Sensory Systems/Other Animals/Echolocation Toothed Whales

Introduction
Marine mammals such as whales, dolphins and porpoises have developed sensing abilities that have allowed them to go into deep sea and spread across the world’s oceans. These mammals belong to the order of Cetacea. Toothed whales (Odontocetes), a parvorder of Cetacea which consists of at least 71 species, including sperm whales, killer whales, porpoises and dolphins, have acquired an astonishing type of sensing mechanism, called echolocation or bio sonar. It allows them to successfully navigate and hunt prey at places where vision is limited due to great depth or turbulences. Research has shown that it provides them with a three-dimensional view of their environment and further gives them the ability to differentiate and recognize characteristics of objects, which is a key biological benefit. Echolocation has therefore played a major role in the evolutionary success of toothed whales, which have emerged 34 million years ago. However, it is not only used by toothed whales, but can be found in all sorts of other animals as well. Microchiropteran bats, for example, have a highly-developed bio sonar system, but also shrews, two genera of birds and megachiropteran bats make use of this sensing ability.

Principle of Echolocation
The basic principle of echolocation is to obtain information about the environment from the received echoes of emitted sound waves (see Figure_Echolocation). Odontocetes produce pulse-like clicking sounds in a high-frequency range of 10kHz to 200kHz. These clicks are mostly in the ultrasonic range (>22.1kHz) and thus not perceivable by humans. The duration, frequency, interval and source level of the created pulses vary between different species and depend on environmental conditions such as ambient noise, reverberation, target distance and target characteristics. For example, sperm whales use a range of 10-30kHz to echolocate, while porpoises and many dolphins broadcast signals greater than 100kHz. Once a reflected sound wave is detected, time delay and intensity are used to gain information about distance and orientation of the incoming signal. Odontocetes can dynamically control the interval and source level of the transmitted signals. Usually, the clicks are transmitted at a rate that enables the signal to return before the next click is sent out. Thus, the repetition rate increases as a target gets closer. Furthermore, the output level of the click is usually higher when a target is further away and lower when it is closer.

Function
Echolocation in toothed whales is used for orientation and hence navigating the oceans. Further, it allows them to find prey and avoid predators. This is achieved by the active detection, localization, discrimination and recognition of objects in the surrounding environment. Research suggests that in some species, e.g. Hector's Dolphins, the produced sounds are also used in social context.

Sound Production Mechanisms
The high-frequency sound generation in Odontocetes happens in a structure called monkey lips/dorsal bursae (MLDB), which is located in the upper nasal passage. The MLDB complex is built up of the fatty dorsal bursae, the monkey lips, the bursal cartilages, and the blowhole ligament. By moving air between the monkey lips, the MLDB complex starts to vibrate and hence sounds are generated. These sounds are sent out through a fatty-filled area in the upper forehead called the melon, which acts as an acoustic lens to focus the directional sound beams ahead of the animal (see Figure_SoundMechanisms). The melon contains fats that are composed of lipids very rich in oil. These lipids are also called acoustic tissue, since they conduct sound well and may also play a role in focusing the outgoing beam. A study by Aroyan has shown that not only the melon, but also the skull and the dorsal bursae (air sacs) play important roles in forming the forward beam that is transmitted into water. The air sacs reflect any upward or downward directed sound, while the nasal passage and cranium reflect any backward directed sound. It has to be noted that although these mechanisms account for almost all Odontocetes, sperm whales pose an exception. Their head structure and hence the sound production and hearing mechanisms are different to those of dolphins and other toothed whales and are still subject to ongoing research.

Sound Reception Mechanisms
Odontocetes have the astonishing ability to hear over a broad range of frequencies, even ranging beyond 100kHz. The apparatus for the reception of acoustic signals is located in the lower mandible (see Figure_SoundMechanisms). The rear portion of the mandible consists of a thin pan bone, which is directly connected to the auditory bulla through a fatty-filled channel. Sound waves are conducted from the mandible to the bulla through this low-density channel. The auditory bulla, properly called “tympano-periotic complex”, consists of the middle ear (tympanic bulla) and the inner ear (periotic bulla). Except for the connection to the mandible, the tympano-periotic complex is completely separated from the skull, which is an important factor in underwater sound localization. From the middle ear, which is filled with acoustic tissue, signals travel to the inner ear. In the inner ear, hair cells located in the cochlea are stimulated and convert the acoustic signal into electrical nerve signals. These hair cells are connected to ganglion cells that transmit the electrical signals to the brain via the auditory nerve. Compared to humans and other mammals, there are quite some differences in the structure of the inner ear. The major differences are a larger auditory nerve, a longer basilar membrane, a small semi-circular canal and a higher ratio of ganglion to hair cells. The time between emitted clicks and auditory response, also called latency of response, can be as short as 7-10μsec. This auditory nervous response is faster than that of a rat, even though a rat's head is a lot smaller.

Sound localization, i.e. the ability to spot the direction and distance of an incoming sound, depends highly on the medium. In land mammals, binaural cues, i.e. differences in arrival time and differences in intensity, help the localization process. Research suggests that odontocete also make use of this technique. It is assumed that the large spread between the ears and the functional separation from the skull are the reason for accurate underwater sound localization in toothed whales. By receiving sounds through tissue in the mandible and not through an eardrum as in terrestrial mammals, hearing loss due to increasing pressure in deeper waters is avoided. An interesting characteristic of the emitted sound beam is that it is inhomogeneous, i.e. only signals traveling along the straight axis of the beam are undistorted. Thus, objects lying in the direction of the major axis of the emitted beam are most likely to be recognized.

Sound Transmission and Characteristics of Signals
The sounds produced by toothed whales are some of the loudest in all animals with peak-to-peak amplitudes up to 225dB. There is a distinction of the echolocation signals in Odontocetes. One group, whistling Odontocetes (most dolphins) project shorter clicking sounds of 40-70μsec and bandwidths over 100kHz, while non-whistling Odontocetes (sperm whale, Hector’s dolphin) produce longer sounds of 120-200μsec with a bandwidth of around 10kHz. The maximum detection range varies between species. Experiments have shown ranges of 113m for bottlenose dolphins and 26m for harbor porpoises. Sperm whales can detect objects as far away as 500m. These numbers should be considered with caution, however, since measurements are hard to compare and also depend on environmental aspects such as background noise and turbulences.

Smell and Taste
There are no olfactory lobes as well as no vomeronasal organ in toothed whales, thus they are lacking the sense of smell. Taste buds are found on tongues of some Odontocetes such as bottlenose dolphins, but have atrophied in most species. It is thus assumed that they only have a very weak sense of taste if any at all. There are, however, some indications that toothed whales have developed additional sensory organs to substitute for the sense of taste, as they do respond to certain substances in surrounding water.

Vision
Vision persists and works relatively well underwater and above water, although Odontocetes do not rely on their sight as much. Their eyes are especially adapted to the different conditions underwater: The eyeballs and corneas are flatter than in terrestrial mammals in order to allow as much light as possible to enter. To achieve maximum vision, they have enlarged pupils and the incoming light is reflected twice through a reflective layer called tapetum lucidum. The receptive layer predominantly consists of rods with far fewer cone cells. Hence, colour vision in toothed whales is limited. As toothed whales rise to the surface, the pupils shrink in order to prevent damage from direct sunlight. For further protection of the eyeballs, glands that produce a secrete which cleans the eyes exist. Toothed whales can see roughly 10.7m ahead underwater, a little less above the surface.

Touch
The skin of toothed whales consists of a thin layer that is very sensitive. The most sensitive areas include the head, the belly, the genital organs and the flippers. The sense of touch plays an important role in communication, e.g. touching bodies as a way of greeting, and other social contexts.

Geomagnetism
Another sense that toothed whales seem to be making use of is geomagnetism. Besides using echolocation, they may navigate by sensing the earth's magnetic field for longer distance journeys. When following their movements, scientists have discovered that they often travel along lines of the earth's magnetic field. They suggest that Odontocetes use the flux of the magnetic field in two ways: Whales travel parallel to contours of a map provided by the topography of the local magnetic field. To monitor position and progress on this map, they use regular fluctuations in this field. Live strandings seem to be connected to this sensory ability and are explained by irregular field fluctuations, e.g. caused by military sonar or solar storms, or when the route crosses land.