The first description of manatee vocal folds in literature was by Murie (1872), wherein he states “…Stannius and Rapp have failed to notice the existence of a small recess or pseudo-sacculus laryngis at the anterior extremity of the vocal cord, as in the Dugong…the vocal cords are the reverse of prominent, and deficient in inferior excavation.” However, after Murie (1872), previous studies of the sirenian larynx have yielded conflicting observations on the existence of vocal folds (vocal “cords”), the source of vocalizations in terrestrial mammals. Nair and Lal Mohan (1975) observed during dugong vocalization that the nostrils were closed and wrinkles appeared on the skin of the frontal area. Such wrinkles were not observed in the larger female dugong, which did not make any sound, and they commented that there seemed to be some coordination between the movements of the wrinkles and the sound production (Nair and Lal Mohan, 1975). Domning (1977) observed that the vocalis and ventricularis muscles are absent in both dugongs and, based on literature, in manatees, although he later found possible equivalents of these muscles in T. inunguis (Domning, 1978). Harrison and King (1980) reported that sirenian vocal folds are absent and are replaced by fleshy, prominent cushions. Gambaryan and Sukhanov (1986), give a detailed description of the laryngeal and other muscles of T. manatus, with interpretations that differ from those in Domning (1977). Dong et al. (1992) also reported that dugongs have no vocal “cords” in the larynx, but described false vocal “cords” that have lost their function as such at the bottom of the laryngeal vestibule. Reidenberg and Laitman (1995), however, describe the thick opposing tissues in the laryngeal lumen as likely homologs of mammalian vocal folds. Although postulated, these laryngeal tissues were never proven to be homologous to the vocal folds of terrestrial mammals, and they further postulated that not all sounds appear to be generated at the larynx. According to Anderson and Barclay (1995), low-pitched whistles of dugongs are more likely an abnormality in the respiratory system rather than a means of communication, given their production during breathing. Behavioral observations indicate that chirp-squeaks and other sounds of the dugong originate in the frontal region of the head rather than in the larynx (Anderson and Barclay, 1995), suggesting a mechanism similar to that of odontocetes (Cranford et al., 1996). However, not all cetaceans (whales, including dolphins and porpoises) produce sounds from the nasal region, as evidenced by the discovery of vocal fold homologs in the larynges of mysticetes (Reidenberg and Laitman, 2007). Other marine mammals (e.g., pinnipeds) also use the larynx for sound production (Reidenberg and Laitman, 2010).
The only structure found to be suitable for generating sounds in our specimens were the tissues in the laryngeal lumen. These tissues met all the criteria for being called vocal fold homologs (Reidenberg and Laitman, 2007): they are oriented perpendicular to airflow, they are attached to the arytenoid cartilage, they can be abducted and adducted, they are controlled by the lateral and dorsal intrinsic muscles including the posterior cricoarytenoid, they contain a ligament that attaches to the thyroid cartilage, they are innervated on the cranial surfaces by the superior laryngeal nerve (internal branch) and appear to be innervated on their caudal surfaces by the recurrent laryngeal nerve, and they can completely occlude the airway.
Manatee vocal folds are the homologous structures to the true vocal folds of other mammals; however, they do not have a sharp edge as in many land mammals. This blunt edge may affect the quality of their fundamental frequencies. Sound production occurs as opposition of the manatee vocal folds restricts airflow through a narrow slit, resulting in fold vibrations that produce the fundamental frequency. Laryngeal vibrations can pass through the overlying fatty tissues of the throat (lingual and cervical), that in turn may transfer sound to water with very little energy loss. Although dissections on Amazonian manatees were not conducted, the same mechanism for sound production as in the West Indian manatee is thought to occur. Researchers found the vocalizations to be very similar in most respects except that they differ in duration and fundamental frequency (ranged from 2.5 to 5 kHz for T. manatus and 2.6–5.9 kHz for T. inunguis) (Evans and Herald, 1970; Sonoda and Takemura, 1973; Nowacek et al., 2003).
The velocity of sound transmission through solids (e.g., bone), gels (e.g., fat, skin, muscle, cartilage), and fluids (e.g., seawater, freshwater) is linearly related to the densities of the media (Mast, 2000). Soft tissue density varies around 10% from that of seawater and velocity varies around 15% (Aroyan, 1996). Tissues containing more structural elements (e.g., collagen) have higher densities and sound velocities than water (Goold and Clarke, 2000), while those with greater fat content retain lower densities and sound velocities (Mast, 2000). Energy is reflected at density interfaces, resulting in a transmission loss as sound travels between the various media. Tissues with a density close to water will allow a more efficient energy transfer from inside the body to the surrounding water. Chapla et al., (2007) found that the soft tissues of the manatee head have a density similar to that of seawater, suggesting that sound waves could propagate easily from one medium to the other.
The composition of the lingual and cervical fatty tissue in manatees has not been studied. The fat could provide an impedance matching mechanism for more efficient sound propagation into water. The odontocete melon, which is also composed of fatty tissues, occupies the forehead region of the skull and acts as an acoustic channel for sounds propagating out of the head (Cranford and Amundin, 2003). Muscles surrounding the melon appear to change its shape, and may enable it to function as a variable acoustic lens (Norris and Harvey, 1972). The lingual fat pad may allow rostro-ventral sound transmission through the floor of the mouth, while the cervical fat pad may allow latero-ventral projection of sounds from the throat region.
Fats are useful for sound transmission to water due to their relatively low density (compared with thicker connective tissues) that is impedance-matched with water. Sound transmission is not limited to outgoing sounds. Bullock et al. (1980) and Ketten et al. (1992) noted that the manatee's zygomatic process is lipid-filled, and suggested that it may conduct received sounds to the ear, much like the acoustic fat found in the acoustic window in the mandibles of cetaceans (Norris, 1968). The zygomatic process was found to have significantly lower density than other bones (Fawcett, 1942; Caldwell and Caldwell, 1985); however, the lipids it contained were composed almost entirely of triacylglycerols (Ames et al., 2002) and not the isovaleric acid typical of cetacean acoustic fat by which sounds are conducted (Varanasi and Malins, 1971). Cranford et al. (2008) found an intriguing finite element model (FEM) result concerning the pathway by which sounds reach the ears of a Cuvier's beaked whale (Ziphius cavirostris). The simulations revealed a previously undescribed “gular pathway” for sound reception in the whale. The propagated sound pressure waves enter the head from below and between the lower jaws, pass through an opening created by the absence of the medial bony wall of the posterior mandibles, and continue toward the bony ear complexes through the internal mandibular fat bodies (Cranford et al., 2008).
Although manatees do not have nasal fat, they may still use that region to transfer sounds to the water. The dorsum of the nasal cavity was observed to swell and collapse during vocalizations of the live manatees in the study, both the Antillean and Amazonian. These movements may act as a drum-head, transferring pulses as pressure waves into the water. Alternatively, the movements may indicate flow of air through the larynx. A flexible wall in the nasal cavity could expand to allow airflow for a longer period before the respiratory tract becomes pressurized. Once the outflow reservoir (nasal cavity) is fully expanded and pressurized, airflow will cease and so will sound production. Reversal of this flow, however, may allow the air to be recycled for another vocalization without losing any air out of the nostrils. This could allow manatees to remain submerged longer while continuously vocalizing between breaths. An expandable/collapsible nasal cavity has additional advantages: it can serve as a variable resonating chamber and act to amplify or mute certain frequencies termed formant frequencies (or formants). Air spaces (e.g., nasal cavity) within soft tissues are efficient reflectors of acoustic energy (Aroyan, 1996). The manatee's closest relative, the elephant, also produces variable formants. The elephant's expandable trunk and large nasal cavity likely are involved in modifying these sounds (Soltis, 2010). Stoeger et al. (2012) found that African elephants may be switching vocal paths (nasally and orally emitted rumbles) to actively vary vocal tract length (with considerable variation in formants) according to context.
The definitive path of sound transference to water has not yet been established for manatees; however, the presence of both a flexible nasal cavity and multiple fat pads may indicate an ability to vary the nature of the laryngeally emitted sounds, much like their elephant cousins. Manatees may be transferring sounds through several different transmission pathways: floor of the mouth (lingual fat pad), throat (cervical fat pad), and nose (flexible drum-head of the nasal cavity).
Sound travels a greater distance than light under water. Light only travels a few hundred meters in the ocean before it is absorbed or scattered. Given that sound travels much farther underwater than in the air, for marine mammals the use of sound in an aquatic environment is indispensable compared to vision. It is therefore no surprise that marine mammals have evolved different mechanisms for sound transmission and reception. Bullock et al. (1980), Ketten et al. (1992), and Ames et al. (2002) suggest that the position, porosity and oil-filled nature of the zygomatic process of the squamosal bone (ZPSB) of the Florida manatee may have a similar sound conduction function to that of the intramandibular fat body (IMFB) of the bottlenose dolphin and other odontocetes. The ability to use lipids to permit or enhance directional hearing underwater would be extremely useful for manatees to communicate or avoid oncoming boats (Ames et al., 2002). Even though the lipid composition in the manatee ZPSB differs in some ways from the lipid composition in odontocete IMFB and melon (Ames et al., 2002), the presence of the porous bone of the ZPSB may, in conjunction with the lipids of that bone, provide a channel for sound conduction as Bullock et al., (1980) suggested. Future comparisons between disparate species may indicate that convergent evolution mechanisms are present.