Summary. — It seems very difficult to reach any conclu- sion in the face of such contradictory evidence. The failure to obtain response to sound vibration in earless fish would seem to offer crucial evidence, and yet the cutting of the eighth nerve must produce profound changes in the motor apparatus of the fish. It must be remembered that the re- action of the fish to auditory stimuli (at least those which can be surely observed, such as the movements of the pectoral fins, starts, etc.) are not very marked at best and even those movements may be dependent upon the impulses which normally come from the semicircular canals, vesti- bules, etc. Elimination of these impulses, which occur when the eighth nerve is cut, might easily account for the 394 AUDITORY AND RELATED FUNCTIONS facts observed in earless fishes. It seems strange, since Parker so clearly recognizes the fact that sounds made under water are reasonably intense, that he did not repeat Bateson's experiment of tapping objects together under water outside the range of vision of the fish. Such an experiment upon one of the forms which gave positive re- sults would have been far more conclusive than all of the evidence he gathered through cutting the eighth nerve. Certainly the forms of apparatus used by Parker and by Bigelow to produce intense sounds are open to the severest kind of criticism. It would indeed have been hard to devise apparatus which would have offered more secondary criteria.
The lateral line organs. — Examination of the external markings of the fish shows a line which extends along the side from the head to the tail. The line is pierced at in- tervals by small pores, which lead into an underlying canal, the lateral line canal. This canal branches at the head into three divisions: one passes forward and above the eye;. a second forward and below the eye; and the third down- ward and over the lower jaw. The system as a whole is known as the lateral line system. The system in one or another form appears in amphibia in the water inhabiting stage as well as in fishes. The lateral line system is richly supplied with sensory structures, which look not unlike the ordinary taste buds. Microscopic examination shows that these sensory structures as a whole are made up of supporting cells and sensory cells, which are pear-shaped and supplied with cuticular hairs. It is around the base of these cells that the medullated nerve fibers end. The sensory innervation comes largely from the seventh and tenth cranial nerves. Various opinions have been held as to the function of these organs. As long ago as 1870 Schulze developed the view that the stimulus was to be found in mass movements of the water and in sound waves of too great length to affect the ear. Other views have been advanced as to their probable function. Certain observers who have made operative experiments have held the view that they were organs for the production of gas in the THE LATERAL LINE ORGANS 395 swim-bladder; that they were organs for secreting slime; that they were necessary to orientation, equilibration, etc. Recent experiments by Parker tend to support Schulze's (theoretical) view that they are intermediate in character between the skin and the ear and that the stimulus to which the lateral line organs respond is a water vibration of low frequency. By a very simple operation (sectioning the sensory nerves which run to these organs) the whole system can be thrown out of gear. When these nerves are ' sectioned the fish almost invariably recover. They are then hardly distinguishable from normal fish. This differ- ence, however, appears: If normal fish are observed in an aquarium it will be found that any slight jar or oscillation of the tank will cause them to dart at once to the bottom. The fish whose lateral line organs have been thrown out of gear will not respond to such a stimulus. They swim about even when the tank is violently agitated.
Hofer, however, does not accept this conclusion of Parker. He carried out an extensive series of investigations upon the lateral line organs. He asserts that the stimuli cited by Parker as affecting the lateral line system — such as slow vibrations obtained by jarring the aquarium, blowing waves across the water, dropping in stones, etc. — affect really only the cutaneous receptors. Hofer was enabled to get re- actions to these stimuli w^hen the lateral line system had been destroyed in certain fish (Cyprinus carpio, Cottus gohio, Esox Indus). They are more prompt and pronouncd when the fish are left for some time in a weak solution of strychnine. The reason why Parker failed to get such responses in fish whose lateral line organs were destroyed is due to the choice of a poor method of operation — one which destroyed along with the lateral line system certain of the cutaneous nerves supplying the skin of the head region (according to Hofer the skin of the body of the fish is not supplied with touch spots, i.e., with organs for the reception of such stimuli as fixed bodies, etc. In the head region the skin is supplied with such spots, also with warm spots, but it is lacking in cold spots). The loss of the very sensitive cutaneous areas of the head thus apparently 396 AUDITORY AND RELATED FUNCTIONS accounts for the results obtained by Parker. From numer- ous experiments Hofer concludes that the lateral line organs are stimulated only by the streaming movements of the water. Such streams exert continuous pressure which differs in direction and in force. Their function in guiding the fish in migration is apparent. The stream or current of water need only possess slight intensity — a stream too slight to influence the labyrinths will arouse the lateral line system. Hofer states that the organs are not directly involved in reactions to fixed objects. On the other hand, as the fish approaches fixed objects currents are generated which, when reflected towards the animal, stimu- late the lateral line organs. In this way these organs act like distance receptors. Increasing or decreasing the depth of the water (hydrostatic pressure) does not arouse the receptors in the lateral line organ.
BIBLIOGEAPHY Allen, Jessie, " The Associative Processes of the Guinea Pig," Jour. Comp. Neu. and Psych., 1904, XIV, 293.
Bateson, W., " The Sense Organs and Perceptions of Fishes, with Remarks on the Supply of Bait," Jour. Mar. Biol. Assoc, United Bernoulli, A. L., " Zur Frage des Horvermogens der Fische," PflUger's Archiv fur Physiol., CXXXIV, 633.
BiGELOW, H. B.. " The Sense of Hearing in the Goldfish, Carassius Auratus L.," Amer. Nat., 1904, XXXVIII, 275.
Cole, L. W., " Concerning the Intelligence of Baecoons," Jour. Comp. Neu. and Psych., 1907, XVII, 211.
Craig, Wallace, " The Voices of Pigeons Regarded as a Means of Social Control," Am. Jour. Sociol., 1908, XIV,, 86.
Franz, S. L, " Uber die sogenannte Dressurmethode f. Zentralnerven- systemuntersuchungen," Zenfhl. f. Physiol., 1907, CXXI, p. 583.
Hahn, W. L., " Some Habits and Sensory Adaptations of the Cave- Inhabiting Bats," Biol. Bull., 1908, XV, 135 and 193.
Helmholtz, H. L. F. von, On the Sensations of Tone as a Physi- ological Basis for the Theory of Music. New York, Longmans, Hofer, Bruno, " Studien iiber die Hautsinnesorgane der Fische," Berichte aus der Kgl. Bayerischen Biologischen Versuchsstation Johnson, H. M., "Audition and Habit Formation in the Dog," Be- havior Monographs, Ser. No. 8.
BIBLIOGRAPHY 397 Kalischee, 0., " Weitere Mitteilung iiber die Ergebnisse der Dressur als physiologiseher Untersuchungsmethode auf den Gebieten des Gehor-, Geruehs- und Farbensinns," Arch. f. Physiol, 1909.
" Zur Function der Schlafenlappens des Grosshirns," Sitz. der K. Preuss. Akad. d. Wisschftn., 1907, p. 204.
Keeidl, a., " Ein Weiterer Versuch tiber das angebliche Horen eines Glockenzeichens durch die Fische," ihid., 1896, LXIII, 581.
" Ueber die Perception der Schallwellen bei den Fischen," Arch. ges. Physiol., 1895, LXI, 450.
Lashley, K. S., '■ Reproduction of Inarticulate Sounds in the Parrot," Jour. Animal Beh., 1913, III, 361. Lee, F. S., " The Function of the Ear and the Lateral-Line in Fishes," Am. Jour. Physiol., 1898, I, 128. MuNK, H., JJeher die Functionen der Grosshirnrinde. Berlin, 1890. Paeker, G. H., " The Effects of Explosive Sounds Such as Those Produced by Motor Boats and Guns upon Fishes," Bureau of Fisheries, Document 752.
" The Function of the Lateral-Line Organs in Fishes," Bull. Bureau Fisheries, 1904, XXIV, 183.
" Hearing and Allied Senses in Fishes," Bull. U. S.
" The Sense of Hearing in Fishes," Amer. Nat., 1903, XXXVII, 185. " The Structure and Function of the Ear of the Squeteague," Bull. U. S. Bureau Fisheries, 1908, XXVIII, 1211. Pfungst, 0., Clever Hans. New York, Holt, 1911. Retzius, G., Das Gehdrorgan der Wirheltiere. Morphologische- Histologische Studien. I. " Das Gehororgan der Fische und Amphibien." Stockholm, 1881. RoTHMAN, Max. " LTeber die Ergebnisse der Horpriifung an dressierten Hunden," Arch. f. Physiol., 1908, p. 103. Rouse, J. E., "The Mental Life of the Domestic Pigeon," Harv.
" Respiration and Emotion in Pigeons," Jour. Comp.
Sackett, L. W., " The Canada Porcupine: A Study of the Learning Process," Behavior Monographs, Ser. No. 7. Selionyi, G. p.. Contribution to the Study of the Reactions of the Dog to Auditory Stimuli. St. Petersburg, 1907. (In Russian.) Shepherd, W. T., "The Discrimination of Articulate Sounds by Cats," Am. Jour. Psych., 1912, XXIII, 461.
" The Discrimination of Articulate Sounds by Rac- coons," Am. Jour. Psych., 1911, XXII, 116.
" On Sound Discrimination by Cats," Jour. Animal " Some Mental Processes of the Rhesus Monkey," Psy- chological Monographs, Ser. No. 52.
Swift, W. B., " Demonstration eines Hundes dem beide Schlafen- lappen extirpiert worden sind," Neurol. Centhl., XXIX, 686.
" Psychological Results in Reaction to Tone Before and After Extirpation of the Temporal Lobes," Jour. Animal 398 AUDITORY AND RELATED FUNCTIONS SzYMANSKi, J. S., " Lernversuche bei Hunden und Katzen," Archiv f. d. ges. PhysioL, 1913, CLII, 307.
WiEDERSHEiM, R.., Vergleichende Anatomie der Wirbeltiere. Jena, Gustav Fischer, 1906.
Wilson, G. J., and Pike, F. H., " The Effects of Stimulation and Extirpation of the Labyrinth of the Ear and Their Relation to the Motor System." I, Experimental. Phil. Transactions of the Royal Society of London, Series B, CCIII, 127.
Yerkes, R. M., The Dancing Mouse. New York, Macmillan, 1907.
" Inhibition and Reinforcement of Reactions in the Frog," Jour. Comp. Neu. and Psych., 1904, XIV, 124.
" The Instincts, Habits, and Reactions of the Frog," III, Auditory Reactions of Frogs, Harv. Psych. Stud., 1903, I, " The Sense of Hearing in Frogs," Jour. Comp. Neu.
Yekkes, R. M., and Morgulis, S., " The Method of Pawlow in Com- parative Psychology," Psych. Bull., 1909, VI, 257.
Zeliony, G. S., " Ueber die Reaktion der Katze auf Tonreize," Zeit.
Zenneck, J., " Reagiren die Fische auf Tone," Arch. f. ges. Physiol., ZoTH, O., " Ein Beitrag zur den Beobachtungen und Versuchen an japanischen Tanzmatisen," Archiv. f. d. ges. Physiol., 1901, LXXXVI, 147.
CHAPTER XIII SMELL, TASTE, AND THE '' COMMON CHEMICAL SENSE " I. Smell. — Olfactory reactions in mammals. — Romanes' test of the hunting dog. — Difficulties in the way of explaining the hunting behavior of dogs. — Experiments on the olfactory sensitivity of birds. — The sense of smell in fishes. — Experiments by Parker and Sheldon. II. Taste. — Location of gustatory organs. — ^Her- rick's experiments upon the functional significance of the taste buds. — Parker's experiments upon the gustatory responses of fishes. 111. The " common chemical sense." — Introduction. — Sheldon's experiments upon the smooth dogfish. — The " common chemical sense" in amphibia. — Summary.
I. Smell I. Smell Olfactory reactions in mammals.^ — Behavior can con- tribute but little at the present time towards the solution of the many problems which arise in the field of smell in mammals. In the course of a number of years of work upon the other senses several incidental observations have been made upon mammals which show that olfactory stim- uli influence behavior, but few specific studies have so far been instituted. The technical difficulties in the way of making careful experiments are very great. Smell sen- sitivity in the white rat has been tested incidentally several times in connection with experiments upon learning: It has been shown that this animal, when given the opportunity of going to two food boxes, the one of which contains a bottle filled with bread, the other of which contains a similar bottle without food and a piece ^ We know from Read's recent work that the olfactory nerves are large and numerous in the dog and in the cat, and that they are larger and more numerous in the former than in the latter. In both dog and cat nearly one-half of the ethmoturbinal folds bear olfactory structures, which is a much larger distribution than we find in man.
400 SMELL of buried cheese, runs quickly to the food box con- taining the empty bottle and the buried cheese. Certain experiments have been made to test whether rats track one another through entrances, etc. The following apparatus was used: Four rectangular boxes with wooden sides and wire netting at the two ends were constructed. Through one of the wire ends of each box a pasteboard mailing tube three inches in diameter was admitted. Strips of paper were rolled and used to line the tubes. Two of the tubes whose positions could be varied were kept smelling of the odor of a rat and two were kept free from such odor (the lining was changed after each test). The animal could obtain food in any one of the four boxes after pass- ing through the tube attached to it. The animals were admitted to the restraining cage first on the West side, then in order, East, North, and South. The young rats failed to show any tendency to track one another. On the other hand, when adult males and females not living in the same cage were tested, the results were positive. In 24 trials the total number of tubes entered smelling of the opposite sex was 19, whereas the total number entered free from odor of opposite sex was 5. When white rats were tested on the problem given the ring dove (see p. 406) they learned after a short time to run towards the source of the odor (oil of bergamot). In a total of 59 trials where there were 3 chances of error on each test the male rat's responses were right in 62^ of the trials, the females, 71^. Considering the small number of trials given this high percentage of correct responses is remarkable. In- cidental tests upon raccoons, porcupines, and monkeys fail to show any great use of the sense of smell. Cole states that the raccoon will find a piece of sugar lying upon the floor of the cage more quickly than a piece of meat. Mon- keys occasionally discard an object after smelling it before putting it into the mouth (but rarely). The Cebus will occasionally smell an object, discard it, and then wipe the hands upon the body.
Romanes' test of the hunting dog. — The dog's sense of smell is probably very highly developed. In a well-known HUNTING BEHAVIOR OF DOGS 401 experiment Romanes tested the ability of a setter to track her master's scent.
He used twelve men, forcing them to walk Indian file, each man taking care to step in the tracks of the leader. " I took the lead while the game-keeper brought up the rear. When we had walked two hundred yards, 1 turned to the right, follow^ed by five of the men; and at the point where I had turned to the right, the seventh man turned to the left, followed by all the remainder. The two parties...having walked in opposite directions for a consider- able distance, concealed themselves, and the bitch was put upon the common track of the whole party before the point of divergence. Following this common track with rapidity, she at first overshot the point of divergence, but quickly recovered it and without hesi- tation chose the track which turned to the right." ^ Difficulties in the way of explaining the hunting be- havior of dogs. — It is believed by hunters that the com- mon hounds used for hunting rabbits in the South can follow a trail 10 to 12 hours old without back-tracking! It has been stated that the bloodhound has an even more highly developed sense of smell. Some writers have gone so far as to say that the animals will follow a trail at least 24 hours old and in the direction taken by the quarry. In trying to explain how the dog follows a trail always in the forward direction we meet with a number of difficulties. It is generally supposed that the dog is able to do this on the basis of the difference in the intensity between the tracks earlier made and those made later. Johnson finds on theoretical grounds that this explanation is not satisfactory. He presents the difficulties in the way of such a view so clearly that we quote his statements at length: " Suppose that in each of a series of tracks, a, h, c, etc.. a like quantity of the same single smell-substance had been deposited by the rabbit; that the tracks had been made one second apart, and that a was made three hours ago. It is evident (changes of chemical composition heing excluded) that the smell-substance is greatest in quantity when first deposited. It becomes dissipated in time so that in this case there is hardly enough left in the track a to affect the dog.
" If the smell-substance is deposited in a gaseous state its diffusion could be represented by one of the well-known ' curves of decay.' The absolute intensity of the stimulus (i.e., the amount of odorous 402 SMELL substance present in the track at a given moment of time) may, within limits, be formulized: Log St = Log So — kt, wherein So equals the amount of the substance first deposited, t the time which had elapsed since the deposit was made, and k a con- stant function dependent on conditions of temperature, pressure, etc, " In the case under consideration the stimulus-intensity at the track a is nearly zero when it is presented to the dog. The absolute difference of stimulus-intensity at a, b, and c would have to be ex- tremely small, since the difference in the respective values of t is of the order of one part in nearly 11,000. Further: even this differ- ence between a and h would exist only if they were simultaneously presented. Since the dog is supposed to be following the trail of the rabbit, for him to be affected by even a part of the difference between a and 6 it is necessary that he travel faster than did the rabbit in making the tracks. If the dog travels at the same rate as did the rabbit, when he reaches 6 its intensity will be just equal to that of a when a was passed. Moreover, in actual practice other difficulties arise. Suppose the rabbit has run from moist ground to dry ground. The smell-substances are diffused more rapidly under conditions of relatively small humidity than under conditions of greater humidity. The stimulus-intensity of the recently made tracks on dry ground could thus be less than those made earlier on the wet ground. In such case our assumption fails to explain the dog's failure to show confusion.
" But the dissipation of the smell-substance may be a complex process. For instance, it may be deposited, not in a gaseous state, but as a liquid or solid. In such case vaporization must precede diffusion. Vaporization, conditions being constant, proceeds at nearly a uniform rate in the open air. The amount of substance present in a gaseous state might thus be as great at a very advanced stage of dissipation as at an earlier stage. Since the substance to be odorous must be gaseous, we are not warranted in assuming that the stimulus-intensity is greater at a recently made track than at one made earlier, unless we know that all the smell-substance in the later track has been vaporized.
" There may be other factors such as chemical changes by which the deposited substance becomes odorous, etc., but consideration of them only increases the presumption against the intensity-difference theory.
" It has been suggested also that the dog may have an acute olfactory sensitivity to the form of the tracks made by his quarry and follow the trail from heel to toe. Certain features of the dog's behavior certainly indicate that he is very sensitive to differences of spatial position of olfactory stimuli. Another suggestion is that the smell-substances deposited by the different parts of the foot or body may differ specifically in stimulating quality, and that the dog is affected by this difference. Assuming either of these sug- gestions as a complete explanation of the dog's hunting behavior would require us to expect a bloodhound striking a man's trail at right angles, to back-track if the man had walked backward instead of forward across the field.
SMELL IN BIRDS 403 SMELL IN BIRDS 403 " Dr. P. W. Cobb has suggested a simple hypothesis; that the dog's sense of direction may be due to the trailing of ground smell- substances. For instance: the smell-substances affecting a dog trailing a man who had crossed a mint-bed might be (1) ground -|- man; ( 2 ) ground -j- man -\- mint, the mint being intense; (3) ground -|- man -|- mint, the mint-smell-substances diminishing rapidly in the direction the man had taken. The hypothesis impresses the writer as being valuable, although it does not afford a complete explanation of the facts as variously alleged.
" The value of careful field-tests should be apparent. The question may well be raised whether the hunting-behavior of the dog is really an olfactory response. A comparison of the field-behavior of anosmic dogs and normal dogs of the same litter and of a hunting breed, such as the beagle-hound, should prove highly interesting. It would be well worth while to ascertain as a beginning what responses a good hunting dog actually makes when introduced to trails the time and direction of which had previously been ascertained. The effect of numerous disturbing factors which could be introduced, some of which have been suggested above, ought to be quite inter- esting. It is to be hoped that some one with proper facilities and ample training may become interested enough to make an experi- mental investigation in this field."
Of the ' ' field of smell ' ' in mammals; of their * ' posi- tiveness " or *' negativeness '^ (preferences) to certain smells and of the groups or classes of smells to which they are sensitive, we know almost nothing.
Experiments an the olfactory sensitivity of birds. — The question of the influence of smell stimuli on the be- havior of birds has always been an interesting one. Some birds possess both well-developed central and peripheral apparatus. Below (Fig. 65) are shown the dissections of the brain of the fulmar — a bird allied to the petrel and albatross— which has a well-developed olfactory system, and that (Fig. 66) of the raven, which has a poorly de- veloped olfactory organ.
No incontestable positive evidence has ever been obtained to show that birds are sensitive to olfactory stimuli. The anecdotal literature is lengthy and interesting, but incon- clusive. As an example we cite the following observation, which appears in the literature: An observer states that while digging sweet potatoes in a field he noticed a luxu- riant growth of vines over a small mound and that the po- tatoes dug at this place were unusually large. On inquiry he learned that a horse and a cow had been buried there SMELL SMELL during the previous winter. In the afternoon and all dur- ing the next day vultures came in scores, swooping to the -.ca Fig. 66. Coevus Corax (Raven) Dorsal view showing the minute olfactory lobes and the slender olfactory nerves. The posterior ends of the nasal cham- ber are included. (Both cuts from R. M. Strong, Journal Mor- Fig. 65. Fulmarus Glacialis ( Fulmar ) Dorsal view of portion of dis- sected head with the brain case material, which separates the eyes from the brain, removed. The right nasal chamber and a posterior portion of the left nasal chamber are exposed. The pos- terior turbinal of the right side has been opened at d to show the turns or rolls of its structure. The middle and anterior tur- binals have been mutilated slightly in the dissection, c.a., anterior turbinal; cm., middle turbinal; c.p., posterior turbinal.
ground about the mound. These birds continued to come for several days but in lessening numbers. No taint could SMELL IN BIRDS 405 be detected in the air. The experiments of Audubon are well known. The ones cited below were conducted with some care. The first four experiments were made by Audubon himself; the remaining ones are cited by Audu- bon from other sources.
1. An entire deer skin, including the hoofs, and provided with artificial eyes, was stuffed with dried grass, the whole being allowed to become " perfectly dry." The stuffed skin was exposed in a large field, and the observer concealed himself not far away. In a few minutes a vulture, soaring about, saw the deer skin and sailed down to it. The hide was torn open, and much grass was pulled out.
2. A large dead hog was hauled to a ravine and concealed by a covering of cane. As the weather was warm, the body became " extremely fetid " in a couple of days. Dogs found the carcass and fed heartily upon it, but vultures sailing over from time to time did not find it.
3. A young pig was killed, and its blood was scattered about on the ground. The body was concealed by a covering of leaves. Vul- tures found the blood and followed it down the ravine to the body, which was then discovered and devoured.
4. Two young vultures were kept for some weeks in a cage where they became accustomed to receiving food. The birds were in the habit of hissing and gesticulating when they saw food approaching. However, when food, either fresh or putrid, was brought up to the immediate rear of the cage where the vultures could not see it, no excitement was shown.
5. A dead hare, two dead birds, and a wheelbarrow full of offal from a slaughter house were deposited on the ground at the foot of Bachman's garden in South Carolina. A frame was raised above the pile at a distance of twelve inches from the ground, and this was covered with brush, allowing air to pass under freely. Though hundreds of vultures passed over in the next twenty-five days, none noticed the meat.
6. A coarse painting on canvas of a sheep skinned and cut open was placed on the ground, where it was noticed by vultures. They walked over the painting and tugged at it with their beaks. _ The painting was then placed within fifteen feet of the offal mentioned above, but the offal was not touched.
7. The most offensive portions of the offal were next placed on the ground, and these were covered by a thin canvas cloth on which were strewn several pieces of fresh beef. Vultures came and ate the beef, but they did not discover the offal beneath the canvas. A rent was then made in the canvas, whereupon the offal below was seen and eaten. (Taken largely from Strong.)
The following experiment of Darwin on condors like- wise gave negative results: " The condors were tied, each by a rope, in a long row at the bottom of a wall and having folded up a piece of meat in a white 406 SMELL paper, I walked backwards and forwards, carrying it in my hand at the distance of about three yards from them, but no notice was taken. I then threw it on the ground, within one yard of an old bird; he looked at it for a moment with attention but then re- garded it no more. With a stick I pushed it closer and closer, until at last he touched it with his beak; the paper was then instantly torn off with fury, and at the same moment, every bird in the long row began struggling and flapping its wings."