Vibrational communication is widespread in insect social and ecological interactions. Of the insect species that communicate using sound, water surface ripples, or substrate vibrations, we estimate that 92% use substrate vibrations alone or with other forms of mechanical signaling. Vibrational signals differ dramatically from airborne insect sounds, often having low frequencies, pure tones, and combinations of contrasting acoustic elements. Plants are the most widely used substrate for transmitting vibrational signals. Plant species can vary in their signal transmission properties, and thus host plant use may influence signal divergence. Vibrational communication occurs in a complex environment containing noise from wind and rain, the signals of multiple individuals and species, and vibration-sensitive predators and parasitoids. We anticipate that many new examples and functions of vibrational communication will be discovered, and that study of this modality will continue to provide important insights into insect social behavior, ecology, and evolution.

https://www.jstor.org/stable/10.1641/0006-3568(2005)055[0323:TBEOIV]2.0.CO;2

The Behavioral Ecology of Insect Vibrational Communication

Publisher Summary Chordotonal organs are generally found in Insecta and Crustacea. In insects, chordotonal organs occur in great morphological diversity, and are found at nearly every exoskeletal joint and between joints within limb and body segments. Morphologically, a chordotonal organ is a cluster of sensilla connected to movable parts of skeletal cuticle or to the tracheal system, or sometimes inserting into a connective tissue strand. It is noted within some chordotonal organs, neurons are clustered into one or two groups, termed scoloparia that can be morphologically separated from each other. Chordotonal organs are not normally associated with external cuticular structures, such as hairs, bristles, or campaniform sensilla. The chapter describes the histological methods, diversity in distribution, structure and function, ultrastructure, mechanics of the scolopidium, physiological responses of chordotonal organs, processing of information and development of chordotonal organs, and evolution and homology. Combining the technologies of neurophysiology with those of genetics, electron microscopy, membrane biochemistry, and biophysics can elucidate the mechanisms that provide chordotonal sensilla with their different physiological properties.

Chordotonal Organs of Insects

1.

The responses of fifty-eight neurons in the cricket brain to auditory stimuli were studied by intracellular recording, after which the cells were marked with Lucifer Yellow. These auditory interneurons could be assigned to three classes on the basis of anatomical criteria: (i) neurons (AN1 and AN2) ascending from the prothoracic ganglion into the brain, (ii) brain neurons (BNC 1) with arborizations overlapping those of ascending cells, and (iii) brain neurons (BNC 2) with arborizations that had no overlap with those of ascending cells.




2.

All the ascending neurons had one projection field in common, an area in the anterior dorsal region of the diffuse neuropil lateral to the alphalobe. This field overlaps one of the projection fields of the BNC 1 neurons. Other projection fields of the BNC 1 neurons are frequently found in the posterior ventral region, at the boundary between the proto and deutocerebrum; the latter overlap projection fields of the BNC 2 cells, the arborizations of which are often not clearly distributed in more than one distinct region (Figs. 1–4).




3.

The threshold curves and suprathreshold responses revealed that all three classes (AN, BNC 1 and BNC 2) include cells with low frequency (5 kHz) and others with broad-band (2–20 kHz) tuning; high-frequency (10–20 kHz) tuning was found only in AN and BNC 1 cells. Within the region to which the cells were tuned, sensitivity decreased in the order AN, BNC 1, BNC 2 (Figs. 2–4). A frequently observed property of BNC 2 neurons was independence of sound intensity in the suprathreshold intensity region. The response latency increased in the order AN, BNC 1, BNC 2 (Figs. 5, 6).




4.

The effect of stimulus temporal structure was studied by presenting ‘constant-energy-chirps’, trains of sound pulses (syllables) varying in duration and repetition interval. The low frequency AN1 neurons, like other prothoracic neurons, copy such signals over a broad range of repetition intervals. Copying by the BNC 1 neurons was less accurate, and the responses of BNC 2 neurons were often not detectably synchronized with the syllables of the stimuli (Figs. 7–10).




5.

Strikingly, the magnitude of the BNC 2 responses was in some cases (7 out of 15) found to vary with repetition interval; curves for the BNC 2 responses vs. repetition interval match closely those for the behavioral tracking response of females given an identical stimulus paradigm, and are independent of intensity at intensities 10 dB or more above threshold. By contrast, the responses of AN and most BNC 1 neurons are uniform, regardless of stimulus intensity, over the entire range of repetition intervals studied (Fig. 11).




6.

Some BNC 2 neurons responded to constantenergy chirps only with short and intermediate or with intermediate and long repetition intervals, resembling the high-pass and low-pass neurons found in frogs (Fig. 12). This finding, the systematic latency differences, and the anatomical relationships among the AN, BNC 1 and BNC 2 cells all point to a rather specific picture of the way that the male calling song is recognized.

Temporal selectivity of identified auditory neurons in the cricket brain

The vibrational songs of several species of cydnid bugs and ‘small cicadas’ (leafhoppers and planthoppers) living on various types of plants are recorded by means of laser vibrometry. The recorded vibrational songs are analysed with respect to amplitude, frequency spectrum and structure in the time domain (Figs. 2–5). The emission of vibrational songs from singing insects on plants is simulated. A small magnet is glued to the surface of the plant and moved by means of an electromagnet about one cm away (Fig. 1). The vibrations are recorded by means of laser vibrometry. The propagation velocity of the vibrations increases with the square root of frequency, i.e. in the way expected for bending waves. The mechanical properties of plants ranging from soft bean plants to stiff reeds and maples are measured. The results are used for calculating the theoretical propagation velocities of bending waves. The measured and the calculated values are rather close (Table 1). Although the mechanical properties of the plants studied vary widely, the propagation velocities at a certain frequency are of the same order of magnitude (Table 1). In all the plants studied, only little vibrational energy is lost by friction at frequencies below some kHz. Communication by means of bending waves is possible over distances of some meters. The bending waves are reflected with little loss of energy both from the root and from the top of the plant. The vibration signals may therefore travel up and down the plant several times before decaying completely (Fig. 7). The vibration at a certain spot on the plant depends not only on the distance to and nature of the emitter, but also on the modes of vibration of the plant. The amplitude of vibration does not decrease monotonically with distance from the emitter (Fig. 6). These filtering properties of the plants mean that it is essentially impossible to predict which frequencies in the signals will be amplified or attenuated in the plant at the location of the receiving animal. The vibrational signals recorded from the animals cover wide frequency bandwidths. The signals are therefore well adapted to the filtering properties of the plants, but the signals of the species studied here do not appear to be particularly adapted to specific properties of the host plants. The muscular power needed for communication by means of various types of vibrational signals is calculated. The result of this calculation supports the conclusion that the signals recorded here are carried by means of bending waves. The communication strategies open to small insects are considered. Vibrational signals appear to be an efficient means of communication, but only certain types of signals are suited, because the plants cause a considerable distortion of the signals. One kind of distortion, the dispersive property, may — in theory — be used by the listening animals to obtain information about the direction and distance to the singing animals.

Plants as transmission channels for insect vibrational songs

Insects are capable of detecting a broad range of acoustic signals transmitted through air, water, or solids. Auditory sensory organs are morphologically diverse with respect to their body location, accessory structures, and number of sensilla, but remarkably uniform in that most are innervated by chordotonal organs. Chordotonal organs are structurally complex Type I mechanoreceptors that are distributed throughout the insect body and function to detect a wide range of mechanical stimuli, from gross motor movements to air-borne sounds. At present, little is known about how chordotonal organs in general function to convert mechanical stimuli to nerve impulses, and our limited understanding of this process represents one of the major challenges to the study of insect auditory systems today. This report reviews the literature on chordotonal organs innervating insect ears, with the broad intention of uncovering some common structural specializations of peripheral auditory systems, and identifying new avenues for research. A general overview of chordotonal organ ultrastructure is presented, followed by a summary of the current theories on mechanical coupling and transduction in monodynal, mononematic, Type 1 scolopidia, which characteristically innervate insect ears. Auditory organs of different insect taxa are reviewed, focusing primarily on tympanal organs, and with some consideration to Johnston's and subgenual organs. It is widely accepted that insect hearing organs evolved from pre-existing proprioceptive chordotonal organs. In addition to certain non-neural adaptations for hearing, such as tracheal expansion and cuticular thinning, the chordotonal organs themselves may have intrinsic specializations for sound reception and transduction, and these are discussed. In the future, an integrated approach, using traditional anatomical and physiological techniques in combination with new methodologies in immunohistochemistry, genetics, and biophysics, will assist in refining hypotheses on how chordotonal organs function, and, ultimately, lead to new insights into the peripheral mechanisms underlying hearing in insects.

The structure and function of auditory chordotonal organs in insects.

The acoustic behaviour of the bushcricket Tettigonia cantans II. Transmission of airborne-sound and vibration signals in the biotope.

Neurophysiology of the vibration sense in locusts and bushcrickets: Response characteristics of single receptor units

In grasshoppers, the auditory and vibrational senses converge on the same ventral-cord neurons. All neurons in the ventral cord that discharge impulses in response to either airborne-sound or vibration stimuli also receive synaptic inputs from the other sensory system. The latter elicit either subthreshold excitation or inhibition. The coding of the conspecific song in the responses of most ventral-cord neurons ofTettigonia cantans is considerably improved when the stimulus consists not of simulated natural sounds alone, but of such sounds together with either maintained vibration or vibration matched to the temporal structure of the song. Stridulating tettigoniids produce both airborne and substrate-conducted sound. Thus the perception of airborne sound and vibration, and their simultaneous processing in individual ventral-cord neurons, may be of fundamental importance — not only in localizing a nearby sound source, but also in facilitating the recognition of conspecific signals.

The coding of airborne-sound and vibration signals in bimodal ventral-cord neurons of the grasshopper Tettigonia cantans

ABSTRACT. Analysis of the ultrasonic content of the calling songs of two tettigoniids, Decticus verrucivorus L. and Tettigonia cantans Fuessly, showed that the major secondary energy peaks in the ultrasonic range are only about 15–20 dB below the main audible frequency peaks. The song of the acridid, Locusta migratoria L., contains no appreciable secondary peaks at ultrasonic frequencies, Bifunctional acoustic‐vibratory interneurones are present in the ventral nerve cord of all three species. They are divided into three categories, according to their response characteristics: VS (vibration and sound), S (sound) and V (vibration) neurones. All the unit‐types capable of coding sound signals in the ventral cord (VS and S neurones) are sensitive to frequencies of up to 100 kHz, with one exception (S3). In tettigoniids, three of these unit‐types are more sensitive at ultrasonic frequencies than they are at the audible frequencies of their conspecific songs. Among the vibratory neurones (V), one unit‐type receives inhibitory inputs from ultrasonic acoustic primary receptors. The possible importance of ultrasonic perception in the natural environment is briefly discussed.

The responses of central acoustic and vibratory interneurones in bushcrickets and locusts to ultrasonic stimulation

1.

A new type of ascending interneurone (AN3) responding to airborne sound has been characterised morphologically and physiologically in the prothoracic ganglion of the cricketGryllus campestris (Fig. 1).




2.

The structure of AN3 is generally similar to that of two ascending neurons described previously (AN1, AN2).




3.

AN3 is highly tuned and very sensitive (threshold at CF, 30–35 dB SPL; Q10=3) to the calling song frequency. The tuning is enhanced by inhibitory sidebands on both the low and high frequency side (tuned to 3 kHz and 16 kHz respectively; Fig. 1).




4.

The other two AN types also show two-tone suppression effects which generally act so as to enhance the contrast of the response to the best frequency (Fig. 3–5). In contrast to AN3 and AN1, AN2 shows a great variability in its responses to low frequency sounds.




5.

AN3 and AN1 respond preferentially to the conspecific calling and aggression songs, supplementing each other in the intensity domain. AN2 responds only unspecifically to the calling and aggression songs but strongly to courtship syllables (Fig. 6).




6.

Stimulation with artificial song models reveals that the song specificity of AN3 and AN2 is due mainly to the frequency content of the songs. In AN2, an additional influence from the temporal structure becomes apparent (Fig. 6).

Roland Kühne

Papers

The acoustic behaviour of the bushcricket Tettigonia cantans II. Transmission of airborne-sound and vibration signals in the biotope.

Neurophysiology of the vibration sense in locusts and bushcrickets: Response characteristics of single receptor units

The coding of airborne-sound and vibration signals in bimodal ventral-cord neurons of the grasshopper Tettigonia cantans

The responses of central acoustic and vibratory interneurones in bushcrickets and locusts to ultrasonic stimulation

Two-tone suppression and song coding by ascending neurones in the cricketGryllus campestris L.