Behavior of the Lower Organisms

There is much variation in the complexity of behavior even among species living under similar conditions. Some of the free-swimming species are very supple, changing form continually. Such is the case, for example, with Lacrymaria olor, which stretches its long neck in every direction, shortens it until it has almost disappeared, reextends it, and seems to explore thoroughly the surrounding region. Such an organism has, of course, much better opportunity for effective behavior by the method of trial than has such a rigid form as Paramecium.

Similar differences are found among the creeping infusoria, and among the fixed species. Some fixed infusoria contract frequently, while others contract only rarely. In some cases the contraction occurs at regular intervals, even when there is no indication of an external stimulus. This is the case with Vorticella. There is no evidence that in infusoria periods of rest, comparable with the sleep of higher animals, are alternated with periods of activity. Hodge and Aikins (1895) kept a single Vorticella continuously under observation for twenty-one hours, besides intermittent study for a number of clays. They found that there was no period of inactivity. During five days the cilia were in continuous motion, food was continuously taken, and contractions were repeated at brief intervals.

A number of fixed infusoria live, like Stentor rceselii, in tubes, some gelatinous, some membranous in character. As a rule these tubes are formed in a very simple manner. The material of which they are composed is secreted by the outer surface of the animal. In the repeated contractions and extensions of the body this material is worked off, in the form of a sheath. The tube may become thicker by the secretion of more material on the surface of the animal. It often grows in length, either as the animal becomes longer or as it migrates farther out toward the open end of the tube. In the secreted material, which is often transparent, all sorts of foreign substances may become embedded, in the following way: They are carried as particles to the oral disk by the cilia. Thence they pass backward over the surface of the body, till they reach the gelatinous substance of the tube, where they become embedded. Thus in most cases the formation of the tube seems a direct consequence of the secretion of the mucus-like substance over the body of the animal, taken in connection with the usual movements. The intervention of any special type of behavior directed toward the end of forming the tube seems unnecessary. But in some cases, as we have seen in our account of Stentor, the tube is formed at the beginning by a definite set of movements, of a character especially fitted to produce such a structure. For details as to different kinds of tubes, and their structure and method of formation, reference may be made to Butschli's great work on the infusoria (1889).

A set of phenomena that is deserving of careful study for its implications as to the nature of behavior is that involved in the activities preliminary to conjugation. It is possible that the organisms are in a modified physiological condition at this time, behaving differently from usual. Critical observations on this subject, of such a nature that we can use them for our present purpose, are too few in number to make possible a unified account of these phenomena. An account of the facts for Paramecium is given on page 102. The field is one deserving of much further work.

The food habits of the infusoria are among the most interesting of their activities to the student of animal behavior. As to their food habits, we can with Maupas (1889) divide the infusoria into two classes. The first includes those that bring the food to the mouth by means of a vortex produced by the peristomal cilia ; the second those that go about in search of food, seizing upon it with the mouth, like a beast of prey. The former live chiefly upon minute objects, the latter upon larger organisms. There is, of course, no sharp distinction between the two classes. Most of the infusoria with strong vortices move about more or less in search of food, and most of those that seize upon their prey after a search are aided by a more or less pronounced vortex. Thus the roving or searching movements and the vortex are factors common to the food habits of most of the infusoria. The positive contact reaction further plays a most important part in obtaining food.

Those species that depend primarily upon the ciliary vortex for obtaining food usually feed upon bacteria and other minute organisms and upon finely divided organic matter, — bits of decaying plant or animal material. Of this class of organisms Paramecium and Stentor are types. In some, as in Paramecium, the food is limited to most minute bodies, such as bacteria and small algae. Stentor and others may take larger objects. Other infusoria and even rotifers of a considerable size are often seen embedded in the internal protoplasm of Stentor. Such animals are caught in the strong ciliary vortex, carried to the buccal pouch, which often contracts in such a way as to prevent their escape, and are then taken through the mouth into the internal protoplasm.

How do these organisms succeed in getting the food that is fitted for them ? Is there a selection of food, and how is it brought about ? Much of the difficulty as to the selection of food is solved by the conditions under which these animals usually live. They are found as a rule in water which contains decaying vegetable or animal matter, and therefore swarms with bacteria. Hence the usually ciliary current brings food continuously, and little selection is necessary. The animals take, within wide limits, all that the ciliary current brings. Bits of scot, India ink, carmine or indigo, chalk granules, and the like are swallowed along with the bacteria, though of course they are useless as food. They are merely passed through the body and ejected along with the indigestible remains of the food. They do no harm, and the animal may continue to take them indefinitely, provided it receives in addition a sufficient amount of real food. If the ciliary currents do not bring food, of course the organisms die after a time. It is well known that infusoria appear suddenly in immense numbers, or disappear with equal rapidity, according as the conditions are favorable or unfavorable.

But the animals do determine for themselves, to a certain extent, what things they shall take as food, and what they shall not. This is not done, so far as can be observed, by a sorting over of the food by the cilia, as the water current carries it to the mouth. It is true that not all the particles in the vortex produced by the cilia pass into the mouth. But this is due to the simple mechanical conditions. The vortex is very extensive, and the mouth is very small, so that only a fraction of the water in the vortex can ever reach the mouth. Hence inevitably a large share of the particles in the vortex are whirled away. But this is true of particles which are valuable for food as well as of those which are not. If Stentor is placed in water containing immense numbers of small algal cells which are useful as food, it is found that as many of these pass through the vortex without being taken as happens in the case of worthless particles of soot or carmine.

Choice of food occurs in a somewhat cruder fashion than through a sorting of the individual particles by the cilia. It takes place through the reaction with which we have become familiar in studving the behavior of the organisms under various stimuli. Thus in Paramecium the rejection of unsuitable food takes place through the avoiding reaction. If the ciliary current brings water containing various chemicals in solution, or if large solid objects are brought to the mouth, or too great a mass of smaller particles, the Paramecium shifts its position in the usual way. It backs more or less, turns toward the aboral side, and moves to another place. The avoiding reaction is in itself always an expression of choice, in so far as it determines the rejection of certain conditions of existence. In Stentor and Vorticella choice of food occurs in a similar manner, though in these fixed infusoria there is, as we have seen, usually more than one way of rejecting unsuitable conditions.

In Stentor the following behavior is at times observed. The animal is outstretched and feeding quietly in the usual way. Many small objects pass into the buccal pouch and are ingested. Suddenly a larger, hard-armored infusorian, Coleps, is drawn into the pouch. At once the ciliary current is reversed and the Coleps is driven out again. Then the current is resumed in the usual direction. Vorticella and other fixed infusoria often reject large objects in the same way. But besides reversing the ciliary current, these organisms may, when the ciliary current brings unsuitable material, bend over into a new position, contract, or leave their place of attachment and swim away. All these reactions have been described in detail in our account of the behavior of Stentor.

Thus the choice of food in all these organisms depends merely upon whether the usual negative or avoiding reactions are or are not given. The avoiding reaction is the expression of such choice as occurs. Looking at the matter from this standpoint, we are forced to conclude that the entire behavior involves choice in almost every detail. The animals, as we have seen, are giving the avoiding reaction in a certain degree, from a slight widening of the spiral course to the powerful backward swimming, almost continuously. The straightforward course is the expression of positive choice or acceptance; the avoiding reacting of negative choice or rejection. No distinction can be made between choice and the usual behavior. Indeed, choice is the essential principle of behavior based on the method of trial.

What happens if the organisms settle down and attach themselves in a region where no food exists ? This question seems not to have been specially investigated. But it is known that under most kinds of unfavorable conditions, — conditions which interfere with the normal functions, — the animal, after a time, leaves its place and swims away to a new location. Doubtless this happens also when food is lacking. We may sum up the food habits of this first class of ciUates as follows : They settle down in a certain region and then bring a current of water to the mouth. The particles in this current are taken as food, without any sorting, so that many that are not useful are ingested along with the others. But if decidedly unsuitable material is brought, then the animal reacts as to other unfavorable stimuli — reversing the current, contracting, shifting position, or finally moving away to a new place. The method of trial of varied movements is at the basis of the behavior here as elsewhere.

The second class of ciliates includes those which move about in search of their food, preying upon larger organisms and seizing them with the mouth. Maupas has well called these the hunter ciliates. The method of taking food in these animals often resembles in many respects that of the species already described. Thus Stylonychia runs about here and there, producing a strong vortex leading to its mouth. This often carries other infusoria, of considerable size, to the mouth. These are then seized and worked gradually back into the internal protoplasm. Some species move about more rapidly and more extensively, while the ciliary vortex is reduced so that it is of little consequence for food getting. On coming in contact with another infusorian the latter is seized by the usually armored mouth ; this is opened widely and the prey is swallowed. In this way such infusoria often feed upon other animals almost or quite as large as themselves, the mouth opening widely and the body becoming greatly distended.

An excellent example of one of these hunter ciliates is furnished by Didinium. This animal (Fig. 113) is cask-shaped, with a truncate anterior end, bearing in its centre the mouth on a slight elevation. The body bears but two circles of cilia. By the aid of these, Didinium swims about rapidly, revolving to the right on its long axis and frequently changing its direction. On coming in contact with a solid object it stops, pushes forward against the object the conical projection which bears the mouth, and

revolves rapidly on its long axis. The mouth ing paramecium. After Balis armed with a number of strong ribs ending bianiin points, which apparently project a little from the cone bearing the mouth. When pushed forward against a soft organism, these points apparently pierce and hold it. The revolution on the long axis has the appearance of a process of boring into the body. The mouth now opens widely and swallows the prey. Paramecium often falls a victim to Didinium in this way (Fig. 113). Sometimes the Didinium is smaller than its prey, forming after the feeding process a mere sac over its surface.

The point which interests us at present is that Didinium reacts in the way described not merely to objects which may serve as food, but also to all sorts of solid bodies. In other words, the process is one of the trial of all sorts of conditions. On coming in contact with a solid, Didinium " tries " to pierce and swallow it. If this succeeds, well and good; if it does not, something else is " tried." In a culture containing many specimens of Didinium, the author has seen dozens of individuals reacting in this way to the bottom and sides of the glass vessel, apparently making persevering efforts to pierce the glass. Others "try" water plants, or masses of small algae, about which many specimens gather at times. Of course they get no food in this way. On coming in contact with each other, the animals react in the same way, often becoming

attached to each other, and sometimes forming chains of four or five. But they never succeed in swallowing one another. They often try rotifers in the same way, but the outer integument of these organisms is so tough that Didinium does not succeed in piercing it, and the rotifer escapes. Stentor and Spirostomum are often fastened upon, but usually escape, owing to their large size, great activity, and rather tough outer covering. The reason why Paramecium is usually employed as food rather than other organisms is clearly due to the fact that when the Didinia try these, they usually succeed in piercing and swallowing them, while with most other objects they fail.1

Didinium is a type of the hunter ciliates in this respect. The process of food-getting is throughout these species one of trial of all sorts of things. There is no evidence that in some unknown way the infusoria perceive their prey at a distance, nor that they decide beforehand to attack certain objects and leave others unattached. They simply "prove all things and hold fast to that which is good." We cannot do better in emphasizing this point than to quote a portion of the words of the veteran investigator Maupas, as given in Binet's "The Psychic Life of Micro-Organisms" (pp. 48, 49): —

"These hunter infusoria are constantly running about in search of prey; but this constant pursuit is not directed toward any one object more than another. They move rapidly hither and thither, changing their direction every moment, with the part of the body bearing the battery of trichocysts held in advance. When chance has brought them in contact with a victim, they let fly their darts 2_ and crush it ; at this point of the action they go through certain manoeuvres that are prompted by a guiding will. It very seldom happens that the shattered victim remains motionless after direct collision with the mouth of its assailant. The hunter, accordingly, slowly makes his way about the scene of action, turning both right and left in search of his lifeless prey. This search lasts a minute at the most, after which, if not successful in finding his victim, he starts off once more to the chase and resumes his irregular and roving course. These hunters have, in my opinion, no sensory organ whereby they are enabled to determine the presence of prey at a distance; it is only by unceasing and untiring peregrinations both day

1 Balbiani (1873) described Didinium as discharging trichocysts from the mouth region against its prey, thus bringing it down from a distance. This account has not been confirmed by other observers, and the writer has never seen anything of the sort in the innumerable cases of food-taking in Didinium which he has observed. It can hardly be doubted that the trichocysts represented in Balbiani's figure (our Fig. 113) really come from the injured Paramecium, and not from the Didinium.

2 This use of the trichocysts has not been confirmed by other writers and was not absolutely observed by Maupas himself. and night that they succeed in providing themselves with sustenance. When prey abounds, the collisions are frequent, their quest profitable, and sustenance easy; when scarce, the encounters are correspondingly less frequent, the animal fasts and keeps his Lent. The Lagynus crassicollis, accordingly, never sees its victim from a distance and in no case directs its movements more toward one object of prey than toward another. It roams about at random, now to the right and now to the left, impelled merely by its predatory instinct — an instinct developed by its peculiar organic construction, which dooms it to this incessant vagrancy to satisfy the requirements of alimentation."

It is evident that these words of Maupas are an excellent description of behavior based on the general method of trial of all sorts of conditions though varied movements, and they bring out clearly the essential principles in the food reactions of infusoria. The same method of behavior is found, as we have seen, throughout almost the whole circle of activities in these organisms ; the food reactions epitomize the entire behavior. While unicellular forms are the very lowest organisms, an account limited to their behavior alone might give us a one-sided view of the principles of behavior in the lower organisms. The Metazoa differ from the Protozoa structurally in the important facts that their bodies are made of many cells and that they have a nervous system. Does the behavior of such organisms differ essentially from that of the Protozoa? Have we been dealing in our study of unicellular organisms with a peculiar group, whose behavior is of a character essentially different from that of other animals ? How far do the general principles to be deduced from the behavior of Protozoa hold for animals in general ? To answer these questions is the province of the following chapters.

We shall take up in detail the behavior of only one of the lowest groups of Metazoa — the ccelenterates. This will be followed by a chapter on some of the main features of behavior in other invertebrates. A general analysis of behavior in both Protozoa and the lower Metazoa is found in the third part of the book. The Ccelenterata or Cnidaria form, perhaps, the lowest of the larger groups of Metazoa. This group includes the fresh-water Hydra, hydroids, sea anemones, corals, and jellyfishes or medusae. The behavior of the corals and of hydroids has been comparatively little studied, so that the present account will be limited mainly to Hydra, the sea anemones, and medusae.

All of these animals are made up of many cells, of many different kinds, and usually arranged in three more or less irregular layers. Of special interest from the standpoint of behavior are the nerve cells. In Hydra these consist of comparatively few, small cells with long, branched processes, scattered among the ectoderm and entoderm cells. They apparently serve to connect the other cells. In the sea anemones the nerve cells are more numerous than in Hydra, but are likewise scattered throughout the body, in both ectoderm and entoderm. They are somewhat more numerous in the neighborhood of the mouth than elsewhere. In Medusae the nervous system is more concentrated. The cells and fibres form two rings about the edge of the body : one lies just beneath the ectoderm of the exumbrella, the other beneath that of the subumbrella. These rings are interconnected by scattered fibres. A plexus of nerve fibres covers the entire concave surface of the subumbrella and manubrium, beneath the ectoderm. This plexus is compared by Romanes as regards texture to a sheet of muslin. Nerve cells and fibres are found also in the tentacles, but are not known on the convex surface of the exumbrella. The two marginal nerve rings are often spoken of as the "central nervous system" in medusae.

In the ccelenterates we take up animals with action systems differing much from those of the organisms we have hitherto studied. The chief movements are due to contractions and extensions of parts of the body and tentacles, produced by contractions of the muscle fibres. The body is flexible, and being radially symmetrical may contract or bend with equal ease in any direction. Under natural conditions, Hydra and the sea anemone are usually attached and at rest, while the medusa may be in movement. Let us examine the behavior under such conditions, when no observable stimulus is acting on them, aside from the usual conditions of existence.

If we observe an undisturbed green Hydra attached to a water plant or the side of a glass vessel, we find that it usually does not remain still, but keeps up a sort of rhythmic activity. After remaining in a certain position for a short time it contracts, then bends to a new position, and reextends (Fig. 114). In this new position it remains for one or two minutes, then it again contracts, changes its position, and again extends. This continues, the changes of position occurring every one or two minutes. In this way the animal thoroughly explores the region about its place of attachment and largely increases its chances of obtaining food. This motion seems to take place more frequently in hungry individuals, while in well-fed specimens it may not occur.

Thus contractions take place without any present outward stimulus ; the movements are due to internal changes of some sort, like those of Vorticella. The same behavior may be produced, as we shall see later, by external stimuli. In the yellow Hy- dra such movements do not occur — at least not with such frequency. Fig. 114. — Spontaneous changes of positions in an undisturbed Hydra. Side view. The extended animal (1) contracts (2), bends to a new position (3), and then extends (4).

Fig. 115. — Diagram of different positions taken by Hydra, as seen from above. After Wagner. This is apparently correlated with the fact that the yellow Hydra has very long tentacles, which lie in coils all about it, so that exploratory movements are not necessary in order to reach such food as may be If a green Hydra is left for long periods undisturbed, it does not remain attached in the same posi- 1 tion, but moves about from place to place. The movements often take place in random directions, — the animal starting first in one direction, then in another. Figure 116 shows the movements of a green Hydra, which was left alone for some days in the bottom of a large, clean glass dish, the light coming from a window at the right. This movement is probably brought about by Fig. n6. -Path followed by a green hunger — the animals taking a new

Hydra that was left for some days undisturbed position when food becomes Scarce. on the bottom of a clean glass dish. After £L , . . 1 different ways. In the commonest method the animal places its free end against the substratum, releases its foot, draws the latter forward, reattaches it, and repeats the process, thus looping along like a measuring worm (Fig. 117). In other cases it attaches itself by its tentacles, releases its foot, and uses the tentacles like legs. A still different form of locomotion has been described, in which the animal is said to glide along on its foot; how this is brought about is not known.

In sea anemones, rhythmical contractions of the undisturbed animal have apparently not been described. But Loeb (1891, p. 59) finds that Cerianthus if not fed will after a time leave its place in the sand and creep about, finally establishing itself in a new place. The common sea anemone Me- tridium moves about frequently from place to place on the sides or bottom of the aquarium, and so far as can be observed, this seems often due simply to hunger or other