Box 4.1. Aural location of host by a parasitoid fly
Parasitoid insects track down hosts, upon which their immature development depends, using predominantly chemical and visual cues (section 13.1). Locating a host from afar by orientation towards a sound that is specific for that host is rather unusual behavior. Although close-up low-frequency air movements produced by prospective hosts can be detected, for example by fleas and some blood-feeding flies (section 4.1.3), host location by distant sound is developed best in flies of the tribe Ormiini (Diptera: Tachinidae). The hosts are male crickets, for example of the genus Gryllus, and katydids, whose mate-attracting songs (chirps) range in frequency from 2 to 7 kHz. Under the cover of darkness, the female Ormia locates the calling host insect, on or near which she deposits first-instar larvae (larviposits). The larvae burrow into the host, in which they develop by eating selected tissues for 7–10 days, after which the third-instar larvae emerge from the dying host and pupariate in the ground.
Location of a calling host is a complex matter compared with simply detecting its presence by hearing the call, as will be understood by anyone who has tried to trace a calling cricket or katydid. Directional hearing is a prerequisite to orientate towards and localize the source of the sound. In most animals with directional hearing, the two receptors (“ears”) are separated by a distance greater than the wavelength of the sound, such that the differences (e.g. in intensity and timing) between the sounds received by each “ear” are large enough to be detected and converted by the receptor and nervous system. However, in small animals, such as the house fly-sized ormiine female, with a hearing system spanning less than 1.5 mm, the “ears” are too close together to create interaural differences in intensity and timing. A very different approach to sound detection is required.
As in other hearing insects, the reception system contains a flexible tympanal membrane, an air sac apposed to the tympanum, and a chordotonal organ linked to the tympanum (section 4.1.3). Uniquely amongst hearing insects, the ormiine paired tympanal membranes are located on the prosternum, ventral to the neck (cervix), facing forwards and somewhat obscured by the head (as illustrated here in the side view of a female fly of Ormia). On the inner surface of these thin (1 mm) membranes are attached a pair of auditory sense organs, the bulbae acusticae (BA) — chordotonal organs comprising many scolopidia (section 4.1.3). The bulbae are located within an unpartitioned prosternal chamber, which is enlarged by relocation of the anterior musculature and connected to the external environment by tracheae. A sagittal view of this hearing organ is shown above to the right of the fly (after Robert et al. 1994). The structures are sexually dimorphic, with strongest development in the host-seeking female.
What is anatomically unique amongst hearing animals, including all other insects studied, is that there is no separation of the “ears” — the auditory chamber that contains the sensory organs is undivided. Furthermore, the tympani virtually abut, such that the difference in arrival time of sound at each ear is < 1 to 2 microseconds. The answer to the physical dilemma is revealed by close examination, which shows that the two tympani actually are joined by a cuticular structure that functions to connect the ears. This mechanical intra-aural coupling involves the connecting cuticle acting as a flexible lever that pivots about a fulcrum and functions to increase the time lag between the nearer- to-noise (ipsilateral) tympanum and the further-from-noise (contralateral) tympanum by about 20-fold. The ipsilateral tympanic membrane is first to be excited to vibrate by incoming sound, slightly before the contralateral one, with the connecting cuticle then commencing to vibrate. In a complex manner involving some damping and cancellation of vibrations, the ipsilateral tympanum produces most vibrations.
This magnification of interaural differences allows very sensitive directionality in sound reception. Such a novel design discovered in ormiine hearing suggests applications in human hearing-aid technology.