The Animal Mind: A Textbook of Comparative Psychology

E. H. Harper, on the other hand, working on the earthworm Pericheia bermudensis, declares that if the light is strong enough there are no random movements of the head at all, but the first movement is a direct reflex away from the light. When the light is only moderate, the appearance of random movements is due to the fact that the worm is less sensitive in a contracted than in an expanded ~ state. Locomotion consists in a series of contractions and expansions, and ‘“‘as each extension begins in a state of lower sensibility, the anterior end may be projected toward the light, only to be checked when its increase of sensibility with extension makes the stimulus appreciated” (288).

A similar suggestion that orientation may occur either by a definite reflex or as the outcome of random movements, according to the animal’s physiological condition, is to be found as early as the work of Pouchet on fly larve. He noted that the courses taken by the larve were either straight, “‘or they present to right and left indentations due to the wavering movements which the animal makes . . . in a certain number of cases, as if to take at each instant a new direction.”’ These individual differences might have been accounted for, says Pouchet, by differing degrees of hunger in the larve (614). Herms (296) reports that to low intensities sarcophagid flies orient by random movements: while to high intensities they orient directly. Bittner, Johnson, and Torrey (58) find that the earthworm orients to light without any random movements. Hadley (274) finds the same true of larval lobsters, Crozier (159) of a holothurian, and Bancroft (16) reports of Euglena, a protozoén which has the spiral method of swimming characteristic of so many animals in this group, that “there is nothing of trial and error here: the organism orients as definitely as its spiral locomotion will allow.”

When the “ direction theory ”’ of the tropism was receiving more attention than at present, evidence that an animal oriented in response to the direction of the light rather than to the comparative intensity of stimulation on symmetrical points was taken as arguing against Jennings’s view of the tropism as a response to changes in light intensity produced by random movements. Attempts were made to demonstrate the direction theory experimentally. A typical experiment of this type was that of Strasburger (695), made long before Jennings’s views were in the field, upon the swarm spores of certain plants. He placed over the vessel containing them an India ink screen, thicker at one

end so as to cause gradations in the intensity of the light reaching the vessel. When the light fell perpendicularly through this screen, the distribution of the swarm spores through the vessel was nearly uniform; that is, the differences of intensity had no effect. When the screen was removed, and the light fell at an angle, the spores immediately oriented themselves to its direction, and preserved this orientation even when the screen was replaced. They would move toward the light even when by so doing they passed into a region of less intense illumination. Jennings suggested that these results were due to the fact that “turning the sensitive anterior end away from the source of the light”? would diminish the effective illumination of the animal more than passing into a slightly less illuminated region. That is, the two ways of changing the intensity of the stimulus, moving forward into a darker region, and turning the head end away from the light, are here opposed : the latter effect is stronger than the former, hence the organisms make the negative reaction when the head end is turned from the light, and move toward the shaded region. “Tf the difference in intensity of light in different parts were increased till the change in illumination due to progression is greater than the change due to swinging the anterior,end away from the source of light, then the positive organisms would gather in the more illuminated regions”

In no class of animal responses to stimulation is the effect more dependent upon the codperation of a number of conditions than in those involving orientation to light. Many influences have been found to reverse the sense of light reactions, transforming negatively phototropic into positively phototropic animals, and vice versa. That such reversal should occur in response to increase or decrease of the intensity of the light is what one would naturally expect; if a certain intensity of illumination is favorable to the life processes of an animal, it would seem appropriate for it to seek light of that intensity but avoid light of greater intensity. Many animals, like Gonionemus, are positive to light of moderate intensity and negative to strong light (802). The females of the crustacean Labidocera migrate to the surface of the water at nightfall because, like the earthworm, they react positively to faint light; and move downward at sunrise because they are negative in their response to intenser light (534). On the other hand, Holmes observed that Orchestia agilis, an amphipod crustacean, would, if brought from strong to weaker light, become negative for a short time; the meaning of such a change it is difficult to conjecture (330). Sudden reduction of light causes a temporary negative phase also in Convoluta roscoffensis (253).

Prolonged action of light may alter phototropism: the “depth migrations,” that is, the periodical movements toward and away from the surface of the water, in the freeswimming larve of the barnacle, Balanus, are due apparently to the fact that an exposure of several hours of light will make positive animals negative, even though the light at the end of the period of exposure is decidedly fainter than it was at the beginning (269). The positive reactions of the water insect Ranatra increase in violence the longer the light acts; on the other hand, after’ being kept in darkness for several hours, Ranatra is negative on first being taken out (335). Daphnias kept in darkness for a time become decidedly negative to diffused daylight,

whereas if kept in light they would have been positive. A sudden change in light intensity, either brightening or darkening, has the effect of making positive Daphnias temporarily negative (532). Temperature changes influence response to light. The ob- _ vious suggestion here would be that since increased temperature often accompanies increased intensity of light, animals that are positively phototropic only up to a certain degree of illumination ought to become negative when the temperature is decidedly raised. This, however, is by no means always the effect produced by increased temperature. Strasburger’s swarm spores became positive in higher temperatures, negative in lowered ones (695). Orchestia agilis, which we have just seen becomes temporarily negative on being brought from strong into weak light, may be made positive again if the water is slightly warmed. When the same animal is dropped into water, it becomes strongly negative, but it will show a positive response if the water is heated almost to a fatal point (330). Essenberg (209) finds that certain aquatic insects are more strongly positive when the temperature is increased. On the other hand, the copepods and annelid larve studied by Loeb were made negative by increased, positive by lowered, temperature. Other crustaceans, e.g. Daphnia (808, 185), had their responses to light unaffected by a fairly wide range of temperature changes.

Increasing or decreasing the density of the water will also affect phototropism. In some copepods diluting the water produced negative responses to light, while increasing its density brought about those of the opposite sign (425). Diluting the water produced negative phototaxis in the larve of Palemonetes (451). Parker failed to find any such effect in the case of the copepods studied by him (534). W. Ostwald has called attention to the possibility that “internal friction”? between the organism and the medium may affect various tropisms. Freshly caught Daphnias which are negative or indifferent, quickly become positive if gelatine or quince emulsion is added to the water. Since they would become so in time anyway, Ostwald thinks the mechanical friction of the sticky liquid simply acts as a “‘sensibilator” and brings on this positive phase sooner

Change in the purity of the water also sometimes produces change of sign in the response to light. The amphipod Jassa, negative in ordinary sea water, becomes positive in foul sea water (330). The presence of chemicals is an influence probably identical with the one just mentioned. Various Crustacea have had the direction of their reactions changed by carbonic or other acids, ammonium salts, ether, chloroform, paraldehyd, and alcohol (430). Acids and salts will reverse the responses of May fly larve (794). The ultra-violet rays will make positive Balanus larve temporarily negative and have a similar effect on Daphnia (502).

The state of hunger or satiety in an animal must be reckoned with: the caterpillars of Porthesia, for example, are decidedly positive when hungry, much less so when fed (423). The slug Limax maximus, ordinarily negative to strong light, is positive to light of any intensity when hungry Mechanical stimulation is most striking in its effect on light reactions. Pouchet in 1872 noted that fly larve after having been shaken fail to display their usual orientation to light (614). The copepod Temora longicornis, usually negative, can be made positive by shaking it (425). Very curious phenomena of a similar nature have been observed in the case of some Entomostraca. Certain individual

specimens of the ostracod Cypridopsis appeared to be decidedly positive, others negative. Careful experimental analysis of the conditions revealed the following as the true state of affairs. The animals are predominantly negative. But contact with a mechanical stimulus has the effect of making them positive; thus a negative animal that is picked up in a pipette, or merely comes in contact with the end of the trough in swimming away from the light, may become positive. In course of time such a positive animal will become negative of its own accord, so to speak, without further mechanical stimulation, but such stimulation, if applied, makes it negative at once (718).

Similar experiments upon Daphnia and Cypris gave results of the same general character. The strong positive tendency of the former may, by several times taking the animal up in a pipette, be made very temporarily negative; the opposite effect could not be well tested because of the difficulty of preserving the negative state long enough to experiment onit. In the case of Cypris, an individual temporarily negative could be made positive by picking it up, but the positive phase could not be similarly reversed. No other sudden stimulus produces the effect which is thus induced by mechanical contact (800).

The effect of contact was observed by Holmes in the terrestrial amphipod Orchestia agilis. The most permanent phase of these animals is positive, although they are at rest under seaweed on the beach by day. But when they are thrown into the water, they become strongly negative, no matter what the intensity of the light ; and to a considerable extent this effect is independent of the temperature (330, 106). In the case of the copepod Labidocera estiva, being picked up in a pipette will make the females, ordinarily positive, negative for a time. The males are normaliy

slightly negative, but picking them up, instead of reversing this tendency, increases it (534). The strong positive phototropism of the ‘‘water scorpion” Ranatra, an hemipterous insect, may be made negative by handling, and especially by dipping in water (335). Periodical changes in the sense of response to light have been observed in animals subjected to periodical changes in environment. The gasteropod mollusk Littorina lives on the rocks of the seacoast in regions where it is covered with water at high tide and exposed to the air at low tide. According to the height at which they are found, some of these animals undergo the alternations of wetness and dryness at the ordinary tidal periods, twice a day, while others are reached by the water only at the special high tides occurring every fourteen days. Mitsukuri showed that when the waves of a rising tide cover these mollusks, they display negative phototropism and seek shelter in rock cavities ; while as soon as they are again exposed to the air, their phototropism becomes positive and they emerge in search of food. Further, he found that a Littorina whose phototaxis was negative could be made positive by being subjected to the action of a stream of water for a time (496). Bohn later studied the effects of placing black or white screens near the animals at various angles to their crawling movements, and found that the black screens exerted an attractive influence at certain times, the white screens at others. These changes in the “‘sense” of the phototropism correspond in time to the oscillations of the tide, even though the animals are studied in the laboratory; they tend gradually to grow less pronounced, however, under such circumstances. Further, the level from which the Littorinas are taken influences the nature of their response to light. Those from high levels, “which undergo pro-

longed and intense desiccation, habitually move following the direction of the luminous field in the negative sense; the Littorinas from low levels, which undergo only short and slight desiccation, move, habitually, following the direction of the luminous field in the positive sense.” The former become positively phototropic at the time of highest water, the latter negatively phototropic at the time of low water. In all cases, the tendency is for the animals to become negative at low-water time. The attraction of the dark screens represents that of the dark surface of the rocks (80). Similar oscillations corresponding to the periodicity of the tides were observed in the annelid Hedista diversicolor (80), in the sea-anemone Actinia equina (65), and in the hermit crab (192, 194).

It is probable that such rhythmic changes in the sense of light response are due to the effect of a rhythmically recurring cause, such, for instance, as the mechanical disturbance caused when the waters of the rising tide begin to agitate the pool in which the animal dwells, or to the wetness or dryness of the tissues. Bohn has suggested this explanation for the oscillation of Hedista, just mentioned. He supposes that when the annelid is dry, light has the power of exciting muscular movements, that is, a kinetic effect. This means that when the worms have accidentally crept into the shade they come to rest. If one eye has its illumination diminished, there is an inhibition of muscular activity on that side, and consequently a turning in that direction. At the period of high tide, when the muscles are wet, the action of light on the animal is inhibitory and the above phenomena are reversed (80). Heat and dryness make terrestrial amphipod crustaceans positive to light; cold and wetness make them negative (106).

“mourning cloak” butterfly, Vanessa antiopa, on coming to rest in bright sunlight, orients itself with the head away from the light. When it moves, on the other hand, it flies toward light of any intensity (537). Bohn also has noted that certain butterflies orient themselves when alighted in such a way that the posterior part of the eyes is toward the light. When in this position there is a tendency for the wings to be spread apart, while when the insect is facing the light the wings are closely folded (82). The effect on the wings was noted in Vanessa also, and, it is suggested, may have some function in bringing the sexes together (537). The pomace fly when at rest is not oriented at all. Light exerts upon it merely the effect of stimulating it to movement, a kinetic, not a directive, effect. When the movement has been started, however, it is directed toward the light. But owing to the kinetic influence of the light, when the insects have been long exposed to sunlight they tend to come to rest in the more shaded portions, with their heads away from the light, for this is the position in which they are least stimulated to movement. The kinetic effect increases with the intensity of the light, but its directive effect, through which orientation is secured after the movement is started, was at least in one case lost under intense light (116). Brundin (106) has suggested that the effect of mechanical stimulation in reversing light reaction may be due to the state of activity it induces.

The background, finally, sometimes determines the sense of the reaction. Keeble and Gamble found that while the crustacean Hippolyte varians would move toward the light whether it was on a white or black background, Macromysis inermis was negative on a white ground and positive on a black ground (396). The behavior of an organism which, by the unequal contraction of symmetrically placed muscles, is forced around into a position directly facing or turning tail to light, the light acting as a continuous stimulus and not through changes in intensity, is without any parallel in human experience, and hence suggests no psychic accompaniment. Yet there seems to be a considerable amount of evidence that such a type of reaction does occur, given the proper amount of stimulus and the proper physiological condition in the animal. It is a fact of much interest, however, that when we reach organisms beyond a certain point in the ascending scale of complexity, the tropic type of response to light begins to give place to more variable responses suggesting analogies with our own behavior. The individual experience of an animal strongly modifies its tropisms, as we shall see in a later chapter. Brundin (106) says that in certain amphipod crustaceans which he studied, the ‘‘mode of behavior exhibits a transition from the stage at which the creature is at the mercy of its environment to a stage at which it is beginning to hold its own against the forces which have shaped it.” Quite possibly, however, the ability to modify tropic response by individual experience is found in all animals, and not merely in those above a certain stage; it does seem to be true, though, that the tropisms are more readily overthrown by other influences, the higher the animal. Thus Holmes (337) says of fiddler crabs that phototropism is easily overcome by fear; although they are strongly positive they will run away from a moving light. “Light,” he says, ‘‘is followed much as an animal pursues any other object of interest”; and Turner (728) has made similar com-

ments on the behavior of certain insects to light. Bohn says of the mollusk Littorina that when its tissues are neither very wet nor very dry, it ceases to respond with a fatal necessity to light; ‘“‘the animal seems, as it were, to disengage itself from the influence of external forces, seems no longer to behave like a pure machine: it goes to the stones and seaweed where it may find shelter and nourishment as if it saw and was conscious of them”’ (80).

Orientation to light and orientation to gravity are not without mutual influence in determining the behavior of an animal. Supposed instances of this have been noted in the case of the periodically changing geotropism of Convoluta roscoffensis (253) and in the copepods observed by Esterly (210). The relations of gravity and light responses in the larve of the squid, a cephalopod mollusk, seem to be as follows. The larve have a tendency to rise to the surface of the water both in darkness and in light, suggesting negative geotropism. Two test tubes were arranged by Loeb, one lying horizontally and at right angles to a window, the other inclined at an angle of 45 degrees from the upright position, and with the upper end directed away from the window. Larve were placed in both tubes; those in the former showed positive phototropism by collecting at the end nearest the window, but those in the latter gave evidence that their negative geotropism was stronger than their positive phototropism by rising to the upper end, although it was farthest from the source of light (428). It is not usual for geotropism thus to come off victorious in a contest with other tendencies. Jennings says, “As a general rule the reaction to gravity is easily masked by

reactions to other stimuli” (378, p. 150). In the mollusks observed by Bohn, the tendency in ascending or descending the rocks is to orient the body in the line of the greatest slope. When light and gravity are acting together upon the animal, its movement seems to be a resultant of the two, but if the mollusk is made to move on a vertical plane, gravity thus exerting its maximal force, the influence of the light disappears altogether; and if the animal is put in an upside-down position by further tipping of the surface, the sense of its phototropism is reversed; that is, it may be repelled instead of attracted by a dark screen (80). The fairy shrimp, Branchipus, is positively geotropic in light, negatively geotropic in darkness (454).

A curious tendency has been noted by many observers in insects with both eyes blinded; namely, to fly straight up into the air. Forel thought they did so because in no other direction could they escape obstacles (231); but this fact they would have to learn by experience, for which, in some cases at least, they do not take time. Plateau believed the rising into the air was due to sensations produced by the action of the light on the surface of the body, leading the insects in the direction of the strongest light, which usually comes from above. He supported this view by showing experimentally that a blinded insect would not rise if set free at night, while on the other hand, if liberated in a lighted room, it would, in spite of the blinding, fly toward the light or the lightest part of the ceiling (596, 599). In the butterfly Vanessa, Parker thinks the rising due to negative geotropism, as the insect flew upward in a darkened room (537). Axenfeld suggested that it might be caused by light penetrating the integument of the head (9).

One force, which, as was noted in Chapter III, produces orientation, namely, the electric current, we shall leave out of account. It is not a stimulus to which animals are normally subject, and though its action on living matter is of great interest to the physiologist, the comparative psychologist’s difficulty in finding a psychic interpretation for the facts may justify setting them aside. Similar considerations apply to orientation to centrifugal force. There remain the orientations that have been termed respectively “‘rheotropism” and ‘‘anemotropism,’”’ responses to currents of water and to currents of air.

The tendency shown by many aquatic animals to orient themselves with head up-stream, and to swim against the current, was formerly thought to be a response to the pressure exerted by the current — a reaction leading the animal to resist pressure. Lyon, however, pointed out that this explanation assumes rheotropism on the animal’s part. It is because the animal opposes the current that the current exerts any pressure. If it merely allowed itself to be carried passively along, and if the current surrounding the animal flowed with uniform velocity in all its parts, no stimulus whatever could be exerted by the water pressure (448). It seems probable that eyeless animals do not, as a matter of fact, orient themselves against a current of this sort, and that rheotropism in their case occurs when a current of unequal velocity disarranges their movements, or when they are in contact with a solid body. Thus Jennings has suggested that in Paramecium the reaction is due to the fact that unless the animal has its head to the current, the flow of the latter will interfere with the normal backward stroke of the cilia, causing

negative reactions until the disturbance is removed by proper orientation (378, p. 74). In animals with eyes, however, there is reason to think that apparent rheotropism is largely an affair of vision. Lyon’s theory of rheotropism in fishes is that the fish orients itself and swims in such a way that its surroundings, the bottom of the stream, for example, shall appear to the sense of sight to be at rest, an hypothesis which, as we shall see, was adopted by Radl to explain the “hovering” of insects in one place (622). Lyon supports it by experiments where the bottom or sides of the aquarium were caused to move in the absence of any current in the water, and the fish was found to follow them. When the fish was. placed in a revolving glass cylinder, it followed the revolutions, although there was a slow current, of course, in the same direction, against which, on the pressure theory, the fish should have moved. Still more decisive was the experiment where young fish were placed in a corked bottle full of water which was submerged and put near a wall covered with alge. When the bottle was moved in one direction, all the fish went to the opposite end, although no current could have been produced. Again, a wooden box with ends of wire netting, the bottom covered with gravel and the sides with seaweed, was used; fish (Fundulus) were placed in it, and the box was held lengthwise in a strong current. The fish oriented themselves, but as soon as the box was released and allowed to float away, they lost their orientation, though their relation to the current was in no way altered. Blind fish, Lyon found, oriented themselves by touch, sinking to the bottom. There does, however, appear to be, in some cases, a genuine pressure reaction to current, for when water is rushing through a small hole into a tank containing blind fish, they keep their heads to the current

without touching anything. Here the different parts of the stream have different velocity, and pressure stimuli are actually applied to the skin. There must be pressure reaction, also, when fish actually swim up-stream instead of merely maintaining their places against a current (272). Such a reaction was displayed, probably, by some shrimps which, being in the water with the fish in the revolving tank experiment, did swim against the current instead of with it (448).

Some very interesting behavior touching on this same point was observed by Garrey in a school of the little fish called sticklebacks. He noted that if any object was moved along the side of the aquarium containing them, the whole school would move along a parallel line in the opposite direction. If an individual fish happened to be heading directly toward the object, it would turn in the opposite direction from the one in which the object was moved; if it was heading somewhat in the opposite direction already, it would turn farther in that direction until parallel with the object’s line of motion; if it was heading somewhat in the same direction as the object, it would “back off hesitatingly,” and reverse itself by a turn in either direction, usually taking the way around toward which it was already partially headed, if the object was rapidly moved, but the other way around if the object’s motion was slow. At first sight this behavior seems to display an instinct precisely opposite to that of keeping the visual field constant. Yet the sticklebacks, when . placed in a cylindrical glass tank inside of a black and white striped vessel, moved with the latter when it moved, proving that they possessed the usual tendency shown by Lyon to be involved in rheotropism. Garrey points out that movement in the opposite direction is produced not

when the whole visual field moves, but when it is at rest, and one object in it moves. Can it be, he asks, that the moving object ‘‘fixes the attention” of the fish and produces an apparent motion of the background in the opposite direction, which motion the fish follows? (254.) Rheotropism in water arthropods may be similarly accounted for, and in the opinion of R4dl, this same tendency explains the habit swarms of insects have of hovering over the same place, a phenomenon which Wheeler thought might be due to odors emanating from the soil (780). In- sects will often be found to follow an object over or under which they are grouped in the air, if it be moved (622). Swarms of insects may be noted in the air over a country road, following its windings and apparently oriented by the contrast between the road and the dark banks on either side. When, however, resting insects turn so as to keep their heads to the wind, the reaction is evidently really due to the wind and not to their visual surroundings (646). Probably the disturbance to their wings produced by any other position causes them to rest only in the “head-on” orientation.

The responses of animals to different intensities of heat seem not to involve a definite orientation of the body. A temperature above the optimum produces wandering movements, which cease when the animal happens to reach the proper temperature (480, 483, 808). SPECIALIZED response to a stimulus in motion, that is, one which successively affects several neighboring points on a sensitive surface, is also frequently met with in animal behavior. Its usefulness is obvious: a stimulus in motion is very commonly a living creature, hence either an enemy or food. In any case it must be reacted to with extreme promptness. Reactions of this class may be distinguished as tactile or visual according as the moving stimulus is mechanical or photic.

We find good examples of specialized reactions to motile touch in the coelenterates. The sea-anemone Aiptasia gives its most violent reaction, involving all the tentacles at once, when touched by a moving object (521). The medusa Gonionemus makes, in the case of a moving mechanical stimulus, its single exception to the rule of responding by the feeding reaction to edible substances only. The tentacles are wound corkscrew fashion about a glass rod drawn across them, they bend in toward the mouth, and the bell margin bearing them contracts; the feeding reaction goes no further, however. But the response is differentiated from that to any other form of stimulation by its greater speed: the reaction time is from .3 to .35 of a second, compared with .4 to .5 of a second for other stimuli