Show Summary Details

Page of

PRINTED FROM the OXFORD RESEARCH ENCYCLOPEDIA, NEUROSCIENCE (neuroscience.oxfordre.com). (c) Oxford University Press USA, 2016. All Rights Reserved. Personal use only; commercial use is strictly prohibited. Please see applicable Privacy Policy and Legal Notice (for details see Privacy Policy).

date: 18 October 2017

Biosonar and Sound Localization in Dolphins

Summary and Keywords

Toothed whales and dolphins, odontocete cetaceans, produce very loud biosonar sounds in order to navigate and to locate and catch their prey of fish and squid. Underwater biosonar was not discovered until after 1950, but the initial experiments demonstrated a unique sensory modality that could find small targets far away and distinguish between objects buried in mud that differed only by the metal from which they were made. Dolphins determine the distance to their prey by evaluating very small time differences between the outgoing signal and the echo return. The type of outgoing signal varies greatly from low frequency, explosively loud sperm whale clicks, to frequency modulated mid-frequency beaked whale sounds, to very high frequency (over 100 kHz) harbor porpoise signals. All appear to be made by specialized pneumatic phonic lips closely connected to sound projecting fatty melons that focus sound before sending out narrow echolocation sound beams. The frequency of most hearing is matched to echolocation, with the areas of best hearing of the animals being the areas of principal outgoing signal frequency. The sensation levels of hearing are under the animal’s control with “automatic gain control” operating to assure the best hearing of the echo returns. Angular localization of the bottlenose dolphins, for discriminating the minimum audible angles of clicks, is less than one degree in both the horizontal and vertical directions. This remarkable localization performance has yet to be fully explained, but new hypotheses of gular pathways, shaded receiver models, and internal pinnae may provide some explanations as a theory of auditory localization in the odontocetes develops.

Keywords: localization, biosonar, MAA, odontocetes, toothed-whales, internal-pinna, jaw-hearing, AEP, shaded-receiver, echolocation

Performance Capabilities of Dolphin Biosonar

Toothed whales, including dolphins, have been measured to make arguably the loudest sounds produced by any animal when they are producing their sonar, or echolocation, clicks. Sperm whale echolocation signals measured in the center of their beam can be over 236 dB (Mohl, Wahlberg, & Madsen, 2003), while laboratory bottlenose dolphins, detecting a hollow 7.62 cm (3 in.) stainless-steel ball 100 to 120 meters away, averaged clicks of 227 dB within a click train in a noisy environment (Au, 1980). Why are their clicks so loud? Why do they make so much noise? Most of the work to date indicates that the biosonar system of toothed whales and dolphins has evolved primarily as a foraging tool to find and catch food, and the loud signals allow them to find small targets, sometimes at long distances.

Dolphin echolocation was not verified as a sensory modality until the mid-twentieth century (Kellogg, 1958; Norris, Prescott, Asa-Dorian, & Perkins, 1961). Much of the early work examining the biosonar of small toothed whales and dolphins was conducted with animals in laboratory settings. Dolphin sonar capabilities were of great interest to sonar developers, including both Soviet and Western scientists and navies during the cold war, because of the animal’s demonstrated superior performance when compared to technological systems (Ayrapetyants & Konstantinov, 1974; Belkovich & Dubrovskiy, 1976; Busnel, 1966; Busnel & Fish, 1980; Nachtigall & Moore, 1988). Not only were the dolphins better, they were also much faster at solving a variety of sonar problems. When dolphins were trained to detect small steel balls over 100 meters away, using only biosonar, the balls were hung from cables and the trainer-researchers actually had to use binoculars to see whether or not the balls had been properly inserted into the waters of Kaneohe Bay, Hawaii. Finding such small targets in a very noisy natural environment was not an easy task. Biosonar performance, however, is not limited to detecting targets, the targets had to also be discriminated from background noise and other non-targets. Small toothed-whales, including dolphins, excel when telling small differences between targets (Nachtigall, 1980), including the ability to tell the difference between targets, buried over a foot into mud, that differ only in the metal from which they are made (Nachtigall, Au, Roitblat, & Pawloski, 2000; Roitblat, Au, Nachtigall, Shizamura, & Moons, 1995).

Dolphin echolocation requires that a signal be sent out and an echo be returned. Sound travels nearly five times as fast under water as it does in air, so very quiet echoes are heard very rapidly after the emission of very loud outgoing signals. Most dolphins that have been measured produce outgoing clicks in a series of pulses called click trains. When “locked onto a target” of interest the animals normally do not produce another pulse until the echo from the preceding pulse has returned. Thus as a bottlenose dolphin approaches a target, and as the distance gets shorter, the time between pulses goes down and the overall frequency of the occurrence of the pulses goes up. We humans hear this change as an increase in the pitch of the click train. Most wild dolphins that are fishing tend to produce a very vigorous burst of pulses at the end of the train just before they catch the fish; the burst leaves very little time between the individual pulses, and thus is called the “burst pulse.”

Outgoing Clicks, Two-Way Travel Time, and Distance Localization

Bottlenose dolphins searching for a target at a fixed distance when they are not moving produce the next outgoing click around 20 milliseconds after the return of the echo from the preceding click (Au, 1993). Fine measurements of time between clicks in the click train allow an investigator to calculate the distance to the target. One can measure the two way travel time of sound, measure distance by time, account for the 20 msec lag before the production of the next outgoing click, and know the distance from the dolphin to the target (Penner, 1988). Penner (1988) used this finding to examine performance and attention. The time between echolocation clicks turned out to be an accurate way of knowing the distance to which the animal was attending. If targets were only presented at one distance per experimental session, the animal attended to only one distance, and performance was very good when targets were presented as far as 100 meters away. If, however, targets were presented at five different distances per session and could be presented at any of those distances on any given trial, the dolphin’s attention was divided, and performance began to drop when targets exceeded distances of 60 meters. These correct percent performance levels were verified by examining the time between clicks. Single session far-distance detections showed precise interclick intervals with the time between clicks equaling the two-way travel time plus 20 msec. Sessions with poor performance and targets at many distances showed interclick intervals equal to detecting the farthest target regardless of distance to the target.

It is apparent that the dolphin can vary the interval between the echolocation clicks in order to optimize the distance it is examining. One might assume, given that echolocation is a foraging tool, that the dolphin varies the distance to keep a fish “in its sights” as it closes, and the distance between the dolphin and the fish changes as the dolphin approaches to catch the fish. Changing the rate of click output to match the quick changes in a fish’s path and distance requires a special neurological and cognitive ability. Distance localization works primarily by evaluating very small differences in the time of echo returns and adjusting the time of the next click to maximize the probability of tracking the target, closing in, and capturing it. Time is very important to judging distance and localizing targets.

Click Production Mechanisms

How does an animal working with fast traveling sound produce loud echolocation signals that are very precisely timed and rapidly changed? Initial investigators assumed that the animals produced echolocation signals using their vocal chords (Purves, 1967). This notion was countered by others who had been examining the unique sound production mechanism of click production in the sperm whale called the monkey lips, which was essentially a pneumatically driven set of lips in the “nose” of the whale (Norris, 1969) (see Figure 1). While the sperm whale has a single set of lips, most odontocetes have two sets of lips located just behind a fatty melon that transmits sound from the lips to the front of the head and into the water (Cranford, Amundine, & Norris, 1996). No longer called the “monkey lips,” the click production mechanisms have been more accurately renamed the phonic lips (Cranford, 1999). The two sets of phonic lips found on most echolocating cetaceans are balanced in size, and interesting discussions are ongoing as to whether one or two sets of lips are used in producing echolocation clicks (Cranford et al., 2013; Madsen, Lammers, Wisniewska, & Beedholm, 2013). Most everyone, however, now well agrees that the echolocation clicks are generated by passing air through the phonic lips.

Biosonar and Sound Localization in DolphinsClick to view larger

Figure 1. “Monkey Lips” click production mechanism in the nose of an infant sperm whale during dissection.

Credit: Photograph taken during a dissection of an infant sperm whale during the class “How Do You Test the Hearing of a Great Whale,” organized by Paul Nachtigall. The photo was on the camera of Colleen Reichmuth, photographer unknown.

Once produced, the echolocation signals pass from the lips into the melon. The melon is made up of different densities of specialized acoustic fats and oils and it serves to focus and direct sound (Varanasi & Malins, 1972). Most odontocete melons are surrounded by small muscles and tendons and air sacs (Cranford, Amundine, & Norris, 1996). Active control over the angular characteristics of the outgoing sound beam has recently been demonstrated (Kloepper, Buck, Smith, Supin, Gaudette, & Nachtigall, 2015; Kloepper, Nachtigall, Donahue, & Breese, 2012) while odontocetes echolocate.

Properties of Outgoing Clicks

The outgoing echolocation sound is not simply loud and directional, it is also tuned to the hearing characteristics and environmental use of the sound by the animal. Most aquatic echolocators produce outgoing clicks in peak frequency ranges that are ultrasonic to humans. The frequencies are high and the individual clicks themselves are very short—usually between 50 and 200 microseconds. Echolocation is a dynamic sensory modality. Dolphins actively pursue prey and adjust their signals as they chase and catch fish. The outgoing signals must be optimized to do a variety of things including detecting, recognizing, discriminating, localizing, and tracking moving targets. Evolution has optimized the outgoing signals of the animals to accomplish these tasks, and there are differences in signals depending on the species and their environments (Surlyke, Nachtigall, Popper, & Fay, 2014).

Many of the early echolocation measurements were conducted with bottlenose dolphins swimming in tanks. Evans (1973) found that the peak frequency for the broad band pulses of the bottlenose dolphin in tanks was 70 to 80 kHz ,while subsequent work by Au (1993), measuring the clicks of dolphins in noisy Kaneohe Bay, showed peak frequencies exceeding 120 kHz. The signals increased by over 40 dB and an octave in frequency when measured in the noisy bay. The initial audiogram by Johnson (1966) however, indicates that either of these diverse high peak frequencies would likely have been be heard equally well because of the broad range of dolphin hearing . There are a variety of dolphin-like whales including the false killer whale, the Risso’s dolphin (Madsen, Kerr, & Payne, 2004) and the beluga whale (Turl, Penner, & Au, 1987), for example, that produce similar sorts of signals and likely modify their echolocation signals in a similar manner. Other species however, use echolocation signals at even higher (and less variable and broad) frequencies. Harbor porpoises produce narrow band frequency signals, which are normally over 100kHz (Møhl & Anderson, 1973). Quite a few smaller odontocetes including for example (a) Peale’s dolphins, (b) Commerson’s dolphins (Kyhn, Jensen, Beedholm, Tougaard, Hansen, & Madsen, 2010), (c) hourglass dolphins, and (d) Hector’s dolphins (Kyhn et al., 2010) produce somewhat similar narrow band high frequency clicks. Because investigators can go out and measure clicks while animals are feeding, more is known about the types of clicks that are produced by the animals than how clicks are actually used by many species.

Generally speaking, the larger the species of toothed whale, the lower its overall frequency range. The somewhat larger beaked whales tend to produce frequency-modulated relatively narrow band clicks (Madsen, Johnson, Aguilar de Soto, Zimmer, & Tyack, 2006) with peak frequencies below (or near) their area of best hearing close to 50 kHz (Pacini et al., 2011). While there are yet no satisfactory hearing measures for the sperm whale, on-axis measurements of the clicks of the large male sperm whales indicate that most clicks have a center frequency at the low range of 15 kHz (Madsen, Wahlberg, & Møhl, 2002), but with loud click source levels ranging up to 236 dB. It is very likely that sperm whales produce such loud clicks because they hunt for squid at far ranges. Squid do not have swim bladders containing air like many fish, which make brighter biosonar targets, and the sperm whale puts out a very loud, pencil-thin echolocation beam to detect squid targets at distance. That acoustic level of their loudest clicks is equivalent to a small explosion.

Hearing and Echolocation

Echolocation requires that the animal not only make the loud outgoing signal but also listen to the quiet returning echo. All of the vital acoustic information about the prey, the reason for making the big click in the first place, is found in the echo return. Being able to hear that echo return well is vital to successful echolocation. Making clicks as loud as small explosions may be a fine way to produce a louder echo return but it comes with a drawback. Loud sounds hinder hearing because they produce forward masking, making it difficult to hear a sound directly after a loud sound. Because loud sounds “mask” the hearing of whatever comes right after them. Can you imagine listening for a quiet echo right after a small explosion?

The measurement of how well the animal hears both its own outgoing signal and the echo can be accomplished by measuring the animal’s auditory evoked potentials to sound. Supin, Nachtigall, Pawloski, and Au (2003) first measured an echolocating odontocete’s hearing of its own echoes using a false killer whale trained to report a target’s presence or absence by recording the whale’s evoked potentials picked up from the whale’s skin surface, on the head over the brain, with soft rubber suction cups containing gold surface electrodes. The efficacy of the evoked potential procedure for measuring false killer whale audiometry had been previously established by Yuen, Nachtigall, Supin, and Breese, (2005). Levels of auditory-evoked potentials for both outgoing clicks and returning echoes from a false killer whale echolocating targets from one to eight meters away (Supin, Nachtigall, Au, & Breese, 2004) are presented in Figure 2. There are at least two very interesting observations about hearing during echolocations that are obvious from this one figure of averaged evoked potentials. The first observation is that despite a very large difference in the outgoing click intensity and the echo return, the whale heard them at nearly the same level. At one meter distance, it actually appears that the whale hears the echo return much better than the much louder outgoing click! Secondly, despite the fact that there is a difference in over 36 dB in the intensity of the echo return between a target 1 m away and a target 8 m away, the animal hears the echoes at about the same level (Nachtigall & Supin, 2008). Like conventional technological sonars, the biosonar of the whale adjusts its hearing in an automatic gain control of hearing. Targets are localized by varying the time between outgoing echolocation clicks, and then the hearing of the echo signals is adjusted to best analyze target features.

Biosonar and Sound Localization in DolphinsClick to view larger

Figure 2. Echolocation related auditory evoked potential records at different target distances. Distances of 1 to 8 m are indicated on the figure near the records. Bold arrow marks the outgoing pulse-related excursions, while thin arrows mark the echo related excursions.

Reproduced with permission from: A. Ya. Supin and P. E. Nachtigall (2004). The interaction of outgoing echolocation pulses and echoes in the false killer whale’s auditory system: Evoked potential study. Journal of the Acoustical Society of America, 115, 3218. Copyright 2004, Acoustical Society of America.

The adjustment of hearing has been seen not only in the adjustment of hearing levels with distance to the target but also when target conditions change. When laboratory experiments are conducted that focus on echolocation target detection, proper psychophysical experimental design demands that both target-present and target-absent conditions be presented. Auditory Evoked Potential (AEP) hearing levels were measured for both target-present and absent trials for targets with two different target strengths. When targets are absent, one can presume the animal has to spend a bit of extra effort searching to see whether or not the target is there. Hearing, in fact, has been shown to be 20 dB more sensitive during target absent trials (Supin, Nachtigall, & Breese, 2005) when the animal must, in fact, search to locate a target. The fact that the animal does not change its outgoing signals yet hears them 20 dB differently leads to an interesting question: How does the animal adjust its hearing?

Bats adjust their hearing during echolocation to protect their hearing during loud outgoing calls (Kick & Simmons, 1984) via a stapedial reflex in which the middle ear stapedial muscle contracts, with the outgoing call eliminating the middle ear amplification, using an acoustic reflex. Though the hearing change was originally assumed to be primarily reflexive, Suga and Jen (1975) indicated that hearing change during echolocation was perhaps 60% reflexive and 40% caused by efferent control from the central nervous system. The physiological preparations Suga and Jen used with bats will unlikely be duplicated with dolphins, but the non-reflexive components can be examined by measuring learned changes in dolphin hearing. Whales clearly change their hearing during echolocation, but that could be reflexive. Can they also change their hearing when faced with loud sounds that have little to do with their own echolocation—sounds from the outside?

Nachtigall and Supin (2013) paired a warning signal with a loud sound presented to a false killer whale. When the warning signal, (which was also used as the stimulus to measure hearing), directly preceded the loud sound, the whale dampened her hearing sensation level by nearly 15 dB. Similar learned changes in hearing levels have been demonstrated for the bottlenose dolphin (Nachtigall & Supin, 2015) and the beluga whale (Nachtigall, Supin, Estaban, & Pacini, 2016). It would appear as though most odontocetes that echolocate also have the ability to learn to change their hearing sensation levels in anticipation of the onset of loud sounds.

Sound Localization

Those animals that use echolocation for their survival and existence represent the epitome of adaptation for sound localization.

(S. D. Erulkar, 1972, p. 304)

Echolocating dolphins and whales must not only echolocate targets accurately in distance, they must also critically locate and track them horizontally and vertically. The traditional use of the term auditory localization refers to this sort of ability to localize in horizontal and vertical planes. It is most often investigated using passive cues with sound sources and the animal firmly positioned in space, and it is an integral component of auditory processing for most vertebrate animals. While the basic localization has been studied primarily with fixed targets and animals in fixed positions, one can readily imagine a dynamic localization process occurring when a dolphin or whale is actively swimming and chasing a fish. As Norris (1969) indicated, by slightly moving the snout (scanning movements), the dolphin likely produces fine angular discrimination by changing sensitivity with movement. So far, one can only extrapolate from data obtained in the static situation. Sound localization is currently a very understudied, and therefore poorly understood, ability in odontocetes. A very clear and thorough summary of early findings is available in Branstetter and Mercado (2006).

Humans locate sound in air where sound travels five times slower than it does in sea water. Sound is localized by humans differently depending on frequency. Frequencies below 1.5 kHz are localized using interaural time differences. When the wave lengths of the frequencies get shorter as they go higher, say above 3 kHz, where the wavelength is less than half of the distance between the two ears, most of the information may be gained from interaural intensity differences because the head can shadow the sound from the ear farther away from the sound source. Moore and Au (1975) found that, despite the difference in sound speed, the California sea lion localized sound using multiple cues that are comparable to (but slightly different) from those used by humans. Moore examined the minimum audible angle for discriminating the source of pulsed pure tones in the sea lion and found that interaural phase cues were the primary cue below 1 kHz, and interaural intensity functioned as the main cue with signals above 4 kHz. Like the human, for frequencies below 1 kHz, the head size to wave length ratio underwater would effectively eliminate any possible interaural intensity differences, and (because he used slow rise time signals) interaural phase cues would be the only remaining cue available for localizing signals below 1 kHz.

When considering possible cues used by dolphins, things are a bit different. Dolphins hear and use very high frequencies (Johnson, 1966). Renaud and Popper (1975) examined the sound localization ability of a young male Atlantic bottlenose dolphin by looking at Minimum Audible Angles (MAA) for different sorts of sounds presented in the horizontal and vertical planes. The animal was voluntarily restrained in a fixed position on a bite plate, with sounds presented from two different transducers. The animal’s task was to swim to the bite plate, listen for a sound, then swim to the side and press a paddle indicating which side the sound came from. Sounds were pure tones from 6 to 100 kHz and also transient signals resembling echolocation clicks. The pure tones were presented in pulses resembling the timing of echolocation click trains, with sound levels presented at sensation levels of 40 dB. Pure tone MAAs for 6 kHz were 3.6, 90 kHz—3.2, and 100 kHz—3.8. These were very similar but significantly different from better MAAs found between 10 and 90 kHz with the best at 2 at 50 kHz. The comparisons to MAAs, when clicks were presented in horizontal and vertical planes, were shown to be 0.7 in the vertical and 0.9 in the horizontal planes. Obviously, clicks produced superior localization. Humans are presumed to be quite good at localizing sound, and humans (Butler, 1969; Mills, 1958) locate sound in the horizontal plane down to 1 degree, but they do not have that ability in the vertical plane, where it falls below 7 degrees. It is somewhat surprising that an animal without external pinna, in a fixed position, can produce a MMA of 0.7 degrees in the vertical plane. It is surprising because dolphins have two ears and most of auditory localization is presumed to occur by a comparison of intensity cues between the two ears. It is presumed that the animals hear best on the sides, left and right, because their ears are located there and sound paths to the ears have long been presumed to be primarily through the left and right jaw-bones where each become very thin and is termed a pan-bone (Norris, 1969). These sound cues are assumed to be either binaural time or binaural intensity differences from the left and right sides. If those were the primary localization cues for the dolphin, and the animal heard through its lower jaws, one would assume that, as in humans, horizontal localization MAAs should be far better than vertical MAAs. Renaud and Popper (1975) explained the excellent results in the vertical plane through the “detection and memory of intensity information.” Presumably the animal heard better with the lower portion of its rostral area and compared it via memory to sounds presented from the upper portion. Excellent performance in the horizontal plane was attributed to intensity differences because one side of the animal’s head and lower jaw was shadowed by the other side during stimulus presentation, and previous work had demonstrated the dolphin’s ability to discriminate intensity differences down to 1 dB. Localization in the horizontal plane could therefore be explained by differences in intensity caused by head shadowing of sound.

Subsequent work, combined with previous observations, however, may offer an alternative explanation for the excellent performance of Renaud and Popper’s dolphin when determining the location of sounds in the vertical plane. Norris (1969) also noted that original work by Yanagisawa et al. (1966), mapping the areas of best hearing on anesthetized “porpoises” (Norris called dolphins porpoises in the 1960s), showed four areas of best sensitivity. Two areas of peak sensitivity above the mouth on the forehead, and two on opposite sides of the head on the lower jaws. Areas on the lower jaw were the most sensitive, but the additional areas on the anterior melon, or forehead region, were nearly equally sensitive to those on the lower jaw. So, rather than there being two areas of peak sensitivity, there were four. Two of these were below the midline and two well above. This work was conducted both in air and under water.

Additional and subsequent work by Møhl et al. (1999), also measuring areas of peak sensitivity with evoked auditory potentials, found that there was a point of sensitivity on the Atlantic bottlenose dolphin 20 dB better than that measured directly around the external auditory meatus. That point was located midway across the melon on the animal’s forehead. The best sensitivity was found forward of the pan bone on the lower jaw, and it was 38 dB better than the spot over the external auditory meatus. Unfortunately, points analogous to those examined by Yanagisawa, which may have been even more sensitive, were not measured. Only one point above the midline was tested by Møhl et al. (1999) leaving an intriguing problem to be investigated, however both studies show hearing sensitivity in the area of the melon, and one showed sensitivity nearly equal to that on the lower jaw. If the dolphin has sensitive hearing both on its lower jaw and on its upper melon, there is an alternative explanation for Renaud and Popper’s (1975) findings of nearly equal MAA’s in the horizontal and vertical planes. The animal could be comparing sound intensities from above and below its jawline, from sound received from its lower jaws and from its melon, to determine sound direction in the vertical plane. If there are four primary sound paths, localization would certainly be enhanced by comparing intensity cues from multiple points.

A Comparison of Multi-Pupil Hearing and of Multi-Frequency and Multi-path Hearing

The idea that the dolphin may split its primary sound paths from the traditional two into four would require an additional modification of the neural structures supporting the perceptual processes for localization. While that would seem to add a very unusual complexity, there may be a very similar process going on in the dolphin visual system. Most mammalian eyes have a single pupil, and that pupil focuses onto an area of the cornea richest in sensory neurons termed the fovea centralis. Odontocete eyes, when functioning in very dark conditions, like those found when diving very deeply, have a single pupil shaped a bit like a quarter moon. However, when the animal is near the surface in brighter light conditions, the pupil closes down and creates two pupils—one at each end. Each of these pupils is small, perhaps functioning a bit like a pin-hole camera. They are separated in each eye, and each of the separate pupils has a fovea centralis (Mass & Supin, 2002). Thus each eye has two fovea. The whale must integrate a visual field from four, rather than two, primary areas of peak visual sensitivity. This integration at the neural level is perhaps not trivial but may be less of a task for the auditory system than for the visual system. The odontocete auditory system is very advanced. The relative size of the odontocete brain is well known, the auditory pathways are very well developed early, and they seem to have been the dominant functional system in odontocete evolution (Oelschläger & Kemp, 1998). The development of the auditory system is “largely responsible for the size increase of the brain as a whole” Oelschläger and Kemp (1998, p. 210). Given this development and its focus on auditory processing, the integration of a four areas of best auditory sensitivity for auditory localization using traditional intensity and time cues does not seem out of the question.

More Than Time and Intensity

There is more information available to animals from a sound for localization than can be obtained through traditional time and intensity cues. The human pinna, with its convolutions, does much more than simply serve as a sound gathering device. The various structures of the pinna transform time relationships within the sound itself. The pinnae serve to differentially delay sound by frequency, and sound becomes characterized by the position of its source. The head structure and the pinnae serve to transform sound frequencies and time (Erulkar, 1972) to find the location of the sound in a shaded receiver model. It is obvious that odontocetes do not have external pinnae, but sound can enter the head at many places given the similar density of water and the dolphin’s tissue. The four areas of peak sensitivity measured by Yanagisawa et al. (1966) were not isolated entry points; they were simply points of peak sensitivity. Given the multiple entry points and the possibility of shaded areas caused by varying pathways and air sacs, it is not unreasonable to assume that there may be internal pinnae in odontocetes.

Møhl et al. (1999), when measuring areas of peak sensitivity, measured both sensitivity and latency. The areas found to be the most sensitive were not heard the soonest. Sounds heard on the lower jaw were the most sensitive, but sounds heard at the area of the external auditory meatus were processed the soonest. They proposed that this discrepancy between latency and sensitivity “may indicate the presence of a shaded receiving transducer, where input is weighted according to direction of arrival and position across the aperture of the receiver, in this way the directional characteristics of the ear can be shaped” (p. 3424). Although not stated, perhaps the necessary initial measurements for an internal pinna were made with this study. The study was limited, however, in that the signals presented were only broadband synthetic generic dolphin clicks. The hearing of differential frequencies was not examined.

Although not openly published beyond the doctoral dissertation, Taylor (2013) examined sound localization by examining hearing thresholds, depending on the direction from which the sound came and its frequency. These thresholds of varying frequencies reveal a fascinating picture of dolphin hearing differences when both position and frequency of the sound source were varied. An adult bottlenose dolphin was trained to swim into a head-sized hoop and bite onto a bite plate to fix his position 1 m under water. He was also trained to wear soft rubber suction cups containing skin surface electrodes to pick up evoked auditory potentials just behind the blowhole over his brain. Various acoustic signals consisting of 20 msec sinusoidally amplitude-modulated tones with a modulation frequency of 1 kHz, were played, and his AEP thresholds were determined and compared. The tones for each of 3 carrier frequencies—5.6, 22.5 and 38 kHz—were individually presented from transducers in front of the animal in 21 different positions. Seven transducer positions were created in each of three horizontal planes. One plane at 0̊ with the jawline a second 0.5m above, and a third 0.5m below. In the vertical plane transducers were moved 30°, 60°, and 90° from the center line. Transducers were always 1.5m away from the animal. The 21 different hearing thresholds taken from the 21 transducer positions revealed interesting hearing patterns. Generally, the highest frequency sounds were heard best directly in front of the animal, while low frequency sounds were heard better, off to the sides. When clicks were also examined in the same way, the best hearing was in the direct center, from the lowest source that was below the animal.

These data support an interesting new model of odontocete hearing pathways. The accepted notion of odontocete hearing is that sound passes through the lower jaw pan bones on the lower side of each jaw of the odontocete on the way up to the ear Norris (1968). Cranford, Krysl, and Hildebrand (2008) simulated sound sources and finite element modeling of tissues of the Cuvier’s beaked whale (Ziphius cavirostris). They found a prominent sound reception channel in between and below the two lower jaws and termed it the “gular pathway.” In this pathway, the sounds entered the head from below and between the lower jaws, passed through an opening created by the absence of a medial bony wall (because there were no posterior mandibles), and continued on toward the bony ear complexes through the mandibular fat bodies. This sensitive direct pathway from below the animal’s head and in the center would corroborate Taylor’s empirical findings of the direction from which echolocation clicks were best heard.

Conclusion

Biosonar, or echolocation, requires precise location of sounds in space. It is easier to measure the outgoing signals of stationary animals than it is to measure the hearing of animals while they are moving and echolocating. Much of the early work examining echolocation revealed fascinating abilities, but echolocation is a process that involves both outgoing signals and hearing echo returns. A hearing system that has been empirically demonstrated to have a minimum audible angle of less than one degree in both the horizontal and vertical planes underwater is a hearing system worth understanding. The processes underlying this excellent performance should provide cues to maximize sound localization. The initial work of measuring hearing while whales echolocate, and even the basic pathways of sound to the ear, have revealed interesting new processes and hypotheses, but there is much to be done before a reasonable and thorough theory of the hearing and location of sounds in space during active whale and dolphin biosonar is developed.

Further Reading

Au, W. W. L. (1993). The sonar of dolphins. New York: Springer.Find this resource:

Branstetter, B. K., & Mercado, E., III. (2006). Sound localization by cetaceans. International Journal of Comparative Psychology, 19, 25–61Find this resource:

Cranford, T. W., Krysl, P., & Hildebrand, J. A. (2008). Acoustic pathways revealed: Simulated sound transmission and reception in Cuvier’s beaked whale (Ziphius cavirostris). Bioinspiration and Biomimetics, 3(1).Find this resource:

Erulkar, S. D. (1972). Comparative aspects of the spatial localization of sound. Physiological Review, 52, 237–360Find this resource:

Madsen, P. T., Wahlberg, M., & Møhl, B. (2002). Male sperm whale (Physeter macrocephalus) acoustics in a high-latitude habitat: Implications for echolocation and communication. Behavioral Ecolology & Sociobiolology, 3, 31–41Find this resource:

Nachtigall, P. E., & Supin, A. Ya., (2013). A false killer whale reduces its hearing sensitivity when a loud sound is preceded by a warning. Journal of Experimental Biology, 216, 3062–3070.Find this resource:

Norris, K. S. (1969). The echolocation of marine mammals. In H. T. Andersen (Ed.), The biology of marine mammals (pp. 391–424). New York: Academic Press.Find this resource:

Renaud, D. M., & Popper, A. N. (1975) Sound localization by the bottlenose porpoise Tursiops truncatus. Journal of Experimental Biology, 63, 569–585.Find this resource:

Supin, A. Ya., Nachtigall, P. E., Au, W. W. L., & Breese, M. (2004). The interaction of outgoing echolocation pulses and echoes in the false killer whale’s auditory system: Evoked potential study. Journal of the Acoustical Society of America, 115, 3218–3225.Find this resource:

Surlykke, A., Nachtigall, P. E., Popper, A. N., & Fay, R. (2014). BioSonar. New York: SpringerFind this resource:

References

Au, W. W. L. (1980). Echolocation signals of the Atlantic bottlenose dolphin (Tursiops truncatus) in open waters. In R. G. Busnel & J. F. Fish (Eds.), Animal sonar systems (pp. 251–282). New York: Plenum Press.Find this resource:

Au, W. W. L. (1993). The sonar of dolphins. New York: Springer-Verlag.Find this resource:

Ayrapetyants, A. I., & Konstantinov, A. I. (1974). Echolocation in nature. Isdatel’stvo Nauka (in Russian). English Translation, Joint Publications Research Service.Find this resource:

Belkovich, V. M., & Dubrovskiy, N. A. (1976). Sensory bases of cetacean orientation. Moscow, Russia: Isdatel’stvo Nauka. (In Russian) English Translation, Joint Publications Research Service.Find this resource:

Branstetter, B. K., & Mercado, E., III. (2006). Sound localization by cetaceans. International Journal of Comparative Psychology, 19, 25–61.Find this resource:

Busnel, R. G. (1966). Animal sonar systems: Biology and bionics (Vols. 1 and 2). Jouy-en-Josas, France: NATO Advanced Studies Institutes.Find this resource:

Busnel, R. G., & Fish, J. F. (1980). Animal sonar systems, New York: Plenum Press.Find this resource:

Butler, R. A. (1969). Monaural and binaural hearing in noisebursts vertically in the median sagittal plane. Journal of Auditory Research, 3, 20–335.Find this resource:

Cranford, T. W., Amundine, M., & Norris, K. S. (1996). Functional morphology and homology in the odontocete nasal complex: Implications for sound generation. Journal of Morphology, 228, 223–285.Find this resource:

Cranford, T. W. (1999). The sperm whale’s nose: Sexual selection on a grand scale. Marine Mammal Science, 15, 1133–1157.Find this resource:

Cranford, T. W., Elsberry, W. R., Van Bonn, W. G., Jeffress, J. A., Chaplin M. S., Blackwood, et al. (2013). Observation and analysis of sonar signal generation in the bottlenose dolphin (Tursiops truncatus): Evidence for two sonar sources. Journal of Experimental Marine Biology and Ecology, 407, 81–96.Find this resource:

Cranford, T. W., Krysl, P., & Hildebrand, J. A. (2008). Acoustic pathways revealed: Simulated sound transmission and reception in Cuvier’s beaked whale (Ziphius cavirostris). Bioinspiration and Biomimetics, 3(1).Find this resource:

Erulkar, S. D. (1972). Comparative aspects of the spatial localization of sound. Physiological Review, 52, 237–360.Find this resource:

Evans, W. E. (1973). Echolocation by marine delphinids and one species of fresh-water dolphin. Journal of the Acoustical Society of America, 54, 191–199.Find this resource:

Johnson, C. S. (1966). Sound detection thresholds in marine mammals. In W. Tavolga (Ed.), Marine bioacoustics (pp. 247–260). New York: Pergamon Press.Find this resource:

Kellogg, W. N. (1958). Echo ranging in the porpoise. Science, 128, 982–988.Find this resource:

Kick, S.A., & Simmons, J. A. (1984). Automatic gain control in the bat’s sonar receiver and the neuroethology of echolocation. Journal of Neuroscience, 4, 2725–2737.Find this resource:

Kloepper, L. N., Buck, J. R., Smith, A. B., Supin, A. Ya., Gaudette, J. E., & Nachtigall, P. E. (2015). Support for the beam focusing hypothesis in the false killer whale. Journal of Experimental Biology, 218, 2455–2462.Find this resource:

Kloepper, L. N., Nachtigall, P. E., Donahue, M. J., & Breese, M. (2012). Active echolocation beam focusing in the false killer whale (Pseudorca crassidens) Journal of Experimental Biology, 215, 1306–1312.Find this resource:

Kyhn, L. A., Jensen, F. H., Beedholm, K., Tougaard, J., Hansen, M., & Madsen, P. T. (2010). Echolocation in sympatric Peale’s dolphins (Lagenorhynchus australis) and Commerson’s dolphins (Cephalorynchus commersonii) producing narrow-band high- frequency clicks. Journal of Experimental Biology, 213, 1940–1949.Find this resource:

Madsen, P. T., Johnson, M., Aguilar de Soto, N., Zimmer, W. N., & Tyack, P. (2006). Biosonar performance of foraging beaked whales (Mesoplodon densirostris). Journal of Experimental Biology, 208, 181–194.Find this resource:

Madsen, P. T., Kerr, I., & Payne, R. (2004). Echolocation clicks of two free-ranging delphinids with different food preferences: False killer whales Pseudorca crassidens and Risso’s dolphins, Grampus griseus. Journal of Experimental Biology, 207, 1811–1823.Find this resource:

Madsen, P. T., Lammers, M., Wisniewska, D., & Beedholm, K. (2013). Nasal sound production in echolocating delphinids (Tursiops truncatus and Pseudorca crassidens) is dynamic, but unilateral: Clicking on the right side and whistling on the left side. The Journal of Experimental Biology, 216, 4091–4102.Find this resource:

Madsen, P. T., Wahlberg, M., & Møhl, B. (2002). Male sperm whale (Physeter macrocephalus) acoustics in a high-latitude habitat: Implications for echolocation and communication. Behavioral Ecolology Sociobiology, 3, 31–41.Find this resource:

Mass, A., & Supin, A. Ya. (2002). Visual field organization and retinal resolution of the beluga. Delphinapterus leucas. Aquatic Mammals, 28(3), 241–250.Find this resource:

Mills, A. W. (1958). On the minimum audible angle. Journal of the Acoustical Society of America, 30, 237–246.Find this resource:

Møhl, B., & Anderson, S. (1973). Echolocation high frequency component in the click of the harbour porpoise Phocoena phocoena. Journal of the Acoustical Society of America, 54, 1368–1372.Find this resource:

Møhl, B., Au, W. W. L., Pawloski, J. L., & Nachtigall, P. E. (1999). Dolphin hearing: Relative sensitivity as a function of point of application of a contact sound source in the jaw and head region. Journal of the Acoustical Society of America, 105, 3421–3424.Find this resource:

Møhl, B., Wahlberg, M., & Madsen, P. (2003). The monopulsed nature of sperm whale clicks. Journal of the Acoustical Society of America, 114, 1143–1154.Find this resource:

Moore, P. W. B., & Au, W. W. L. (1975). Underwater localization of pulsed pure tones by the California sea lion (Zalophus californianus). Journal of the Acoustical Society of America, 58, 721–727.Find this resource:

Norris, K. S. (1968). The evolution of acoustic mechanisms in odontocete cetaceans. In E. T. Drake (Ed.), Evolution and environment: A symposium (pp. 297–324). New Haven, CT: Yale University Press.Find this resource:

Norris, K. S. (1969). The echolocation of marine mammals. In H. T. Andersen (Ed.), The biology of marine mammals (pp. 391–424). New York: Academic Press.Find this resource:

Norris, K. S., Prescott, J. H., Asa-Dorian, P. V., & Perkins, P. (1961). An experimental demonstration of echolocation behavior in the porpoise, Tursiops truncatus (Montagu). Biological Bulletin, 120(2), 163–176.Find this resource:

Nachtigall, P. E. (1980). Odontocete Echolocation performance on object size, shape, and material. In R. G. Busnel & J. F. Fish (Eds.), Animal Sonar Systems (pp. 71–95). New York: Plenum Press.Find this resource:

Nachtigall, P. E.Au, W. W. L., Roitblat, H. L., & Pawloski, J. L. (2000). Dolphin biosonar: A model for biomimetic sonars. In: M. Nagai (Ed.), Proceedings of the First International Symposium on Aqua Bio-Mechanisms (pp. 115–121). Honolulu, HA: Tokai University.Find this resource:

Nachtigall, P. E., & Moore, P. W. B. (1988). Animal sonar: Processes and performance. New York: Plenum Press.Find this resource:

Nachtigall, P. E., & Supin, A. Ya. (2008). A false killer whale adjusts its hearing when it echolocates. Journal of Experimental Biology, 211, 1714–1718.Find this resource:

Nachtigall, P. E., & Supin, A. Ya. (2013). A false killer whale reduces its hearing sensitivity when a loud sound is preceded by a warning. Journal of Experimental Biology, 216, 3062–3070.Find this resource:

Nachtigall, P. E., & Supin, A. Ya. (2015). Conditioned frequency dependent hearing sensitivity reduction in the bottlenose dolphin (Tursiops truncatus). Journal of Experimental Biology, 218, 999–1005.Find this resource:

Nachtigall, P. E., Supin, A. Ya., Estaban, J. A., & Pacini, A. F. (2016). Learning and extinction of conditioned hearing sensation change in the beluga whale (Delphinapterus leucas). Journal of Comparative Physiology A, 202(2), 105–113.Find this resource:

Norris, K. S. (1969). The echolocation of marine mammals. In H. T. Andersen (Ed.), The biology of marine mammals (pp. 391–423). New York: Acedemic Press.Find this resource:

Oelschläger, H. H. A., & Kemp, B. (1998). Ontogenesis of the sperm whale brain. Journal of Comparative Neurology, 399, 210–228.Find this resource:

Pacini, A. F., Nachtigall, P. E., Quintos, C., Schofield, D., Look, D. A., Levine, G., et al. (2011). Audiogram of a stranded Blainville’s beaked whale (Mesoplodon densirostris) measured using auditory evoked potentials. Journal of Experimental Biology, 214, 2409–2415.Find this resource:

Penner, R. H. (1988). Attention and detection in dolphins. In P. E. Nachtigall & P. W. B. Moore (Eds.), Animal sonar: Processes and performance (pp. 707–713). New York: Plenum Press.Find this resource:

Purves, P. (1967). Anatomical and experimental observation on the cetacean sonar system. In R. G. Busnel (Ed.), Animal sonar systems: Biology and bionics (Vols. 1 & 2, pp. 197–270). Jouy-en-Josas, France: NATO Advanced Studies Institutes.Find this resource:

Renaud, D. M., & Popper, A. N. (1975). Sound localization by the bottlenose porpoise Tursiops truncatus. Journal of Experimental Biology, 63, 569–585.Find this resource:

Roitblat, H. L., Au, W. W. L., Nachtigall, P. E., Shizamura, R., & Moons, J. (1995). Sonar recognition of targets embedded in sediment. Neural Networks, 8, 1263–1273.Find this resource:

Suga, N., & Jen, P. H. (1975). Peripherla control of acoustic signals in the auditory system of echolocating bats. Journal of Experimental Biology, 62, 277–311.Find this resource:

Supin, A. Ya., Nachtigall, P. E., Au, W. W. L., & Breese, M. (2004). The interaction of outgoing echolocation pulses and echoes in the false killer whale’s auditory system: Evoked potential study. Journal of the Acoustical Society of America, 115, 3218–3225.Find this resource:

Supin, A. Ya., Nachtigall, P. E., Au, W. W. L., & Breese, M. (2005). Invariance of echo-responses to target strength and distance in an echolocating false killer whale: evoked potential study. Journal of the Acoustical Society of America, 117(6), 3928–3935.Find this resource:

Supin, A. Ya., Nachtigall, P. E., & Breese, M. (2006). Source level to sensation level ratio of transmitted biosonar pulses in an echolocating false killer whale. Journal of the Acoustical Society of America, 120, 518–526.Find this resource:

Supin, A. Ya., Nachtigall, P. E., Pawloski, J. E., & Au, W. W. L. (2003). Evoked potential recording during echolocation in a false killer whale Pseudorca crassidens. Journal of the Scoustical Society of America, 113, 2408–2411.Find this resource:

Surlykke, A., Nachtigall, P. E., Popper, A. N., & Fay, R. (Eds.). (2014). BioSonar. New York: SpringerFind this resource:

Taylor, K. A. (2013). Directional hearing and a head-related transfer function (HRTF) of a bottlenose dolphin (Tursiops truncatus) (PhD thesis, University of Hawaii). UMT Dissertation Publishing, Ann Arbor, Michigan.Find this resource:

Turl, C. W., Penner, R. H., & Au, W. W. L. (1987). Comparison of target detection capabilities of the beluga and bottlenose dolphin. Journal of the Acoustical Society of America, 68, 497–502.Find this resource:

Varanasi, U., & Malins, D. C. (1972). Triacylglycerols characteristics of porpoise acoustic tissues: Molecular structure of diisovaleroylglycerides. Science, 176, 926–928.Find this resource:

Yanagisawa, K., Sato, G., Nomoto, M., Katsuki, Y., Ikezono, E., Grinnell, A. D., et al. (1966). Federation proceedings. Physiology (Abstract), 1539.Find this resource:

Yuen, M. E., Nachtigall, P. E., Supin, A. Ya., & Breese, M. (2005). Behavioral and auditory evoked potential audiograms of a false killer whale (Pseudorca crassidens). Journal of the Acoustical Society of America, 118, 2688–2695.Find this resource: