Most terrestrial mammals rely heavily on vision and ; smell. These senses are limited in water by the absorption of light and the slow physical movement of water, respectively. As a result, marine mammals have evolved to use sound and hearing as their primary means of communication and sensing their world.
This article briefly reviews basics of sound and the physical ways in which sounds are produced by marine mammals. The main focus is on characteristics of sounds made internally by marine mammals. Certain species stand out as particularly unusual or particularly well studied, and these get special attention. Other species are treated in taxonomic groups, when their acoustic characteristics are similar or less well known. Especially whales and dolphins often leap clear of the water or slap tail or flippers onto the water surface, creating percussive sounds. These sounds are variably thought to be expressions of playing, socializing, or aggressiveness. They are not treated in detail here.
I. Fundamentals of Sound
Imagine throwing a rock into a calm lake. You can easily picture the ripples, or water waves, that move out in an expanding circle. In these ripples, the water’s surface moves up and down, in a smooth progression from crest to trough. Sound waves are similar to these water waves. The “crests” of a sound wave are areas of high pressure, and the “troughs” are areas of low pressure. Like the water wave, there is a smooth progression between these areas of high and low pressure. A sound wave is a propagating (moving forward) alternation of these areas of high and low pressure. The wave is formed by a structure that vibrates, such as a radio loudspeaker or our larynx.
Several major terms are used to describe the characteristics of sound. The amount of time it takes for a complete cycle between the highest pressure to the lowest, and back to the highest, is referred to as the period of the wave and is measured in seconds. The reciprocal of that time measurement, the period, is called the frequency of the wave, measured in seconds-1, or more commonly hertz (Hz). The longer the period, the fewer number of cycles will occur in a fixed amount of time, and the lower the frequency of the sound. In music, this low frequency is called one with low pitch, or a bass sound. High-pitched sounds of a flute or violin are high in frequency. Frequency is a physical characteristic of sound, whereas pitch is our perception of sound. Humans hear from about 18 to 20,000 Hz (or 20 kHz). Therefore, sounds below 18 Hz are termed “infrasound,” whereas those above 20 kHz are termed “ultrasound.”
Marine mammalogists often want to know the loudness of a sound, whether produced by a whale, dolphin, ship, or oil rig. The loudness, or amplitude, of a sound is described in decibels (dB), but “in-air” decibels and “in-water” decibels are different from each other. In water, sound amplitude is measured and referred to as a certain number of dB references to one mi-cropascal. This is usually written XX dB re 1 jxPa. Because sound amplitude decreases with distance, the standard of describing amplitude is usually referred to as 1 m from the sound source, or XX dB re 1 jxPa at 1 m. Sounds that are not very loud tend to be below 100 dB, and very loud sounds are above 160 to 180 dB.
A signal is said to be frequency modulated (FM) when its frequency changes over time. Dolphin whistles are usually frequency modulated. Amplitude-modulated (AM) signals are those where the amplitude changes over time. Many mysticete calls are amplitude modulated and sound like “growls.”
When one examines a display of sound waves per time, or a spectrogram, one often sees “extra lines” above the main “line” of the spectrogram. The “main line” of the spectrogram is the lowest frequency contour, termed the fundamental frequency. Additional “lines” about the fundamental frequency represent the harmonics. Harmonics are integer multiples (e.g., 2X, 3X, 4x) of the fundamental frequency. They are the result of the physical characteristics of the sound-producing structure, and they alter the sound. Harmonics occur with frequency-modulated calls and ar e stricdy integer multiples of die fundamental frequency. Amplitude-modulated calls frequently have a stack of closely spaced bands that look like harmonics, but are side bands that are the product of die rate of amplitude (loudness) modulation (Fig. 1).
II. Sound Production Mechanisms
A. Humans
Unlike most marine mammals, humans exhale to vocalize. The energy for vocalization conies from exhaling. The lungs force air through the larynx. The vocal cords in the larynx open and close as the air rushes past them, breaking the exhalation up into a series of air puffs, or an undifferentiated sound. These air pulses then pass through the vocal tract of the throat, tongue, mouth, and lips. All of these structures move during speech to change the shape of vocal tract, literally shaping the buzzing sound from the larynx into speech.
B. Dolphins
There has been considerable debate over the sound production mechanism in toothed whales, or odontocetes. Only recent work has begun to clarify the issue. As in humans, the energy for vocalizations comes from pushing air. The similarity ends there, as odontocetes lack vocal cords. Odontocetes have a structure in the upper portion of their heads called dorsal bursae that have structures protruding into the nasal passage called phonic lips. Air appears to be pushed past these phonic lips, and the result is that they slap together and send the neighboring tissue into vibration. Once past the phonic lips, the air enters the vestibular sac, just below the blowhole. The air can either be pushed back into the lower nasal passage or it may be released into the water. Whistling dolphins sometimes emit bubble streams. All odontocetes, except the sperm whale (Physeter macrocephalus), have two of these dorsal bursae/phonic lip structures. It appears that they can operate the two structures independently, creating two different sounds simultaneously. Toothed whales produce clicks, click trains (often so rapid as to be heard as a “buzz”), and—especially many species of dolphins—whistles. Some but not all click types are used for echolocation to scan the environment, as also in bats.
Once the sound is produced, it is directed out into the water through a structure called the melon. The melon sits on top of the skull, behind the rostrum of dolphins. The melon is a complex structure that couples the vibrations produced by the dorsal bursae/phonic lips complex to the water. It also functions as an acoustic lens to “focus” clicks into a beam. This is similar in function to the focusing of light into a beam by the lens and reflector of a flashlight (Fig. 2).
C. Baleen Whales
There is no equivalent in mysticetes to the dorsal bursae/phonic lip structure found in odontocetes. Mysticetes have a larynx, but it lacks the vocal cords found in humans. It is likely that the larynx does have a sound production function, but it remains undetermined. Cranial sinuses are also suspected to play a part in vocal production, but the details remain uncertain. Visual observations of singing humpbacks reveal that they do not exhale, even while singing for 20 min or longer.
Figure 1 Spectrogram of part of a humpback whale (Megaptera novaeangliae) song. The first sound is shown as a broad, fuzzy structure, typical of amplitude modulated sounds. The second sound, the “V”-shaped structure, is a frequency modulated sound.
Figure 2 Diagram of sound production structures in the head of a dolphin.
This indicates that they are recycling air within their body to vocalize.
D. Sirenians and Carnivores (Pinnipeds, Polar Bear, and Sea/Marine Otters)
Noncetacean marine mammals appear to make sounds similar to those of their terrestrial relatives, generally by vibrations in the throat. Sea lions (Otariidae) bark underwater, and manatees (Trichechus spp.) and dugongs (Dugong dugon) have a rich repertoire of sounds. Underwater, these sounds are generally made without air being released from the mouth, and it is surmised that air is shunted between the lungs and mouth/nasal structures.
III. Characteristics of Vocalizations by Group and Selected Species
A. Pinnipeds
1. Phocid Seals Phocid, or true, seals live in a wide variety of environments, from tropical islands to the ice packs of the Arctic and Antarctic. While the underwater sounds of all species have not been described in detail, it is likely that all make underwater sounds. In-air sounds tend to consist of barks or growls, sometimes produced at the surface but more usually produced while mating and pupping on land or ice. Such sounds are often aggressive or warning signals, as when, for example, a human approaches an animal too closely. Pups tend to have higher frequency in-air “mew” sounds, apparently useful for mother/pup interactions and potential pup recognition. Underwater sounds are described in more detail later.
a. weddell seals (leptonychotes weddellll) Wed-dell seals are a very vocal species. Their repertoire has been categorized into 12 calls, labeled by letters, and subdivided into 34 types. These calls range between 100 Hz and 12.8 kHz. The function of some of these calls has been suggested. T calls are long downsweeps and are thought to function in territorial advertisement. C calls are pulses of intermediate frequency, which appear to be used as an aggressive display. M calls are a long low-frequency tone, and H calls are low-frequency pulses. Both M and H calls are thought to be used as a high-intensity threat. G and L calls are both low-frequency-modulated sweeps, thought to be used as a low-intensity threat. Functions have not been proposed in similar detail for other phocid species.
Calling rates are lowest in winter and highest in spring. It has been suggested that calls produced from the pupping season through the mating period function as male advertisement “song.” Weddell seals also make numerous in-air vocalizations during this time period that sound similar to those produced underwater, a richer in-air repertoire than produced by most (and possibly all) other phocid seals. Recordings of Weddell seals at different locations indicate that there are geographic differences in calls between breeding populations.
b. leopard seals (hydrurga leftonyx) Recordings of a captive leopard seal included vocalizations reaching as high as 164 kHz. These included frequency-modulated chirps, buzzes, and a click train. The presence of ultrasonic clicks suggested a possible echolocation function, but no data support echolocation in leopard or any other seals.
As in Weddell seals, recordings of leopard seals made in distant locations showed differences in the calls between the two areas. The repertoire of leopard seals shows considerable variability. Their calls range from low-frequency tonal calls, both narrowband and wideband high-frequency pulses, and frequency-modulated calls ranging from 500 Hz to 8 kHz. The most frequent calls of leopard seals are surprisingly soft, given its role as a top-level predator. Many other seals, including the Weddell seal, produce harsh calls during aggressive interactions. It has been suggested that the leopard seals solitary existence reduced the need for territorial calls. However, when hauled out on ice or land, leopard seals that were approached by a researcher made explosive, broadband vocalizations termed “blasts” and “roars.”
c. bearded seals (erignathus barbatvs) Like Weddell seals, bearded seals are well known for their long calls and songs. Bearded seals produce distinctive trills, which typically consist of a series of discrete frequency sweeps. Trills can begin at 2.5 kHz and gradually sweep down in frequency to a few hundred hertz. Most trills are characterized by decreasing frequency, but some variations can have near constant frequency or even alternations of frequency increases and decreases. Trills last from 4 to 16 sec. In some populations, the long trill is followed by a rapid upsweep to 3 kHz and lasts 1-2 sec. The vocalizations of bearded seals are thought to function as male advertisement displays during the mating season (Fig. 3).
d. ringed seals (pusa hisfida) Ringed seals, like many seals, were long thought to be silent. However, they are now known to produce at least four types of calls. These are low-and high-frequency barks, frequency-modulated tones between 2 and 4 kHz, broadband growls that range up to 6 kHz, and frequency-modulated chirps. It is likely that ringed seals produce higher frequency calls that have not been recorded, as their best hearing sensitivity is at 45 kHz. Animals usually have their best hearing in the same frequency range in which they vocalize. Source levels for all of the recorded ringed seals are relatively low, between 95 and 130 dB re 1 (xPa. None of the recorded calls occurred exclusively within the breeding season. The proportion of calls produced did vary with season, however.
Figure 3 The long downward trill and rapid upsweep of a bearded seal from Alaska is shown in this spectrogram.
e. hooded seals (cystophora cristata) The acoustic repertoire of hooded seals can be grouped into three major classes. Class A and B signals are produced by normal vocal mechanisms, whereas class C signals are produced by the hood and septum, a set of specialized anatomical structures in this species. Class A calls tend to be the most common vocalization and are produced both in air and underwater. All of these calls are pulsed and rarely frequency modulated, with energy ranging from 500 Hz to 6 kHz. Class A calls are used in a variety of circumstances, including female responses to displaying males, who also make a variety of A calls. Female and pup interactions also use A calls. Class B calls are described as growls or roars. These growls tend to be made by females fighting with males and by males fighting with other males. Other variants of B calls are used as low-level threats. Class C signals are produced by the inflation and deflation of the hood and septum. They are short-duration, broadband with rapid onsets, and little or no frequency modulation. These calls have been described as “bloops,” “wooshes, and metallic “pings,” clicks, and “knocking” sounds. It is possible that only males make class C sounds.
f. harp seals (PAGOPH1LUS GROENLAND1CUS) Harp seals aggregate at the ice edge in March in the northwest Atlantic. At least 19 different call types have been described for the species. The call types range from a nearly pure sine wave to pulsed sounds, high-frequency chirps, broadband “warbles,” trills, squeaks, and grunts. The maximum source level of these calls is between 135 and 140 dB re 1 |xPa. Harp seals also produce clicks that are about 25 dB louder than their other calls. A long-term observation has shown that within one breeding area these call types are stable over a period of tens of years. The calls may help individuals locate the herd; harp seal aggregations can be heard from 30 to 60 km away. Once in the aggregation, calls may be used to find a mate. Comparisons of different breeding aggregations found many shared calls and some that were unique to the breeding areas, again suggesting that there may be distinct breeding populations. In-air recordings revealed that harp seal pups have an unusually wide variety of vocalizations. These tend to be longer than calls from other phocids and are very complex, showing a wide variety of frequency and amplitude modulation.
g. elephant seals (MiROVNCA spp.) Elephant seals mate on land and males compete for dominance, and thereby access to females. Males use threat displays and actual fights to establish dominance. Male elephant seals make three main types of calls during aggression; “snoring,” “snorting,” and “clap threatening.” “Snoring” is used as a low-intensity threat, and dominant males “snort” more aggressively when approached by a challenging male. Snorts range between 200 and 600 Hz. The “clap threat” ranges up to 2.5 kHz. It is thought that in-air threat calls produced by males are also transmitted through the ground, and these seismic signals can produce responses from other elephant seals. Females produce a low-frequency “belch roar” in aggressive situations and a 500 Hz to 1 kHz bark to attract the pup. Pups produced a higher frequency, up to 1.4 kHz, call that is used to maintain contact with the mother or to elicit attention. As in other seal species, both the mother’s and the pup’s call have individual characteristics that are used to recognize each other acoustically.
Underwater sounds have been recorded, but only described cursorily as sounding like a bell, cymbal, or guitar.
h. walruses (odobenus rosmarus) Social interactions between walruses hauled out on the ice often include vocalizations. Adults use roars, grunts, and guttural sounds as threats. Roars are long, loud calls that last a second or more and have most of their energy at low frequency. Grunts are brief calls lasting between 100 and 400 msec and vaiy greatly in amplitude. Grunts range from 50 to 250 Hz. Guttural sounds are the most common threat vocalization, consisting of a series of low-frequency, wideband pulses. These can range from 13 Hz to 4 kHz. Barks are short, frequency-modulated calls that range from 90 to 260 msec in length and between 300 and 500 Hz. They are frequently given as a series. Barks are used by adults to indicate submission, and louder barking may indicate more submission. Calves bark in a wider variety of situations. Calves separated from their mother bark loudly and then may continue to bark softly once they are rejoined. The structure of the bark changes as the calf matures, gradually becoming a longer single call, with both frequency and amplitude modulation. Females produce a soft short call between 0.3 and 1.0 sec long. The call is usually frequency modulated, either as a downsweep or as an alternation of up-and-down sweeps. This call serves as a female contact call, produced when female and pup are in close proximity to each other. Females do not have a loud contact call to attract the calf, as in some other phocid species.
Males on the mating grounds produce a gong-like sound as a courting display, both in air and underwater. This sound is produced by inflated throat pouches, at times augmented by flippers striking the throat. Male walruses also make aggressive clacking sounds with their teeth.
2. Otariid Seals: Sea Lions and Fur Seals While a considerable detail of sounds for several select phocids has been presented, relatively little time has been spent on eared seals. Most of them are known to make bark-like sounds or other “groans and grunts” in air, and the barks of a group of hauled-out California sea lions (Zalophus californianus) are loud and far-reaching (to at least 3 km on a still night). Barks tend to have most energy below 2 kHz. These sounds and other interactions result in a physical structuring of the society on a beach or headland. Sea lions also bark underwater, in similar fashion as in air, but otariids tend not to have the complex social signals of many phocids. This is probably because those phocids tend to mate in the water, and sounds are often, although not always, related to social/sexual interaction. Otariids, however, tend to mate on land, and they are in large part relatively quiet in the sea.
Nevertheless, there are sets of clicks, snorts, bleats, and growls produced underwater by Steller sea lions (Eumetopias jubatus), and clicks and high-frequency “sheep-like” bleating sounds by northern fur seals (Callorhimis ursinus). The clicks of some species have led some researchers to postulate that otariid seals might echolocate, but repeated investigations in captivity have not shed light on this possibility. If they do use echoes for environmental information (and they are likely to do so at a very basic level, at least), this is not nearly as sophisticated as the echolocation capability of many dolphins and bats.
B. Carnivores
1. Sea Otters (Enhydra lutris) Sea otters produce airborne sounds that have been described as whines, whistles, growls, cooing sounds, chuckles, and snarls. They may produce harsh screams when stressed. Airborne vocalizations serve to maintain the mother-pup bond. When a modier dives, the pup at the surface often vocalizes continuously until the mother resurfaces. If the mother does not find the pup upon surfacing, she vocalizes and the pup responds. Pups also vocalize to elicit nursing or grooming. The frequencies of these calls lie between 3 and 5 kHz. No underwater vocalizations have been recorded, although they may exist.
2. Polar Bears (Ursus maritimus) Polar bears may not be quite as vocal as many other carnivores. Males chuff and snort, with powerful rapid exhalations, especially in competitive interactions with other males. Females produce low mew-like calls that may be used for mother/pup recognition.
C. Cetaceans
1. Baleen Whales
a. gray whales (eschr1cht1vs robustvs) Gray whales most frequently produce sounds referred to as “knocks” and pulses. These range in frequency from < 100 Hz to 2 kHz. A series 2-30 pulses last an average of 1.8 sec. Knocks are most common when gray whales are feeding. They are fairly vocal while feeding, relatively quiet while migrating, and most vocal during mating activities in Mexican waters. The source levels of gray whale vocalizations range between 167 and 188 dB re 1 jxPa.
Four major signal types have been recorded from migrating gray whales. The first is composed of clicks and metallic-sounding “boings.” Boings consist of 8-14 pulses in bursts of up to 2 sec. The frequencies range from below 100 Hz to above 10 kHz. The second sound is a continuous low-frequency moan, ranging between 100 and 200 Hz. The third is another moan with a pulsed structure. The fourth is a pulsed “grunt,” a broadband noise, produced by underwater exhalations. The first two types have been recorded predominantly from whales migrating offshore, in deeper water. Whales migrating nearer to shore in shallower water predominantly make the latter two sounds.
Click trains have been recorded from gray whales in Mexico, off Vancouver Island, and from the captive gray whale “Gigi.” The click trains range from 2 to 6 kHz and last between 1 and 2 msec. Between 9.5 and 36 clicks/sec are produced.
b. fin and blue whales (balaenoptera physalvs and b. musculvs) Fin and blue whales are the two largest species of extant cetaceans. These two species share the common characteristic of producing very low-frequency sounds. Both of these species are well known as sources of “20-Hz” sounds. In fact, both of these species do make calls in this extremely low-frequency region, but their range is wider than initially thought.
While fin and blue whales share their low-frequency characteristics, their calls differ in length. Fin whales produce primarily low-frequency downsweeps that are about 1 sec in length, whereas 20-Hz blue whale calls are typically 20 sec in length. Calls from both of these species generally occur in long, regularly spaced patterns. Sometimes the pattern includes “doublets,” i.e., a double pulse with a longer interval between successive doublets.
The frequency range of these calls varies in different ocean basins. Most fin whale calls from the Atlantic are 1-sec down-sweeps from -23 to -18 Hz. These “20-Hz” pulses regularly occur as a long, regular patterned series of calls. The interval between pulses typically ranges from 6 to 37 sec.
These calls are so low in frequency that they are detected on seismic equipment (geophones). It has been suggested that low-frequency sounds occur predominantly in winter and spring, during the mating time. However, fin whales are known to produce 20-Hz signals year-around, and if their calls are used as a reproductive display, then fin whales may be advertising constantly.
Atlantic fin whales also produce higher frequency calls, usually downsweeps, from 100 to 30 Hz. None of these appear to be produced in a regular manner of the 20-Hz pulses. It has been suggested that these calls are used for social communication. Fin whales also produce low-frequency broadband rumbles, centered around 30 Hz. It has been suggested that these calls indicate that the whale has been “surprised,” as it was recorded when whales were near drifting ships or other objects. The 30-Hz rumble has also been recorded during social interactions between fin whales. Impulsive sounds have been associated with feeding and may be the result of bioinechani-cal action rather than vocalization.
Blue whale calls are much longer than fin whale calls. Blue whale calls share two common characteristics: a fundamental frequency between about 10 and 40 Hz and a long duration between 10 and 30 sec. Variations on this theme are found. Calls recorded off Chile had fundamentals as low as 12.5 Hz and the harmonics ranged up to 200 Hz. These three-part calls lasted an average of 36.5 sec. All three parts of the call were amplitude modulated. These low-frequency moans were accompanied by short 390-Hz pulses.
Blue whales in the Indian Ocean are reported to produce a song, or repeated sets of sounds. These songs consist of four distinct notes. The first, second, and fourth notes are pulsive while the third is a pure tone. The total length of the four notes is approximately 2 min. Song has not been reported for any other population, and it is possible that song may have been recorded from pygmy blue whales (B. in. brevicauda).
Blue and fin whale calls are loud and of generally low frequency. These characteristics allow the calls to travel over great distances, and the sounds of these whales have been recorded to be heard at least several hundred kilometers away. It has been hypothesized that whales may hear each other over extents of ocean basins, especially if sounds are channeled into depths of water where characteristics of temperature and pressure interact to “carry” the sounds efficiently. Even if this occurs infrequently, the normally long distances of communication capability indicate that these whales may be considering themselves as parts of an “acoustic herd” over at least 100 or 200 km and may be exchanging basic information about the whereabouts of food or mating opportunities from afar. Research is only now delving into this possibility, although it was presented as a hypothesis by Roger Payne and Douglas Webb in the 1970s.
c. minke whales (b. acutorostrata and b. bonaeren-sis) Minke whales are known to produce a variety of different calls and show significant geographic variation in their call structure. Minke whales are difficult to observe in the wild and therefore it has taken many years to even associate some call types with minke whales. Others have only been described in recent years and others almost certainly remain undiscovered. The one seemingly consistent feature of their vocalizations is a low-frequency, short-duration downsweep. This downsweep generally descends from about 250 to 50 Hz and lasts between 0.2 and 0.3 sec. Australian minke whales (B. acutorostrata unnamed subsp.) make a vocalization so unusual that it has been termed the “star wars” call. This call consists of a series of three 100-msec pulses ranging between 50 Hz and 9.4 kHz. These pulses are produced simultaneously with harmonically unrelated low-frequency, amplitude-modulated pulses between 50 and 750 Hz. Following the pulses, the whale produces a pulsed tone at 1.8 kHz along with a tonal call at 80 Hz. The tonal call shifts up to 140 Hz as the final component of the complex set of vocalizations. The communicative purpose is unknown.
d. humpback whales (megaptera novaeangliae) Two baleen whales are known to repeat sets of notes in predictable fashion, or sing. There may be others. The iour-note song of Indian Ocean blue whales was mentioned earlier. However, humpback and bowhead whales (discussed later) are well known for their wide vocal repertoires.
Roger Pavne and Scott McVav first described the songs of humpback whales in 1971. Only males sing, almost exclusively on the mating grounds in winter, and it is surmised that song is a mating display; intersexual, for males to attract females; in-trasexual, as a male dominance display; or both. Humpback whale songs have a hierarchical structure, from the shortest utterance to long bouts of singing that can last for days. Individual calls (somewhat analogous to musical notes) are referred to as song units. These units are repeated and combined to form phrases. These phrases are repeated to form longer themes. A song is typically composed of between 4 and 12 themes. Songs can last from 5 to 30 min in length before beginning again. Individual humpbacks are known to sing for as short as a few minutes and for 48 hr or longer. There is a tremendous variety of song units, including upsweeps, downsweeps, and complex FM sweeps. Numerous types of amplitude-modulated signals are produced, sometimes described as moans, grunts, rumbles, and ratchets (Fig. 4).
Song units range widely in frequency, from about 20 Hz all the way up to 10 kHz. Individual units can range Irom fractions of a second to several seconds in length.
Individual whales slowly change the structure of their songs over time. To illustrate this, consider a theme with two upsweeps and a growl. One type of change would be the addition ol a third and then a fourth upsweep. Alternatively, the FM upsweeps might exhibit less and less change in frequency until they become pure (constant frequency) tones. These could then actually reverse their frequency modulation and gradually become downsweeps. These changes typically occur gradually, over a period of about 1 month. However, the pace of change in song structure is variable as well. In some years the song changes slowly and in other years it evolves rapidly. It is not known what is responsible for this variation in rate. Whales of an area pay attention to and copy each other so that all whales of a population sing essentiallv the same song, with only minor variations.
Once they have evolved, individual themes do not appear to be reused. All of the themes are created de novo. A comparison of 19 years of songs recorded from the west Atlantic found that while general types of song units do reoccur, none of the same combinations ever reappeared.
Humpback whales also produce a rich repertoire of non-song vocalizations, generally termed social sounds. Social sounds can be thought of a subset of the song units, uttered in a nonpatterned fashion. On the mating grounds, these sounds appear to be used as acoustic threat displays in conjunction with visual displays and direct physical contact.
Finally, humpbacks produce a third class of calls, known as feeding calls. Humpbacks feed through a variety of lunges through the water at different orientations. Their mouth is held open during these lunges, and the ventral pleats expand and fill with water and prey. When humpbacks feed on small fish, they may use a cooperative feeding strategy. This entails a group of 6-12 or more humpbacks all vertically lunging through the surface of the water in a coordinated fashion. Humpbacks produce the feeding call while they are maneuvering underwater. The call has been suggested to either coordinate the movements of the whales or manipulate prey. Recent experiments played back feeding calls to herring, which responded by fleeing from the call. These observations suggest that prey manipulation is the most likely function of this call.
Figure 4 The hierarchical structure of humpback whale song.
The feeding call is a nearly constant frequency tone lasting between 5 and 10 sec. It has been compared to the sound of a train whistle. It is often repeated in a series of calls, and there is sometimes a shift of frequency at the end of the series of calls. There is variation in the frequency of the call, but most are between 500 and 550 Hz.
e. bowhead whales (balaena mysticetus) Humpbacks were the first whale to be recognized as a singer. However, extensive acoustic recording during the population census of bowhead whales off the North Slope of Alaska revealed that bowheads sing as well. Songs have been recorded during the spring migration from the Bering Sea to the Chukchi Sea. Songs are usually heard at the beginning of the migration and less at the end, suggesting that most of the singing occurs in the Bering Sea in the winter.
Song notes are usually longer than nonsong moan and gruntlike calls. Bowheads sing between one and three themes, most often two. Unlike humpback whales, bowhead songs regularly show substantial change in structure in successive years. Within a year, all whales sing the same basic version of song, but there is considerable inter- and intraindividual variation. Most of the sound energy of bowhead calls and song sequences is below 1000 Hz. The songs are frequently composed of both AM and FM components. Bowhead whales produce fewer units and in a narrower frequency range than humpbacks, yet bowheads have an unusually large variation in the tone of their songs, producing a wide variety of different sounding song notes.
In addition to songs, bowheads produce a wide range of calls. There are two main groups, the simple, low-frequency FM calls and complex calls. The FM calls can be categorized by their FM contours, i.e., upsweeps, downsweeps, constant tones, and inflected (change in contour). FM calls are almost always under 400 Hz in frequency. The complex calls have been described as pulsive, pulsed tonal, and high. High calls have frequencies above 400 Hz and sound like a whine. The pulsed tonal is a combination of both frequency and amplitude modulation. Pulsive calls are a mixture of pulses, with both frequency and amplitude modulations. Pulsed tonal calls are often below 400 Hz, but pulsive calls can exceed 1000 Hz.
Because observation conditions are often limited in the Arctic, it has been difficult to associate behaviors with these vocalizations. However, some observations have provided information on some calls. A mother and calf were separated and as they approached each other, loud FM calls were heard. Once they were rejoined, the calling stopped. Migrating bowheads will sometimes produce “signature calls” for a period of minutes up to at least 5 hr (or longer). These signature calls are often made in the context of whales countercalling with each other. Thus it has been suggested that these calls are used to maintain group cohesion. Unlike signature whistles of dolphins, the signature calls of bowheads do not appear to be specific to individuals, and individuals will switch signature call types. These signature calls may also be used to help orient in the ice field. A group of whales has been observed approaching a large block of ice. The early arriving whales only swam around the ice when they were very close. The following whales deflected much earlier, suggesting that they were listening to the echoes of the early whales and using the acoustic information to avoid the ice. Certainly one can imagine that swimming toward quiet areas (where there is no ice to reflect sound) is preferable to swimming toward an area with a strong echo (which could be caused by a large vertical piece of ice).
f. the rest of the balaenopterids: sei and bryde’s whales (b. borealis and b. edeni/brydei) Sei whales have been recorded only several times in the northwestern Atlantic. Sei whales produce two phrases each 0.5 to 0.8 sec long. The phrases are composed of 10-20 FM sweeps between 1.5 and 3.5 kHz. each 30-40 msec in duration. There was an interval of 0.4 and 1 sec between the two phrases.
Recordings off California have revealed that Bryde’s whales make short low-frequency moans. Moans are between 70 and 245 Hz and last between 0.2 and 1.5 sec. Source levels range between 152 and 174 dB re 1 |xPa. Bryde’s whales also make a pulsed moan, which ranges between 100 and 900 Hz and between 0.5 and 51 sec in duration. The pulse rate varies between adults and calves. Finally, calves have been recorded making a series of discrete pulses between 700 and 900 Hz. These were recorded from calves when the adult was diving and from a captive juvenile.
Low-frequency moans have been recorded from Bryde’s whales in the Caribbean, the eastern tropical Pacific, and off New Zealand. Caribbean whales produced 45-Hz calls that had harmonics and were between 1 and 4 sec long. Whales in the tropical Pacific produced calls of 35 and 42 Hz without harmonics and a call of 52 Hz that did have harmonics. Calls from New Zealand were centered on 22-28 Hz and 70 Hz; these calls did have harmonics.
g. right whales (CAPEREA MARGINATA and EVBALAENA spp.) Calls from pygmy right whales have only recently been recorded. A juvenile was recorded in a harbor and produced only one sound type. It was a short tonal downsweep that began between 90 and 135 Hz and swept down to 60 Hz. Pulses lasted between 140 and 225 msec in duration and were separated by intervals of 430 to 510 msec. Source levels were estimated between 153 and 167 dB re 1 |xPa. These calls were very simple and their function is unknown.
The northern (E. glacialis and E. japonica) and southern (E. australis) species of right whales have generally similar calls, but only those of the South Atlantic have been described in some detail. Southern right whale calls have been described in terms of their frequency sweep or structure. They produce an “up” call, an upsweep from 50 to 200 Hz that lasts for about a second. This call appears to be used to bring individuals together, because calling stops once the whales join. “Down” calls are downsweeps from 200 to 100 Hz that are also about a second in length. They may serve to maintain acoustic contact, if not physical proximity. “Constant” calls range between 50 and 500 Hz and are 0.5 to 6 sec in duration. The frequency of these calls remains nearly constant.
Southern right whales make a variety of other sounds, such as high-frequency FM sweeps, amplitude-modulated pulses, and mixed pulses with both amplitude and frequency modulation. Blows (breaths) and slapping body parts on the surface also make sounds. The group type and behavioral context affect the mix of these sounds that are produced. Simple calls were usually used at long ranges and more complex vocalizations were used at shorter ranges.
Baleen rattle is a sound thought to be produced when right whales engage in surface feeding and the upper jaw and the upper portion of the baleen plates are out of the water and the lower portions of the baleen are in the water. As water flows through the baleen plates, they apparently rattle together, producing a series of short broadband pulses between 1 and 9 kHz, with most of the energy between 2 and 4 kHz. This sound is audible both in air and underwater, and may be simply a byproduct of feeding.
2. Toothed Whales The toothed whales, or odontocetes, are all vocal animals par excellence. They probably all produce clicks for echolocation, and many produce complicated sets of rapid click trains and whistles, the latter two for communication. This article summarizes sperm whale clicks and the known or believed communication sounds of other odontocetes. Even though toothed whales may be thought of as the most vocally active of all marine mammals, relatively little is known about the details of most species in sound production variability, especially in potential use of meaning of sound. This lack of detail of understanding may, of course, be because of the richness of the repertoires. A school of 500 socializing or feeding dusky dolphins, for example, produces a cacophony of sounds out of which it may be impossible for us to distinguish a particular individual or subgroup. It is likely that the dolphins themselves find meaning in this richness, but then they have evolved into this society, both genetically and behaviorally.
a. sperm whales (PHYSETER MACROCEPHALUs) Sperm whales are the largest toothed mammals on earth and have a disproportionately huge head. It is likely that the evolution of that head has in large part been driven by the loud and complicated structure of their clicks, used certainly for communication and probably (although there is some argument on this point) for echolocation as well.
Sperm whales produce a variety of clicks in a variety of contexts. Clicks can occur singly at various intervals, in a short pattern of distinct clicks called a coda, or in a long sequence of tightly spaced clicks known as a creak. The frequency content of clicks differs between sexes. Large males have lower frequency content in their clicks than females and young males.
“Usual” clicks are produced in a regular sequence of clicks at intervals of 0.025 to 1.25 sec and have a duration between 2 and 24 msec. The click interval varies greatly between individuals, but appears to be stable within the click trains of an individual whale (Fig. 5).
Codas are stereotyped, repetitive patterns of clicks. They were originally suggested to serve the function of individual identification, analogous to signature whistles in bottlenose dolphins. Later work, however, has shown that a population of hundreds of sperm whales shared only 13 coda types. This contradicted the individual identification hypothesis, but they do appear to play a role in social communication.
“Creaks” are produced when clicks are produced at a high repetition rate. Creaks sound more like a continuous buzzing sound than individual clicks.
Mature males produce another type of click, called a “slow click” for its low repetition rate, these clicks also have a longer duration, with a mean of 72 msec compared to a 24-insec mean for “usual clicks.” Slow clicks have consistent energy concentrations at 1.8 and 2.8 kHz, whereas the energy distribution in the spectra of usual clicks is much more variable.
There are competing hypotheses to explain the unique head of the sperm whale. Malcolm Clarke has pointed out that the spermaceti tissue that occurs in the head is a special lipid that changes density, and therefore buoyancy, based on its temperature. He holds that a sperm whale cools the spermaceti organ to make it denser than water, thus aiding diving. When the whale wants to surface, it warms the spermaceti, thereby decreasing its density and making it buoyant.
The more traditional theory holds that the spermaceti organ is the analogue of the melon in dolphins, and it is used to transmit and focus the sound energy of the sperm whale. While there is no doubt that the sperm whale does produce clicks, their functions are still being determined. It is most probable that some sperm whale vocalizations are used for social communication. Differences in structure reveal some information about the sender. However, whether or not clicks are used for echolocation remains unclear. The issue is based on the dual questions of how loud sperm whales are and how much sound is reflected by squid. Squid make up the majority of the diet of the majority of sperm whales. However, squid do not have the bones and air spaces found in bony fish and therefore reflect much less sound than fish. If a sperm whale is going to obtain an echo from a target that reflects little sound, it will have to produce a tremendous amount of sound to get even a weak echo. The question of whether sperm whales can echolocate squid remains unresolved. It is possible that they may be visual predators on squid and acoustic predators on fish. It appears even more likely with relatively recent research findings that sperm whales can at least echolocate onto the surface of the water from below and to the bottom. They therefore can probably place themselves accurately at depth and may even be able to make out details of bottom topography by listening to their click echoes.
Figure 5 The spectrogram and waveform of “usual” sperm whale clicks.
Although a detailed description of probable click production is beyond the scope of this article, it is likely that clicks are made near the front of the huge head. A part of a click’s energy moves toward the rear of the head, bounces off the upward curving skull of the whale, and is reflected forward. Part of that bounced sound can be reflected backward again because of the placement of an air sac near the front of the head, and thereby one click package can be composed of the main click and a series of tightly spaced intrahead echoes. It is unknown to what degree this complex click package may help in possible echolocation or provide certain information, perhaps size due to differences in click structure by size of head. At any rate, the major sounds of sperm whales are sets of clicks, and these are likely to be critically important in communication among group members. They may also be important for males to gauge each other on the mating grounds and perhaps for females to gauge males. Sperm whale sounds provide a rich set of unanswered questions and potential for further research.
b. killer whales (orcinvs orca) Killer whales that feed on fish in the northeast Pacific tend to live in stable societies of matriarchies that change only by birth, death, and rare splitting, generally when the group or pod becomes very large. Even males born into a pod tend to stay with the pod for life, a condition unusual for any mammalian species. It is not known whether this great stability is a general characteristic for killer whale pods worldwide simply because other groups have not been studied in as much detail (Fig. 6).
On the early 1980s, researcher John Ford discovered that killer whales, who make echolocation clicks, other clicks likely used for communication, pulsed calls of a very rapid click-like structure, and whistles, have different dialects per pod. The sounds composing the dialects tend to be within the range of human hearing and predominate around 500 Hz to 10 kHz. Two pods that feed on fish in generally the same area, and who come into acoustic range of one another now and then, can rapidly and at distance distinguish which pod is approaching. Presumably, they can then decide, based on past experience, whether it is prudent to interact at closer range with the other pod or to change course. Researchers who study the pods can distinguish them as well and have placed hydrophones in inlets and bays diat announce the arrival or passing by of certain well-known pods.
Figure 6 A typical spectrogram of a killer whale call. This spectrogram also shoxvs amplitude-modulated calls (banded) followed by frequency-modulated upsiveeps.
Dialects may have simply evolved because of behavioral drift as animals that travel together hear each other more than those that do not. However, it is likely that the different dialects now serve important social functions for group cohesion and intergroup recognition. Killer whales in other areas of the world “all” have slightly different sounds as well, but it is presently unknown whether adjacent and at-times interacting pods have a dialect system similar to the system in the Pacific northeast.
c. belugas (delphinafterus leucas) Sometimes known as the “canaries of the sea,” belugas produce a wide variety of whistles, amplitude-modulated pulses, and echolocation clicks. While previous attempts have been made to categorize beluga calls, their nonclick sounds defy categorization. A thorough analysis of the calls of belugas shows that each and every sound can be a point on a continuum between other sounds. Belugas also have the ability to alter the frequency of their echolocation clicks. Individual belugas that were moved from one area to another shifted the frequency of their echolocation clicks from -60 kHz to -100 kHz, apparently to avoid the increased background noise in their new habitat in the lower frequency range. Unlike other odontocetes, belugas are able to alter the physical shape of their melon, perhaps to adapt to sound transmission differences due to their movements between the open ocean and less saline estuarine waters.
d. narwhals (monodon monoceros) Narwhal clicks are some of the most intense sounds ever measured, up to 218 dB re 1 |a,Pa. These clicks range up to 100 kHz, with peaks at 20 and 40 kHz. Clicks tend to be produced in two types of series: click trains have between 3 and 10 clicks per second, whereas click bursts contain between 110 and 150 clicks/sec. It has been hypothesized that click trains are used for searching for prey and that the much faster click bursts are used as the animal closes in on its prey, analogous to the click repertoires of some bat species.
e. beaked whales (ziphiidae) Very little is known about beaked whale sounds. This group is difficult to locate and frequently difficult to approach. There are a few recordings from the wild and from captivity. Whistles are known to range from 500 Hz to at least 10.7 kHz, while clicks range up to 125 kHz. It is believed that these ultrasonic clicks are used for echolocation, and indeed this is a plausible assumption. However, echolocation has not been investigated in detail in the beaked whale group. Whistles, as in dolphins, are most likely used for social interactions.
f. dolphins (delphinidae) Dolphins also have echolocation clicks, burst-pulse sounds that consist of rapid sequences of clicks, and (for many dolphins but not all) pure tone whistles. While echolocation and other clicks can have frequencies above 100 kHz, most whistles of dolphins center around 7 to 15 kHz (and are therefore within the human hearing range). Each single whistle tends to last about 1 to 2 sec., rarely up to 3 sec. While the repertoires of many species and populations of delphinid cetaceans [including the killer whales mentioned previously, as well as pilot whales (Globicephala spp.) and other open ocean animals] have been described, we know by far most about the common bottlenose dolphin (Tursiops tmncatus), mainly due to studies in captivity. Researcher Randy Wells and colleagues, working in the Sarasota-Bradenton area of west Florida, have also carried out excellent sound analyses of vocalizing bottlenose dolphins in nature.
There are no universally accepted classifications of the specifics of communication sounds, although begin-frequency, end-frequency, and kind of frequency modulation within the structures of whistles are usually used for descriptions. In bottlenose dolphins, researchers tend to come up with about 20 to 30 distinct whistle sounds, with many intergrading variations among them.
Bottlenose dolphins (and probably quite a few other species as well) have individualized whistle contours that are called signature whistles. With practice, humans can distinguish up to about seven vocalizing dolphins in an aquarium tank, and the dolphins can probably do even better. Signature whistles are certainly used by dolphins to recognize each other, but they also appear to be used in other social contexts. For example, one dolphin will often mimic the signature whistle of another animal in order to begin social contact. Perhaps the mimicry itself is a form of saying “hello.”
Interestingly, signature whistles in Florida bottlenose dolphins appear to be more alike in mothers and their male offspring than in mothers and their daughters. The Sarasota population of dolphins is generally matriarchal, with daughters being closely affiliated for many years or for life, but sons leaving the natal group as subadults. It has been hypothesized that sons and mothers thereby recognize each other easily after prolonged times (perhaps extending to years) apart. This recognition could be important in avoiding inbreeding and in facilitating other kin-related social behaviors, such as lowered aggression. While signature whistles have been studied intensively in recent years, the true functions are not yet known.
There is some debate on which dolphin species and populations exhibit individualized sounds such as signature whisdes. In common dolphins (Delphinus spp.), there appears to be a lack of sound “signature” per individual, and it has been guessed, but with little data support, that there may well be regional dialects per population or subpopulation. as in killer whales.
The complexity of sounds may well have to do with the complexity of behavior or some aspect of level of individual and therefore group “excitement.” In long-finned pilot whales (Globicephala melas), for example, whales that are resting make very simple nonwavering whistles. Whistle complexity increases during feeding and bouts of socializing, and variability of whistles and other sounds increases greatly when two groups approach each other. Similar situations appear to exist for other delphinids, although detailed analyses of sounds per patterns of behavior have not been carried out. mainly because behavior below the waves is usually poorly known.
In at least Hawaiian spinner dolphins (Stenella longirostris) (and possibly in all other social dolphin and other toothed whale groups), there is a general relationship in amount of whistling, burst pulsing, and echolocation clicking with apparent alertness of the group. A resting group produces few sounds, whereas a feeding or socially active one produces many. This means that it is likely that each individual vocalizes more, but it is unknown whether this is merely an average for the group with much individual variation (perhaps different by age, social status, and gender) or whether each animal indeed indicates its state of alertness by the number (and complexity) of sounds produced.
Whistles are generally regarded as social communication signals, and clicks are typically thought to be used for echolocation. However, certain species, including some phocoenid porpoises, are specialized for very high-frequency hearing. These do not produce whistles, and they may use their high-frequency clicks for communication as well as echolocation.
Much has been written about the supposed “intelligence” of dolphins, and they are indeed large-brained highly behaviorally flexible social mammals. However, the supposition by many lay people that dolphins “have language.” which implies sentence structure of some sort, with nouns, verbs, and modifiers, is unlikely to be the case. Dolphin sounds are complex, but appear to serve mainly signaling, emotive, and recognition functions. It is likely that as sounds of toothed cetaceans are studied in more detail in the near future, we will discover further complexities and marvelous adaptations besides that anthropomorphic wish for language.
g. porpoises (phocoenidae) Porpoises show a great range in vocalizations. The most commonly studied species is the harbor porpoise (Phocoena phocoena). Harbor porpoise vocalizations cover an extreme frequency range from 40 Hz to at least 150 kHz. Their vocalizations are composed of five major components. The first is of low-frequency calls ranging from 1.4 to 2.5 kHz. produced at high amplitudes. There are probably used for long-range detection. Midfrequency calls, between 30 and 60 kHz, are produced at low amplitude. Broadband midfrequency calls are made between 10 and 100 kHz. High-frequency components range between 110 and 150 kHz and are used for detection and classification of objects. All of these calls are variations of click trains. The repetition rate of clicks appears to be fairly constant within a click train when animals are “at ease” and varies between 15 and 36 clicks per second. When alerted by a prey item or other object at short ranges, harbor porpoises can produce between 500 and 600 clicks per second. The last type of vocalization are whistles, which range between 40 and 600 Hz.
D. Sirenians
1. Manatees The Caribbean manatee (Trichechus inana-tus) tends to produce sounds between 0.15 and 0.5 sec in duration. They show a relatively complex structure and range between 600 Hz and 12 kHz, but are typically 2.5 to 5 kHz. The fundamental frequency is at times less intense than the first harmonic. Calls consist mainly of chirp-squeaks, squeals, and screams. Amazonian manatee (T. inunguis) calls are similar in structure, although they may be higher in frequency (6-8 kHz) than those of the Caribbean manatee. The frequency content of vocalizations differs by sex. with female calls lower in frequency than those of males. Neither species is thought to echolocate. Manatees do not vocalize often, but do so under conditions of fear, aggravation, and male sexual arousal. Mothers and calves appear to use acoustic signals to facilitate rejoining each other.
2. Dugongs (Dugong dugon) Dugongs appear to vocalize more often than the normally quiet manatees, with one study recording vocalizations in over half of recording attempts. Dugongs appear to produce three major types of sounds: chirp-squeaks, barks, and trills. They also produce intermediate sounds with multiple components of the three main types. Chirp-squeaks are short frequency-modulated signals that extend upward to 18 kHz. They are about 60 sec in duration, typically have a slight downward trend in frequency, and have between two and five harmonics. Barks are loud broadband signals that range between 500 Hz and 2.2 kHz. No frequency modulation is seen, and the barks last between 0.03 and 0.12 sec. Trills are a series of individual notes, lasting between 100 and 2200 msec. The notes typically begin at about 3.1 kHz and rise to 3.9 kHz. The frequency sweep is not linear, but rather an oscillating up and down. The functions of these sounds are not yet totally clear, but there are good indications that they are used for social communication.
IV. Conclusions
Marine mammals have a very rich behavioral tapestry of sounds. The carnivores that come to land or ice to breed produce some in-air sounds but generally are not nearly as vociferous as their totally terrestrial taxonomic relatives. Almost all marine mammals become loquacious underwater, however. The basic description here merely hints at this richness in an environment where sight and smell are not transmitted as efficiently as sound. Sound is used for communication and for wresting information from the environment. While only toothed whales are thought to have sophisticated echolocation, it is likely that many sounds give information on depth of water, obstruction ahead, or even silent conspecifics simply by the alteration of sound reflections in different environments.
Our acceptance that sound is critically important to marine mammals also gives us cause for worry. Since the advent of motorized shipping and now ever more with industrial seismic, intense military sonar and other human sources of sound, major parts of the oceans are becoming extremely noisy from nonbi-ological sources. We do not yet know the details of how noises can affect communication, masking, passive listening, and behavior and nervousness of mammals exposed to them.
