Behavior of the Lower Organisms

In Opalina ranariim the first marked effect of the electric current is to cause the animals to swim to the anode instead of to the cathode. Its reaction seems thus in striking contrast with that of other ciliate infusoria. We must examine the reaction in Opalina, following Wallengren (1902), to see how this result is brought about. Opalina is a large, flat, disk-shaped, parasitic infusorian, living in the large intestine of the frog. For experimental work it is examined in physiological salt solution, as it soon dies in water. There is no mouth, since food is obtained by absorption over the entire body surface. The body is closely set with fine cilia. The anterior end of the body is more pointed than the posterior. From the anterior portion there extends backward at one edge a convex region, ending at a sort of notch in the middle of the body (Fig. 107, x). This convex region is set with cilia having, as we shall see, a somewhat different function from those of the remainder of the body. The side bearing this convexity is usually known as the right side.

Opalina swims with anterior end in front, at the same time usually revolving on its long axis. When stimulated by contact with a solid, or in other ways, it turns toward the side bearing the convexity — the right side. Observation shows that this movement is due to the fact that the cilia on the convexity of the right side now strike forward instead of backward, thus necessarily turning the animal toward the side bearing them. In this way the typical avoiding reaction of Opalina is produced.

If a preparation of Opalina in physiological salt solution is subjected to the action of a weak electric current, the animals swim to the anode. Examining the individuals, it is found that the cilia on the anode half of the body strike backward, those on the cathode half forward, exactly as in Paramecium. Why then does Opalina swim to the anode instead of to the cathode? The secret of this difference lies in the following facts. The cilia of the convexity of the right side (Fig. 107, x) are very easily reversed by a weak current. The cilia of the opposite side, on the other hand, are little affected by a weak current. Their usual backward stroke is decreased in power, and doubtless some of the cilia are reversed, but the general effect of their action is still to drive the animal forward. Let us suppose that the Opalina is at first transverse to the electric current, with right side to the cathode, as in Fig. 107, 1. As soon as the current

Fig. 107. — Diagrams of the movements of the cilia, and of the direction of turning, in the reaction of Opalina to the electric current. After Wallengren (1902). begins to act, the cilia of the right (cathodic) side become directed forward, while those of the left (anodic) side remain directed backward. The result is of course to turn the animal to the right, toward the cathode. Thus the specimen passes through the position shown in Fig. 107, 2, and comes into a position with the anterior end directed toward the cathode (3). The cilia of the anterior part of the body are now directed partly forward, those of the posterior half backward. In this position, as we know, Paramecium remains ; indeed, the whole reaction thus far is essentially like that of Paramecium. But in Opalina, so long

as the current is weak, only the cilia on the convexity of the right side strike powerfully with their reversed stroke, — these being the cilia that are reversed in the usual avoiding reaction. The other reversed cilia strike only weakly. In consequence the animal must turn toward the right side, reaching the position shown in Fig. 107, 4. Here most of the strong cilia x of the convexity are still striking forward, hence the animal still turns toward the right. A little beyond 4, — between this and 5, — the animal reaches a position where the tendencies to turn in opposite directions are equal.1 But the turning which has been initiated in positions 1-4, as a rule has given the animal sufficient momentum to carry it past this dead point, so that it reaches the anode pointing position (Fig. 107, 7). Here the cilia of both sides of the anterior end are directed backward. When striking backward the cilia x of the convexity are no more powerful than those of the opposite side. Hence there is now no tendency to turn farther, and the anode-pointing position is retained. Since the backward stroke of the anterior cilia is more powerful than the forward stroke of the reversed posterior cilia, the animal is carried forward to the anode. Thus in a weak current the position with anterior end directed to the anode is the stable one, so that in the course of time, after some oscillation, the animals reach this position and swim toward the anode.

Now if the current is considerably increased in strength, the cathodic cilia are caused to strike more strongly forward than before. Their motor effect therefore nearly equals that of the anodic cilia, so that the forward movement toward the anode is made much slower. If at the time the current is made the Opalina is in an oblique position, as will usually be the case, or if as a reaction to other stimuli during the passage of the current it passes out of the position with anterior end to the anode, then another effect is produced. Suppose it comes thus into the position shown in Fig. 107, 8. Then the larger number of cilia tend to turn it to the right, as is shown by the arrows at 8. It thus comes into position 1, where all the cilia assist in turning it to the right ; it continues in the same way through position 2 to position 3, with anterior end pointing to the cathode. With a weak current, as we have seen, this position is not a stable one; the stronger forward beating of the cilia on the convexity of the right side cause the animal to continue to turn to the right. But with a stronger current this becomes changed. Since even in a weak current the cilia of this convexity strike as strongly forward as they can, their forward stroke is not increased when the current is

1 If the animal at this point or earlier turns on its long axis, as it frequently does in its usual locomotion, it must now swing back through the cathode-pointing position, till it again reaches a position corresponding to 4 or 5. made stronger. But as the current is increased, the forward stroke of the cilia on the left side of the anterior half of the body becomes more powerful, — just as happens with all the anterior cilia in Paramecium. Hence, when the current reaches a certain strength, the cilia of the left side, in an Opalina pointing toward the cathode, beat as strongly forward as do those of the right side. There is then no cause for turning toward either the right or the left. The position with anterior end directed toward the cathode has become a stable one. Thus, when a strong current is passed through a preparation of Opalinas, most of them become directed after a time toward the cathode, and swim slowly in that direction. A number may be at first directed toward the anode, but as soon as these by any chance get out of the anode-pointing position, they also become directed toward the cathode.

With a still more powerful current the Opalinas retain nearly or quite the position with anterior end to the cathode, but move backward (or sometimes sideways) toward the anode. Wallengren believes that this is a passive movement due to the cataphoric action of the electric current. In Paramecium, as we have seen, there is a similar movement under these conditions, but due to the fact that the cathodic cilia beat more effectively forward than do the anodic cilia backward.

Thus altogether we find that in Opalina the electric current acts on the motor organs in fundamentally the same way as in Paramecium. But owing to peculiarities of the action system of Opalina, this results, with a weak current, in movement forward toward the anode; with a stronger current in movement forward toward the cathode; with a still stronger current in movement backward or sideways toward the anode. Reviewing our results as to the effect of the continuous electric current on the ciliate infusoria, we find a complete agreement throughout in the action of the current on the motor organs, with the greatest possible diversity in the resulting movements of the animals. In all cases the cilia in the anode region strike backward, as in the normal forward movement, while the cilia of the cathode region are reversed, striking forward. With different strengths of current, and with infusoria of different action systems, this results sometimes in movement forward to the cathode ; sometimes in movement forward to the anode ; sometimes in a cessation of movement, the anterior end continuing to point to the cathode ; sometimes in a backward movement to the anode ; sometimes in a position transverse to the current, the animal either remaining at rest or moving across the current. These variations depend upon the

differences in the strength of beat of the cilia of different regions of the body under currents of different strength. The different effects produced may be classified, as to their causes, in the following way: — 1. The orientation with anterior end to the cathode is due to the fact that the cilia of the cathodic side strike forward ; of the anodic side backward. This may be assisted or hindered by the usual tendency of the organisms to turn when stimulated toward a certain structurally defined side.

2. The movement toward the cathode in weak or moderate currents is due to the fact that under these conditions the backward stroke of the anodic cilia is more powerful than the forward stroke of the cathodic cilia. 3. The cessation of progression in a stronger current, with retention of the cathode-pointing orientation, is due to the fact that as the current is increased the forward stroke of the cathodic cilia becomes more powerful, till it equals the backward stroke of the anodic cilia.

4. The swimming backward toward the anode in a still stronger current is due to a continued increase in the power of the forward stroke of the cathodic cilia, so that they overcome the tendency of the anodic cilia to drive the animal forward. (In Opalina, Wallengren believes that this backward movement is due, at least partly, to the cataphoric effect of the current.) 5. The unstable transverse position seen in some cases (Spirostomum) is due primarily to the fact that the cilia of one side of the elongated body are more powerful, when striking either backward or forward, than are the corresponding cilia of the opposite side. As a result, neither the position with anterior end to the cathode nor that with anterior end to the anode is a stable one, and the animal is compelled to oscillate about a transverse position. This result is accentuated by the slenderness and suppleness of the body in these species.

6. The orientation with anterior end to the anode seen in certain cases (Opalina in a weak current) is due to the fact that the cilia of one side of the anterior half of the body are more readily reversed than the opposing cilia, and their reversed stroke is more powerful, though their usual backward stroke is not. The result is that the position with anterior end to the cathode becomes unstable, while the position with anterior end to the anode is stable so long as accidental causes do not produce slight deviations from it.

7. The transverse or oblique position, at rest or with movement athwart the current, is due to interference between the contact reaction and the effect of the current. This position is maintained only when the more powerful cilia of the peristome are striking forward ; that is, when the peristome is directed toward the cathode. When the peristomal cilia are thus striking forward, their action is comparatively ineffective, so that it does not overcome the attachment to the substratum, in the contact reaction.

What is the cause of the reaction to the electric current ? The most striking phenomenon in a general view is usually a movement of the organisms en masse toward the cathode or anode. It is well known that the electric current has the property of carrying small bodies suspended in a fluid toward the cathode or anode, depending on the conditions. This phenomenon is commonly known as cataphoric action, or as electrical convection. When the movement of small organisms toward one of the electrodes is mentioned, the first thought that comes to mind is of course the possibility that they are thus passively carried by the cataphoric action of the current. But this view can be maintained only on the basis of an extraordinarily superficial acquaintance with the facts. Careful study shows, as we have seen, that the current has definite and striking effects on the cilia, and that it is to these effects that the peculiarities of movement under the action of the current are due. Nevertheless, the theory that the phenomena are passive movements due to the cataphoric action of the current continues to be brought gravely forward at intervals, and doubtless this will continue. The fundamental fallacy of this theory is the idea that we must account in some way by the action of the current for the fact that the organisms move. This is quite unnecessary, for they move equally without the action of the current. The movement is spontaneous, so far as the electric current is concerned. It takes place by the agency of the motor organs of the animal, driven by internal energy, and acting upon the resistance furnished by the water. It is only the changed direction of the movement that the electric current must account for.

There is no place for the agency of the cataphoric action in transporting the animals, for they are visibly transporting themselves, just as they were before the cataphoric action began. It is absolutely clear that the movements of the cilia, described in the preceding pages, are at the bottom of the observed behavior, and any explanation of the reaction to electricity must account for the influence of this agent on the cilia. This the theories of passive movement by cataphoric action make no attempt to do.

The clearest disproof of the theory that the movement is a passive one due to cataphoresis is of course the well-established positive proof that the movement is an active reaction of the organism. But the theory can be disproved on other grounds. Statkewitsch (1903 a) shows that dead or stupefied Paramecia that are suspended in viscous fluids are not moved by cataphoric action, while living Paramecia in the same fluids swim to the cathode. Dead or stupefied Paramecia placed in water in a perpendicular tube through which an electric current is passed sink slowly and steadily to the bottom, whatever the direction of the current, while living specimens pass upward when the cathode is above. If the anode is above and a very strong current is used, the living animals swim backward to the anode, as described on page 98. They therefore move upward against gravity, while dead or stupefied specimens with the same current sink slowly to the bottom of the tube. It is thus clear that neither the forward movement to the cathode nor the backward movement toward the anode is directly due to the cataphoric action of the current, for this action is not capable of producing the observed movements.

The cataphoresis might of course act in some way as a stimulus to induce the observed active movements of the cilia. This is apparently the view toward which Carlgren (1899, 1905 a) and Pearl (1900) are inclined. This is of course a theory of a radically different character from that which we have been considering. Just how this effect would be produced through the known physical action of the current has not been shown. Coehn and Barratt (1905) hold that Paramecia in ordinary water become positively charged, through the escape into the water of the negative ions of the electrolytes which the body holds, while the positive ions are retained. As a result of this positive charge, the electric current tends to carry the animals to the cathode; the infusoria are held to follow this tendency and swim with the pull of the current toward the cathode. In a solution containing more electrolytes, it is held that the positive ions escape from the protoplasm; hence the animals become negatively charged. They therefore pass to the anode when placed in a solution of sodium chloride or sodium carbonate. This theory leaves unaccounted for precisely the essential feature of the reactions, — the cathodic reversal of the cilia. It likewise fails to account for the fact that as the current becomes stronger the passage to the cathode ceases and the animals begin to swim backward to the anode, and for the further fact that individuals which have become accustomed to a solution of sodium chloride or carbonate no longer swim to the anode, but pass to the cathode as usual. These facts appear to be absolutely fatal to the view under consideration. Little is to be hoped of any theory that neglects what is clearly the fundamental phenomenon in these reactions, — the cathodic reversal of the cilia.

Another theory has held that the reaction to the electric current is due to the electrolytic effect of the current on the fluid containing the animals (Loeb and Budgett, 1897). The water of course contains electrolytes. These are separated by the current into their component ions, and the products of this electrolysis may be deposited on opposite poles of a body immersed in the fluid. There is some reason to suppose that an alkali may be deposited on that portion of the surface of the infusorian where the current is entering its protoplasm (the anodic surface), an acid where it is leaving the protoplasm (the cathodic surface). The relative amount of such action is unknown, but the suggestion is made that the observed effects of the current are due to these chemicals. This very interesting and suggestive theory seems, however, not to be supported by other known facts. The effects of different chemicals on the ciliary

action are known, and it is not true that acids produce continued reversal of the cilia, alkalies the opposite effect, as would be necessary in order to make this explanation satisfactory. Any effective chemical, either acid or alkali, produces, as we know, the avoiding reaction, with its succession of coordinated Fig. 108.— Diagram of the effects of the elecchanges in the ciliary movements. trie current on the cilia showing that the regions • ag Ludloff (l8g5) and

respectively, do not correspond to the regions where StatkewitSch (1903) SIIOW, the the current is leaving and entering the body. characteristic anodic and Cathodic effects do not correspond throughout to the regions where the current is entering or leaving the protoplasm. If a Paramecium has an oblique position, as in Fig. 108, the current enters the body on the entire left side, and leaves the body on the entire right side. Hence, on the theory we are considering, all the cilia of the left side ought to act alike, and in the opposite manner from the cilia of the right side. But this is not true. On the left side the cilia of the region b beat forward, those of c backward ; on the right side the cilia a strike forward, d backward. A similar distribution of the discharge of trichocysts under the influence of the induction shock is shown to exist by Statkewitsch. The distribution of the effects of the current on the cilia and on the trichocysts therefore does not correspond to the distribution of the regions where the current is entering and leaving the protoplasm; hence the latter cannot explain the former.

Another theory, somewhat less definite than the one last mentioned, but widely accepted, is the following. The electric current is conceived to have a polarizing effect on the organism, resulting in the different action of the cilia on the two halves. At the anodic half the current is considered to cause a backward movement of the cilia, or "contractile stroke"; at the cathodic half, a forward movement or "expansive stroke" (Verworn, 1899; Ludloff, 1895). The precise cause of this action is not given, but as supporting the possibility of this view, the experiments of Kuhne (1864, page 99) and Roux (1891) on the polarizing effects of the current may be cited. Kuhne showed that the violetcolored cells of Tradescantia become under the influence of the electric current red at the anodic end, green at the cathodic end, ■ — indicating that the anodic end becomes acid, the cathodic end alkaline. Roux showed that under the electric current the frog's egg becomes divided into two halves of different color. Furthermore, the two halves of a cell in the electric current become physically somewhat different, owing to the cataphoric action. There is a tendency for the fluids of the body to be carried to one end, — the cathodic, — while the solids are carried to the other, — the anodic. As a result of such chemical or physical polarization, or of both, it is then conceivable that the body of the infusorian may become divided into two halves, differing in such a way that the cilia act in opposite directions. On this view the backward stroke of the cilia on the anodic half of the body is as much a specific effect of the current as is the forward stroke of the cathodic cilia. Op- posed to this view is the consideration that the action of the anodic cilia is as a matter of fact not different from that in the unaffected animal, and the further fact that the cathodic effect is limited, in a weak current, to only the cathodic tip of the animal.

If both the backward and the forward positions of the cilia are specific effects of the current, it is difficult to see why the former should prevail so strongly over the latter in a weak current. On the other hand, if we consider the cathodic action alone as a specific effect of the current, interfering with the normal backward stroke of the cilia, then it becomes at once intelligible that this interference should be least in a weak current, and should increase as the current becomes more powerful. In producing its characteristic effect chiefly at the cathode, the action of the electric current on infusoria agrees with its action on muscle, as Bancroft (1905) has recently pointed out.

The most thorough study of the fundamental changes produced by the electric current is that made by Statkewitsch (1903 a), and his conclusions are entitled to high consideration. Statkewitsch subjected Paramecia that had been stained in the living condition with certain chemical indicators, — neutral red and phenol-phtalein, — to the influence of the electric current. He found that the current caused chemical changes within the protoplasm, the endoplasmic granules and vacuoles becoming more alkaline in reaction. Statkewitsch therefore concludes that the peculiar effect of the electric current on the cilia is due to a disturbance in the usual equilibrium of the chemical processes taking place in the protoplasm. The results of this disturbance are first shown, so far as the ciliary action is concerned, in the cathodic region, spreading thence over the remainder of the body, as illustrated in Fig. 61.

For any satisfactory theory of the reaction to the electric current, one thing is essential; it must account for the cathodic reversal of the cilia. It is perfectly clear that this is the characteristic feature of this reaction, and a theory that will account for this reversal will at once clear up the curious and apparently contradictory effects produced under various conditions. Theories which do not take this into account are at the present time anachronisms ; they fail to touch the real problem.

Whatever be the cause, it is clear that the behavior of infusoria under the action of the electric current differs radically from the behavior under other conditions. The position taken by the organism is not attained by trial of varied directions of movement, as in the reactions to most other stimuli, but in a more direct way. Different parts of the body are differently affected by the current, so that the behavior is not coordinated and directed toward a unified end, as in the reactions to other stimuli. The motor organs of the different parts of the body tend to drive the animal in different directions. The movement actually occurring is a resultant of these differently directed factors. It is therefore sometimes in one direction, sometimes in another, depending on the relative strength of the opposing factors. The animal thus does not approach an optimum nor cease to be stimulated, whatever the direction taken. Sometimes indeed no position of even comparatively stable equilibrium is possible (Spirostomum).

These peculiarities of the reaction to the electric current are due to the forced reversal of the cilia in the cathodic region of the body, — an effect not produced by any other agent. If the current produced only its anodic effect, the reaction to electricity would be, so far as the evidence indicates, precisely like that to other agents. The cathodic reversal of the cilia interferes with the normal behavior of the organism. Thus the action of the infusoria under the electric current is not typical of the behavior under other stimuli. It may be compared to the behavior of an organism that is mechanically held by clamps and thus prevented from showing its natural behavior. It is interesting to note that this cramped and incoherent behavior is found only under the influence of an agent that never acts on the animals in their natural existence. The reaction to electricity is purely a laboratory product.

We have seen that in Paramecium the behavior varies to a certain extent in different individuals or under different conditions. Similar variations might be described for other free swimming infusoria. But these observations do not tell us whether the behavior may change in the same individual or not. Does a given individual always react in the same way to the same stimulus under the same conditions? Or may the individual itself change, so that it behaves differently even when the external conditions remain the same, — as we know to be the case in higher animals? To answer these questions it is necessary to follow continuously the behavior of a single individual, and this can be done most satisfactorily in attached organisms, such as Stentor and Vorticella. We shall base our account on the usual behavior of Stentor rceselii, which illustrates well the points in which we are at present interested.

Stentor rceselii Ehr. (Fig. 109) is a colorless or whitish, trumpetshaped animal, consisting of a slender, stalklike body, bearing at its end a broadly expanded disk, the peristome. The surface of the body is covered with longitudinal rows of fine cilia, while the edge of the disk is surrounded by a circlet of large compound peristomal cilia or membranellas. These make a spiral turn, passing on the left side into the large buccal pouch, which leads to the mouth. The mouth thus lies on the edge of the disk, nearly in the middle of what may be called the oral or ventral surface of the body. The smaller end of the body is known as the foot; here the internal protoplasm is exposed, sending out fine pseudopodia, by which the animal attaches itself.

Stentor rceselii is usually attached to a water plant or a bit of debris by the foot, and the lower half of the body is surrounded by the so-called tube. This is a verv irregular sheath formed by a mucus-like secretion from the surface of the body, in which are embedded flocculent materials of all sorts. It is frequently nearly transparent, so as to be almost invisible. Stentor rceselii is found in marshy pools, where much dead vegetation is present, but where decay is taking place only slowly.