rather, these represent qualitatively different attempts to locomote towards and away from the sound source, respectively.We discuss the possibility that central integration of these opposing tendencies might contribute to anomalous phonotaxis.

SELECTIVE PHONOTAXIS IN TETTIGONIA CANTANS AND T. VIRIDISSIMA IN SONG RECOGNITION AND DISCRIMINATION

Abstract The selectivity of female phonotaxis in Tettigonia cantans and T. viridissima was investigated on a Kramer treadmill, with respect to the specific differences in temporal pattern and spectrum of the songs of both species. In choice situations, both species preferred the conspecific song over the heterospecific one. The courses of both species were deflected by about 15–20° from the position of the conspecific song, that of T. viridissima being away from, that of T. cantans in the direction of the heterospecific song. In no-choice situations, song models with the temporal pattern of T. cantans did not attract T. viridissima. Models with the conspecific time pattern but heterospecific spectrum were as attractive as the conspecific model. In contrast, T. cantans was attracted by T. viridissima song presented alone. In choice situations, either spectral or temporal differences were sufficient for discrimination. The preference for the conspecific model gradually disappeared with stepwise reduction of its intensity and was reversed at −12 dB. Acoustic communication alone can serve species isolation in T. viridissima; however, premating isolation in T. cantans must involve other mechanisms. The orientation during the choice situations suggests a serial processing of song recognition and localization for the Tettigonia species.

The effect of mating on phonotactic behaviour in Gryllus bimaculatus (De Geer)

Abstract. Phonotaxis of G. bimaculatus females is expressed by a course‐consistent, directional approach to a conspecific model calling song emitted alternatingly at sound intensities of 50–90 dB SPL and appears at the age of 6–7 days, the onset of maturation. Mating abolishes phonotaxis after about 1 h. By that time, the content of the attached spermatophore has migrated into the females sper‐matheca. Removal or emptying of the spermatheca, or severing the ventral nerve cord, fully reinstates phonotaxis, whereas ovariectomy has no effect. We suggest that mechanoreceptors record the expansion of the filled spermatheca and that the inhibitory message is communicated via the ventral nerve cord anteriorly to an unknown control centre in the brain. The loss of phonotaxis is combined with reduced locomotor activity and results in the female no longer being attracted to another calling male.

Thermistor telemetry of ventilation during prey capture by dragonfly larvae (Cordulegaster boltoni, Odonata)

Summary1.A technique was developed for using a thermistor to record the ventilation of freely movingCordulegaster boltoni larvae.2.The thermistor recordings show that the ventilation is slow and regular during the resting phase of the circadian cycle and changes in a characteristic way during the various phases of hunting and food consumption.3.The larvae respond to visual stimuli by interrupting ventilation. Thus this technique can be used as a better measure of distance and time at which a larva detects a stimulus than visual observation. By this measure,Cordulegaster larvae can detect prey objects at a distance of 10–15 cm and an illuminance of 5–10 Lux. To be effective, such stimuli must move at angular velocities of 10°/s or more; otherwise they are ignored.4.Application of this method extends the range of measurable behaviour of freely moving aquatic insects. In particular, it allows one to establish conditions under whichCordulegaster larvae detect prey even before they respond with a visible movement.

Phonotactic response of female crickets on the Kramer treadmill: methodology, sensory and behavioural implications

Since population-level variation in female mating preferences can shape intraspecific communication systems within the context of sexual selection it is essential to quantify these preferences and their sources of variation. We calculated individual female response functions for four male calling song traits in the field cricket Gryllus bimaculatus, by performing untethered phonotaxis measurements on a spherical locomotor compensator (Kramer treadmill). Firstly, we quantify the population-level sources of phonotactic variation and correct for factors that adversely affect this measurement. Secondly, we develop methodology for the characterisation of individual female phonotactic response functions suitable for population-level analyses and demonstrate the applicability of our method with respect to recent literature on Orthopteran acoustic communication. Phonotaxis towards a preferred stimulus on different occasions is highly repeatable, with lower repeatabilities away from the most preferred signal traits. For certain male signal traits, female preference and selectivity are highly repeatable. Although phonotactic response magnitude deteriorated with age, preference functions of females remained the same during their lifetimes. Finally, the limitations of measuring phonotaxis using a spherical locomotor compensator are described and discussed with respect to the estimation of the selectivity of female response.

Interneurons descending from the cricket cephalic ganglia that discharge in the pattern of two motor rhythms

Summary1.When male field crickets (Gryllus campestris L.) sing, abdominal respiration is usually synchronized with the chirps of the calling song. These experiments were designed to find a neuronal correlate of this synchronization.Animals with freely moving wings and abdomen are caused to produce normal song by brain lesions, during which the activity of single fibers in the cervical connectives is recorded extracellularly together with the myograms of the wing muscles and the expiratory abdominal flank muscles.2.In each of three animals a descending neuronal spike pattern was found (I, II, III, respectively) in which bursts of impulses alternate with the chirps and the corresponding abdominal ventilatory activity (AVA). In silent males the bursts alternate with the AVAs and other abdominal movements.3.The beginning of the neuronal burst is correlated with the end of the preceding chirp, no matter how long it is, and the end is correlated with the onset of the following chirp. The relationship to the chirp-coupled AVA is less clear-cut.4.The muscle potentials in the chirp-coupled AVA are grouped so as to resemble the syllable pattern (animal I). Between these groups increasing numbers of neuronal impulses appear toward the end of the chirp. When the chirp is shifted with respect to the AVA, the spikes continue to follow the syllable rhythm.5.A relation between Pattern I and the AVA becomes evident in the case of AVAs lasting through two chirps. The neuron fires more rarely during such AVAs than it does between AVAs coupled to a single chirp.6.In silent males the neuronal burst both ends and begins later with respect to the AVA, and the discharge rate is lower.7.After transection of all nervous connections to thorax and abdomen Patterns I and II are irreversibly altered. That is, the correlation of the neuronal pattern with the motor patterns must require ascending inputs from these regions. During singing these inputs would have to be correlated primarily with the rhythm of stridulation, whereas in the silent phase they would be correlated with the activity rhythm of the abdominal dorsoventral muscles alone.