Behavior of the Lower Organisms

strongly marked avoiding reactions, not differing in principle from what we find in Paramecium or Oxytricha. All the species which usually move along on a surface may at times swim freely They then as a rule revolve on the long axis, both when progressing and in the avoiding reaction. On the other hand, almost all the species which characteristically swim freely through the water do at times move along surfaces. They may then react to stimuli in the same way as do the Hypotricha. Such forms as Bursaria and Loxophyllum are transitional between the free swimming species and those that creep along surfaces; they are found about as often in one situation as in the other.

In the Ciliata thus far considered the reaction method is evidently that of the selection of certain environmental conditions through the productions of varied movements. When its movement leads to stimu- Fig. 80. — Path of Colpidium. At 2 it is slightly stimulated; it thereupon turns toward the aboral side (3-4) and continues its curved course. lation, the animal responds by trying many new directions, till one is found which does not lead to stimulation. The reaction is less flexible in the ciliates which creep along surfaces than in the free swimming ones. In the former, owing to the lack of revolution on the long axis, all the directions tried he in a single plane. But under many powerful stimuli even these species usually leave the surface on which they are moving; they then react in the freer way characteristic of unattached organisms, trying directions lying in many different planes.

There exists also a large number of ciliates which become more or less permanently attached by the part of the body opposite the mouth. This attached portion is usually drawn out to form a slender stalk or foot. Examples of such infusoria are Stentor (Fig. 31, b) and Vorticella (Fig. 31, c). Some of these species are found attached under all usual conditions ; such are Vorticella and Carchesium. Others are frequently found swimming freely; this is the case, for example, with Stentor cceruleus. Some infusoria become fixed in only a temporary way, by a mucous secretion. Such are Spirostomum and Urocentrum, which are often found suspended from solid objects by a thread of mucus (Fig. 82). Even the species which are most firmly fixed may under powerful stimuli detach themselves and swim away. The heads of Vorticella and Carchesium thus at times detach themselves from their stalks and swim about like Paramecium. At such times they may also creep over surfaces, just as do the Hypotricha. The behavior when free is essentially similar in its main features to that of Paramecium or Oxytricha.

In the attached condition the mouth and peristome are usually above, surrounded by a wreath of large cilia. These cilia are in continual movement, in such a way as to bring a current of water from above to the mouth. Some fixed infusoria contract at intervals with marked regularity, even when there is no external stimulation. Such is the case in Vorticella. The reactions to stimuli are much modified as compared with those of the free swimming species. The avoiding reaction becomes broken up into a number of factors, any one of which may take place more or less independently of the others. Thus, Stentor reeselii may respond to stimulation either by a reversal of the cilia, driving away the water currents, by bending over toward the right aboral side, or by withdrawing into its tube. Each of these reactions corresponds to a certain definite feature in the avoiding reaction of free infusoria. Owing to the disintegration of the avoiding reaction into independent parts, the behavior of these fixed infusoria become more varied and more highly developed than that of the unattached species. We shall have occasion to treat of this in detail later, in our account of the modiliability of reactions in Protozoa.

In the responses of infusoria to contact with solid objects we may distinguish the same two reaction types that we found in Paramecium. The animal may react in what might be called a "negative" way, avoiding the object, or it may react "positively," placing itself against the solid body. The negative response to contact with solid bodies is the typical "avoiding reaction." The animal moves backward, turns toward a certain definite side, then swims forward again. In other words, it tries a new direction. If this leads again against the obstacle, the animal again reacts in the same way, and this is repeated, till through frequent trials the obstacle is avoided.

There are certain important points regarding the relation of the direction of movement in this avoiding reaction to the part of the body that is stimulated. Since the animal usually swims forward under natural conditions, it will as a rule come in contact with large solid objects at its anterior end. Further, small objects may be carried by the ciliary currents to the oral side. Thus the movement backward and the turning toward the aboral side in the avoiding reaction remove the animal from the source of stimulation. But experimentally other parts of the body can be stimulated. Thus in Oxytricha (Fig. 79), we may with the tip of a fine glass rod stimulate either the left (oral), or the right (aboral), side. In either case the animal backs and turns to the right. If the right side is repeatedly stimulated, the animal continually wheels toward the stimulated side; if the left side is touched, it wheels continually away from the stimulated side. Thus the direction of movement in the reaction is not determined by the side stimulated, but by the structural relations of the organism. On the other hand, if we stimulate the posterior end sharply, the animal does not respond by the typical avoiding reaction, but simply runs forward. The direction of movement is in this case determined by the part stimulated. These results have been found to hold also in many other infusoria.

Experiments of the kind just described have shown that the anterior end is as a rule much more sensitive than the remainder of the body surface. A light touch, having no effect at the posterior end, produces a strong reaction when applied to the anterior end. It is a general rule that unlocalized mechanical stimuli, such as are produced by jarring the vessel containing the animals, have the same effect as stimuli applied to the anterior end; they induce the avoiding reaction.

In the positive contact reaction, the animal places itself in contact with the solid object and remains against it. It may now continue quiet, while the oral cilia bring a current of water containing food to the mouth. But sometimes the animal runs over the surface of the solid, using its cilia as if they were legs. This, as we have Fig. 81. — Side view of Stylonychia creeping along Seen, is the Common method a surface. After Putter (i9oo). of locomotion in the Hypo-

tricha. A side view of one of the Hypotricha while creeping along a surface is shown in Fig. 81. In other cases the animal secretes a layer The contact reaction is often directed toward very minute objects, as we have set forth in detail in the case of Paramecium. It then serves the purpose of helping to obtain food. In some of the fixed infusoria such behavior is especially striking. Thus, if a small object touches gently one side of the disk of Stentor, the animal may bend over toward it. This reaction may be seen when a small organism in swimming about comes against the disk of the animal, then attempts to swim away. The Stentor bends in that

direction, so as to keep in contact with to the bottom by a thread of mucus the Organism as long as possible. At and remaining stationary with anterior tex tends to draw the prey to the Stentor's mouth. This reaction may be produced experimentally by attaching a bit of soft, flocculent debris to the tip of a fine glass rod, and allowing this to touch the disk of Stentor, then drawing it gently to one side. The Stentor follows it, often bending far over (Fig. 83). The animal may thus bend in any direction — to the right, to the left, or toward oral or aboral side.

When infusoria are in contact with solids, their behavior always becomes much modified. The spiral movement of course ceases, and the reaction to many stimuli — especially such reactions as depend largely on the spiral movement — either cease or become changed. Animals that when free place the axis of swimming in line with gravity, usually take up, when in contact with solids, any position without reference to gravity. To high temperatures attached specimens respond much less readily than do free swimming ones. Stentor caruleus responds readily to light when free swimming, directing its anterior end away from the source of light; when attached, it does not react in this way. Many infusoria show a modified reaction to the electric current when in contact with solids. The flagellates Chilomonas, Trachelomonas, Polytoma, and Peridinium react readily to

the electric Current when free Swimwhich is pulled by the experimenter to the (Putter, 1900, p. 246). Most ciliates when in contact with solids react less readily to the electric current, and frequently when the reaction does occur, it is of a different character from usual. While free specimens place themselves in fine with the current, attached infusoria often take up a transverse or oblique position with the peristome or oral side directed toward the cathode, — just as happens in Paramecium. This is true in general for the Hypotricha.

What is the cause of the interference of the positive contact reaction with the reaction to other stimuli ? It is necessary, as we have seen in our discussion of this reaction in Paramecium, to distinguish two factors in the contact reaction ; one physical, the other physiological. The physical factor is found in the fact that the organism actually adheres to the surface of the solid, — in many cases, at least, by means of a mucous secretion. This physical adhesion would of course tend to prevent that rapid movement under the influence of a stimulus which is shown by free individuals. Thus, the animal might attempt to react

Fig. 83. — Stentor rceselii bending over to remain in contact with a shred of debris in the usual way, — showing the same ciliary movements as free individuals, — but might find itself stuck, and unable to escape. Doubtless sometimes this condition of affairs is realized ; it is described, for example, by Putter as present in the reaction of attached specimens of Colpidium and some other infusoria. But in many cases this physical factor will not account for the observed behavior. Infusoria in contact may take different positions without difficulty, and could easily place themselves in line with gravity, yet as a rule they do not do so. Attached Stentors could easily bend into a position with anterior end away from the light, yet their position shows no relation to the direction of the light rays. There is nothing in the physical adherence to a surface that should compel the animal to take a transverse position in the electric current, rather than a position parallel to the current, yet this is what occurs in attached specimens. It is clear that there is a physiological factor involved. Contact with solids tends to make the animal act in one way, the other stimulus in another; hence the two must interfere. If we object, as some authors have done, to the admission that the contact reaction interferes with the reaction to other stimuli, we are compelled to admit in any case that the reactions to other stimuli do interfere with the contact reaction, and one admission has as much theoretical significance as the other. It is evident that when two agents influencing the organism in opposite ways act simultaneously, the effect of one must give way to that of the other, or the two must combine to produce a resultant. It is impossible that each should produce its characteristic effect. The interference of the contact reaction with the reactions to other stimuli is one of the most striking phenomena to be observed in the behavior of these lower organisms.

It is always necessary to distinguish carefully the behavior of free swimming specimens from those that are in contact with surfaces, for the two differ radically. The reactions to chemical stimuli take place in all accurately known cases through the typical avoiding reaction. As a rule the motor organs of the infusoria, both flagellates and ciliates, act in such a way that a current of water passes from in front of the animal to the anterior end and mouth, as illustrated for Paramecium in Fig. 35. Thus when a chemical is dissolved in the water, a "sample" of it is brought to the most sensitive part of the body. If the chemical is of such a nature as to act as a stimulus, the animal swims more slowly, stops, or moves backward, turns toward the customary side (usually the aboral side), until it no longer receives the chemical, then moves forward in the new

direction. Thus the region containing the chemical is avoided. In many cases this reaction takes place in a very pronounced manner; the animal shoots far backward, whirls rapidly toward the one side, and repeats the reaction many times. In other cases the reaction is less pronounced, and motion merely becomes a little slower as long as the chemical is received in the ciliary current, while at the same time the animal quietly swings its anterior end about in a circle (as in Fig. 37 or 38). This continues until it finds a direction from which no more of the chemical is received ; in that direction it swims forward. If the movements of the animal are not precisely observed, the method by which the reaction occurs may in such cases be easily misunderstood.

There are various chemicals in which certain infusoria gather, producing collections like those formed by Paramecium in acids (Fig. 43). In all cases in which the facts are accurately known, these collections are formed in the same way as are those of Paramecia. The animals enter without reaction into the region where the substance is present, then respond by the avoiding reaction whenever they come to the outer boundary of the area containing the substance. Thus every individual that enters the area of the chemical remains, and in the course of a longer or shorter period a collection is formed here. In many cases this indirect method of gathering together is strikingly evident, and the individuals may be clearly seen to move about within the area containing the chemical, in the manner represented in Fig. 44. If the infusoria observed are very minute, so that differentiations of the body are to be seen only with great difficulty, if their movements are rapid, and if in the avoiding reaction they do not swim backward, but merely stop and turn toward one (structurally defined) side, at the same time revolving on the long axis, then the reaction method is not so evident on a cursory examination. In such cases, if the relation of the direction of turning to the structural differentiations of the body and to the revolution on the long axis are not carefully determined, the animal will be supposed to turn directly, without variations of any sort, into the chemical. This was formerly supposed to be the universal method of reaction to chemicals. The cause for the turning was supposed to be found in the difference in the concentration of the chemical on the two sides of the organism. The animal turned directly toward the side of greater concentration ("positive chemotaxis") or of less concentration ("negative chemotaxis").

This method of reacting to chemicals is no longer supposed to exist for infusoria by any one familiar with the reaction method described in the foregoing pages, so far as I am aware, save in the case of certain very minute organisms, — fern spermatozoids, Saprolegnia swarm spores, and the flagellate Trepomonas agilis (Rothert, 1901, p. 388). But it is notable that in none of these cases has the relation of the direction of turning to the differentiations of the body been observed, and this is the crucial point for determining the nature of the reactions. The fact that it is only for these very difficult objects that the direct turning is maintained must make us cautious in accepting this exceptional result.1

Let us now leave the method of reacting, and turn to certain more general phenomena. In what chemicals do infusoria gather? What chemicals do they avoid ? In no other infusoria is the behavior toward different chemicals so well known as in Paramecium. Chilomonas collects in acids in general, and especially in solutions of carbon dioxide, just as Paramecium does. Spontaneous gatherings are often formed by Chilomonas, and it seems probable that these are due, as in Paramecium, to the carbon dioxide produced by the animals themselves (Jennings and Moore, 1902). Cyclidium glaucoma and Colpidium colpoda likewise collect in carbonic and other acids. Opalina, Nyctotherus, and Balantidium cntozoon, living in an alkaline medium, gather in acids, but if transferred to an acid medium, they gather in alkali (Dale, 1901). Many other infusoria show no tendency to gather in acids. Loxocephalus granulosus and Oxytricha aeruginosa form spontaneous collections resembling precisely those of Paramecium, but they are not due to the same cause. These species do not collect in solutions of carbon dioxide, nor in other acids. When they are mingled with Paramecia in the same preparation, they collect in one region, while the Paramecia collect in another. It is apparent that Loxocephalus and Oxytricha produce some substance to which the collections are due, and that this substance is not carbon dioxide. A number of other infusoria form spontaneous collections, the cause of which has not been investigated. Many of the commonest species do not form such collections.

There are many chemicals in which one or another species of infusoria have been found to collect. Most of the details are of comparatively little general interest from the standpoint of animal behavior, so that we shall not take them up here. An excellent summary of these results will be found in Davenport's "Experimental Morphology" (Vol. I, pp. 32-45). Certain general features are important for our purposes ; these we may bring out briefly. First, from the way the collections are brought about, it is evident that whether given infusoria tend to collect in a certain solution or not depends on the nature of the solution in which they are already found. This has been illustrated in detail for Paramecium. Paramecia in

strong salt solution collect in weak salt solutions or in tap water; Paramecia in tap water collect in distilled water; Paramecia in distilled water collect in weak acids. In the same way, if two solutions are open to any given infusorian, they tend to collect in that one by which they are least repelled. Thus "attraction," as determined by the formation of collections, is a relative matter ; the infusoria, like higher organisms, often have to put up with merely that by which they are least repelled. To say that a certain infusorian gathers in a given substance A, therefore, signifies little more than that it is less repelled by this substance A, than by the substance in which it was found at the time the experiment was tried.

Most flagellates and ciliates are repelled by strong solutions of chemicals of almost all sorts. This is true even for strong solutions of the same substances in which they collect when the solutions are weak. In such substances we can therefore distinguish an optimum concentration. Below the optimum the organisms are indifferent, while above the optimum they are repelled. Expressing the facts more concretely, at the indifferent concentration no reaction is caused when the organism passes into the solution or out of it ; at the optimum concentration no reaction is caused when the organism passes into the solution, but the avoiding reaction is induced on passing out, while at concentrations above the optimum the organisms react at passing inward. The result is then in every case that they tend to gather in the optimum.

The reaction is in each case caused by a change from one concentration to another. The amount of change necessary to cause the reaction has been shown, in the case of fern spermatozoids (Pfeffer, 1884), to bear a definite relation to the concentration of the solution in which the organisms are immersed. In other words, the amount of change necessary to cause the reaction varies according to Weber's law. Thus in the fern spermatozoids the concentration of malic acid necessary to produce a collection of the organisms must be about thirty times that in which the organisms are already immersed.

Massart (1891) found that specimens of Polytoma nvella in his cultures were not repelled by chemicals even in the strongest solutions. Such cases are very exceptional ; other investigators have found that even this same organism (from other cultures) is repelled by various chemicals (Pfeffer, 1904, p. 808, note). The variability and inconstancy of the reactions of infusoria to chemicals deserves emphasis. Whether infusoria of a given species react to a certain chemical or not, and how they react, depends upon the past and present conditions of existence of the individuals. The general outlines of the reactions can be determined for any species, but

the details, especially from a quantitative standpoint, vary in accordance with the environmental influences acting upon the individuals in question. As a rule, infusoria collect in solutions of substances which may serve them as food. This is almost invariably true for substances which form the usual food of the organism under natural conditions. When the amount of oxygen present in the water is low, most infusoria collect about bubbles of air or other sources of oxygen.

Infusoria sometimes gather in substances which do not serve for food or respiration, but which serve other important purposes in the physiology of the species concerned. Thus, the flagellate spermatozoids of ferns were found by Pfeffer to gather in solutions of malic acid. This substance is found in the fern prothalli, and probably occurs in the mouth of the archegonium, into which the spermatozoids must enter in order that fertilization may take place. The tendency to collect in malic acid then doubtless plays a part in bringing about fertilization in ferns. The collection of Paramecia in carbon dioxide seems to be another case of a reaction which is useful to the organisms, though the substance causing it does not itself serve as food.

Many infusoria collect, under certain circumstances, in substances which do not serve as food and are not known to play any useful part in the biology of the animal. Thus, Pfeffer found that the flagellate Bodo saltans gathers in most of the salts of potassium, as well as in various salts of lithium, sodium, rubidium, caesium, ammonium, calcium, strontium, barium, and magnesium. This signifies only, as we have already seen, that they are less repelled by solutions of these substances than by the fluid in which they are situated. In most cases, as soon as a substance is sufficiently concentrated to be injurious it becomes repellent.

Whether the repellent effect of chemicals is due to the chemical properties of the solution, or to its osmotic pressure, has been rigidly determined only for Paramecium. In this animal, as we have seen, the osmotic pressure is usually not the cause of the reaction. There is much evidence that this is true for most species, but accurate quantitative evidence is needed on this point. Infusoria in general react to heat and cold in much the same way as does Paramecium, — through the avoiding reaction. The way the reaction occurs is most easily seen in the Hypotricha. The phenomena to be observed are of special interest, because they show clearly how a movement of a large number of individuals in a certain uniform direc-

tion (•'orientation") may be brought about by the selection of varied movements. The common hypotrichan Oxytricha Jallax, abundant in vegetable infusions, is well fitted for the study of this reaction. A large number of specimens are placed on a slide or trough. When one end of the trough is gradually heated by passing water at a temperature of 40 degrees beneath it, the Oxytrichas at this end are seen to become very active, darting about in all directions (Fig. 84). As the temperature rises, they give the avoiding reaction, — darting backward, and turning to the right. This is alternated with rapid dashes forward. Whenever a specimen passes toward the warmer end of the trough, or when it comes in contact with the sides or end, it responds with the avoiding reaction. But a specimen passing away from the heated region, in the direction of the arrow at 14

(Tig. 84), does not Fig. 84. — Reaction of Oxytricha to heat. The slide is heated at give the reaction tne enc^ *• An Oxytricha in position i reacts as indicated by the arrows, i ... repeatedly moving backward, turning to the right, and moving forward, Utcause ll IS passthus occupying successively the positions 1-14. When it finally being from a hot to comes directed away from the heat, as at 13-14, it ceases to change its 1 . rpi direction of movement, but continues to move straight ahead, thus COOl region. 1 ne reaching a cooler region.