Tympanal Hearing Research Articles

A tympanal hearing organ in scarab beetles.

We describe the paired hearing organ of the scarab beetle Euetheola humilis. The auditory structures of the beetle are typical of other insect ears in that they have a thinned tympanic membrane backed by a tracheal airsac with associated chordotonal sensory structures. The tympanic membranes of the beetle are part of its cervical membrane and are located behind the head, where the cervix attaches dorsally and laterally to the pronotum. Each membrane is approximately 3 microns thick. The chordotonal sensory organ, which lies within the tracheal airsac, contains 3-8 scolopidia that attach by accessory cells directly to the tympanic membrane. Neurophysiological recordings from the neck connective of the beetle revealed that the auditory system is sensitive to frequencies between 20 and 80 kHz and has a minimum threshold of approximately 58 dB at 45 kHz. The neurophysiological audiogram is identical to the behavioral audiogram for a head roll, one behavioral component of the beetle's startle response elicited by ultrasound. Blocking experiments show that the membranous structures on the cervix are indeed the hearing organs. Neurophysiologically determined thresholds increased by more than 35 dB when drops of water covered the tympanic membranes and were essentially restored to the control level when the water was later removed. At least three other genera of Dynastinae scarabs have similar tympanum-like structures located in their cervical membranes. Behavioral and neurophysiological data show that the frequency tuning of species in two of these genera, Cyclocephala and Dyscinetus, is nearly identical to that of E. humilis. Our discovery represents only the second group of beetles known to respond to airborne sounds. However, the hearing organs of these scarab beetles differ in structure and placement from those of the tiger beetles, and thus they represent an independent evolution of auditory organs in the Coleoptera.

Nymphal development of the auditory system in the praying mantis Hierodula membranacea Burmeister (Dictyoptera, Mantidae).

Like other praying mantises, Hierodula membranacea has a single midline ear on the ventral surface of the metathorax. The ear comprises a deep groove with two tympana forming the walls. A tympanal organ on each side contains 30-40 scolopophorous sensillae with axons that terminate in the metathoracic ganglion in neuropil that does not match the auditory neuropil of other insects. Nymphal development of the mantis ear proceeds in three major stages: 1) The tympanal organ is completely formed with a full complement of sensillae before hatching; 2) the infolding and rotations that form the deep groove are completed primarily over the first half of nymphal development; and 3) over the last five instars (of ten), the tympana thicken and broaden to their adult size and shape, and the impedance-matching tracheal sacs also enlarge and move to become tightly apposed to the inner surfaces of the tympana. Auditory sensitivity gradually increases beginning with the fifth instar and closely parallels tympanum and tracheal sac growth. Late instar nymphs have auditory thresholds of 70-80 dB sound pressure level (SPL). Appropriate connections of afferents to a functional interneuronal system are clearly present by the eighth instar and possibly much earlier. The pattern of auditory system ontogeny in the mantis is similar to that in locusts and in noctuid moths, but it differs from crickets. In evolutionary terms, it is significant that the metathoracic anatomy of newly hatched mantis nymphs matches very closely the anatomy of the homologous regions in adult cockroaches, which are closely related to mantises but are without tympanal hearing, and in mantises that are thought to be primitively deaf.

Tympanal Hearing in Insects

Tympanal Hearing in Insects

Tympanal hearing in insects.

Specialized hearing organs, known as tympanal organs, have evolved in at least seven different orders of insects. Tympanal organs are usually defined by the presence of a tympanal membrane (or eardrum). They are backed by an air-filled space or cavity and are innervated by a chordotonal sensory organ. In some insects, however, a recognizable tympanal membrane may not be easily identified by visual inspection, yet may possess tympanal hearing organs. In insects that possess them, tympanal hearing organs may mediate the detection of predators, prey, and potential mates and rivals. Unlike the ears of vertebrates, which are localized to cranial segments, the ears of insects may be found in a bewildering variety of locations on their bodies, depending on the species. The embryological and evolutionary origins of tympanal organs are related to ancestral states as proprioceptive chordotonal organs.

The tympanal hearing organ of a fly: phylogenetic analysis of its morphological origins

A key adaptation for any parasitoid insect is the sensory modality that it uses to locate its host insect. All members of the speciose family Tachinidae (Diptera) are parasitoids, but only flies of the tribe Ormiini use acoustic cues to find their hosts. Ormiine flies are parasitoids of various genera of crickets and katydids. Gravid females of one ormiine species, Ormia ochracea, hear the reproductive calling song of male field crickets and home in on those calls to locate their hosts. While many flies possess various kinds of "ears" to detect airborne sounds, only ormiine flies have been reported to possess true tympanal hearing organs. Such organs are well-known to occur in their cricket and katydid hosts. The ormiine ear is an evolutionary innovation within Diptera. Our objective was to trace the phylogenetic origins of the tympanal hearing organ among higher flies. Since the ormiine hearing organ is a complex organ within the prothorax, we examined possible precursor structures in the prothoraces of selected Diptera. We have uncovered a suite of characters that define the ormiine ear. These characters in the prothorax include a pair of prosternal tympanal membranes, a pair of chordotonal sensory organs, and modifications of the tracheal system. We have been able to identify and trace the presumptive homologs of these ormiine characters through selected species of related Diptera, using the method of outgroup comparison.

The tympanal hearing organ of a fly: phylogenetic analysis of its morphological origins

The tympanal hearing organ of a fly: phylogenetic analysis of its morphological origins

The tympanal hearing organ of the parasitoid fly Ormia ochracea (Diptera, Tachinidae, Ormiini)

Tympanate hearing has evolved in at least 6 different orders of insects, but had not been reported until recently in the Diptera. This study presents a newly discovered tympanal hearing organ, in the parasitoid tachinid fly, Ormia ochracea. The hearing organ is described in terms of external and internal morphology, cellular organization of the sensory organ and preliminary neuroanatomy of the primary auditory afferents. The ear is located on the frontal face of the prothorax, directly behind the head capsule. Conspicuously visible are a pair of thin cuticular membranes specialized for audition, the prosternal tympanal membranes. Directly attached to these membranes, within the enlarged prosternal chamber, are a pair of auditory sensory organs, the bulbae acusticae. These sensory organs are unique among all auditory organs known so far because both are contained within an unpartitioned acoustic chamber. The prosternal chamber is connected to the outside by a pair of tracheae. The cellular anatomy of the fly's scolopophorous organ was investigated by light and electron microscopy. The bulba acustica is a typical chordotonal organ and it contains approximately 70 receptor cells. It is similar to other insect sensory organs associated with tympanal ears. The similarity of the cellular organization and tympanal morphology of the ormiine ear to the ears of other tympanate insects suggests that there are potent constraints in the design features of tympanal hearing organs, which must function to detect high frequency auditory signals over long distances. Each sensory organ is innervated by a branch of the frontal nerve of the fused thoracic ganglia. The primary auditory afferents project to each of the pro-, meso-, and metathoracic neuropils. The fly's hearing organ is sexually dimorphic, whereby the tympanal membranes are larger in females and the spiracles larger in males. The dimorphism presumably reflects differences in the acoustic behavior in the two sexes.

Acoustically cued countermeasures taken by insects in response to predatory bats that hunt with biosonar

Insectivorous bats detect and hunt down their prey by means of ultrasonic biosonar signals and some insects have evolved ultrasound-sensitive ears to detect bats and to take evasive action. This has been known since the early 1960s, largely due to the pioneering work of K. D. Roeder, who documented the interactions between bats and moths, that hear ultrasound. Since then, studies of the auditory behavior of insects have revealed that ultrasound hearing has evolved in at least five orders of nocturnally active, flying insects and it is suspected that it serves to detect the biosonar signals of bats. In spite of the taxonomic diversity (unrelatedness) of these insects, all insects that hear ultrasound have evolved a tympanal hearing organ with particular and characteristic ‘‘design features’’ in their structure and function. When some of these insects are stimulated with ultrasound during tethered flight, they exhibit short latency startle responses that appear to be escape behavior, ranging from directional steering to cessation of wingbeat. It is clear that the predatory relationship between bats and their insect prey has resulted in the evolution of evasive behavior in insects, made possible by the evolution of a hearing organ sensitive to ultrasound.

A novel hearing organ in an acoustic parasitoid fly

Female parasitoid flies (Ormiaochracea: Tachinidae) are attracted to singing male crickets [W. Cade, Science 190, 1312 (1975)]. Gravid female flies orient to calling crickets to deposit larvae, which burrow into the cricket in order to feed and grow to adulthood. To detect and locate cricket songs over long distances, these flies evolved a tympanal hearing organ previously unkown in flies. Electrophysiological recordings reveal low auditory thresholds (20 dB SPL between 4–6 kHz) matching the peak of the power spectrum of the host’s song (Gryllusrubens, 4.5–5 kHz). Such sensitivity is consistent with long distance hearing. The ear, composed of two adjacent thin tympanal membranes, contains two mechanoreceptive sensory organs that are both located in a single air-filled chamber. Laser vibrometry suggests that this tympanal arrangement provides a novel mechanism for directional sound reception. Some aspects of its vibratory behavior in a sound field will be reported. [Work funded by NINDCD-DC00103 and Hatch NYC-191403.]