Evolution

Tympanal ears have evolved independently at least 20 times within the class Insecta, and this number surely underestimates the number of ears that do exist. Still, hearing appears to be the exception, not the rule, for insects, with only 7 of the 25 recognized extant neopteran orders having tympanate species. The Orthoptera (crickets, grasshoppers, and katydids) and the Lepidoptera (moths and butterflies) boast the largest number of eared species. In two of the most speciose orders, the Diptera (flies and mosquitos) and the Coleoptera (beetles), tympanal ears are rare, and surprisingly, the Hymenoptera (wasps, ants, and bees) are completely atympanate as far as we know. Following is a brief introduction to the major taxonomic groups for which tympanal ears have been identified to date.

Orthoptera

Orthopteran ears come in two different forms and are divided nicely by the taxonomy of the order. The Acridoidea (locusts, grasshoppers) have ears on either side of the first abdominal segment. The tympanal membranes are nearly circular, opaque, and clearly visible upon inspection with the naked eye. Tracheal sacs connect both ears, allowing the locust to determine the direction of a sound source. The acridid ear is one of the few insect ears known to have the capability of pitch discrimination. About 60 to 80 scolopidia form four separate groups that attach to different regions of the eardrum, which, in turn, resonate to different sound frequencies. The ears of extant acridids function primarily in conspecific communication, but comparative evidence suggests that the primitive function was for predator detection.

In the suborder Ensifera [crickets (Gryllidae), katydids (Tettigoniidae)] the ears occur just below the "knee" region, on the tibia of the forelegs. Each leg has two eardrums—one on each side of the leg (Fig. 3). The tympanal membranes are connected to other sound input sources (the spiracles, contralateral ear) via a system of tracheal tubes and air chambers, which play important roles in directional hearing. The ensiferan auditory chordotonal organ (crista acoustica) has typically between 60 and 80 sense cells arranged in a linear array down the leg, connecting indirectly to the tympanal membrane by tracheal air sacs. Like the acridid ear, the ensiferan ear is capable of pitch discrimination. Presumably, the function of hearing in primitive Ensifera was conspecific communication, which remains the primary function in extant species. Some species are sensitive to ultrasound and use their ears to detect bats in addition to communicating with conspecifics. Fossil records demonstrate that the ancestors of modern Ensifera, which predate the appearance of bats by at least 100 million years, had ears on their legs and therefore, ultrasonic hearing for defense against bats seems to have evolved secondarily.

Lepidoptera

Tympanal ears have evolved more times within the Lepidoptera than any other insect order. To date, at least seven ears of independent origins have been described. Ears are located in the mouthparts (Sphingoidea), at the base of the forewings (butterflies: Hedyloidea, Nymphalidae), in the thorax (Noctuoidea), or on anterior abdominal segments (Tineoidea, Pyraloidea, Drepanoidea, Geometroidea, Uraniidae). Moth ears are among the simplest of all insect ears in that they have very few auditory sensory cells (one, two, or four). K. D. Roeder first demonstrated that the primary function of hearing in moths is to detect the ultrasonic echolocation cries of insectivorous bats. Despite their simplicity, moth ears are capable of determining the distance and direction of an approaching bat. Flying moths evade bats by either turning away from a distant bat or engaging in evasive and erratic flight maneuvers to avoid a sudden and unexpected attack. W. E. Conner has shown that some species, including many day-flying tiger moths (Arctiidae), use their hearing in social interactions. In most Arctiidae, ultrasound production functions to either jam a bat's echolocation calls or warn the bat of a distasteful meal (aposomatic display), but in those species that use sounds for social interactions, both hearing and sound production have secondarily taken on different roles.

FIGURE 4 Nocturnal butterflies of the superfamily Hedyloidea possess ultrasound-sensitive ears on their wings that mediate evasive flight maneuvers to avoid bats. (A) A male Macrosoma heliconiaria (Hedylidae). (B) Lateral view of M. heliconiaria, showing the general location of the right ear. An arrow points down the canal toward the tympanic cavity where the tympanic membrane resides. Scale bar, 3 mm. (C) Scanning electron micrograph of the right tympanal ear. The hind wing and a dense fringe of scales have been removed to reveal the tympanic cavity. Ca, canal; Cj, conjuctiva. Scale bar, 110 jlm. (D) Consecutive video images (30 frames/s) of a free-flying M. heliconiaria responding to a short (~250 ms), high-frequency (25 kHz), high intensity (>100 dB) sound. The direction of flight is marked with an arrow and the stimulus onset with an arrowhead. (E) Scanning electron micrograph of the two most proximal chordotonal organs (arrows), viewed from inside the tympanic chamber. The largest organ attaches to the proximal border of the tympanal frame (black arrow). TM, tympanic membrane. Scale bar, 50 jlm. (A and E courtesy of J. Yack. B—D were modified, with permission, from J. E. Yack and J. H. Fullard, 2000, Ultrasonic hearing in nocturnal butterflies. Nature 403, 265-266.)

Hearing in butterflies has only begun to be explored. The hedylid butterflies of the neotropics, unusual because of their nocturnal habits, have ultra-sound-sensitive ears on their wings that function as bat detectors (Fig. 4). Some diurnal butterflies of the family Nymphalidae possess ear-like structures on their wings, and there is evidence that the "cracker" butterfly (Hamadryas feronia) uses its ears for conspecific communication. No doubt there will be further examples of butterfly hearing in the near future, since tympanal-like structures have been described anatomically in many species.

Homoptera and Heteroptera

Most people are familiar with the loud "buzzing" sounds of cicadas (Cicadidae) during hot weather; these are typically males calling to females. Cicada ears are located within cavities on the ventral side of the second abdominal segment. They are among the largest of all insect ears, with over 1000 scolopidia in each ear. It has been suggested that the large number of sense cells enhances the ear's sensitivity for long distance communication, but cicadas do not appear to have more sensitive hearing organs than other insects with far fewer scolopidia.

Water bugs (subfamily Hydrocorisae) are reported to have ears on various body parts, including the mesothorax, metathorax, or first abdominal segment. The best known is the ear of the water boatman, Corixa (Corixidae), which occurs on the lateral mesothorax between the wing and the leg. The ears, like those of moths, are simple, with only two auditory cells, both tuned to low-frequency sounds (1-2 kHz), within the range of conspe-cific calls. The insect carries a bubble of water with it to allow the membrane to vibrate under water. Unlike for most other insect ears, the tympanal membrane is backed by fluid, not air. Hearing in corixids appears to function primarily for mate attraction.

Diptera

Although it had been well documented that certain parasitic flies were attracted to the songs of crickets, katydids, and cicadas, until recently, it was not known how these flies were eavesdropping on their hosts. Two families of parasitoid flies (Sarcophagidae and Tachinidae) have independently evolved a pair of peculiar ears on their prosternum, just below the head, in the "neck" region (Fig. 5). The gravid females use their ears to locate singing insect hosts upon which to lay their predaceous larvae. The ears of the two parasitoid groups are described earlier in this article. The design features of these dipteran ears show remarkable convergence in anatomy and function, despite the fact that tachinids and sarcophagids are only distantly related. This suggests that evolutionary and developmental constraints are at work here in ways that we do not yet understand.

Mantodea

Until recently, praying mantids were thought to be deaf; now we know that 65% of all mantid species can hear. The ears

FIGURE 5 The prothoracic tympanal ear of a parasitoid tachinid fly, Ormia ochracea (Tachinidae). (A) A female fly resting on its host (Gryllus integer). (B) A light micrograph of the prosternal ear in a female. The outline of the tympanal membrane is indicated with arrows. (Photographs provided courtesy of D. Robert, R. Hoy, and G. Haldimann.)

FIGURE 5 The prothoracic tympanal ear of a parasitoid tachinid fly, Ormia ochracea (Tachinidae). (A) A female fly resting on its host (Gryllus integer). (B) A light micrograph of the prosternal ear in a female. The outline of the tympanal membrane is indicated with arrows. (Photographs provided courtesy of D. Robert, R. Hoy, and G. Haldimann.)

occur in the most bizarre location: the two tympanal membranes face one another inside a narrow groove between the metathoracic legs. The mantid ear is functionally an "auditory cyclops" because the close proximity of the ear drums (less than 150 |lm) provides no directional information to the animal. The ears function as bat detectors and are most sensitive between 25 and 50 kHz.

Coleoptera

Tympanal ears have been described in two beetle families to date. Several species of the genus Cicindela (Cicindelidae) have ears on the dorsal surface of the first abdominal segment, beneath the wings. Some scarabs (two tribes in the subfamily Dynastinae) have ears located just beneath the neck membranes (pronotal shield). The ears of both families are tuned to ultrasonic frequencies, and there is strong evidence that they function as bat detectors. It is a little bit surprising that there are not more examples of hearing in beetles. Given the large number of species, the wide diversity of niches worldwide, and numerous reports of sound production, we expect that more examples will be uncovered.

Neuroptera

Green lacewings (Chrysopidae) have an ear near the base of each forewing in a location similar to that of the ears of some butterflies. The ear consists of a swelling of the radial vein, with a region of very thin cuticle on the ventral side that functions as a tympanal membrane. Like the corixid ear, the tympanal chamber is predominantly fluid filled. The ears respond to sounds between 40 and 60 kHz and are sufficiently sensitive to detect echolocating bats at close distances.

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