Figure 12-7. Natural diversity in bat head morphology, as artistically rendered by Ernst Haeckel in his Art Forms in Nature (available in reprint as Haeckel 1899).

middle ear and then the inner ear, where the sound waves are transduced from mechanical energy into electrical energy and transmitted to the brain for interpretation. However, a feature specific to echolocating bats is that the portion of the basilar membrane in the cochlea that receives sonar sound frequencies is especially sensitive and spiral ganglion cells of the brain that receive these frequencies are overrepresented relative to others.

That said, this exquisite ability to detect prey with echolocation may outrank the bat's ability to actually capture the prey once it has been detected. One study found that only about 40 percent of attempts by red bats are successful on the first try (Obrist and Wenstrup 1998). This is in part because many of the moths and other insects that bats prey upon can hear the sounds that bats emit in their echolocation calls, and in fact their hearing is most sensitive to the frequencies emitted by their most common predator and so can initiate evasive maneuvers while the bat is still fairly distant. Thus, although we think of bats as having a rather refined and exotic sensory capability (perhaps because we do not have it and hence romanticize it), echolocation is, like other systems, imperfect and highly variable among bat species, especially when the responses of moths and other prey have kept pace. If it were not so, there would be no prey—and no echolocating bats.

Hearing in Arthropods

Hearing in insects—the detection of air- or substrate-borne vibration—is used for detecting predators and for signaling to and locating mates. The mechanoreception of air- or water-borne vibration is found in seven of 27 orders of insects (Hoy et al. 1998). However, many more insects produce vibration through the branch or leaf upon which they perch by knocking against it with a leg or other body part and detect it coming from the same source with their hearing organ. Insects with body lengths less than 1 cm are generally restricted to ultrasound emissions, which are useful only at short range or in free space. Ultrasound is distorted and attenuated by most habitats; thus small insects that rely on ultrasound probably do not use sound for social communication but to detect prey or predators. Larger insects can emit sounds above about 1 kHz (Michelsen 1992), which can penetrate vegetation. Most insects that use hearing for social communication have frequency analyzers, whereas those that use it only to detect prey or predators do not seem able to detect frequency.

Interestingly, despite the bat problem, not all Lepidoptera (moths and butterflies) are able to detect sound, and the ability of those that can is highly variable, both in range and in the complexity of the actual hearing apparatus itself and its location on the body, which can be anywhere from the wings to abdomen to thorax to legs to head. Some nocturnal butterflies have "ears" on their wings that are sensitive to ultrasound (Yack and Fullard 2000); some moths hear with their mouthparts (Gopfert and Wasserthal 1999), but in all moths that can hear, the ear is tympanal and specialized to the frequency of bat ultrasonic emissions.

Insect mechanosensory organs are classified as type I or type II (Eberl et al. 2000). Type I organs have bipolar neurons with an axon extending to the CNS and a dendrite on the opposite end (see Figure 12-1). These organs are surrounded by specialized supporting cells. Type II organ cells are single multidendritic neurons with no obvious ciliary structure. Most insect sensory organs are type I (Eberl, Hardy et al. 2000).

The insects that are able to detect airborne sound have either tympanal organs, which as noted above can be almost anywhere on the body (thorax, abdomen, sternum, legs, wings, antennae), or flagellar organs. Which type of organ an insect has determines how far afield the sound it detects comes from. Tympanal organs are sound pressure detectors and as such are for detecting sound from far away. Near a sound source, on the other hand, most sound energy may be detected particle movement, and flagellar organs, which are protruding structures such as hair or antennae that function as particle velocity detectors are sufficient (Eberl 1999).

An insect's body is covered with a hard protective coating called the cuticle. Poking through at many spots are sensory bristles. These are of various types and are regularly spaced along the body, perhaps produced by reaction-diffusion types of patterning mechanisms (see, e.g., Gerhart and Kirschner 1997). Each appears to develop from a single precursor cell, and the different types of final structure are determined by combinatorial expression of numerous transcription factors (TFs) and activation-inhibition signaling not yet understood.

One of the bristle types is a sensillum known as a chordotonal organ (sometimes referred to as a stretch receptor), shown in Figure 12-8. Chordotonal organs can be specialized to perform various functions including stretch reception (of the outer chitinous shell) and a related sense of hearing. Tympanal chordotonal organs are internal structures that span two cuticle plates, where there is a thinning of the cuticle, a thin membrane that covers an air-filled sac. A four-cell structure senses

Insect Tympanal Organ

Chordotonal Organ scolopale cap tympanum scolopale cell

Insect Tympanal Organ

Chordotonal Organ scolopale cap tympanum

attachment cell scolopale cell cilium scolopale rods ciliary root

Figure 12-8. Basic structure of insect chordotonal organs. Redrawn from (Gray 1960) with permission.

attachment cell scolopale cell cilium scolopale rods ciliary root

Figure 12-8. Basic structure of insect chordotonal organs. Redrawn from (Gray 1960) with permission.

vibratory movement at this location and is innervated by a single neuron. The sensory organ is sometimes called the scolopidial organ, in reference to the spindlelike sheaf of ciliary origin, the scolopale cell, into which the dendrite of the nerve cell extends. The scolopale cells and the neuron are associated with glial and support cells. These are located at basically fixed sites in a given species. Auditory chordo-tonal neurons project to similar sites in the CNS but what happens when the signal reaches the CNS varies among insect species, as acoustic information is extracted from the sensory input in a way specific to the sounds relevant to each insect. Although there is a wide variety of "acoustomechanical transformers" among insects, the way the mechanical signal is converted to electrochemical response in the nervous system is quite consistent across taxa (Eberl 1999).

Some of the genetics of chordotonal organs in Drosophila is known. The tympa-nal chordotonal organs are similar to the vertebrate inner ear (Eatock and Newsome 1999; Fritzsch and Beisel 2001). Both have ciliated mechanoreceptive cells and accessory or supporting cells. Homologous genes and mechanisms are involved in the development of mechanosensors in both insect chordotonal organs and vertebrate inner ears (Eberl 1999), and all ciliated mechanoreceptors share a common transduction system (Kernan and Zuker 1995).

A neurogenic TF, Atonal, is expressed early in embryonic development in all chordotonal organ progenitor cells (this gene is also expressed in photoreceptors). In Atonal mutants, all chordotonal organs are absent except for one scolopidium in the abdominal linear array of five pentascolopidial organs called Ich5 (Lage et al. 1997). Other genes are known to be required, including Egf receptor signaling in precursor cells in most but not all of the eight scolopidia in each abdominal segment. Detailed studies have been done of specific gene expression in these developing organs, which essentially have to do with their patterning, number, and location.

Although most insect auditory organs are chordotonal, some also use other means of detecting air vibration. Insects such as cockroaches and crickets have, either in addition or alone, specialized bristle organs on their cercae, or antennalike sensory appendages projecting from their tails, that are deflected by wind currents and can be very sensitive to sound (Eberl 1999). Bees have flagellar antennae on their heads that are thought to decipher the acoustic components of the waggle dance that is used for communicating the location of pollen sources and to detect song within the hive. Drosophila discriminate species-specific courtship songs at close range with their Johnston's organ, a collection of chordotonal organs in the antennae.

Crickets and cicadas call for mates over long distances by stridulation, the rubbing of ridged surfaces on their legs or wing margins, and detect sound with tympanal organs located on their front legs. Cricket songs also attract parasites (Ormiine tachinid flies, which have sternal tympanal ears for directional hearing to locate their hosts). In a defensive mechanism referred to earlier, some moths use their tympa-nal organs to detect the ultrasonic echolocating calls of predatory bats and respond by altering their flight patterns. Indeed, other arthropods have an even more diverse repertoire of sound-making and sensing devices. Lobsters have ridged surfaces called plectra on the base of their antennae that they rub against a file organ to generate sound. This seems to be for warning off predators, because the lobsters do not appear to use this for mating or defensive reactions.

Lateral Line

All the primarily aquatic vertebrates, cyclostomes (agnaths), fish and amphibians, have hair cells in the "touch organs," or mechanosensors, in their outer skin. This organ is the lateral line, and it is sensitive to minute water displacements from vibration as well as changes in pressure, caused both by the fish itself and by other nearby animals or fish, and so is used for various behaviors including finding prey and escaping approaching predators, social behavior such as schooling, shoaling, and avoidance of stationary objects, and hearing, among others.

The morphology of a particular lateral line system determines just what an animal is going to detect—the spatial distribution of the lateral line's mechanore-ceptive organs, the neuromasts, determines the receptive field of a particular animal, the innervation patterns determine how sensitive the system will be, and the morphology of the neuromasts themselves determines which aspect of water movement the organ will respond to, velocity or acceleration (Maruska and Tricas 1998).

The lateral line and the labyrinth arise from the same embryonic placode. Together, they comprise the acousticolateralis system. The mechanoreceptors of the lateral line, the neuromasts, contain hair cell clusters embedded in the cupula. The organ has two kinds of sensory receptors; the superficial neuromasts on the skin and canal neuromasts recessed in fluid-filled canals beneath the skin. Superficial neuro-masts detect the motion of water flow, and canal neuromasts detect its acceleration. Superficial neuromasts predominate in still water fish and canal neuromasts in fish that live in moving water (Engelmann et al. 2000).

Water enters the lateral line organ through numerous pores on the surface of the skin and flows past the neuromasts. Pressure of the water bends the cupula, and this creates an action potential in the hair cells. (See Figure 16-2.)

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