The Sensory World of Aquatic Organisms
When we consider the senses, we typically think of the "five senses": hearing, seeing tasting, touching, and smelling. Scientists usually look at the senses a bit differently, classifying them according to the medium which is being sensed. A physicist would speak of chemoreception, which involves sensing chemicals in the environment and includes both taste and smell; mechanoreception, which involves sensing mechanical deformation (movement) and includes touch and hearing as well as one's ability to sense movement, acceleration, stress on muscles, pain, and position of various parts of the body (proprioreception); and, finally, radioreception, the ability to detect electromagnetic radiation, commonly known as sight. The ability to sense cold and heat would seem to be a type of radioreception, but we will consider it along with mechanoreception, since these receptors sense changes to the body rather than directly sensing conditions in the outside environment.
Our knowledge of the sensory structures and abilities of other species is better than one might expect, and the physiological and neurological basis of the sensory world of other organisms is also fairly well understood. Rather than simply reviewing what you should have learned, either in General Biology, Zoology, or Physiology, we will focus more on how sensory structures are applied underwater, with only brief introductory comments for each of the senses. You might want to review sensory structures in Keeton or in a Vertebrate Zoology textbook (Pough et al. 1989).
Chemoreception is divided into two main components, the distance sense, which we commonly refer to as smell or olfaction, and the contact sense, which we refer to as taste. In terrestrial organisms, the distinction is drawn out further, as olfaction detects chemicals in the air, while taste detects chemicals dissolved in water within the mouth. However fine the distinction becomes, there is a further one, at least in vertebrates. While the vertebrate sense of smell, perhaps most highly developed in some dogs, seems to be able to distinguish any of the millions of possible chemicals independently, the sense of taste merely averages responses of four generic chemoreceptor types (saltiness, sweetness, sourness, bitterness). Further, taste and smell are often processed together to give a combined sensation.
Olfactory senses overall are keen among some aquatic vertebrates; there is evidence that fish and turtles can distinguish the smell of the area (stream or beach) they were born in and use this information as a navigational tool. Invertebrates also have prodigious powers of olfaction, but these are best investigated for terrestrial species, and little has been done with aquatic species. For instance, we know of the ability of male moths to find female moths via pheromone concentrations so low it is likely that the male's initial contact is with a single molecule, yet we are not really sure to this day (1990) whether aquatic insects have any distance chemoreception at all. Such distance chemoreception is well documented in crustaceans, a group which evolved in water; it may be that insects, which evolved on land and then moved to freshwater, have not yet developed such a sense. In any event, the chemosensory abilities of those invertebrates which have been tested seem to indicate that invertebrates in general have heightened sensitivity to those particular chemicals (pheromones, chemicals given off by food, etc.) that are of primary importance, and lessened ability to sense chemicals of no historical relevance.
Most aquatic organisms have the olfactory cells mounted in a position where they will be exposed to moving water, presumably to limit time lags imposed by diffusion of the chemical through the boundary layer surrounding the sensory cell (remember that the boundary layer is smaller as water speed increases see Craig, 1990 page 352 antennae). For the same reason, perhaps, the olfactory organs are usually anterior on the organism, where the boundary layer is thinner, although many might argue that the anterior position simply allows the organism a better chance to smell what it's getting into. Vertebrates bear the olfactory cells in the nostrils, usually with arrangements for moving water over them; the taste cells are located on the tongue. Fish, the original aquatic vertebrates, have chemoreceptors scattered all over their bodies, but with particular attention to sensory structures such as the lips or barbels (Fig. 1). Invertebrates bear the olfactory structures on various parts of the body, often tentacles or antennae near the head, but also on mouthparts, feeding structures, legs, feet, tails, and so on.
Chemoreception in water is probably different than it is in the air. Chemicals move more slowly in water than in air. Also, the effect of currents cannot be overlooked (Fig. 2). Overall, in a stream or other aquatic system, chemical sensing is probably not as useful as it is in the air; for instance, pheromones seem to be rare in water, and use of smell to detect predators or prey is probably not as useful since organisms in still water can easily move faster than the chemicals they give off, and since in running water there is no sense of what is to the sides or downstream of the organism. Still, olfaction is useful at close distances and where light levels are low. The presence of chemosensory structures on the legs and feet of some aquatic arthropods suggest that these structures are really used more like mechanoreceptors to sense the chemical nature of the substrate (or whatever they have grabbed).
Figure 1. Location of taste receptors on a catfish. Each black spot indicates a set of chemosensory cells. Note that they are concentrated particularly on the barbels (whiskers) (From Pough et al. 1989).
The sense of taste in aquatic organisms is probably very similar to the sense of taste in terrestrial organisms. In both cases, the chemicals which will be tasted must be dissolved in water, and the only difference between the aquatic organisms and terrestrial organisms is that food comes wet to aquatic organisms.
Figure 2. Olfaction with and without a current. In the upper drawing, the current forces the scent of the prey (P) into a long narrow plume. Organisms upstream (A) or to the side (B, D) cannot smell the prey, although organisms far downstream (C) can. Without a current, the scent diffuses in a circle, meaning that any close organism (E, F, G, I) can detect the prey, while an organism further away (H) cannot.
The senses of mechanoreception are at least as well developed in aquatic organisms as in terrestrial ones. Among vertebrates, there are sensors in the skin that are sensitive to light and deep pressure, pain, heat, and cold. Other sensors gauge the strain on muscles, tendons, and ligaments and thus send information to the brain on the relative position of the various parts of the body in relation to each other. Organisms with exoskeletons are not as well endowed with such a range of sensors. The pressure sensors, for instance, would be of little use beneath a hard exoskeleton.
Most arthropods use setae, socketed hairs with nerve cells at the base, to detect contact with other structures, wind or water currents, etc. Special setae at joints are responsible for proprioreception. Setae are often contained in structures with small crystals; these structures are known as statocysts; movement of the crystals as affected by gravity or acceleration in any direction is sensed by the setae and passed onto the brain. This gives organisms with statocysts a sense of gravity (which way is up?) and motion. A very similar, but more complex, system is used by vertebrates. Many vertebrates also use specialized hairs, such as those around the muzzle of a seal, to heighten the sense of touch.
The sense of hearing - distance mechanoreception - is used to detect movements in the fluid (air, water) surrounding the organism. This often gives information about what is happening some distance from the organism. The world, particularly the undersea world, is a noisy place, Jacques Cousteau's book The Silent World notwithstanding. Waves, undersea tectonic activity, swimming animals, vocalizations, rainfall, etc., all set up vibrations in the water that can be considered sound. Streams in particular are very noisy environments, with current sounds and rocks clicking together.
Some basic physics of sound: Sound travels faster in water than in the air; the exact speed varies with density and thus with temperature, salinity, depth, and pressure. Adjacent layers of water with different densities can bend sound waves in unusual ways, creating effects where one organism might not hear another organism directly below it, while a third organism miles away at the right level might hear clearly. The U.S. Navy, which uses sound to locate enemy vessels (and depends on its own vessels not being heard), spends a lot of money studying how sound travels in the ocean, and knows more about it that anyone else - but they're not telling. Sound travels through a medium (despite what you hear on Star Trek, explosions in space are noiseless) and arrives as a series of pressure oscillations between high and low pressure. Humans can typically hear oscillations between about 30 oscillations per second (hertz) up to 20,000 hertz; dogs, of course can hear higher pitched sounds and thus their hearing extends past 20,000 hertz. Also, as a general rule, higher-pitched sounds are more directional, while it is hard to localize low-pitched sound. Placement of midrange and tweeter components, which carry the higher frequencies, in a stereo system is more critical than placement of the woofers, which carry only the bass (low-frequency) sound; bass does not contribute to the stereo image.
Certain organisms, such as whales and a few fish, use sound to communicate, but overall the practice does not seem to be as common in the water as it is on land where the air is full of the sounds of animals, particularly birds and insects, communicating. Perhaps this is the reason for Jacques Cousteau's title. But is there no communication taking place, or is it just so different that we don't recognize it? Two phenomena I will mention here suggest that the latter may indeed be the case.
One of the most fascinating experimental studies I have read (and you will too) was done recently by Barbara Peckarsky and R.S. Wilcox (Peckarsky and Wilcox 1989). Peckarsky has been studying predatory encounters between stoneflies (the predators) and mayflies (the predatees) in streams. She has been working for some time to document the ability of both predator and prey to sense each other chemically at a distance, an ability that her behavioral data indicates should exist. As a sidelight, she began to wonder if stoneflies could hear the mayflies as they swim away. She teamed up with Wilcox, who has a real mind for experimentation, and got some very interesting results.
First, they took living mayflies and glued tiny magnets to their backs. They got the mayflies to swim near a speaker placed in the water. The vibrations of the magnet as the mayflies swam induced tiny currents in the magnet of the speaker, and these currents were amplified and digitally recorded. The recordings were placed on microchips, much in the same way that music is sampled (you can buy a keyboard for about $30 which can do this). They then placed dead mayflies or clear plastic models of mayflies with attached magnets in the water near living stoneflies and a speaker, and this time played back the amplified signal (the cone on the speaker was removed to prevent the actual sound waves from forming). The signal sent to the speaker caused it to produce magnetic waves which cause the magnets on the dead mayflies or models to vibrate the same way as the living mayfly had when it swam. The stoneflies paid a lot of attention to the models whenever the sound was on, indicating that they could 'hear' the swimming movements. Peckarsky called it a "hydrodynamic cue", but a vibration of about 2,000 hertz is well within what we normally call sound.
Similar abilities are well known to ichthyologists, long familiar with the lateral line of fish. The lateral line senses movement of the water around the fish. Much of this movement is what we typically would call sound (fish have a separate sense of hearing also). It is hard to imagine how the fish perceives that outside world through the lateral line, since we have no comparable sense. Still, we can observe fish in which the lateral line is damaged, and find that it is important for the fish to have an intact lateral line if it is to school with other fish, avoid predators, find prey, navigate between obstacles, and so on, particularly in turbid waters.
Other aquatic organisms which use distance mechanoreception include a wide variety of neuston which sense surface waves. For some, like water striders, this translates into an ability to find struggling (wave-making) organisms trapped in the surface film and thus home in on a potential meal; water striders also send their mating calls by vibrating the surface and making waves. Other organisms, such as the whirligig beetles (Gyrinidae), are even more sophisticated; they can use the waves they create as a type of sonar. Waves made by a gyrinid bounce off objects in the water and return, and the beetle is able to use this information. How thousands of these beetles in an aggregation make sense of the many waves formed is still a bit of a mystery, however; presumably they use some kind of encoding system as do bats.
Use of sonar to tell how far away structures are is not confined to beetles, however. The skill is well-documented in many marine mammals, which produce sounds by making clicks with their tongues or other parts of the nasal-esophageal complex. These clicks are often at very high frequencies to improve both directionality and resolution, and may be further focussed by bodies of fat or oil in the head. It has been demonstrated that dolphins can resolve between objects very close in size; overall performance is probably better than what can be achieved with eyes in slightly turbid water. And, of course, sonar works equally well in turbid water or at night.
Reception of electromagnetic information by organisms usually occur in that range of the spectrum having wavelengths between about 300 and 700 nanometers that we call light (Fig. 3). The shorter wavelengths in this range have the most energy and are known as ultraviolet or UV. Next comes the visual spectrum (for humans) or blues, violets, greens, yellows, oranges and reds. Finally, at longer wavelengths, is the infrared, or IR. Vision is restricted to these wavelengths for physical reasons. Shorter wavelengths carry too much energy and would damage the sensitive structures needed for sight. Longer wavelengths often don't have enough energy, are difficult to focus, and when they are focussed require extraordinarily large eyes because of the long wavelength.
Figure 3. The electromagnetic spectrum. The region we call visual light (for humans, at least) is expanded in the upper figure. Wavelengths in the upper figure are in nanometers; in the lower they are in meters.
All light-related senses rely on photoconversion of chemicals by light in specialized nerve cells or photoreceptors. At the simplest level, photoreceptors simply indicate the presence or absence of light, and such a sense is all that many organisms need. More complicated photoreceptors can detect light intensity as well. The next step up is to form an image, and the biological world has taken two major paths. The compound eye used by invertebrates is composed of many separate components or ommatidia, each of which forms an image. Such an eye is very good at picking out movement; less good at picking out patterns. The camera eye, used by vertebrates and mollusks, is composed of a single optical unit with many individual neurons. Camera eyes form single images in the brain, and are better at picking up patterns than at detecting movement.
Color vision is possible in both systems. One simple method of obtaining color vision is to place pigments, which allow only selected wavelength to pass, in the light path of a neuron. When a neuron shadowed by a green pigment, for example, fires, the brain gets a message that green light has been detected. Vertebrate photoreceptors come in two basic types; rods, which are very light sensitive and form colorless, slightly fuzzy images in low light, and cones, which require more light and are individually sensitive to either red, green, or blue light. Cones form color images of great resolution. The ratio of rods to cones is high in nocturnal mammals (most mammals are color blind), and low in most birds (which have very acute vision).
Another important aspect of vision is the location of photoreceptors. Simple photoreceptors may be scattered all over the body, but more advanced systems are usually outgrowths of the brain itself. Often two eyes may overlap for at least part of their field-of-view, this allows for binocular vision and accurate depth perception, an advantage for predators or organisms moving in complex environments. Eyes which do not overlap to any great extent may allow the organism to take in more at a glance, and are of particular use to prey species.
Water is not a good visual medium. As we saw earlier, light is attenuated in water, and turbidity exacerbates the problem. In many aquatic habitats, there really isn't enough light to see by our terrestrial standards. Organisms living in such water make extensive use of other senses, and are usually drab in color since color is meaningless. Colorful aquatic organisms usually signal the availability of light and clear water; it is no accident that colorful tropical fish come from clear waters, and that coral reefs, always located in shallow clear water, have an abundance of colorful species. Remember, though, that color perception changes with species and as the spectral composition of light changes with depth, so the "true color" of an organism can only be judged through the eyes of other inhabitants of its normal habitat.
Another problem that may occur with aquatic organisms which move between terrestrial and aquatic habitats is that of refraction. Simply put, refraction is bending of light that occurs whenever light moves from one medium to another - from water to air, or water to glass, for instance. Eyes which are adapted for the refraction that occurs at the interface of the solid, clear cornea and the air, for instance, will not be able to focus as well when the air is replaced by water. Organisms such as diving birds or turtles can compensate to some extent by having eyes with greater ability to focus, but this is only a partial solution. Humans solve the problem by using glass or clear plastic to encase a small volume of air over the corneas; this practice results in a distorted, but very clear image (the distortion manifests itself as magnification). Other organisms take another path. Both archerfish (camera eyes) and whirligig beetles (compound eyes) have developed additional eyes, so that they have one pair for use above water, and one below. The archerfish uses its terrestrial eyes to look for insects which it will knock into the water with a squirt of water, and its underwater eyes to watch for predators; the gyrinid uses all four eyes to scan for predators, which may come from above or below (they use their sonar to find food).
Because of the way light is attenuated in water, the ability to sense light above and below the human visual spectrum is not as common in water as it is on land. Insects in water probably can see some things in the UV spectrum, but apparently nothing like the IR vision of rattlesnakes has developed in H2O, where IR is absorbed quickly.
What water takes away in terms of radioreception of visual wavelengths is more than given back, however. Water is a much better conductor of electrical current than air is, and a number of organisms can detect electrical and magnetic forces. On the simple end, there are bacteria which can align themselves with the Earth's magnetic field; on the complex end there is the knifefish, which can discriminate between very small objects even in turbid water using its electric sense (Fig. 4).
Figure 4. Electric sense in the knifefish. Electrical fields set up by the fish (lines) are affected by nearby objects (circles). Strong conductors such as living organisms (dark circle) cause the lines to converge, and this can be sensed by the fish. Weak conductors, such as inanimate objects (light circles), cause the lines to diverge (from Lissman, H.W. 1963).
All organisms produce electrical currents. A variety of aquatic organisms can detect these currents with specialized neurons. Such electrical sense has been found in a number of invertebrates and many aquatic vertebrates including sharks, fish, and even mammals such as the duckbill platypus. Electrical senses are important in turbid waters such as muddy rivers or the vicinity of a bleeding victim after a shark takes its first bite (scarlet billows, through the water ....). Often, the electrical sense neurons are concentrated near the head or in a structure that is placed in contact with a muddy bottom, such as the barbels on the chin of a catfish (which also have chemoreceptors), or the bill of a platypus. Other organisms go so far as to create their own weak electrical currents (modified muscles can do the trick) and actively search out prey. The latter is done by the knifefish, a denizen of muddy Amazon tributaries (Fig. 4). Active electrical senses work best when the body is straight, so the knifefish has abandoned normal propulsion via the tail in favor of propulsion vial undulations of the dorsal and ventral fins. Still other electrical fish, such as the electric eel, catfish, and ray, take the generation of the electrical current a step further; they typically generate enough electrical current to stun their prey or dissuade a potential predator.