NEW WINDOWS ON THE WORLD: SENSORY MODALITIES BEYOND HUMAN PERCEPTION
Knut Schmidt-Nielsen, Department of Zoology, Duke University, Durham, N. C. 27706, USA
Publisher Summary
This chapter discusses the sensory modalities beyond human perception. Sensory information can be either chemical or physical in nature. Chemical stimuli are familiar to humans through olfaction and taste, but many physical stimuli are beyond human perception. Sound frequencies beyond the range of hearing are important to many animals, both at very high frequencies and, more unexpectedly, at very low frequencies. For many animals, the ability to perceive light extends into the ultraviolet part of the spectrum to which humans are blind. The polarization of the light is perceived and provides essential information for the orientation of many animals, not only insects but also many vertebrates. Sensitivity to infrasound may be very important to the birds for natural infrasounds originate from many sources, including thunderstorms, earthquakes, jet streams, and wind over mountain ranges. The attenuation of sound is inversely related to the square of the wavelength and infrasounds can, therefore, travel over long distances and can be detected at hundreds or even thousands of kilometers from their source.
INTRODUCTION
It was a great honor to receive the invitation to speak on the subject of recent developments in comparative physiology. In recent years, the interest in comparative animal physiology has increased rapidly, and, in addition, the developments have taken several new directions. There has been a trend away from studies of physiological functions in a laboratory setting towards a more meaningful perspective on animals as they function in nature, because a living, free animal is not the same as a laboratory specimen confined in a metabolic cage.
In nature animals move, seek food, escape from enemies, seek mates, fight, and run about. Striking advances have been made in the study of running, active animals, a field that will be discussed in the second introductory lecture this morning. The area that I shall discuss is what animals perceive of the world around us, for we now realize that animals obtain information about their environment in ways that a few decades ago were unknown to man. Recent advances in sensory physiology have been revolutionary by telling us that the sensory equipment of humans is incapable of receiving signals that to some animals give the most essential information about their surroundings. Therefore, we can truly say that comparative sensory physiology has opened new windows on the world around us.
SENSORY MODALITIES
Information about the environment is essential for survival. Information is needed for finding food to eat, and for avoiding predators and being eaten. Survival of the species depends on reproduction and the ability to locate mates, and often on orientation in the environment and an ability to find a „home” territory. Finally, among many highly organized animals the communication with individuals of the same species is an essential part of normal life.
Sensory information can be either chemical or physical in nature. Chemical stimuli are familiar to us through olfaction and taste, but many physical stimuli are beyond human perception. Sound frequencies beyond the range of our hearing are important to many animals, both at very high frequencies and, more unexpectedly, at very low frequencies. For many animals the ability to perceive light extends into the ultraviolet part of the spectrum to which we are blind. Furthermore, the polarization of the light is perceived and provides essential information for the orientation of many animals, not only insects but also many vertebrates.
The ability to sense electromagnetic radiation extends for some animals into the infrared part of the spectrum. This sensitivity is not based on the photochemical reaction with a visual pigment, but on an entirely novel type of sensory organ.
The ability to sense electric fields is much more widespread than was previously believed. It is common not only in electric fish, but also in a number of much more ordinary fish, both elasmobranchs and teleosts.
Finally, investigations during the last few years have demonstrated that some organisms use the magnetic field of the earth for orientation and navigation. In short, recent developments have revealed that many animals live in a sensory world entirely different from our own.
CHEMICAL STIMULI
For humans chemical stimuli are relatively unimportant while vision provides most of our information about the environment, and blindness leaves us nearly helpless. Hearing is very important for communication, but deafness is not critical to life. The inability to perceive olfactory or taste signals, in contrast, is relatively trivial, in fact so unimportant that we lack a common word to describe it. For animals the situation may be quite different: for many animals chemical senses are essential for life.
I shall say a few words about the impressive chemical sensitivity of fish and briefly discuss its importance. One of the most sensitive fish is the channel catfish, Ictalurus (Caprio 1975, 1977). The chemical receptors on the barbels around the mouth are highly sensitive to dissolved amino acids. The threshold concentration determined by electrophysiological methods is the lowest observed in any vertebrate; for the amino acid L-ala-nine it is between 10−9 and 10−11 molar. We can barely imagine what this dilution means. To reach a concentration of 10−10 M, we would dissolve in an Olympic size swimming pool no more than 23 mg of alanine, or less than 1/100 of a teaspoonful.
Such high sensitivity is not unique to fish. The spiny lobster, Panulirus, is especially sensitive to the amino acid taurine, which is common in many marine animals (Fuzessery 1978). Its sensitivity threshold for taurine is about l0−10 molar, requiring that we dissolve 33 mg of this amino acid in the Olympic pool. Note that an Olympic pool holds 2600 m3, and this amount of sea water contains about 92 tons of sodium chloride and other salts. It is difficult to imagine that the few milligrams of taurine can still be discovered by the sensory equipment of the spiny lobster in the presence of this immense amount of salt.
The old mystery of how a migrating salmon finds its way back to its native stream after spending several years in the ocean has now been clarified, mainly because of the excellent work of Hasler and his collaborators at the University of Wisconsin. Migrating salmon may cover thousands of kilometers in the sea before they run up rivers to shallow mountain brooks several hundred kilometers from the ocean, where they spawn in the very same stream where they were born. They have a remarkable urge to swim upstream, traversing rapids and waterfalls on the way, returning to the very same stream they left years before. After spawning they die, leaving their progeny to migrate to the ocean, grow to maturity, and return to the same stream several years later.
How can the adult salmon find its way back to its native stream? The olfactory sense of the salmon is necessary for the homing, and electroencephalographic evidence confirms its ability to sense chemicals in extreme dilution. Experiments with artificial chemicals not occurring in any natural waters confirm this ability. If salmon are exposed to such chemicals during the period preceding the oceanic migrations, they will return years later to water scented with the very same chemicals. It is clear that each stream in nature must have characteristic and persistent odors that are perceived and recognized by the salmon, and that the imprinted odor memory of the home stream is essential for the return to the spawning grounds (Hasler 1951, Scholz 1976).
The chemical senses are extremely important also for insects. For example, the mustard oils produced by cabbage and related plants of the mustard family attract the cabbage butterfly, which in this way finds the correct plant for deposition of eggs, thus providing the proper food for their growing larvae. These same mustard oils are actually defensive substances that keep other insects from attacking the plants. The cabbage butterfly, however, has been able to overcome the chemical defenses and uses the toxic oils to find the plants.
Chemical substances that serve as sex attractants are essential for the mating of many insects, and several such substances have been identified and synthesized. One example is the queen butterfly, a relative of the monarch. The male carries at the end of its abdomen two brush-like pencils that can be extruded. In courtship the male overtakes the female in flight and with the pencils everted brushes them against her antennae. The chemical that is transferred to the antennae is an aphrodisiac that induces the female to mate, and if the male is deprived of the brushes or merely of the chemical, he is unable to seduce a female (Pliske and Eisner 1969).
Chemical substances and their roles have been more carefully studied in ants than in most other animals. They serve not only as sex attractants, but among the non-sexual workers as trail substances, alarm substances, defensive substances, and so on. A wide variety of such substances have been identified; they are all volatile and their characteristics are well adjusted to the various purposes they serve.
I do not wish to leave the impression that only fish and insects live in a world of chemical signals, because chemical information and communication is important for organisms from uni-cellular to vertebrates. However, for lack of time I must turn to other sensory modalities.
MECHANICAL STIMULI
To humans sound is very important and constitutes our primary channel of communication, but for some animals other kinds of mechanical disturbances are primary channels of sensory information.
A few examples will suffice. Snakes possess two sensory systems which respond to both airborne sound and substrate vibration. Their auditory system is not very sensitive to sound but the sensitivity to head vibration is remarkable; Hartline has shown that at the best frequency a 1 ångström peak-to-peak amplitude is above threshold (Hartline 1971).
Another highly sensitive system is the lateral line of fishes. In a school of fish the movements of the individuals are extremely well coordinated and, to a human observer, they appear nearly perfectly synchronized. Fish in a school often swim at a constant pace and maintain characteristic individual distances, and the school as a whole executes complicated maneuvers that require individuals to respond exceedingly fast to velocity and direction changes of their neighbors. It is the mechanoreceptors of the lateral line that are used for monitoring the swimming speed and direction of travel of the neighboring fish. If a fish is blinded it is nevertheless able to match the velocity changes of its neighbors. It shows as high correlation as do controls, but section of the nerves to the lateral line makes them unable to do so (Partridge and Pitcher 1980).
A very elegant technique has demonstrated the importance of mechanical signals for sex discrimination in a water strider (Gerris remigis). Males of this species can produce surface wave signals at about 90 hertz, and these signals attract receptive females. Dr. Wilcox of the State University of New York glued a tiny magnet to the leg of a female water strider, and through an oscillating magnetic field he made the foreleg oscillate vertically, producing surface wave signals with the characteristic male frequency and amplitude. To exclude vision, the tests were carried out with masked animals. If a masked male approached a female with an inactive magnet, he ...