ECHOLOCATION AND ITS RELEVANCE TO COMMUNICATION BEHAVIOR
Most bats and many marine mammals orient themselves by a natural form of sonar. They emit orientation sounds that are adapted for this purpose and locate many types of objects at a distance by hearing their echoes (Griffin, 1958; Busnel, 1967). They maintain normal orientation during active movements without any possibility of vision, but become disoriented if deprived of hearing or if prevented from emitting orientation sounds. This echolocation behavior escaped notice until electronie technology permitted convenient translation of the orientation sounds of animals into the range of human senses. In the case of bats only the frequency of airborne sound required transposition from the ultrasonic range (20 to 150 kHz) into the frequency range of human hearing. These ultrasonic orientation sounds also have relatively faint audible components that can be heard under favorable conditions once one knows what to listen for (Galambos and Griffin, 1942; Dijkgraaf, 1943). The discovery of echolocation in whales and porpoises required conversion of underwater sounds into sounds conducted through air (Schevill and Lawrence, 1949, 1956; Kellogg et al., 1953; Kellogg, 1961). During the past twenty-five to thirty years, these technological problems have been solved to a sufficient degree that the orientation sounds of bats and marine mammals have been studied in considerable detail (Busnel, 1967; Norris, 1966). While bats of the suborder Microchiroptera and marine mammals of the order Cetacea are the two groups in which echolocation is well developed and well studied, there are isolated cases in cave-dwelling birds (Griffin, 1958; Novick, 1959; Medway, 1962) and suggestive evidence that it may occur in a rudimentary form in some terrestrial shrews (Gould et al., 1964) and rodents (Rosenzweig et al., 1955; Riley and Rosenzweig, 1957).
Echolocation is essentially a solipsistic form of communication as far as we know. The animal emits an orientation sound, hears the echoes, and alters its behavior in an appropriate fashion based upon the information conveyed by these echoes. While the source of echoes may be the body of another animal, only passive physical reradiation of sound waves is involved rather than active reply by the second animal. Hence, echolocation does not properly fall within any reasonable definition of communication behavior, and its discussion in the present volume is justified only by its indirect relevance to the physiological and behavioral phenomena that may be important both in echolocation and in communication. The novelty of echolocation and intrinsic interest in it and in the orientation sounds used by various bats have led to a relative neglect of the possible use of the same or similar sounds for communication. Since cetacean communication is discussed in Chapter 17, this discussion will emphasize echolocation in bats.
Reliance upon echolocation for rapid mobility under difficult conditions places severe demands not only upon the auditory receptors but, more importantly, upon the analyzing capabilities of the animal’s brain. Many bats fly in totally dark caves where irregular rocky obstacles are numerous and unpredictable. They also fly with equal skill in forested areas, avoiding branches, leaves, twigs, vines, and other small objects of considerable complexity. Some cetaceans swim in dark or highly turbid waters where vision is of little if any use. Often there are rocks or other underwater obstructions to be avoided, and some of the smaller porpoises live in muddy rivers and lakes where they must swim close to submerged vegetation, fallen trees, and roots. Two examples are especially impressive in the case of bats: landing on some suitable object and drinking water on the wing. The first maneuver involves flying close to the landing place, slowing, then rapidly turning the body upside down, and finally reaching for toehold with the hind claws. Errors of a few millimeters produce either an unpleasantly hard collision or a fall and the need to repeat the whole procedure. Bats commonly fly low over the surface of water and dip the lower jaw or tongue just sufficiently to drink. An error of a few millimeters would result in either failure to reach the water or in a splashing submersion. Smooth linoleum floors often elicit this type of drinking behavior in captive bats, indicating that the specular reflection of orientation sounds from a horizontal surface is interpreted as a sign of water available for drinking.
The echolocation of stationary obstacles for many years appeared so incredible that no one even suggested that small moving targets might also be detected by sonar. Nevertheless, in recent years convincing evidence has been obtained both from bats and from porpoises that insects and fish, respectively, are pursued under some conditions largely by echolocation (Griffin, 1953, 1958; Griffin et al., 1960; Norris et al., 1961). The accuracy and precision of echolocation implies that the auditory nervous system responds selectively to faint echoes from significant objects, despite a variety of other sounds competing for the animal’s attention. Animals thus endowed might find the analytical requirements of an advanced communication system already at their disposal. While scarcely any solid evidence is available, it may be of interest to discuss the speculative possibility that both echolocation and communication involve the same physiological and behavioral mechanisms.
PROPERTIES OF ORIENTATION SOUNDS
In almost all known cases orientation sounds are quite brief—each one lasting only a small fraction of a second. The most common situation is for the individual sounds to last only about one or a few milliseconds. It is convenient to refer to these sounds as pulses, since those of bats are not clicks with either simple or chaotic waveforms but orderly trains of about ten to several hundred sound waves. Bats orient themselves in air with acoustic probes traveling at approximately 34 cm/msec, and porpoises use more rapidly traveling sound waves underwater with velocities of approximately 155 cm/msec. Under some conditions echoes may return during the latter part of an emitted orientation sound, but many echolocating animals avoid this by adjusting the duration of emitted sounds in relation to the distance between themselves and the objects that are of immediate concern. This avoidance of overlap is almost universal in the best studied bats of the family Vespertilionidae (Cahlander et al., 1964). Cetaceans, when concerned with difficult problems of orientation with respect to objects at short distances, also use very short duration orientation sounds (Kellogg, 1961; Vincent, 1963; Norris et al., 1961). Individually, these are clicks of such short duration that their frequency spectrum is extremely broad. In the best known cases both bats and porpoises shorten the duration of their orientation sounds to less than one millisecond when they are making close approaches to important objects such as morsels of food or, in the case of bats, landing places.
Orientation sounds also vary widely in other acoustic properties. The frequencies are generally high, or at least include wavelengths of a few millimeters or centimeters. This is presumably related to the greater magnitude of echoes from objects that are somewhat larger than the wavelengths of the sounds impinging on them. Another possible advantage is the rapid attenuation of high-frequency sound in air (Beranek, 1949). While restricting the range at which objects can be echolocated, this also limits the reverberations and “clutter” that would otherwise tend to interfere with the important echoes from objects at a close range.
In some cases the frequency within an orientation sound is relatively constant, but it seems to be much more usual for each short-duration orientation sound to contain a rather broad band of frequencies. Among bats, the best studied groups (which are highly specialized for echolocation), there is a rapid downward sweep in frequency, typically an octave or more during each pulse (Griffin, 1950; Novick, 1958). Although earlier comparative studies of a wide variety of neotropical bats indicated highly complex frequency patterns (Griffin and Novick, 1955), recent data obtained with improved methods have shown that the rapid downward frequency sweep is a very widespread, if not universal, component in these groups of bats. The problems of accurate measurement of frequency patterns are complicated by the tendency of bats primarily concerned with large and motionless objects to use orientation sounds of relative low intensity. Those species which are active predators that pursue small moving insects or fish use very considerably louder orientation sounds (Griffin, 1962; Pye, 1967; Suthers, 1965).
There remain to be mentioned two groups of bats which use orientation sounds containing constant or nearly constant frequencies at least during a major part of their duration. These are the Old World family Rhinolophidae and, in neotropical regions, the subfamily Chilonycterinae of the family Phyllostomidae. Both are insectivorous, and, as far as we know, they pursue insects that are as small and move as rapidly as those hunted by the Vespertilionidae mentioned above. Both Rhinolophidae and Chilonycterinae make orientation sounds of relatively long duration, so that echo and emitted signal overlap extensively. In recent years it has been found that both groups have a rapid downward sweep in frequency at the end of the pulse and sometimes also a steeply rising frequency at the start (Novick, 1958, 1965; Novick and Vaisnys, 1964). These frequency-modulated portions seem to be important, and Moehres and his colleagues have recently found that, when Rhinolophus ferrum-equinum flies up to very small and difficult obstacles, the intensity of the frequencymodulated portion of the orientation sound increases markedly (Schnitzler, 1967). I had previously found that under such conditions the duration of the constant-frequency portion decreased while the frequency-modulated portion remained prominent (Griffin, 1962). In the Chilonycterinae, Novick and his colleagues have found that the pulse duration varies during approach to small flying insects in a way that suggests the maintenance of a constant degree of overlap between orientation sound and echo. If the assumptions underlying Novick’s interpretation are valid, the overlap corresponds closely with the frequency-modulated portion of the orientation sound.
The advantage to the bat of this rapid frequency sweep is not clear, but perhaps the most plausible explanation is that it enables a wide range of wavelengths to be reflected from small targets. With small objects approximating the wavelengths of the orientation sounds, the relative intensities of the various frequencies may well provide qualitative information about the nature of the reflecting object. This echo spectrum may be used to achieve discrimination between closely similar objects (Griffin et al., 1965; Griffin, 1967).
One final property of orientation sounds of both bats and cetaceans is the universal tendency for the rate at which they are repeated to increase sharply whenever the animal is faced with a difficult orientation problem—whether it be a bat landing on a crevice in the ceiling of a cave, a porpoise picking up a piece of fish floating close in front of the cement wall of a large tank, or either animal pursuing elusive moving prey. The pulse repetition rates rise from a very few isolated orientation sounds per second to brief bursts at which they are repeated at rates up to 250 per second in bats, and even higher in porpoises. When translated into audible clicks, this crescendo of orientation pulses becomes a buzz.
PROBLEM OF INTERFERENCE
It is misleading to think of echolocation as merely the hearing of isolated echoes. In actual practice under natural conditions, echolocating animals must discriminate certain faint echoes from many other sounds of similar properties occurring at nearly the same time. These include sounds of outside origin and echoes of objects other than the target of immediate concern. Consider, for example, the problems faced by an insectivorous bat relying for its food supply entirely upon echoes from insects measuring only a fraction of the wavelengths of its orientation sounds. These are encountered at unpredictable times and places but, very often, close to other small objects such as leaves or twigs. Any one orientation pulse returns to the bat’s ears echoes from a large number of objecte at different distances and directions. Only one part of this complex of echoes is relevant. All other information must be ignored or used merely for the avoidance of stationary obstacles. Since most of the unimportant targets are larger than the critically important morsel of food, the interfering echoes will very often be more intense than those important to the animal. Yet, despite these difficulties, small insectivorous bats such as Myotis lucifugus capture insects measuring only a few millimeters in wingspread at rates of several per minute during their routing feeding behavior—often under conditions where there is extensive interference from other echoes (Gould, 1955, 1959; Griffin et al., 1960).
The neurophysiological mechanisms employed by bats in such discriminative auditory orientation have been studied rather extensively in recent years by Grinnell (1963a,b,c,d; Grinnell and Grinnell, 1965), Suga (1964a,b, 1965a,b), Harrison (1965), and Henson (1965, 1967). There are some specializations for auditory sensitivity in the ultrasonic frequency range, shared apparently by other small mammals (Ralls, 1967). The auditory areas of bat brains are greatly enlarged relative to those of other mammals, but only posterior to the diencephalon. The medullary, midbrain, and, in particular, the collicular auditory areas are relatively enormous, whereas the auditory thalamus and cortex are only slightly enlarged in comparison to shrews and rodents. Only Grinnel (1963d) has come to grips with the neurophysiological basis of discrimination against interference, and his experiments were directed in part toward explaining the demonstrated resistance of bats to jamming by broad-band interfering noise (Griffin et al., 1963). Evoked potentials from the posterior colliculus in response to short tone bursts similar to orientation sounds could be masked by simultaneous noise from a second high-frequency loudspeaker. In one typical experiment (Grinnell, 1963d, fig. 3), the masking noise raised the threshold for a detectable evoked potential by 43 dB, provided the noise arrived from almost the same direction as the signal. When the noise-generating loudspeaker was moved 60°, however, the threshold fell by about 25 dB. Most of this effect was due to the directional differences in auditory sensitivity, but there was also evidence of neurophysiological interaction within the brain between the nerve impulses from the two ears which served under some conditions to further improve the animal’s ability to detect faint signals despite a masking noise.
When flying bats were pressed to the limits of their abilities to detect fine wires in a severe jamming noise, they performed better than could be accounted for by signal detection theory if only a single communication channel was assumed to be operating between the wire obstacle and the bat’s brain. The flight maneuvers of these bats showed a strong tendency to approach wires obliquely when the jamming noise became truly difficult, and this doubtless served to separate the faint echoes from the jamming noise by taking advantage of their differing angles of incidence. Neurophysiologically, the addition of information arriving via the second ear expanded the discriminative capabilities of the bat’s information-processing system sufficiently to bring its performance well within the theoretical boundary conditions of signal detection theory.
SPECULATION RELEVANT TO COMMUNICATION
This brief review of what is known about the capabilities for discriminative echolocation achieved by less than one gram of bat brain suggests that echolocating animals possess powers of auditory discrimination and information processing that are more than adequate for complex types of communication. But the extent to which bats actually utilize these capabilities for communication remains for future investigation to discover. Cetaceans certainly do communicate by sound, as discussed in another chapter of this book. The search for relevances to justify including a chapter on echolocation in this book has called to mind a puzzling aspect of human echolocation as it is practiced by the blind. A basic challenge is posed by the simple question: Why is it that blind men cannot echolocate as well as bats or dolphins? As more and more has been learned about the echolocating abilities of 7-gram bats, the disparity has increased, to the embarrassing disadvantage of the 1500-gram human brain. Simple arithmetic of wavelengths suggests that a factor of five, or at the most ten, should separate the minimum sizes of objects discriminated because a man is limited to lower frequencies of sound. But where bats catch fruit flies at rates of several per minute, blind men cannot safely drive automobiles, let alone fly airplanes to catch birds—which, of course, would be a directly analogous performance.
This disparity of skill at echolocation can scarcely be due entirely to the hesitant recognition that “facial vision” or “obstacle sense” in the blind is largely, if not entirely, echolocation. More than twenty years have elapsed since this basic conclusion was firmly established by Supa, Cotzin, and Dallenbach (1944), and many direct investigations of human echolocation have been carried out, along with applied research attempting to improve the usefulness of echolocation to the blind (Zahl, 1950; Griffin, 1958; Clark, 1963; and Rice, 1967). It may well be that attempts to transfer responsibility for echolocation to the artificial guidance devices have deflected efforts away from the more tedious, but perhaps ultimately more rewarding attempt to learn how a man could operate like a bat or dolphin within the human range of hearing and with airborne sounds. But whatever deficiencies there may have been in research efforts on this front, thousands of intelligent and able-bodied blind people have been experimenting empirically along these lines for centuries. If it were readily possible, some would probably have learned how to employ echolocation as skillfully as echolocating animals do.
Is there something qualitatively different about bat brains that allows discrimination of echoes imperceptible to much larger and more complex human brains? Extensive investigations of Grinnell and Suga have failed to reveal any neurophysiological differences of a basic nature. To be sure, Henson (1965) has demonstrated the correctness of Hartridge’s speculation in 1945 that the relatively large middle-ear muscles of bats serve to reduce auditory sensitivity during the emission of each pulse of orientation sound. These muscles also relax rapidly enough that good sensitivity is regained in time to listen for echoes arriving after a few milliseconds. Human middle ear muscles do not seem to operate with as short a latency, nor probably with as great a reduction in sensitivity as Henson reports for bats (Wever and Lawrence, 1954). Our complete lack of any information about activities of the intra-aural muscles during human echolocation inhibits further speculation along these lines.
Another approach to this question is stimulated by the subjective reduction in loudness of echoes of any sounds following closely after a much louder sound. This phenomenon can be demonstrated by making a tape recording of a loud sharp click that lasts only a few milliseconds. If the recording is made in any ordinary indoor situation, the click will be followed by a gradually decreasing series of echoes from the walls, floor, and other objects within a few feet of the source of the click and the recording microphone. When played back in normal fashion, these succeeding echoes will not be noticeable any more than they were with the original click, except for a slight dulling of its quality. But if the tape is played back in the reverse direction, so that the echoes precede the sharp click, their gradual build-up over several milliseconds is clearly audible as a hissing sound of growing loudness leading into the click itself. “Click” becomes “shhhick.”
It is not altogether clear how this reduction in subjective loudness of echoes is achieved in the human brain, or even at what neuroanatomical level it occurs. But the information of vital importance to echolocation is obviously contained in the same time span as that during which this suppression of echoes occurs. Perhaps this echo suppression is absent in echolocating animals, and if so, this might explain their superior ability to react to echoes following within milliseconds after a loud orientation sound. These compounded speculations can be useful only in so far as they stimulate new inquiry, and preferably direct experimentation. But they lead to an inverse question, why have human beings acquired the echo-suppression mechanism in the first place? Could it be helpful, if not essential, for the discrimination of speech, especially indoors or in situations where multiple echoes confuse the waveforms of impinging vocal signals that must be analyzed in order to extract meaningful information from messages of another member of the same species? Physicists have sometimes expressed surprise that we can understand speech at all when it arrives in such a jumble of interfering patterns that any direct oscillographic display makes sensible distinctions appear hopeless. To be sure, the well-known emphasis of the auditory analyzing system upon Fourier analysis, and its almost total disregard of phase information, helps explain this discrepancy. But echo interference also complicates close successions of Fourier spectra as well as direct displays of sound pressure as a function of time.
These speculations should suffice to direct attention to a significant but poorly explored aspect of auditory analysis as it presumably operates both in echolocation and in acoustic communication behavior. I will leave to others to judge whether such conjectures could usefully be carried back into the evolutionary history of our remote ancestors at the stage when human speech first developed into a form that we would recognize as such.
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