Advances in Animal and Comparative Physiology: Advances in Physiological Sciences: Proceedings of The 28Th International Congress of Physiological Sciences Budapest 1980

1980

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 would grasp her and readily mate with her. However, if the magnetic field was activated after he had grasped the female, but before copulation had occurred, he would immediately let go, apparently believing he had made a homosexual mistake (Wilcox 1979).

Sound and sonar

What humans perceive as sound is acoustic waves between about 50 and 20,000 Hz, but animal hearing extends beyond this range. It has long been known that dogs are sensitive to much higher frequencies than we can hear, but real progress commenced when Donald Griffin resolved the centuries old mystery of how bats can fly about unhindered in complete darkness, and avoid collision with objects placed in their way. With the aid of microphones responsive to higher frequencies than perceived by humans, Griffin discovered that bats emit high-frequency sound pulses, and that the echoes or reflections of these pulses are used to obtain information about the environment. This led to the discovery of a whole world of ultrasonic signals, audible to a wide variety of animals but not to humans.

In flight insect-eating bats emit continuous trains of short pulses or clicks of sound in the frequency range of 25,000 to 100,000 Hz. Each pulse lasts for a few milliseconds or less, and is followed by a brief pause before the next pulse. The number of pulses may vary from a few per second, up to as many as 200 per second, each pulse lasting less than one millisecond. In principle, the system is the same as echo-sounding or sonar, which is used to determine the distance to a reflecting object based on the time for an emitted signal to return to the emitter (Griffin 1958).

High frequency sound is particularly well suited for the accurate determination of the location of objects. Firstly, short wavelength sound is more directional than longer wavelengths, and secondly, the shorter the wavelength, the smaller is the object that will give a reflection. This is of obvious value for animals that feed on small insects. Experiments in a darkened room show that bats can avoid wires strung across their flight path if they are as small as 0.3 mm thick. As the bats emit sound of 3 mm wavelength (100,000 Hz), they are able to detect the reflection from objects that are no more than 1/10 of a wavelength in diameter.

One group of bats, the fisheating bats (Noctilio), also seem to use acoustic signals to locate their prey. They fly close to the surface of the water with their disproportionately large feet periodically lowered below the surface. Small fish near the surface are speared on the long, sharp, forward pointing claws and are transferred to the mouth. Only the feet enter the water, but it is not certain how the bats perceive the location of prey. One hypothesis is that they depend on echolocation of surface disturbances or ripples caused by a fish close to the surface (Suthers 1965).

Sonar, or acoustic orientation, is useful for many animals that are active in darkness. Not only bats, but some cave-dwelling birds use acoustic orientation. Furthermore, acoustic orientation works well in water. Dolphins and whales use echolocation to find food and avoid collision with obstacles and with the ocean bottom. In open water there are few obstacles, but at night and at depths where no light can penetrate the sonar is of inestimable value.

One particular species, the blind river dolphin of the Ganges and Indus river systems, is particularly interesting. It normally swims on its side, probably a useful adaptation because the normal up-and-down movement of the tail fluke of dolphins might be impractical for an animal that spends much of its time very close to the river bottom. In the murky river water vision is of little or no use, and acoustic cues seem to give all the necessary information about the surrounding world. Its eyes are vestigial and lack a lens, and could at best serve as light detectors.

Infrasound

What I have discussed so far is familiar to many; I will now turn to material that may be less familiar. The first subject is the perception of sound waves at frequencies much below what humans can perceive, so-called infrasound.

Studies by Kreithen (1979) at Cornell University have revealed that homing pigeons can detect extremely low sound frequencies, as low as 0.05 Hz. As 1 Hz is one cycle per second, 0.05 Hz corresponds to one cycle per 20 seconds. The sensory response may be related to the structure of the ear because surgical removal of middle or inner ear structures reduces or eliminates the response to infrasound.

The 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.

We can now ask whether the unexpected sensitivity to infrasounds is a component of the highly complex navigational system of homing pigeons. Could infrasounds that originate, for example, from strong winds blowing over a mountain range give useful geographical information? Direction of the sound cannot be obtained by comparing the phase shift or time of arrival for signals received by the two ears. However, a flying bird could use the differences in the Doppler shift of the infrasound frequency caused by their own flight velocity if they fly towards and then away from the source of the infrasound. If pigeons could detect a 5% change in sound frequency, the Doppler shift caused by their flight would be more than sufficient, for flying at 20 m per second could generate as much as a 12% shift in frequency.

The discovery of sensitivity to infrasound may lead to a revaluation of the many anecdotal reports of abnormal animal behavior prior to earthquakes. Current information is at best suggestive, but knowing that sensitivity to infrasound has just barely been discovered, it would be unwise to predict future developments.

LIGHT AND ELECTROMAGNETIC RADIATION

I now wish to turn to a discussion of light and other electromagnetic radiation. For humans vision undoubtedly provides the most important channel for information about the environment, but animals may perceive qualities that we are unaware of.

A very important approach to animal sensory physiology was developed early in this century by von Frisch. He trained animals to respond to certain sensory cues, and he could then test whether they could discriminate changes in these cues. In this way it was possible to settle the old question of whether animals can distinguish and recognize different colors. The clear and unequivocal answer was that many insects, fishes, birds, and some mammals can indeed discriminate color.

Human vision extends from about 400 nm in the violet to about 750 nm in the red. Is animal light perception within the same range? About one half of the solar radiation that reaches the earth’s surface lies in the near infrared, beyond the 750 nm limit for human vision. It is unlikely, however, that infrared radiation is important in visual processes, for in these wavelengths each light quantum carries insufficient energy to cause photochemical reactions. At the other end, however, in the near ultraviolet, the higher quantum energy has pronounced photochemical effects. The human retina is in fact sensitive to ultraviolet radiation, and it is the filtering effect of the intervening structures that prevents these wavelengths from reaching our retina. This may be an advantage, however, for the chromatic aberration in the eye becomes increasingly severe at shorter wavelengths.

However, the lenses of most diurnal birds are optically clear and presumably transmit ultraviolet light, and it has been shown that pigeons and more recently hummingbirds, can discriminate ultraviolet light (pigeon, Kreithen and Eisner 1978; hummingbirds, Goldsmith 1980).

It has long been known that insects are sensitive to ultraviolet light, and as the structure of their composite eyes yields equal visual acuity at all wavelengths, sensitivity to ultraviolet is no disadvantage.

The sensitivity of insects and of hummingbirds to ultraviolet has a striking counterpart in the coloration of flowers. Many flowers that depend on insects for pollination may look uniformly colored to humans, but in ultraviolet light they reveal striking patterns of nectar guides, invisible to a human observer but revealed by photography.

One question that arises in connection with the sensitivity to ultraviolet is whether a fourth retinal pigment is present, in addition to the red, green, and blue-sensitive pigments associated with trichromatic color vision.

During his work with honeybees, von Frisch discovered an additional visual cue, sensitivity to the polarization of light. In their foraging activities honeybees use the sun to indicate compass direction. To compensate for the movement of the sun across the sky, the bees have an „internal clock" that provides the necessary correction. Von Frisch discovered that on cloudy days, in the absence of a visible sun, bees can still orient in the correct direction provided that a small piece of blue sky can be seen. The light from the blue sky is polarized, and its plane of polarization gives information about the actual position of the sun. Man is normally unaware of this polarization, which for bees provides important information. If bees are made to see the blue sky reflected in a mirror, it makes them orient in the opposite of the correct direction, as expected from the reversal of the plane of polarization caused by the mirror (von Frisch, 1967).

While many invertebrates are sensitive to polarized light, several studies of higher vertebrates have been negative. It was therefore a surprise that homing pigeons apparently use polarized light. Kreithen and Keeton at Cornell (1974) showed that pigeons can be trained to respond to polarized light. Why were these tests successful when other investigators had failed? The reason is a fundamental difference between the eye of the pigeon and our own. The retina of pigeons has specialized regions, each with its own peculiar organization. Pigeons use one portion of the retina for close objects, and a different part for distant targets. Polarized light from the sky comes from overhead and would normally fall on the part of the retina used for distant targets, and if experiments are arranged accordingly, the results are clear, pigeons can indeed detect the polarization of light.

We can now see that a great many visual cues that we as humans are blind to are not only sensed but are of great importance to many animals.

Infrared radiation

The spectrum of electromagnetic radiation extends on both sides of the visible spectrum, and, as I said before, at longer wavelengths than visible light, each quantum carries too little energy to have photochemical effects, Nevertheless, infrared radiation is perceived directly by a few animals that possess specialized infrared receptor organs. Some snakes have so-called facial pits or pit organs on the head that aid in the location of prey. A rattlesnake that strikes at a warm-blooded animal seems to be guided by the infrared radiation from the prey. If a dead animal is at room temperature, the snake will not strike at it, but if a dead rat is warmer than the surroundings, a blindfolded snake will strike correctly at it (Bullock 1956).

Neurophysiological studies confirm that the pit organs are sensitive to infrared radiation in the range of 10,000 nm, which is at the peak of the infrared radiation emitted from a mammalian body. Many other stimuli, sound, vibration, or light of moderate intensity, have no detectable effect on the pit organ. However, if objects at a temperature different from the surroundings are brought into the receptive field around the head, there is a striking change in nerve activity (Barrett et al. 1970).

How does the pit organ work? In the rattlesnake the pit itself is covered by a thin transparent membrane. A pore serves to equalize the pressure on the two sides, and it is therfore improbable that expansion of gas in the inner chamber has any role in the sensation of heat radiation. The hypothesis that the radiation is absorbed by a specific compound, analogous to the light sensitive pigments in the eye, is extremely unlikely because the quantum energy is too low. This leaves the possibility that the sensitivity of the pit organ is entirely thermal. Experiments with pure infrared wavelengths produced by a laser support this hypothesis.

The pit organs are located, one on each side of the head, between the nostril and the eye. Does this indicate that stereoscopic perception is possible, the way our two eyes are used? This seems highly likely, not only from observations of the precision with which a snake can strike, but also from studies of its brain activity.

When infrared radiation falls on the pit organ, electric potentials can be recorded from the optic tectum. This is in itself interesting, for the nerve from the pit organ is a branch of the trigeminal nerve and is completely separate from the optic nerve. Many neurons in the optic tectum respond to stimulation of the pit organ on the opposite side of the head. This has an obvious similarity to the way visual information is handled, with crossover in the optic chiasma being essential for stereoscopic vision and for interpretation of distance. It appears that information from the two pit organs is coordinated and interpreted in a similar way, providing information about distance as well as direction (Gories and Terashima 1973).

Infrared sensing organs are not common and are known only from pit vipers and boid snakes. It is unthinkable, with our present knowledge, that similar organs could function in aquatic animals. The minimal penetration of infrared in water and its high thermal conductivity and thermal capacity would make it virtually impossible to perceive the small amounts of heat involved. However, other sensory qualities can be used in water, and electricity provides one such possibility. Humans have no direct experience in this area which therefore seems quite strange to us.

ELECTRIC FIELDS

Already the ancient Greeks and Egyptians knew that some fish can produce strong electric shocks. As the nature of electricity was unknown to them, they must have found the phenomenon utterly mysterious.

The strongest electric fish produce discharges of several hundred volts, but a much larger number of fish deliver only weak discharges. Strong discharges can be used as defense and to stun prey, but very weak discharges were difficult to understand until it was found that they are used both for communication and to obtain information about the environment.

To utilize electric discharges to receive information, a fish must possess suitable electroreceptive organs. An electric discharge from a fish sets up an electric field around the fish, and this field is distorted to a different degree by conducting and non-conducting objects in the environment. These distortions are perceived by the electroreceptive organs, which are located in the skin and are sensitive to extremely small currents.

Most electric fish live in dark and murky water where the visibility is poor, and they are often nocturnal and have poorly developed eyes. The value of an electric sense is therefore obvious, it permits scanning of the environment when vision is inadequate and it is independent of the day-and-night light cycle. The greatest disadvantage of an electric sense is its very limited range, which usually is no more than a few meters.

The ability to use self-generated impulses to scan the environment has a superficial similarity to the use of sound pulses by bats, but the electric system is different because there is no reflection or echo involved; it depends on the distortion of the electric field.

The ability to sense electric fields is not limited to those fish that produce their own electric pulses; many non-electric fish are able to perceive even very weak external electric fields. For example, sharks, eels, and catfish are extremely sensitive to weak electric fields, and yet lack electric organs. It was suggested by Lissmann (1958) that this electrosensitivity might be used to detect such external sources as the muscular potentials of prey.

That this is indeed the case has been beautifully demonstrated by Kalmijn (1971). He introduced a small flounder into an aquarium and permitted it to hide in the sand at the bottom. A dogfish that was stimulated by a few drops of fish juice would eagerly but haphazardly search the bottom for food, and if it came within ten or fifteen cm of the hidden flounder, it would make a well-aimed strike to uncover and devour the prey. In the next experiment, visual and chemical cues were eliminated by covering the flounder with an electroconductive chamber made of agar, but the dogfish would still strike at the location of the flounder. Agar made up with sea water is electrically transparent, but covering the chamber with a thin insulating film of polyethylene eliminated the sharkf’s response. To provide direct evidence for electroreception, two electrodes hidden in the sand were used to produce electric fields simulating the strength and rhythm of the flounder’s respiratory muscles. As expected, the shark responded to the electrodes as if they were the living flounder. In fact, if a shark was tempted with pieces of fish, it would excitedly search for food, and if it came in the vicinity of the electrodes, it would attack the electrodes instead of taking nearby pieces of fish.

These experiments were performed with captive sharks as well as with skates and rays. However, Kalmijn also carried out field experiments. Near Woods Hole, at a depth of a few meters, a length of plastic tubing was placed on the bottom and observed from a rubber raft on the surface. A small amount of liquified herring was released as a chemical cue from one spot, and stimulating electrodes were placed on both sides of the odor source at a distance of 25 cm. A shark attracted by the olfactory signal would circle around, and when it came near the outlet for the odor signal, one set of electrodes was turned on. The shark now turned sharply towards the electrode and attacked it viciously. If the current was switched to the other set of electrodes, the animal would. let go and strike at the second set of