Box 41 Aural location of host by a parasitoid fly

Visual Organ Insects

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.

pair of acoustic spiracles. In many katydids, the tibial base has two separated longitudinal slits each of which leads into a tympanic chamber (Fig. 4.4b). The acoustic trachea, which lies centrally in the leg, is divided in half at this point by a membrane, such that one half closely connects with the anterior and the other half with the posterior tympanal membrane. The primary route of sound to the tympanal organ is usually from the acoustic spiracle and along the acoustic trachea to the tibia. The change in cross-sectional area from the enlargement of the trachea behind each spiracle (sometimes called a tracheal vesicle) to the tympanal organ in the tibia approximates the function of a horn and amplifies the sound. Although the slits of the tympanic chambers do allow the entry of sound, their exact function is debatable. They may allow directional hearing, because very small differences in the time of arrival of sound waves at the tympanum can be detected by pressure differences across the membrane.

Whatever the major route of sound entry to the tym-panal organs, air- and substrate-borne acoustic signals cause the tympanal membranes to vibrate. Vibrations are sensed by three chordotonal organs: the subgen-ual organ, the intermediate organ, and the crista acustica (Fig. 4.4c). The subgenual organs, which have a form and function like those of non-orthopteroid insects, are present on all legs but the crista acustica and intermediate organs are found only on the fore legs in conjunction with the tympana. This implies that the tibial hearing organ is a serial homologue of the pro-prioceptor units of the mid and hind legs.

The crista acustica consists of a row of up to 60 scolopidial cells attached to the acoustic trachea and is the main sensory organ for airborne sound in the 5 -50 kHz range. The intermediate organ, which consists of 10-20 scolopidial cells, is posterior to the subgenual organ and virtually continuous with the crista acustica. The role of the intermediate organ is uncertain but it may respond to airborne sound of frequencies from 2 to 14 kHz. Each of the three chordotonal organs is innervated separately, but the neuronal connections between the three imply that signals from the different receptors are integrated.

Hearing insects can identify the direction of a point source of sound, but exactly how they do so varies between taxa. Localization of sound directionality clearly depends upon detection of differences in the sound received by one tympanum relative to another, or in some orthopterans by a tympanum within a single leg. Sound reception varies with the orientation of the body relative to the sound source, allowing some precision in locating the source. The unusual means of sound reception and sensitivity of detection of direction of sound source shown by ormiine flies is discussed in Box 4.1.

Night activity is common, as shown by the abundance and diversity of insects attracted to artificial light, especially at the ultraviolet end of the spectrum, and on moonless nights. Night flight allows avoidance of visual-hunting predators, but exposes the insect to specialist nocturnal predators - the insectivorous bats (Microchiroptera). These bats employ a biological sonar system using ultrasonic frequencies that range (according to species) from 20 to 200 kHz for navigating and for detecting and locating prey, predominantly flying insects.

Although bat predation on insects occurs in the darkness of night and high above a human observer, it is evident that a range of insect taxa can detect bat ultrasounds and take appropriate evasive action. The behavioral response to ultrasound, called the acoustic startle response, involves very rapid and co-ordinated muscle contractions. This leads to reactions such as "freezing", unpredictable deviation in flight, or rapid cessation of flight and plummeting towards the ground. Instigation of these reactions, which assist in escape from predation, obviously requires that the insect hears the ultrasound produced by the bat. Physiological experiments show that within a few milliseconds of the emission of such a sound the response takes place, which would precede the detection of the prey by a bat.

To date, insects belonging to five orders have been shown to be able to detect and respond to ultrasound: lacewings (Neuroptera), beetles (Coleoptera), praying mantids (Mantodea), moths (Lepidoptera), and locusts, katydids, and crickets (Orthoptera). Tympanal organs occur in different sites amongst these insects, showing that ultrasound reception has several independent origins amongst these insects. As seen earlier in this chapter (p. 90), the Orthoptera are major acoustic communicators that use sound in intraspecific sexual signaling. Evidently, hearing ability arose early in orthopteran evolution, probably at least some 200 mya, long before bats evolved (perhaps a little before the Eocene (50 mya) from which the oldest fossil comes). Thus, orthopteran ability to hear bat ultrasounds can be seen as an exaptation - a morphological-physiological predisposition that has been modified to add sensitivity to ultrasound. The crickets, bush-crickets, and acridid grasshoppers that communicate intraspecifically and also hear ultrasound have sensitivity to high- and low-frequency sound - and perhaps limit their discrimination to only two discrete frequencies. The ultrasound elicits aversion; the other (under suitable conditions) elicits attraction.

In contrast, the tympanal hearing that has arisen independently in several other insects appears to be receptive specifically to ultrasound. The two receptors of a "hearing" noctuoid moth, though differing in threshold, are tuned to the same ultrasonic frequency, and it has been demonstrated experimentally that the moths show behavioral (startle) and physiological (neural) response to bat sonic frequencies. In the parasitic tachinid fly Ormia (Box 4.1), in which the female fly locates its orthopteran host by tracking its mating calls, the structure and function of the "ear" is sexually dimorphic. The tympanic area of the female fly is larger, and is sensitive to the 5 kHz frequency of the cricket host and also to the 20-60 kHz ultrasounds made by insectivorous bats, whereas the smaller tympanic area of the male fly responds only to the ultrasound. This suggests that the acoustic response originally was present in both sexes and was used to detect and avoid bats, with sensitivity to cricket calls a later modification in the female sex alone.

At least in these cases, and probably in other groups in which tympanal hearing is limited in taxonomic range and complexity, ultrasound reception appears to have coevolved with the sonic production of the bats that seek to eat them.

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