sound reception

Introduction

      response of an organism's aural mechanism, the ear, to a specific form of energy change, or sound waves. Sound waves can be transmitted through gases, liquids, or solids, but the hearing function of each species is particularly (though not exclusively) sensitive to stimuli from one medium.

      If an animal possessing an auditory mechanism comes in suitable contact with a medium vibrating (vibration) at a frequency and intensity within its range of aural (hearing) sensitivity, it may hear the sound. For land animals, the usual vibrating medium is the air; for fishes and other aquatic creatures, it commonly is the water. Yet, under suitable conditions, all hearing animals can perceive sound waves transmitted by media other than the one in which they live; thus, humans can hear noise while underwater. (Additional information is contained in the article sound (acoustics).)

      In the course of evolution, animals have developed a variety of sense organs that respond to mechanical stimuli. There are at least 10 of these mechanoreceptors in vertebrates and perhaps as many in advanced invertebrates. Not all of these structures respond to sound, however, for among them are the simple touch endings of the skin and the motion receptors that serve (mediate) bodily equilibrium. Although the different ways of registering mechanical changes in the environment or within the body represent various structural specializations, it is not feasible to identify any one of them simply in terms of its structure; many different mechanisms, cells, or organs (organ) may perform similar functions. Ears, for example, take many forms in the lower animals and often have little resemblance to these organs in man and other higher vertebrates. Yet the service that they perform in sound reception is similar enough that they may be called ears.

      Although there is no fossil record of the origin and development of auditory structures, in animals with ears the evolutionary process in every instance appears to have been a conversion to an auditory function of structures that previously mediated a simpler form of mechanoreception. Indeed, any mechanoreceptor, even though best adapted to respond to some other form of mechanical stimulation, will respond to vibrations within some region of the sound frequency range if the vibrations have a sufficiently high level of intensity.

      Many attempts have been made to define hearing, often with indifferent success. The task is difficult, and in certain respects the lines of distinction are arbitrary. The ear cannot be identified by any standard structure, nor can it be identified in terms of the stimulus as simply a receiver of sound vibrations. As noted above, mechanical receptor organs will respond to sound vibrations within some region of the frequency range if a sufficiently high level of intensity is provided. Moreover, the ear cannot be characterized in terms of the physical principles by which it operates because these principles vary among the ears of different animal species.

      A definition of hearing, therefore, must be sought in terms of the ear's specialization of function and the relative effectiveness with which it performs this function. Thus, hearing may be characterized as the reception of sound vibrations by an organ, the ear, that has developed for this particular purpose and that has reception of sound as its primary function. This definition excludes the reception of sound vibrations by touch (tactual) endings in the skin, for example, because these structures respond most readily to direct pressure. Before such receptors will respond to sound waves, the vibrational intensity of the sound must be relatively great. Also excluded are the hair sensilla, of which arthropods have many types, whenever it can be shown that these organs respond with greater sensitivity to another stimulus (most often a simple direct deflection of the central hair).

      Theoretically, several aspects of vibration might serve in its detection by an ear. These characteristics include the amplitude (extent) of the motion of particles (e.g., molecules) in a medium, the velocity and acceleration of the motion, the pressure exerted upon an obstacle in the path of the sound waves, and temperature changes occasioned by the vibrations. All of these manifestations have been utilized in attempts to design microphones (microphone) for the detection and measurement of sound, but only two (pressure and velocity effects) have proved to be of any practical value. Thus, those devices that employ these two effects are known as pressure and velocity microphones.

      It seems more than coincidence that these same two aspects of sound, pressure and velocity, are the only stimulus characteristics on which the evolution of ears appears to have been based. Moreover, just as the pressure microphone is the most practical type designed by man, among ears the pressure type is the most widespread and the most highly developed. Ears that distinguish changes in velocity have appeared only in a few lower animals—as an elaborated hair organ in some insects and perhaps spiders and in two special forms among fishes. All other ears are pressure receptors that have taken two lines of evolutionary development, one in most of the insects and another in vertebrates above fishes.

      Considering the usefulness of the sense of hearing to such highly organized animals as man, it may seem surprising that this sense is so limited in its appearance and development among animals. It is found only in two major groups of animals: arthropods (e.g., insects and crabs) and vertebrates (e.g., amphibians, birds, and mammals). The condition that probably limited the development of hearing in other species was the lack of sufficient advancement and flexibility of the nervous system.

      In those animals (animal communication) with auditory structures, hearing serves purposes of great biological value: in its more primitive forms, it is used to sense danger and enemies, to detect prey, and to identify prospective mates; at a more complex level, hearing is involved in communication within social groups and in emotional expressions of various kinds. The cry (sound production) of an infant mouse that has strayed from the nest elicits a response by the mother to retrieve it. The singing of a male thrush asserts a claim to its territory, attracts a female to the area, and warns off other males. Among higher mammals (e.g., monkeys and apes) vocalizations show even greater variety and express a range of meanings that may be interpreted in human terms as expressions of such concepts as danger, aggression, love, and the availability of food. In man, the elaborations of auditory communication can be even more symbolically complex, extending to speech and music (see speech (phonetics)). The significant features in complicated sounds that people perceive and differentiate correspond to the physical dimensions of frequency (the number of waves, cycles, or vibrations per second), intensity, phase, complexity of wave form, and temporal pattern. The variety of distinguishable acoustic forms is enormous.

      Among the most highly refined applications of the auditory sense are those found in such animals as bats and dolphins. These creatures are able to discern objects around them by a process called echolocation; the animal sends out a cry and, by the nature of the echo, is informed of the presence of obstacles or potential prey. For these animals, the sense of hearing provides a service in the dark that closely approaches the reliability of vision in the perception of objects and spatial relations.

Organs of sound reception in invertebrates

      It has long been believed that at least some insects (insect) can hear. Chief attention has been given to those that make distinctive sounds (e.g., katydids (katydid), crickets (cricket), and cicadas (cicada)) because it was naturally assumed that these insects produce signals for communication purposes. Organs suitable for hearing have been found in insects at various locations on the thorax and abdomen and, in one group (mosquitoes), on the head.

      Among the many orders of insects, hearing is known to exist in only a few: Orthoptera (orthopteran) (crickets, grasshoppers, katydids), Homoptera (cicadas), Heteroptera (bugs), Lepidoptera (lepidopteran) (butterflies and moths), and Diptera (flies). In the Orthoptera, ears are present, and the ability to perceive sounds has been well established. The ears of katydids and crickets are found on the first walking legs; those of grasshoppers (grasshopper) are on the first segment of the abdomen. Cicadas are noted for the intensity of sound produced by some species and for the elaborate development of the ears, which are located on the first segment of the abdomen. The waterboatman (water boatman), a heteropteran, is a small aquatic insect with an ear on the first segment of the thorax. Moths (moth) have simple ears that are located in certain species on the posterior part of the thorax and in others on the first segment of the abdomen. Among the Diptera, only mosquitoes are known to possess ears; they are located on the head as a part of the antennae.

      All the insects just mentioned have a pair of organs for which there is good evidence of auditory function. Other structures of simpler form that often have been considered to be sound receptors occur widely within these insect groups as well as in others. There is strong evidence that some kind of hearing exists in two other insect orders: the Coleoptera (beetles) and the Hymenoptera (ants, bees, and wasps). In these orders, however, receptive organs have not yet been positively identified.

Types of insect auditory structures

      Four structures found in insects have been considered as possibly serving an auditory function: hair sensilla, antennae, cercal organs, and tympanal organs.

Hair sensilla

      Many specialized structures on the bodies of insects seem to have a sensory function. Among these are hair sensilla, each of which consists of a hair with a base portion containing a nerve supply. Because the hairs have been seen to vibrate in response to tones of certain frequencies, it has been suggested that they are sound receptors. It seems more likely, however, that the sensilla primarily mediate the sense of touch and that their response to sound waves is only incidental to that function.

Antennae (antenna) and antennal organs

      Many sensory functions have been attributed to the antennae of insects, and it is believed that they serve both as tactual and as smell receptors. In some species, the development of elaborate antennal plumes and brushlike terminations has led to the suggestion that they also serve for hearing. This suggestion is supported by positive evidence only in the case of the mosquito, especially the male, in which the base of the antenna is an expanded sac containing a large number of sensory units known as scolophores. These structures, found in many places in the bodies of insects, commonly occur across joints or body segments, where they probably serve as mechanoreceptors for movement. When the scolophores are associated with any structure that is set in motion by sound, however, the arrangement is that of a sound receptor.

      In the basic structure of the scolophore, four cells (base cell, ganglion cell, sheath cell, and terminal cell), together with an extracellular body called a cap, constitute a chain. Extending outward from the ganglion cell is the cilium, a hairlike projection that, because of its position, acts as a trigger in response to any relative motion between the two ends of the chain. The sheath cell with its scolopale provides support and protection for the delicate cilium. Two types of enclosing cells (fibrous cells and cells of Schwann) surround the ganglion and sheath cells. The ganglion cell has both a sensory and a neural function; it sends forth its own fibre (axon) that connects to the central nervous system.

      In the mosquito ear the scolophores are connected to the antenna and are stimulated by vibrations of the antennal shaft. Because the shaft vibrates in response to the oscillating air particles, this ear is of the velocity type. It is supposed that stimulation is greatest when the antenna is pointed toward the sound source, thereby enabling the insect to determine the direction of sounds. The male mosquito, sensitive only to the vibration frequencies of the hum made by the wings of the female in his own species, flies in the direction of the sound and finds the female for mating. For the male yellow fever mosquito, the most effective (i.e., apparently best heard) frequency has been found to be 384 hertz, or cycles per second, which is in the middle of the frequency range of the hum of females of this species. The antennae of insects other than the mosquito and its relatives probably do not serve a true auditory function.

Cercal organs

      The cercal organ, which is found at the posterior end of the abdomen in such insects as cockroaches and crickets, consists of a thick brush of several hundred fine hairs. When an electrode is placed on the nerve trunk of the organ, which has a rich nerve supply, a discharge of impulses can be detected when the brush is exposed to sound. Sensitivity extends over a fairly wide range of vibration frequencies, from below 100 to perhaps as high as 3,000 hertz. As observed in the cockroach, the responses to sound waves up to 400 hertz have the same frequency as that of the stimulus. Although the cercal organ is reported to be extremely sensitive, precise measurements remain to be carried out. It is possible, nevertheless, that this structure, which is another example of a velocity type of sound receptor, is primarily auditory in function.

Tympanal organs

      The tympanal organ of insects consists of a group of scolophores associated with a thin, horny (chitinous) membrane at the surface of the body, one on each side. Usually the scolophores are attached at one end by a spinous process to the tympanic membrane (eardrum); the other ends rest on an immobile part of the body structure. When the membrane moves back and forth in response to the alternating pressures of sound waves, the nerve fibre from the ganglion cell of the scolophore transmits impulses to the central nervous system. Because the tympanic membrane is activated by the pressure of sound waves, this is a pressure type of ear.

      Simple tympanal organs, such as those found in moths, contain only two or four elements, or scolophores. In cicadas, on the other hand, these organs are highly developed; they include a sensory body (a number of scolophores in a capsule) that may contain as many as 1,500 elements.

      With 80 to 100 scolophores, the grasshopper ear, which has been studied more thoroughly than any other insect ear, is structurally between that of moths and cicadas. Ordinarily, the tympanic membrane is hidden beneath the base of the insect's wing cover. A bundle of auditory nerve fibres runs from one side of the sensory body, which lies on the inner surface of the membrane, and joins other nerve fibres of the region to form a large nerve extending to a ganglion (nerve centre) in the thorax.

Evidence of hearing and communication in insects

Behavioral observations

      That the insect ear serves an auditory purpose has been proved by a large number of experimental observations, particularly those that have dealt most extensively with katydids and crickets. Males of these groups produce sounds by stridulation, which usually involves rubbing the covers of the wings (wing) together in a particular way. One wing has a serrated surface (a “file”) that runs along an enlarged vein; the other wing has a sharp edge over which the file is scraped. The scraping causes the wing surfaces to vibrate; the natural resonances of the vibrations and the particular rhythm and repetition rate of the scraping movements determine the nature of the song, which varies with each species. Most females are silent, but those of a few species have a poorly developed stridulatory apparatus, and weak sounds have been reported. Both males and females have tympanal organs for sound reception.

      The observation that the males of many insect species produce repeated stridulatory sounds during the mating season led to the inference that the primary purpose of these noises was to attract a female. That this is indeed the case was first established by the extensive observations of the Yugoslavian entomologist Ivan Regen, who worked over the period 1902–30 mostly with a few species of katydids and crickets. In one of his earliest experiments, Regen proved (1913–14) that a male katydid of the species Thamnotrizon apterus responds to the sound of another male by chirping. The first male responds in turn to the second male's chirp, and the two insects then set up an alternating pattern of chirping. Although this pattern had been observed earlier, Regen was the first to prove by a series of experiments that it depends upon the sense of hearing. After removing the forelegs, on which the tympanal organs are located, of certain males, he found that even though these insects continued to stridulate, they did so only in individual rhythms that were not affected by the sounds of other males. Any alternation of chirping between deafened males, or between a deafened and a normal male, occurred only rarely, for brief times, and by chance.

      A long series of check experiments by Regen showed that other stimuli, such as light, odours, and surface vibrations, did not affect the chirping behaviour. In these experiments the insects were placed in separate rooms, and their sounds were transmitted by telephone.

      Further experiments carried out by Regen on field crickets (Liogryllus campestris) demonstrated the reactions of females to chirping males. In the most elaborate of these experiments, 1,600 sexually receptive females were released around the periphery of a large enclosed area in the middle of which had been placed a cage containing one or more chirping males. Precise data concerning the frequency with which the females moved toward the cage were obtained by surrounding the cage site with an array of traps in which the females were caught as they moved inward. The results were statistically significant. Normal females (those with intact tympanal organs) moved toward the cage and eventually reached it. The removal of one foreleg and its tympanal organ, however, caused difficulty; the movements were more random and the approaches fewer, although some females did succeed in reaching the cage. When both tympanal organs were removed or if the male failed to chirp, the performance of the females was reduced to chance. They also failed to exhibit the seeking performances if the male's stridulatory organ was modified, as by removing the file, so that little or no sound was produced.

      In 1926 Regen returned to his study of the alternating chirping pattern of katydids and succeeded in having males react to an artificial sound, one that Regen himself produced. He also found that the alternation could be demonstrated with a suitably active male by using a variety of sounds—whistles, percussion noises, and sounds made with his mouth. It was never altogether clear, however, what changes Regen had made in his signals that finally brought success; probably the secret lay in the particular rhythm and timing of the signals. At any rate, this method made possible a study of the general nature of the auditory sensitivity of these insects and the range of sound frequencies to which they responded. It was shown that katydids are most sensitive to the very high frequencies, those that are beyond the limit of the human ear. The instruments available to Regen at the time, however, did not permit a precise measurement of intensity thresholds. (A threshold is the lowest point at which a particular stimulus will cause a response in an organism.)

      Although the work of Regen and others established the basic character of sound reception in insects and its role in communication and mating, other details had to await the introduction of electrophysiological methods in this field as well as the development of electronic methods for the precise production, control, and measurement of sound stimuli.

Electrophysiological observations

      When making electrophysiological observations of an auditory mechanism, an electrode (one terminal, generally a fine wire, in an electric circuit) is placed on a nerve or some other sensory structure in the mechanism. Sounds, presented at different frequencies and intensities, produce neural or sensory changes, which are actually electrical discharges or changes in electrical potential (action potential) of extremely small magnitude. The impulses are picked up by the electrode and transmitted to an instrument with which they can be amplified, observed, and recorded. In both behavioral and electrophysiological observations, the auditory sensitivity of an animal to sounds of different frequencies can be illustrated by a curve.

      The electrophysiological method was first used in research on the insect ear in 1933, with observations mainly on two katydid and one cricket species. The tympanal organ of these insects is located on one of the segments of the foreleg; its nerve goes to a ganglion in the thorax. When an electrode is placed on this nerve, its threshold sensitivity and overall frequency range can be determined by varying the intensity and frequency of the sounds applied to the tympanic membrane. It has been found that the tympanal organ of these insects responds poorly to low tones (those of low frequency) but improves rapidly as the frequency increases to a maximum sensitivity around 3,000 to 5,000 hertz. For higher frequencies the sensitivity declines, until a limit is reached at 30,000 hertz. It is likely that the insect's identification of its own species by means of song is primarily in terms of intensity and time patterns, with the rapid changes of intensity playing a prominent part. The possibility of frequency also entering into the pattern, however, cannot be ruled out.

      A further question concerns the perception of the direction of a sound source. Clearly, if a female is to seek out and find a chirping male, the effectiveness of her performance depends upon an ability to localize the sound. Experiments indicate that the magnitude of electric responses from the tympanal nerve in katydids varies in a systematic manner when a given sound is presented at different angles while the distance is held constant. The insects continue to exhibit this directional pattern even after one of the tympanal organs has been removed. As was mentioned earlier, Regen found that female crickets (cricket) deprived of one tympanal organ were still able to locate a chirping male, though less effectively than when both organs were intact.

Evidence of hearing and communication in spiders (spider)

      Whether spiders have a sense of hearing has long been debated. Early anecdotal observations concerning this matter have now been reinforced with both behavioral and electrophysiological evidence showing without doubt that spiders are sensitive to mechanical vibrations and also to aerial sounds. Whether this sensitivity should be regarded as hearing is considered later in this section, after a review of the anatomical and behavioral evidence.

Anatomical evidence

      The bodies of spiders contain many slitlike openings, called lyriform organs, that have been considered as sensory in nature. Most of these organs probably have a kinesthetic function and thus provide information on local movements of body parts. There is one type of lyriform organ, however, that differs from the others in its location and in certain structural details. It is found on the metatarsal (next to last) segment of each of the eight legs, close to the joint that this segment makes with the tarsus (the last segment, or foot), and consists of a number of slits—about 10 in the common house spider—that partially encircle the leg. Each slit contains a fluid chamber the inner wall of which is pierced by a tubule through which a thin filament runs to one of the two side walls (lamellae) that enclose the slit. This filament is evidently the termination of a ganglion cell that lies deeper in the leg. It has been suggested that an alternating compression of the lamellae stimulates the terminal filament.

      The responsiveness of the common house spider to aerial sounds and mechanical vibrations includes a wide range, from below 20 to as high as 45,000 hertz. Within this range the sensitivity, as measured by electrical potentials, varies widely for aerial sounds; in some experiments narrow regions of frequency have been found in which no responses could be obtained at the highest intensities available. These variations of sensitivity are ascribed to mechanical resonances in the lyriform structure.

      The tarsus evidently plays an important part in responses to sounds. Removal of portions of the tarsus reduces the responses about in proportion to the amount removed; immobilization of the tarsus greatly impairs the sensitivity. It appears, therefore, that the tarsus serves as a sensing element that transmits vibrations to the lyriform organ, which thus is a velocity type of ear.

Behavioral (feeding behaviour) evidence

      It has been reported that spiders react in characteristic ways to a buzzing insect caught in their web. The spider apparently locates the insect at once, runs to it, and attacks it. An inactive object, however, such as a small pebble enmeshed in the web, produces a different response: the spider manipulates the strands of the web, locates the object, and cuts away the filaments surrounding it so that the object drops to the ground. The reactions of a house spider to a mechanical vibrator applied to a point on the web have been observed. Such a stimulus elicits a response similar to that of an active insect if the vibratory frequency is between 400 and 700 hertz. For frequencies above 1,000 hertz, however, the spider reacts either by running to a secluded corner of the web or, if the intensity is too great, by abandoning the web altogether. From this and similar evidence it has been concluded that the spider has the ability of pitch (tone) discrimination between low and high ranges and perhaps can distinguish between tones of the lower range.

      Spiders also react to aerial tones from an artificial source, such as a loudspeaker. These stimuli elicit an orientation response, in which the spider faces the source and reaches out with the two front legs. Thus, in view of the high level of sensitivity to both aerial and mechanical stimuli, the reception of sounds in the spider can probably be regarded as true hearing, and the lyriform organ as a form of ear. It is evidently a velocity type of ear, for there is no tympanic surface to respond to sound pressures, and the small leg segments seem to respond to the oscillatory motions of the air particles.

Sound reception in vertebrates (vertebrate)— auditory mechanisms of fishes and amphibians

      The ear (inner ear) of vertebrates appears to have followed more than one line of evolutionary development, but always from the same basic type of mechanoreceptor, the labyrinth. All vertebrates have two labyrinths that lie deep in the side of the head, adjacent to the brain. They contain a number of sensory endings the primary functions of which are to regulate muscle tonus (a state of partial muscular contraction) and to determine the position and movements of the head and body.

 Generalized sketches of vertebrate labyrinths are shown in Figure 1—>, with the usual locations of the sensory endings indicated for the different vertebrate classes. Two main divisions of these endings are distinguished: a superior division, which includes the three semicircular canals, the organs associated with the sense of balance, and the utricle, a small sac into which the semicircular canals open; and an inferior division, which includes the saccule (also a small sac) and its derivatives. Arising at or near the connection between the utricle and the saccule is the endolymphatic duct, which ends in an endolymphatic sac; this structure probably regulates fluid pressures in the labyrinth and aids in the disposal of waste materials.

 The superior division of the labyrinth (Figure 1—>) is remarkably constant in form throughout the vertebrates except in the cyclostomes (e.g., hagfishes and lampreys), in which the canals and endings are reduced in number. The utricle contains a macular ending, the macula utriculi, and each semicircular canal ends in a crista. In all vertebrate classes except the placental mammals and a few other scattered species, a papilla neglecta is present. It is usually located on the floor of the utricle or near the junction of the utricle and the saccule.

      The inferior division of the labyrinth always contains a saccule with its macula, the macula sacculi, but the derivatives of the saccule vary greatly in the different vertebrate classes. In teleosts (bony fishes), amphibians, reptiles, and birds there is a lagena (a curved, flask-shaped structure), with its macula, the macula lagenae. Only the amphibians have a papilla amphibiorum, which is located near the junction of the utricle and the saccule. In some amphibians and in all reptiles, birds, and mammals, there is a papilla basilaris, which is usually called a cochlea in the higher forms, in which it is highly detailed. The elaborate sensory structure of higher types of ears, containing hair cells and supporting elements, is called the organ of Corti.

      The macular endings consist of plates of ciliated (cilium) cells (cells with short, hairlike projections) along with accessory cells, all surmounted by an otolith (a calcareous mass containing numerous particles of calcium carbonate embedded in a gelatinous matrix) or, in teleosts, by one large mass of calcium carbonate. The crista endings contain moundlike groups of sensory (proprioception) cells with supporting cells; the sensory cells have elongated cilia that are embedded in a gelatinous body, the cupula, which forms a sort of valve across an expanded portion of each semicircular canal. The papillae contain plates or ribbons of ciliated cells in a structural framework that lies on a movable membrane, except in amphibians, in which the papillae are on a solid base. These ciliated cells are not surmounted by an otolithic mass or a cupula, but some of the cilia are attached either directly or indirectly to a tectorial membrane (a membrane with one edge fixed to a stationary base, thus anchoring the cilia) or to an inertia body (a mass lying over the ciliated cells and restraining the movements of the cilia).

      The endings have different functions: the macular organs serve primarily as gravity receptors and detectors of sudden movements; the crista organs serve for the perception of rotational acceleration; and the papillae serve for hearing. As structural relations suggest, the auditory endings are derived either from the other labyrinthine receptors or from the primitive labyrinthine epithelium.

Hearing in fishes (fish)

      The cyclostomes and the elasmobranchs (e.g., sharks and rays) possess a labyrinth with maculae and cristae but have no auditory papillae. There are, nevertheless, two possible ways by which some of these cartilaginous fishes, especially the sharks (shark), react to sounds in the water: by means of the macular organs and by means of the lateral-line apparatus. It is in the bony fishes (teleosts (teleost)) that a true ear whose function is hearing first appears among the vertebrates. This ear, which occurs in a number of forms, has varying degrees of effectiveness as a sound receiver; some fishes hear well, others poorly. The differences arise, at least in part, from the accessory mechanisms that aid in the utilization of sound energy.

The basic auditory mechanisms in teleosts

      In most fishes, especially in many marine forms, the auditory mechanism is relatively simple, consisting of macular endings that evidently have been diverted from their primitive functions as detectors of gravity and motion. The important change is not in the structure of the end organ but in its innervation—the nerve supply has connections that transmit auditory information. It is thought that in most teleosts the change to an auditory function has occurred in the saccular macula, and probably the lagenar macula as well, and that the utricular macula continues as a receptor for gravity and motion.

      The simple macular ending of the teleost ear is stimulated by sound through the operation of an inertia principle. Sound waves pass readily through the water and into the body of the fish, causing most of the tissues to vibrate in a uniform manner. The macular otolith, however, represents a discontinuity; because its density is greater than that of the other tissues, it exhibits an inertia effect (resistance to movement). Its motions not only lag behind those of the surrounding tissues but are probably of lesser amplitude as well. Accordingly, a sound creates a relative motion between the otoliths and the other tissues. More specifically, there is relative motion between the bodies of the hair cells, which rest on a tissue base, and the cilia of these cells, the tips of which are in contact with the otolith. This method of stimulating the auditory hair cells is inefficient, however, because of the relatively small difference in density between the body tissues and the otoliths.

Special stimulation mechanisms

      In certain groups of teleosts the efficiency of hair-cell stimulation has been increased by a discontinuity that is nearly 1,000 times greater than the one between tissue and otolith; this is the discontinuity between the otolith and a gas bubble. Although there are varying anatomical methods of achieving it, the simplest arrangement, which is found in clupeids, mormyrids, labyrinthine fishes, and a few others, consists of a gas-filled sac that lies against one wall of the labyrinth. In clupeids (clupeiform) (e.g., herring), a group in which the utricular macula rather than the saccular or lagenar maculae has an auditory function, long anterior extensions of the swim bladder form air sacs (air sac), one adjacent to each utricular macula. In the mormyrids (mormyrid), which include the elephant-nosed fish (elephantsnout fish), a similar condition exists in early life; during adult development, however, the connections with the swim bladder disappear, leaving the air sacs connected with the saccular and lagenar endings. The gas content of these sacs is then maintained by special glands that extract gas from the blood. Air sacs arise in various other ways.

      One large group of fishes, referred to as the Ostariophysi (e.g., catfishes (catfish), minnows (minnow), and carps), has no air sac adjacent to the labyrinth, but a possibly equivalent condition is achieved through a mechanical connection between the swim bladder and fluid chambers adjacent to the labyrinth. A chain of three or four small bones, known as the Weberian ossicles (Weberian apparatus), extends from the anterior wall of a part of the swim bladder to a fluid-filled chamber called the atrium, which in turn connects by fluid passages with the two labyrinths in the region of the saccule-lagena complex. In this arrangement the discontinuity is between the air of the swim bladder and the chain of ossicles (ear bone) in contact with it; the relative motion arising from sound stimulation is communicated through the ossicular (bony) chain and the fluid channels to the macular endings.

      Regardless of the mechanism employed, however, the ear of all teleost fishes is basically a macular organ. Because it is stimulated by sound that is transmitted to tissues adjacent to the sensory cells and that acts differentially on these cells, this ear is of the velocity type.

Auditory sensitivity of fishes

      Although only limited experimental data are available, it appears certain that, in general, fishes with the accessory mechanisms described above have greater sensitivity and a higher frequency range than do those lacking such mechanisms; while upper frequency limits are about 1,000 hertz for many fishes, they are about 3,000 hertz for the Ostariophysi and other specialized types.

      Many experiments have dealt with the problem of auditory sensitivity in fishes, but the species most extensively tested has been the goldfish, a variety of carp belonging to the Ostariophysi. In one well-controlled investigation, the sound intensities required to inhibit respiratory movements, after conditioning with electric shock, were studied. The greatest sensitivity was found to be around 350 hertz; above 1,000 hertz sensitivity declined rapidly.

      In view of the simple anatomical character of the ear, the question of whether fishes can distinguish between tones (tone) of different frequencies is of special interest. Two studies dealing with this problem have shown that the frequency change just detectable is about four cycles for a tone of 50 hertz and increases regularly, slowly at first, then more rapidly as the frequency is raised.

Hearing in amphibians (amphibian)

      There are three orders of living amphibians: the Apoda, which are legless, wormlike types such as caecilians; the Urodela, which are tailed forms such as mudpuppies, newts, and salamanders; and the Anura, which are tailless forms including frogs and toads. Although members of all three orders have ears, the structures vary greatly in the different groups, and little is known about them except in such advanced types as frogs (frog).

The auditory mechanism in frogs

      Although the frog (Anura) has no external ear (structures on the outside that direct sound vibrations inward), the middle-ear mechanism is well developed. On each side of the head, flush with the surface, a disk of cartilage covered with skin serves as an eardrum. From the inner surface of this disk, a rod of cartilage and bone, called the columella, extends through an air-filled cavity to the inner ear. The columella ends in an expansion, the stapes, which makes contact with the fluids of the inner-ear (otic) capsule through an opening, the oval window. A second opening in the otic capsule, the round window, is covered by a thin, flexible membrane; it is bounded externally by a fluid-filled space that can expand into the air-filled cavity of the middle ear. When the alternating pressures of sound waves cause the eardrum to vibrate, the vibrations are transmitted along the columella and through the oval window to the inner ear, where they are relayed to the round window in a path across the otic capsule by movements of the inner-ear fluids. Along this path are two auditory endings, the amphibian and basilar papillae, the sensory hair cells of which are stimulated by the fluid movements. These movements are transmitted to the ciliary tufts of the sensory cells by a tectorial membrane, which is suspended from the hair cells in such a way that it can be moved by the oscillations of the inner-ear fluids.

      As sense organs for hearing, the papillae, which appear for the first time in amphibians, have cells like those in lower vertebrates that serve the same purpose. There are two types of papillae: the amphibian papilla, which is found in all amphibians, and the basilar papilla, which is found in some amphibians. Because they are located in different places in the inner ear, the papillae probably represent two distinct evolutionary developments. Moreover, they operate on a mechanical principle found in no other animal group: a tectorial membrane, moving in response to sound vibrations that have been transmitted to it by the inner-ear fluids, stimulates the sensory hair cells directly through connections to the cilia of these cells. In all higher types of ears, on the other hand, the sensory cells themselves are set in motion by the sound vibrations, while the tips of the ciliary tufts are restrained in one of several ways.

Auditory sensitivity of amphibians

      Although it is presumed that all amphibians possess hearing of some kind, the evidence is sparse; only salamanders (salamander) other than anurans have been studied experimentally. Salamanders trained to come for food at the sound of a tone responded only at low frequencies, up to 244 hertz in one specimen and to 218 hertz in three others.

      Frogs, which are of special interest because they first live in the water as tadpoles and then undergo a metamorphosis that equips them for life on land, have been studied more extensively. Considerable modifications of the middle-ear mechanism occur during metamorphosis. Presumably, the tadpole larva has an aquatic ear that is later transformed into an aerial type.

      Interest in the hearing of adult frogs has been stimulated by their active and often loud croaking during the breeding season. Evidently, their vocalizations assist in the location and selection of mates. The first experimental study of auditory sensitivity in frogs, carried out in 1905, showed that leg movements in response to strong tactual stimuli may be enhanced or even inhibited by sounds.

      Somewhat later, following some unsuccessful attempts to train frogs to make behavioral responses to acoustic stimuli, two other methods were employed to determine the sensitivity and range of their hearing. One of these was the recording of changes in the electrical potentials of the inner ear and auditory nerve; the other was the observation of changes in the potentials of the skin (electrodermal responses) to acoustic stimuli. As a result of these investigations, inner-ear potentials and electrodermal responses in the bullfrog have been recorded over a range from 100 to 3,500 hertz. In the treefrog (tree frog), these same responses have been found in a range that extended from 50 to 3,000 hertz, with the greatest sensitivity from 600 to 800 hertz, and again at 2,000 hertz.

      The recording of impulses from single fibres in the auditory nerve of bullfrogs and the green frog indicates that two types of auditory nerve fibres are present. This has led to the suggestion that they represent the different characteristics of the amphibian and basilar papillae. It is believed that the amphibian papilla is more sensitive to low tones and that the basilar papilla is more sensitive to high tones.

Auditory structures of reptiles (reptile)

      The living reptiles belong to four orders: the Squamata (lizards, snakes, and amphisbaenians), the Sphenodontida (tuataras), the Testudines (turtles), and the Crocodylia (crocodiles and alligators). The reptile ear has many different forms, especially within the suborder Sauria (lizards), and variations occur in all elements of its structure—the external ear is often absent or may consist of an auditory meatus (passage) of varying length; the middle ear shows several forms in the different groups; and the inner ear varies in the degree of development of the auditory papilla and also in the ways by which the sensory cells are stimulated by sound.

Lizards (lizard)

Auditory structure

      There are about 20 families of lizards, ranging from the chameleon, a divergent type, to the gecko, certain species of which have the most highly developed ears found in the group. The chameleons, of those species studied thus far, have only a few sensory hair cells (40 to 50) in the auditory papilla. The geckos, on the other hand, have several hundred hair cells, and the Gekko gecko has about 1,600, the largest known number of hair cells in any saurian. Other lizard species fall between these two extremes in inner-ear development, with the iguanids (iguanid), the most common lizards in the Western Hemisphere, having from 60 to 200 hair cells, according to the species.

      What may be regarded as the standard type of middle-ear structure in the lizards consists of a tympanic membrane and a two-element ossicular chain that extends from the inner surface of this membrane to the oval window of the otic capsule. The ossicular chain is made up of two parts: the osseous (bony) columella, whose expanded innermost end (the stapes) fills the oval window, and the extracolumella, a cartilaginous extension that usually spreads out in two to four processes that are embedded in the fibrous layer of the tympanic membrane. Geckos have a single middle-ear muscle attached to the lateral part of the extracolumella; evidently, contractions of this muscle stiffen the extracolumella, thereby dampening the ossicular motions and protecting the ear against excessively intense sounds.

      The auditory part (cochlea) of the inner ear consists of a basilar membrane lying in an opening in the limbus, which is a plate of connective tissue. The form of the basilar membrane, which is unlike the structure of the same name in amphibians and is clearly of different origin, varies from a simple oval in iguanids to a long, tapered ribbon in gekkonids. In many species the middle portion of the basilar membrane is greatly thickened, especially in some regions of the cochlea. Over this thickening, which is called the fundus, lies the auditory papilla proper—i.e., that part of the cochlea in which the sensory hair cells are held in a framework of supporting tissues and cells. The hair cells usually occur in regular transverse rows, with the number of cells in a row varying along the cochlea. They have a tuft of cilia, the so-called sensory hairs, of graduated lengths, the longest of which are usually attached either directly or indirectly to a tectorial membrane. This membrane arises from a region of the limbus that is usually elevated, often strikingly so, and runs as a thin web or sheet to the region of the hair cells. Only rarely does the free edge of the tectorial membrane connect directly with the cilia of the hair cells; usually there are intermediate connecting structures that take a variety of forms, from simple fibres to relatively massive plates.

      The function of the tectorial membrane and its connections to the ciliary tuft of a hair cell is to immobilize the tuft when the body of the hair cell moves in unison with the basilar membrane on which it rests. This produces a relative motion between the ciliary tuft and the body of the cell and stimulates the cell. All auditory stimulation depends ultimately upon this relative motion, and the means just described for achieving it can be regarded as the most fundamental process by which sounds are perceived. Although it is employed in the great majority of ears, it is not the only mode of stimulation. Another mode is that in the ears of fishes, in which an otolith lies upon the ciliary tufts and, by its inertia, reduces and alters the motion of the tuft relative to the cell body. Still another method is the one in the frog papilla, in which the tectorial membrane is moved by the cochlear fluids while the body of the sensory cell remains at rest.

      In some lizards the inertia principle has a form different from that found in fishes. In the former, a body called a sallet lies upon the ciliary tufts of a group of hair cells and, by its inertia (or by an equivalent means), restrains the movement of the cilia when the cell body is made to move. The result is a relative motion and a stimulation of the hair cells, like the more common restraint by a tectorial membrane.

      The ears of two lizard families show only the inertial restraint method of stimulation; in several other families this method functions in some regions of the cochlea for certain hair cells. Hair-cell stimulation by two or more different arrangements within the same cochlea, however, is the rule rather than the exception because of its many advantages. Although the tectorial-restraint method provides great sensitivity for individual cells, the sallet system also attains good sensitivity, but in another way: by causing many cells—those in common contact with a given sallet—to work in parallel, thus producing a spatial summation. The sallet system has the advantage of being more resistant to damage by overstimulation from intense sounds. In such lizards as the geckos, for example, in which the hair cells are divided nearly equally between tectorial and sallet systems, an exposure to excessive sound has been observed to break all the tectorial connections to the hair cells while leaving the sallet connections intact. But even though the most sensitive hair cells are inoperative, the animal can respond to sounds, although with lesser acuity.

Hearing abilities of lizards

      The lizards are the lowest vertebrates to have a well-developed spatial differentiation of the cochlea in which different regions respond to different frequencies of tone. The problem of tonal discrimination has been somewhat solved in frogs, in which the differential responses to tones by the two papillae may provide some information concerning the pitch of sounds. The mechanism in frogs, however, is a poor one, as it can give only crude and uncertain cues at best.

      In some lizards, such as iguanids and agamids, a minimum of structural variation occurs along the cochlea; in others (e.g., geckos, which have very extensive differentiation along their extended basilar membranes) the differentiation is almost as great as that in higher vertebrates, including man. Most geckos are nocturnal in habit and use vocalizations to maintain individual territories and probably to find mates.

      Although it has been possible to train two species of lizards (Lacerta agilis and Lacerta vivipara) to make feeding movements in response to a variety of sounds, including tones between 69 and 8,200 hertz, most attempts to train lizards to respond reliably to tonal stimuli have failed. The one useful method thus far developed to study the sensitivity of these animals to sounds involves recording electrical responses in the ear and in the auditory nervous system. Although such observations have provided information about peripheral response to sounds, they do not reveal anything about other processes in the nervous and behavioral systems.

      Electrical responses in the cochlea of many lizard ears show considerable variations: in absolute sensitivity, in the tonal regions in which responsiveness is best, and in the extent of the frequency range. It has been concluded that most lizards have good auditory sensitivity over a range from 100 to 4,000 hertz and relatively poor hearing for lower and higher tones. This auditory range is not very different from that of man, although somewhat more restricted than that of most mammals.

Snakes (snake)

      Without much doubt, snakes developed from some types of early lizards but lost their legs when they adopted habits of burrowing in the ground. Although some snakes burrow, others have taken up different habits: many species live on the surface of the ground, several are largely aquatic, and some live in trees. All, however, show drastic ear modifications that reflect their early history as burrowers; for example, there is no external ear—i.e., no opening at the surface of the head for the entrance of sound. This fact, together with a seeming indifference to airborne sounds, has led to the supposition that snakes are deaf or that they can perceive only such vibrations as reach them through the ground on which they crawl.

      This supposition is incorrect; snakes are sensitive to some airborne sound waves and are able to receive them through a mechanism that serves as a substitute for the tympanic membrane. This mechanism consists of a thin plate of bone (the quadrate bone) that was once a part of the skull but that has become largely detached and is held loosely in place by ligaments. It lies beneath the surface of the face, covered by skin and muscle, and acts as a receiving surface for sound pressures. The columella, attached to the inner surface of the quadrate bone, conducts the received vibrations to its expanded inner end, which lies in the oval window of the cochlea. If the columella is severed, the sensitivity of the ear is significantly reduced.

      Although the sensitivity of the snake ear varies with the species, it is appreciably sensitive only to tones in the low-frequency range, usually those in the region of 100 to 700 hertz. For this low range the large mass of the conducting mechanism and the presence of tissues lying over the quadrate bone are not of any great consequence. Moreover, while the sensitivity of most snakes to the middle of the low-tone range is below that of most other types of ears, it is not seriously so. In a few snakes, however, the sensitivity is about as keen as in the majority of lizards with conventional types of ear openings and middle-ear mechanisms.

      That the ears of the snake receive some aerial sound waves instead of depending exclusively on vibrations transferred from the ground has been proved by recording the potentials in the cochlea of one ear while rotating the animal in front of a sound-wave source so that the ear being studied was sometimes facing the source and sometimes directed away from it. The recorded potentials were significantly greater when the ear was facing the source. There would have been no difference in the responses if the sound first set up vibrations in the ground and these were then transmitted to the body. This observation also shows that the ears of the snake can determine the direction of a sound in terms of its relative intensity in the two ears. Although snakes can perceive vibrations from the ground that are present at a sufficient intensity, this ability is not peculiar to them; all ears respond to vibrations transmitted to the head.

Amphisbaenians

      The amphisbaenians form a little-known group of reptiles. Because they are burrowers and live almost entirely underground, they are seldom seen. The one species in the United States, Rhineura floridana, is found in some parts of Florida; a number of species occur in other regions of the world, especially in South America and Africa.

      The animals construct a maze of underground tunnels, which they patrol in search of such food as grubs and worms. Although small eyes below the body surface can receive light through a transparent scale, amphisbaenians evidently make little use of vision. There is reason to believe, however, that they use hearing to locate their prey.

      Amphisbaenians, like snakes, have no surface indication of an ear; a receptive mechanism below the surface and different from that in snakes conveys vibrations to the inner ear. In the oval window, which occupies the entire lateral surface of the otic capsule, is a stapes. The head of the stapes in most species is directed laterally and forward; it is united by a joint with a rod of cartilage (the extracolumella) that extends forward along the face, in the line of the lower jaw. The extracolumella lies below the surface, where it makes close contact with and finally enters a dense layer of the skin. When the facial region is exposed to sounds, the vibrations are transmitted through the dense layer of the skin to the extracolumellar rod and then through it to the stapes, finally reaching the fluid of the inner ear. That this is the route of sound conduction has been proved by cutting the extracolumella at different places and observing the reduction of recorded responses in the ear.

      The auditory mechanism of amphisbaenians varies somewhat according to species but is substantially as described above. The sensitivity, which also varies with species, is surprisingly high in some species, considering the unusual nature of the mechanism involved. Studies similar to those described for snakes have proved that this ear receives aerial sounds and that it can determine the direction from which the sound originated. As expected, this ear also responds to mechanical vibrations communicated directly to the skull.

Turtles (turtle)

      It is sometimes supposed that the turtle's ear is a degenerate organ, largely or even completely unresponsive to sound. Although the turtle's ear is unusual in some respects, and can be regarded as specialized in its manner of receiving and utilizing sounds, it is not a degenerate organ. There is good evidence that turtles are sensitive to low-frequency airborne waves and that some species have excellent acuity in this range.

      A plate of cartilage on each side of the head serves as a tympanic membrane. Leading inward from the middle of this plate is a two-element ossicular chain consisting of a peripheral extracolumella and a medial columella the expanded end (the stapes) of which lies in the oval window of the otic capsule. Within the otic capsule are the usual labyrinthine endings, including an auditory papilla. The auditory papilla lies in a path between the oval window and an opening (the round window) in the posterior wall of the otic capsule. Unlike the round window in most ears, that in turtles has no membranous covering for transmitting pressure changes to the air-filled cavity of the middle ear. Instead, the opening leads to a fluid-filled chamber, the pericapsular recess, that extends laterally and anteriorly to enclose the external portion of the stapedial expansion of the columella. A pericapsular membrane separates the perilymph (fluid) of the otic capsule from the fluid of the recess. When the stapes is moved inward by the columella at one phase of a sound vibration, the fluid of the otic capsule is displaced, causing a pressure change that, after passing through the sac containing the auditory endings, continues in a circuitous course to the external surface of the stapes. When the columella moves outward, the fluid circuit reverses itself. Hence the result of a continuous sound wave is a surging back and forth of the fluids in the otic capsule and the pericapsular recess at the same frequency as that of the sound.

      The special mechanical arrangement in the turtle ear is fully effective within the low-frequency range. Indeed, the relatively large mass of tissue and fluid involved in the response to sounds is in part responsible for the efficiency of the ear at low frequencies and also for the rapid loss of sensitivity as frequency increases.

      This type of cochlear response to sounds is not peculiar to turtles; it is also found in snakes, through a structural arrangement of similar form. Although it also occurs in amphisbaenids, the fluid path in these animals is entirely different: it proceeds through the perilymphatic recess into the brain cavity and then by an anterior passage across the head to the lateral surface of the stapes.

      Certain experiments involving the turtle's sensitivity to sounds have used training methods (conditioned responses); only a few have met with success. It has been found that turtles of the species Pseudemys scripta, trained to withdraw their head, respond to sound over the low-frequency range, with the greatest sensitivity in the region of 200 to 640 hertz. This result is in close agreement with electrophysiological observations in which it has been found that impulses could be obtained from the auditory nerve of Chrysemys picta (painted turtle) for tones between 100 and 1,200 hertz, with highest sensitivity for tones below 500 hertz. Similar results have been obtained by additional observations of this kind with several other species of turtles, some of which are very sensitive to a narrow band of frequencies in the low-tone range. Evidently, the type of receptor mechanism in the turtle can achieve great sensitivity through mechanical resonance at a particular region of the low-frequency scale.

      Evidence has also been obtained that these responses are to aerial waves and not to vibrations set up in the ground. The sensitivity to surface vibrations was considerably poorer than that to aerial sounds. In addition, cutting the columella seriously impaired the responses to aerial sounds but hardly affected responses to mechanical vibrations applied to the turtle's shell.

Crocodiles (crocodile)

      The order Crocodylia includes four groups of closely related forms: crocodiles, alligators (alligator), caimans, and gavials (gavial). The crocodile ear, although clearly reptilian in general structure, has a number of peculiar features. Leading to a tympanic membrane on each side of the head is a shallow external passage the outside opening of which is protected by an earlid that is closed when the animal enters the water and dives. Beyond the tympanic membrane is a middle-ear cavity, with the one on the right connected to the one on the left by an air passage that runs across the head above the brain. A sound presented to one ear, therefore, reaches the other ear about equally well. A columellar system connects the tympanic membrane to the oval window of the otic capsule, as in other reptiles. The inner ear is highly developed and bears many similarities to the cochlea of birds, described in the next section. Elongated and slightly curved, the cochlea contains about 11,000 sensory hair cells, about seven times as many as found in that of the most advanced lizard (Gekko gecko).

      In comparison to some lizards, the cochlea of Caiman crocodilus, which has been most extensively studied, exhibits only a moderate degree of structural differentiation. Yet in this cochlea fibre bundles that extend from the root portion of the tectorial membrane separate into fine fibres that form individual connections with the ciliary tuft of each hair cell. This arrangement is not a common one, though present in certain lizards, such as the chameleons, and also in some degree in birds. It probably provides a high level of specificity in the stimulation process or as much specificity as the overall mechanical pattern permits.

      The hearing of crocodilians has not been studied very extensively. It has been noted that the breathing rate in a crocodile accelerates in response to loud sounds, such as the firing of a gun, and it has been observed that specimens of the Mississippi River alligator produce vocalizations of roaring or hissing when low-frequency sounds are made by blowing a horn or by plucking a metal rod. Studies of the electrical potentials in the ear of Caiman crocodilus show that it is sensitive to frequencies ranging from 20 to 15,000 hertz.

Hearing in birds (bird)

The avian auditory structure

      Ears of birds show considerable uniformity in general structure and are similar in many respects to those of reptiles. The outer ear consists of a short external passage, or meatus, ordinarily hidden under the feathers at the side of the head. Most birds have a muscle in the skin around the meatus that can partially or completely close the opening.

      The tympanic membrane bulges outward as in most lizards. In the songbirds, however, it consists of two separate membranes, with the outer one apparently serving to protect the inner one from injury. From the inner surface of the tympanic membrane an ossicular chain transmits vibrations of the cochlea. As in lizards, the chain consists of an osseous inner element, the columella, and a cartilaginous extracolumella that extends the columella peripherally and connects with the tympanic membrane.

      The cochlea of birds is similar to that of crocodiles, consisting of a short, slightly curved bony tube within which lies the basilar membrane with its sensory structures. The length of the basilar membrane varies between 2.5 and 4.5 millimetres (0.1 and 0.2 inch) in most birds, but in the owls it may reach 10 millimetres (0.4 inch) or more. At the end of the cochlea is another ending with a different function, the lagena and its macula.

Auditory sensitivity in birds

      Using the conditioned-response method to study auditory sensitivity in a small songbird, the bullfinch, responses over a frequency range from 100 to 12,800 hertz have been observed. The electrophysiological method was first applied to the study of hearing in birds in 1936. In this study impulses from the cochlea of pigeons (pigeon) were recorded for tones usually up to 10,000 hertz and occasionally as high as 11,500 hertz. Although this method has been used since 1936, few detailed and quantitative results have been obtained; nevertheless, one striking characteristic revealed by these studies has been the high degree of sensitivity in the low and middle range and the very rapid decrease in the high tones.

Uses of hearing in birds

      Like other animals, birds use hearing to warn them of enemies and other kinds of danger. To a degree hardly equalled in lower species, they also use hearing in social relations and communication. Many male birds sing to hold their territories and to attract mates. Some birds also use vocalizations to identify their mates or group members. During the breeding period of the emperor penguin, for example, the male leaves his mate for a journey taking many days in order to obtain food. Upon returning to the general area where his mate has remained with a pack of hundreds of birds, the male is able to locate and to recognize his partner by an interchange of calls.

      There is good reason to believe that certain birds, including the swiftlets (Collocalia) of Asia and Australia, the oilbirds (Steatornis) of tropical America, and possibly a few others, are able to use echolocation when flying in the dark caves that they inhabit. Moreover, it is well established that many owls (owl) locate and catch their prey by auditory cues. On a dark night, an owl perched in a tree can hear the rustling sounds made by a mouse in the grass and leaves on the ground below; by accurately localizing this signal, he can make his strike and capture the prey without any visual aid.

Hearing in mammals (mammal)

Auditory structure of mammals

      In the mammals the ear reaches its highest level of development, with well-differentiated divisions of outer ear, middle ear, and inner ear. Except in some of the sea mammals, in which certain modifications and degenerations have taken place, these structures carry out their functions in a remarkably regular manner.

      The outer ear consists of pinna (or auricle) located behind the ear opening and partially enclosing it and an auditory meatus that leads inward. The pinna varies greatly in size relative to the size of the animal, being large enough in many species to serve a useful purpose in the collection and reflection of sounds. Many mammals can move the pinna back and forth to regulate in some degree the entrance of sounds to the auditory meatus, which transmits the sounds inward to the tympanic membranes. In some mammals, such as many of the marine types, the external opening can be closed to keep out water when the animal dives, and in certain species of bats the tube itself contains a valve that can be closed to protect the ear against undesirable sounds.

      The middle ear of mammals consists of a tympanic membrane, an ossicular chain of three elements, and two tympanic muscles. The tympanic membrane bulges inward, unlike the usually outward-bulging membrane of reptiles and birds. The elements in the ossicular chain are the malleus (hammer), incus (anvil), and stapes (stirrup), so named because of the resemblance of the bones to these objects. The malleus is attached to and partly embedded in the fibrous layer of the inner surface of the tympanic membrane. It connects to the incus, which connects in turn to the stapes, the footplate of which lies in the oval window of the cochlea.

      One tympanic muscle extends from an attachment to the skull to an insertion on the malleus. Another muscle has its insertion on the neck of the stapes. By their contractions, both muscles add friction and stiffness to the ossicular chain, thereby reducing its mobility and protecting the inner ear from excessive sounds. The contraction of the muscles is a reflex action and occurs in both ears at the same time in response to loud sounds.

      The inner ear is called the cochlea because in man this structure is a complex tube coiled into about 2.5 turns, thus bearing some resemblance to a snail's shell, from which the term is derived. The name cochlea has now been extended to include the auditory portion of the labyrinth in all animals, even when the structure is not coiled, as in reptiles, birds, and egg-laying mammals. In the mammals in which it is coiled, the number of turns in the cochlea varies with species from a little less than two to as many as four. The guinea pig and its relatives have the largest number of cochlear turns. Extending along the inside of this coiled passage is the basilar membrane, bearing on its surface the sensory structure known as the organ of Corti, which contains the hair cells.

      In mammals a uniform system is employed in the stimulation of the hair cells by sounds. A relatively thick tectorial membrane, anchored securely on one edge to the supporting structure (the limbus), lies with its free portion over the hair cells and with the cilia of these cells firmly attached to the lower surface of this portion. When vibratory movements of the basilar membrane cause the bodies of the hair cells to move, the tips of the cilia are restrained by their attachments to the tectorial membrane. Hence the relative motion between the bodies and cilia of the hair cells stimulates them.

      The sizes, shapes, and spatial relations of many otic structures vary in the different mammalian species, but it is thought that the same basic principles of operation are involved. This uniformity contrasts with their situation in reptiles, in which different systems are present both in different species and sometimes within one ear.

      A number of features are of particular significance in determining the sensitivity and frequency range, which vary with species. Because large masses involve great resistances when moved at high frequencies, the size and mass of the moving parts determine to some degree the variations of sensitivity with frequency and the frequency limits within which the ear operates. The ossicular chain is a mechanical lever, and its lever ratio and the difference in area between the tympanic membrane and the stapedial footplate determine the efficiency of sound transmission from air to the cochlear fluid. The mechanical characteristics of the cochlea and the degree of variation of these characteristics along its extent determine the frequency range of hearing and the degree to which different tones can produce different response patterns. Finally, the numbers and distribution of hair cells along the basilar membrane and the density and specificity of innervation of these cells determine the delicacy and precision with which their periodic activity and spatial patterns are registered by the central areas of the auditory nervous system.

      These anatomical features have been studied in detail in a few animals: among the mammals, mainly in cats, guinea pigs, and to a lesser degree in man. The functional aspects, as shown in responses to sounds and to discriminations among different sounds, have been considered principally in man and to a much more limited extent in other mammals. Some of the auditory characteristics of mammals below man are described in the sections that follow.

Hearing in subhuman mammals

Primates (primate)

      The hearing of other species in the division of mammals to which man belongs has always been of special interest. A number of species have been studied, including monkeys (monkey), marmosets (marmoset), and chimpanzees (chimpanzee) among the primates considered as the most advanced, the anthropoids; and tree shrews, lemurs, and lorises among the more primitive.

      By using a variety of training methods with chimpanzees, monkeys, and marmosets, behavioral thresholds have been recorded in response to sounds of different intensities and frequencies. When compared with each other and with man, it has been found that the hearing sensitivity of these animals and man is remarkably similar over a range of frequencies from 100 to 5,000 hertz, after which the sensitivity begins to differ. The differences observed at the higher frequencies, however, may be partly attributed to variations in experimental procedures. Thus, the results for the chimpanzee stop at 8,192 hertz because this was the highest tone used in the tests. Other observations have shown that chimpanzees can hear tones up to about 33,000 hertz and that young human subjects often hear tones as high as 24,000 hertz. It is also evident that monkeys and marmosets of the species studied can hear still higher tones.

Common laboratory animals

      Certain mammals have long been favourite subjects for various kinds of biological studies in the laboratory, largely because of their convenient size, hardiness under caged conditions, and gentle temperament. Familiar among these are cats, dogs, guinea pigs, rats, mice, rabbits, and, more recently, hamsters, chinchillas, and gerbils. Auditory sensitivity functions have been obtained in these animals by a variety of behavioral and electrophysiological methods.

      When measured behaviorally by conditioned responses and then plotted on a curve, the auditory threshold sensitivity of cats (feline), guinea pigs, and chinchillas (chinchilla) is much the same—a progressive improvement in sensitivity as the frequency is raised until the middle tones (about 500 to 5,000 hertz) are reached, at which point sensitivity tends to remain the same, and then shows a rapid loss in the upper frequencies. There are differences, however, in the maximum sensitivity attained in the middle region, with the guinea pig the least sensitive and the cat the most sensitive of the three species.

      Sensory responses in the cochlea of mammals have been measured electrophysiologically by placing an electrode on the round window membrane. Unlike behavioral curves, however, the curves obtained by plotting the sound required to produce an arbitrary amount of electrical potential of the cochlea do not represent auditory thresholds. Instead, their usefulness is largely in their shapes, which indicate in a relative way the regions of good and poor sensitivity. In addition, these curves represent the performance of the peripheral portion of the auditory mechanism up to the point at which the sound stimulus activates the sensory hair cells in which the potentials are generated. Hence, unlike the curves obtained by behavioral responses, those obtained by cochlear potential methods do not indicate the performance of the central auditory nervous system (the nerve connections between the ear and brain and those parts of the brain in which neural impulses from the ear are processed to produce behavioral responses).

      In the simpler animals, the two types of curves are much alike, judging from the very limited evidence available. In mammals, however, the behavioral curves differ from the cochlear potential curves in three ways. In the behavioral curves there is (1) an exaggerated gain in sensitivity to tones of low frequency, (2) a greater sensitivity to the medium-high tones, and (3) a more rapid loss of sensitivity to the extreme-high tones and a lower frequency of the upper limit. These differences are believed to arise mainly through the elaborate neural processing that takes place in the more highly developed mammalian nervous system, a processing that improves the sensitivitity to high-frequency tones but reaches a limit of effectiveness and finally fails above some frequency limit. With these conditions in mind, the electrophysiological curves can be used to predict reasonably well an animal's behavioral responses to sound waves.

Large mammals

      Because most of the mammals in which hearing has been studied by laboratory methods are small, much less is known about the auditory capabilities of large ones, even of such domesticated animals as horses and cows; nevertheless, it is usually assumed that the auditory capabilities of these animals are much like those of humans. At least they hear sounds in man's vocal range because they seem to respond to verbal signals. Elephants (elephant), for example, trained as working animals, are said to obey as many as 30 different commands. A number of wild animals of medium and large size—raccoons, opossums, and several members of the cat and dog families—have been studied electrophysiologically by the cochlear-response method. Their sensitivity curves are fairly similar in form and in the upper limits attained.

Marine mammals

      Of special interest are the sea mammals, which have been derived from early land species and which have undergone certain changes in order to adapt themselves to at least a partially aquatic existence. In the course of adapting to marine conditions, however, some sea mammals, such as seals (seal) and sea lions (sea lion), seem to have made only limited alterations in their ear structures. In addition to being able to close the meatus when diving, their pinnas have been greatly reduced or essentially lost, a feature of streamlining for rapid progress through the water.

      There are three possible ways that the hearing of marine mammals might be adapted to an aquatic environment: (1) unchanged aerial hearing, with no aquatic adaptation; (2) conversion to an aquatic type of hearing with loss of good hearing for aerial sounds; and (3) development of some kind of double system, with at least serviceable reception of both aerial and aquatic vibrations. In a study of hearing in the common seal, in which responses to aerial and aquatic stimuli were compared, it was found that this animal has a greater sensitivity to aquatic sounds, especially in the upper frequencies, which extended to the remarkably high frequency of 160,000 hertz. Yet, although the seal has made an adjustment for hearing in water, it has not sacrificed the quality of its aerial hearing, which remains at an excellent level, especially for one frequency around 2,000 hertz and another around 12,000 hertz. These differences in auditory senstivity suggest that the mechanisms in this animal for aerial and aquatic hearing are somehow different, but no complete explanation of the adaptations has yet been found.

      Whales (whale), on the other hand, have converted their ears to a truly aquatic form, apparently with some sacrifice of aerial reception. The study of their ears and hearing has been carried out in only a few species of the toothed whales, which produce sounds and use their ears in the process of echolocation (see next section).

      The ear of whales has undergone extensive changes. The pinna is absent and the external ear opening has been reduced to such a minute size, almost a pinhole in some species, that it no longer serves as a path for the entrance of sound. The eardrum, although present in a modified form, seems to serve no useful purpose; it is connected to the malleus only by a ligament, and this connection can be cut without an ensuing loss of sound reception. The usual three ossicles of the middle ear are present, with the footplate of the stapes resting in the oval window. These ossicles are much more massive than the ordinary mammalian ossicles.

      It appears that the whale ear has been converted to a true aquatic type, functioning according to principles similar to those found in the ears of fishes, as described earlier. Sound vibrations in the water readily pass through the tissues of the head and reach the deep-lying middle- and inner-ear structures. Probably the ossicles represent an inertial mass in somewhat the same way that the otolithic body does in fishes. Because of their inertia, the ossicles tend to move with smaller amplitudes and in different phase relations when the tissues of the head, including parts of the cochlea, are set in vibration. This difference in relative motion produces an alternating displacement of the cochlear fluid, which is in contact with the footplate of the stapes and which can be set in motion because of the presence of a pocket of gas in the region of the round window. The performance of the whale ear has been measured in an exact manner throughout the frequency range in one species, the bottle-nosed dolphin (Tursiops truncatus). By a conditioned-response method, it has been found that this animal possesses excellent auditory sensitivity that extends well into the high frequencies.

echolocation in bats (bat)

      Bats are divided into the large bats and the small bats. With one or two exceptions, the large bats live on fruits and find their way visually. The small bats feed mostly on insects, catching them on the wing by a process known as echolocation. As was mentioned earlier, echolocation is a process in which an animal produces sounds and listens for the echoes reflected from surfaces and objects in the environment. From the information contained in these echoes, the animal is able to perceive the objects and their spatial relations.

      Bats produce sounds with the larynx, an organ in the throat that has undergone certain adaptations that make it unusually effective in producing intense, high-frequency sounds. The character of the sounds varies with the species and also with the particular activity. On striking a small object such as a flying insect, the emitted sounds are reflected with only a small fraction of their original energy; the sound is further weakened before reaching the ears of the bat when it must travel some distance through the air.

      Although the frequency of bat (brown bat) cries varies with species, their cries usually occur in a range between 80,000 and 30,000 hertz. In most species, such as Myotis lucifugus and Eptesicus fuscus, the cry is a frequency-modulated pulse of sound; it begins at a high frequency, say, of 70,000 hertz, and in about 0.2 second declines in frequency to about 33,000 hertz. The starting frequency may vary, even in successive cries; a second pulse might begin at 60,000 and end at 30,000 hertz. The greatest energy in the cry is usually in the middle of this frequency range, perhaps around 50,000 hertz in the species mentioned above.

      The use of such high frequencies is an essential feature of the bat's sonar system. In order to determine the nature of objects by reflected sounds, it is necessary that the wavelengths of the sound be small in relation to the dimensions of the objects—indeed, as small as possible if fine details are to be represented.

      An important problem of echolocation is how the bat is able to detect reflected sounds, often in the presence of disturbing noises, and to obtain the information necessary for tracking and catching an insect as well as discriminating between this object and others in the environment. This problem involves considering first the structure of the auditory mechanism in bats and then the nature of their hearing.

      The external ear of bats is usually well developed. In most species the pinna is large relative to the size of the head, and in those species called the whispering bats, because they make such faint sounds, this structure is huge. With its large surface, the pinna acts as an efficient collector and resonator of high-frequency sounds. It is also freely movable and can be rotated and inclined in various ways. The meatus leads inward to the eardrum and, as already mentioned, contains a valve that can be closed to reduce the entrance of sounds. The middle ear of bats is of the usual mammalian pattern—a three-part ossicular (ear bone) chain—but its structure is impressive in the extraordinary delicacy of the moving parts. The two tympanic muscles, however, are relatively large.

      The cochlea of bats also shows the general mammalian form, but there are variations that may be significant for the special functions that are performed by this ear. The basilar membrane is not particularly well developed; it is short in comparison with that of most mammals, and its structural variation from basal to apical ends is only moderate in extent. Whereas most basilar membranes are rather strongly tapered in width, being narrow at the basal end of the cochlea and several times broader near the apical end, in the bat there is only a slight taper, between twofold and threefold. Another curious feature in the cochlea of bats is the presence of local thickenings of the basilar membrane that may add to the stiffness of the cochlear structure.

      The auditory portion of the nervous system has undergone extraordinary development in bats. The regions concerned with hearing are relatively enormous, which is in accord with the great predominance of hearing over the other senses in this animal.

      The hearing of bats has been studied by both electrophysiological and behavioral methods. In the species Myotis lucifugus, electrophysiological measurements of cochlear potentials indicate that response is poor in the low frequencies but improves fairly steadily until the range of 2,000 to 5,000 hertz is reached, at which it tends to level off. Beyond 15,000 hertz there are many irregularities but, in general, the sensitivity declines at a rapid rate. The results of similar studies on a specimen of Eptesicus fuscus are much the same as those for Myotis, though the observations were not extended into the lowest frequencies. The most sensitive range for this species is around 4,000 to 15,000 hertz, after which there is a fairly rapid decline in the upper frequencies.

      The behavioral threshold curve for Eptesicus has a markedly different form. There is a rapid improvement in sensitivity from 2,500 to 10,000 hertz, but the greatest sensitivity is in two peak areas, from 10,000 to 30,000 hertz and from 50,000 to 70,000 hertz, with a separation by a moderate reduction around 40,000 hertz.

      There are other peculiarities of the behavioral sensitivity of Eptesicus to sound stimuli that are of particular interest. The rapid loss of sensitivity to tones around 40,000 hertz may be caused by a failure of neural processing for these tones. The slope of the low-frequency end of the curve is unexpectedly steep, and this appears in a region where the cochlear response is passing through its maximum. Nothing like this has been observed in other animals; it seems to be a peculiarity of the bat.

      When the cochlear responses of bats are compared with similar responses in other small mammals—as, for example, the rat—there is a general similarity in the results. The rat, however, has better sensitivity as measured by this method, reaching a level of especially good acuity in the range from 20,000 to 60,000 hertz, the range in which the bat sensitivity falls off rapidly. As mentioned previously, it must be kept in mind that the sensitivity indicated by the cochlear potentials is mediated in the peripheral mechanism, before involvement of the central auditory nervous system. When the behavioral response is considered, however, the contribution made by the bat's central auditory nervous system can be appreciated: the region of greatest auditory sensitivity, extending from 10,000 to 70,000 hertz, is the same region as the frequency of the echolocation cries and the one in which bats have the greatest need of acute hearing.

      The failure of these bats to exhibit a behavioral response to tones below a frequency of 10,000 hertz can perhaps be explained also in relation to their peculiar use of hearing. This is a region of frequency that has little or no value for echolocation. More than that, it often contains noises of various kinds that, if heard, might be detrimental to this essential function. It has often been observed that bats are not easily disturbed by extraneous sounds of low frequencies, even extraordinarily intense ones. This peculiarity of hearing in bats may account for their resistance to masking sounds. The slight degree of structural differentiation found in the cochlea of bats may represent another aspect of the limitation of their hearing to that part of the sound spectrum most useful in echolocation. Therefore, it appears that the ear of the bat, which is a rather ordinary type of mammalian structure so far as level of auditory sensitivity and degree of tonal differentiation are concerned, has been developed for a particular purpose—namely, the reception of high-frequency sounds within a limited range.

Echolocation in other mammals

      Among the mammals possessing echolocation are the toothed whales (toothed whale). These animals probably produce sounds in the water in two ways: with the larynx and with the complex system of passages connected to the blowhole, which is a nostril in the top of the head. Although many different types of sounds are possible, during echolocation they consist mainly of a rapid series of clicks. These clicks contain many components, but the principal energy is in the high frequencies, from perhaps 50,000 to as much as 200,000 hertz. The use of such high frequencies by these animals is a requirement for effective echolocation in water. Because the velocity of sound is greater in water than in air, the wavelengths are longer; therefore, in order for echolocation to attain the same effectiveness of object discrimination as that achieved by the bat with aerial sounds, an aquatic animal has to use frequencies at least five times as high.

      Whales have good vision when submerged, and apparently their eyes (eye, human) remain fairly serviceable when their heads are out of water. Dolphins can be trained to strike targets or leap over obstacles held several feet above the surface of the water. For many tasks, however, they use echolocation very effectively, such as when catching fish at night or when visibility is poor in murky water. Dolphins have been trained to make fine discriminations of objects when their vision has been completely excluded by blindfolding. Echolocation of some form and degree of effectiveness is suspected in still other animals, such as shrews and sea lions, but the evidence is meagre thus far.

Ernest Glen Wever

Additional Reading

There are no general texts on sound reception. Included below are some of the specialized references dealing with this subject in a technical manner.J. Schwartzkopff, “Mechanoreception,” in Morris Rockstein (ed.), The Physiology of Insecta, vol. 1, pp. 509–561 (1964); M.L. Wolbarsht, “Electrical Characteristics of Insect Mechanoreceptors,” J. Gen. Physiol., 44:105–122 (1960); E.G. Gray, “The Fine Structure of the Insect Ear,” Phil. Trans. R. Soc., Series B, 243:75–94 (1960); C. Walcott and W.G. van der Kloot, “The Physiology of the Spider Vibration Receptor,” J. Exp. Zool., 141:191–244 (1959); E.G. Wever and J.A. Vernon, “The Auditory Sensitivity of Orthoptera,” Proc. Natn. Acad. Sci. U.S.A., 45:413–419 (1959); H. Frings and M. Frings, “Uses of Sounds by Insects,” A. Rev. Ent., 3:87–106 (1958); R.J. Pumphrey, “Hearing in Insects,” Biol. Rev., 15:107–132 (1940); “Sensory Organs: Hearing,” in A.J. Marshall (ed.), Biology and Comparative Physiology of Birds, vol. 2. (1961). See also Brian Lewis, Bioacoustics: A Comparative Approach (1983); William C. Stebbins, The Acoustic Sense of Animals (1983); James F. Willott (ed.), The Auditory Psychobiology of the Mouse (1983).Ernest Glen Wever

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