In sharks, hearing and vibration detection (The Acoustico-Lateralis System) are fundamentally linked. For sharks the inner ears are nestled inside the posterior part of the braincase on top of the head. The only external manifestation of a shark's ears are two small openings on top of the head, just behind the eyes, known as endolymphatic pores.
A shark's main vibration sensing mechanism is the lateral line, which is visible externally by a row of tiny pores along each flank. Anteriorly, this system of pores branches out over the shark's head in complex patterns nested between and around the electrosensory pores. Despite their apparent differences, the shark inner ear and lateral line system are based on the same basic mechanism.
The functional unit of both the shark inner ear and lateral line is the hair cell. Each hair cell consists of a more-or-less globular basal body from one end of which project a series of cilia (hair-like structures). One of these cilia, called a klinocilium, is much longer than the others. The klinocilium extends into a gelatinous dome called a cupola, which is partially exposed to the external environment. On the opposite pole of the basal body is a bundle of five or so sensory nerves. Since water conducts vibrations quite efficiently, any oscillation in the surrounding liquid medium causes the cupola to move correspondingly. This movement causes the klinocilium to bend, which, in turn, provokes the lesser cilia surrounding it to bend in response (reminiscent of cascading dominos). Bending of a hair cell's cilia induces an electrical change in the basal body, which is transmitted - via chemical messengers called neurotransmitters - to the sensory nerve and on to the brain, where the stimulus is interpreted as sensation. All these complex movements and chemical choreography is highly sensitive to even the tiniest vibration in the surrounding water.
The Inner Ear
The shark inner ear is a fluid-filled structure consisting of a cartilaginous sac to which is attached three semicircular cartilaginous tubes. These fluid-filled tubes are set at right angles to one another and are lined with hair cells. Each semicircular tube responds only to accelerations within the plane parallel to its orientation. Thus, collectively, the three semicircular tubes are sensitive to accelerations in all three geometric planes and grant the shark a simultaneous sense of its movements in all three-dimensions of its liquid environment. However, these tubes are not considered to be involved in sound perception (Carrier et al., 2004).
The saccule, lagena, and utricle are three sensory areas that are thought to be involved in both balance and sound perception. They consist of a path of sensory hair cells on an epithelium overlain by an otconial mass. The otoconia (Otolith), made of calcium carbonate granules embedded in a mucopolysaccharide matrix, act as an inertial mass (Tester et al., 1972). As in other fishes, the otolith organ is thought to be responsive to accelerations produced by a sound field, which accelerate the shark and the sensory macula relative to the otoconial mass (Carrier et al., 2004). These otoliths therefore respond to gravity, providing the shark with information about its orientation in the water, be it head up, head down, on its side, right-side-up or upside-down.
Fig 1: Inner ear of the thornback ray, Raja clavata. ed: endolymphatic duct; ac: anterior semicircular canal; pc: posterior semicircular canal; hc: horizontal semicircular canal; s: saccule; u: utricle; l: lagena; mn: macula neglecta; rmn: amus of VIIIth nerve innervating macula neglecta (Carrier et al. 2004).
In a fascinating 1981 paper, otolaryngyologist Jeffrey Corwin reported that in some sharks one of these otolith-equipped parts of the inner ear, known as the macula neglecta (because it had long been ignored by sensory physiologists), responds particularly strongly to vibrations through the top of the skull. Based on his functional morphology studies of many shark species, he proposed that the macula neglecta may provide actively predatory sharks with an enhanced ability to hear sounds originating from above and in front. If true, this would grant sharks directional hearing, despite the close-set arrangement of their inner ear mechanisms. The whole inner ear structure is connected to the outside of the shark's body by yet another fluid filled cartilaginous tube. Thus the shark inner ear is unique among vertebrates in that the fluid inside this organ is in direct contact with the watery medium outside the animal's body.
Central Pathways into the CNS (Central
As in other vertebrates, the ear of the shark is innervated by the VIIIth cranial (octaval) nerve. Studies of afferent connections and the physiology of the octaval nerve form individual end organs (saccule, lagena, utricle and the macula neglecta) show projections ipsilaterally to five primary octaval nuclei: magnocellular, descending, posterior, anterior, and periventricular (Corwin and Northcutt, 1982; Barry, 1987). Much works remains to be done regarding both the anatomy and neurophysiology of the CNS.
Sound Waves in Water
Sound is a multi-stage event that requires four components to occur: a source of vibration, a transmitting medium, a receiving detector, and an interpreting nervous system. Sound energy is carried by the oscillation of particles composing a transmitting medium. In the case of sharks, the transmitting medium is the water through which they swim. Thus, distinguishing what a shark hears with its inner ears from what it senses as vibrations via the lateral line is a kind of Gordian knot comparable to separating singer and song. As a result, many shark sensory biologists refer to the combination of inner ears and lateral lines as the acoustico-lateralis system. Experiments with various species by Arthur Myrberg, Donald Nelson, and their co-workers have revealed that sharks are most attracted to irregular, pulsed sounds of relatively low frequencies. Field and laboratory experiments have demonstrated that sharks can hear sounds with frequencies ranging from about 10 Hertz (cycles per second) to about 800 Hertz, but are most responsive to sounds less than 375 Hertz. In contrast, most adult humans can hear sounds ranging from about 25 Hertz to roughly 16,000 Hertz (young children can hear sounds up to 25,000 Hertz, but much high-frequency sensitivity is lost by late adolescence.) Although sharks and humans detect some low frequency sounds in common, sharks can hear sounds that are inaudible to us. A shark's hearing is adapted to detecting very low-frequency vibrations such as those made by a struggling fish.
Recently de-classified U.S. Navy studies have revealed that the ocean is criss-crossed by meandering ribbons of very cold, dense water surrounded by warmer, less dense water. Since sound travels more efficiently in dense materials, these liquid ribbons act as 'sound tunnels'. Sound inside these tunnels bounces along like light in a fiberoptic cable, with very little loss of energy to outside water masses. During the height of the Cold War, the Navy used a $16 billion system of underwater microphones placed within these networks of sound tunnels to keep tabs on the positions and activities of enemy submarines (the system is known by the acronym SOSUS, for SOund SUrvaillance System). Some cetologists believe that whales may use these sound tunnels to communicate across entire ocean basins. Due to its physiological heat-retaining mechanisms, the White Shark may be able to penetrate these sound tunnels, listening for the low-frequency sounds of potential prey inside the cold, dense ribbons of seawater.
The Lateral Line (Mechanosense)
The ability to detect movement at multiple scales is essential in the lives of fishes. The detection of large tidal currents provides information important for orientation and navigation, and small-scale flows can reveal the location of prey, predators, and conspecifics during social behaviours. The mechanosensory lateral line system is stimulated by differential movement between the body and surrounding water, and is used by fishes to detect both dipole sources (eg: prey) and uniform fields (eg: currents). This sensory system functions to mediate behaviours such as rheotaxis (orientation to water currents), predator avoidance, hydrodynamic imaging to localise objects, prey detection, and social communication including schooling and mating (Combs and Montgomery, 1999). In contrast to the amount of information available on lateral line morphology and function in bony fishes, relatively little is known about mechanosensory systems in elasmobranchs.
Fig 2: Morphology of the lateral line canal system and superficial neuromasts in elasmobranchs. (A) Diagramatic longitudinal section of a pored canal from a juvenile grey reef shark, Carcharhinus amblyrhynchos. Innervated canal neuromasts are arranged in a nearly continuous sensory epithelium and covered by gelatinous cupulae. Pored canals are connected to the environement via tubules that terminate in openings on the skin surface. Scale bar 150µm. (B) Schematic transverse section of a single superficial neuromast (pit organ). The sensory neuromast arrow is positioned between modified scales (S). Scale bar 50 µm. Cupulae is not shown. (Carrier et al., 2004).
Lateral Line Structure and
The shark lateral line consists of a fluid-filled, hair cell-lined tube extending along each flank, just beneath the skin. This tube connects to the external environment via secondary fluid-filled tubules that branch off from the main tube and penetrate the skin at regular intervals. The lateral line system is visible on the surface of the skin by the presence of small pores known as mechanosensory neuromasts. Vibrations in the ocean are transmitted by successive fluid compressions and rarefactions from the secondary tubules to the main tube. These vibrations then move the gelatinous domes of hair cells lining the main tube and alert the shark. As the lateral line system extends along most of a shark's body, it grants the animal a highly directional sense of movements of potential predators and prey in its immediate vicinity. The variety in morphological structure and spatial distribution of the lateral line pores determine functional parameters such as response properties, distance range of the system, receptive field area and which component of water motion (velocity or acceleration) is encoded (Denton and Grey, 1983, 1988). Sharks that have been temporarily blinded in experiments have been able to avoid colliding with the wall of the tank which contained them, apparently by sensing water waves reflected from the tank wall. Thus, even in highly turbid water, where vision is all-but useless, a shark can tell exactly where obstacles and other creatures are, even if it cannot see them.
Lateral Line use in Feeding
The best known behavioural use of the lateral line in sharks is in prey detection. Other uses of the lateral line, particularly in bony fish, include schooling behaviour, social communication, hydrodynamic imaging, predator avoidance and rheotaxis. The concentration of mechanorecpetors on the cephalic region of sharks and ventral surface of batoids, as well as the low frequency, close range of the system, indicates an important role in the detection, localisation and capture of prey. Swimming and feeding movements of invertebrates and vortex trails behind swimming fish can produce water movements within the frequency and sensitivity range of the lateral line system (Montgomery et al., 1995).