ABSTRACT
The locomotory movements of a typical polychaete worm, such as Nereis diversicolor, are of interest in that they are effected by two distinct mechanisms, (i) a series of parapodia which act as levers comparable to the appendages of terrestrial animals, (ii) the longitudinal muscles of the body. When Nereis is moving slowly over a solid surface, only the parapodia are active; during more rapid motion, or when the animal is swimming through water, the movements of the parapodia are co-ordinated with those of the longitudinal muscles and the two mechanisms combine to give a highly co-ordinated locomotory mechanism.
Under all circumstances the movements of one side of a segment alternate with those of the other, and during normal forward progression the unilateral activity of any one segment begins slightly after that of the segment situated immediately posterior to itself. During slow forward movement, waves of activity appear to pass alternately over the parapodia of each side of the body from a point situated at the posterior end of the animal. Such a picture is, however, confusing, for no such centre of locomotory activity is in conformity with the fact that relatively short fragments from any region of the body may, if suitably stimulated, exhibit a well-defined and normal locomotory rhythm. A more useful picture of the facts is derived from the observation of a Nereis, originally at rest, starting to move in a forward direction. Cinematograph records taken under such conditions show that the first parapodia to be active are always situated near the anterior end of the animal, and that in a very short period of time a pattern of parapodiál activity spreads posteriorly over the body by the activation of the parapodia of every fourth to eighth segment (see Text-fig. 1). As soon as one of these active parapodia begins its effective stroke, a cycle of activity begins in the parapodium of the segment lying immediately anteriorly to it, and this in turn is followed by a similar movement of the next anterior neighbour. The original pattern of active parapodia thereby moves anteriorly and gives rise to a series of waves moving, at a relatively low velocity, from the tail of the animal towards the head. The acquisition of the fully active ambulatory state clearly involves two distinct phenomena, (i) the rapid establishment of a distinct pattern of parapodial activity over the whole animal from head to tail, (ii) a much slower spread of activity from each active segment to the one situated immediately anteriorly and ipsilaterally to itself. The number of segments lying between the active parapodia on one side of the animal varies with the region of the body examined and with the frequency of parapodial movement. In the specimens examined, the smallest number was two and the largest number was eight. According to Foxon (1936) the parapodial waves pass posteriorly along the body; such a direction has never been seen during the present observations except during backward progression.
The propulsive action of an individual parapodium has recently been described by Foxon (1936). A point d’ appui with the substratum is effected by the tip of the parapodium when the latter is directed obliquely forwards. The body of the animal is then subjected to a forward pull by the contraction of the adductor muscles of the appendage; when the effective stroke is completed the parapodium faces obliquely backwards. At the end of this phase the parapodium remains inactive until the beginning of the next rapid preparatory stroke. During the preparatory stroke, the tip of the parapodium is lifted from the ground and the appendage swung obliquely forwards and then downwards to effect contact with the ground; the second effective stroke immediately follows. As pointed out by Foxon, the aciculum is retracted during the preparatory stroke and extended during the effective stroke.
When a Nereis is creeping rapidly over the ground, clearly defined activity of the longitudinal muscles of the body can be recognized (Pl. I, fig. 2), for waves of contraction and relaxation pass over the body from tail to head. This undulatory muscular pattern is developed in a manner essentially similar to that described for the pattern of parapodial activity. Very often the wave pattern appears almost simultaneously over the whole body, but a number of photographic records indicate that it starts at the anterior end and spreads very rapidly backwards. As in the case of the pattern of parapodial activity, the muscular waves, as soon as they appear, begin to move anteriorly at a velocity much lower than the rate of backward spread of the undulatory pattern itself. Again, there are two phenomena, (i) the rapid spread of the undulatory pattern over the whole of the body, (ii) the spread of this pattern, at a much lower rate, from one region of the body to the one lying immediately anteriorly to itself.
The motion of a segment during rapid forward ambulation is illustrated by Pl. I, fig. 2. The movements of particular points on the body can be observed by following the movements of the cotton ligatures tied round the body. Four points may be noted: (i) the two ends of each ligature move forward alternately–one end pivoting on the other, (ii) each point on the body remains stationary relative to the earth during the period at which the adjacent ipsilateral parapodium is carrying out its effective stroke, (iii) the parapodium carries out its effective stroke when the underlying circular muscles are relaxed, (iv) each point on the body moves forward, relative to the earth, when the underlying longitudinal muscles are contracted and when the adjacent ipsilateral parapodia are at rest at the end of their effective strokes.
Under favourable conditions, there is no slip between the ground and a region of fully relaxed longitudinal muscles, although there may be considerable slip of the parapodium itself over the substratum.
The motion of a typical segment can be followed diagrammatically in Textfigs. 2-4. The wave, as seen in its initial position on the right side of Text-figs. 2 and 4, is arbitrarily composed of fourteen segments and is moving from right to left. During the passage of one complete wave over the surface of the body each of the fourteen segments, in turn, will be stationary, relative to the earth, when the underlying longitudinal muscles are fully relaxed; it follows that while the wave travels one wave-length over the body, it travels a distance W1-W15 (relative to the earth) equal to fourteen times the length (l) of a fully relaxed segment (B1C1). During the same period the points A1 and B1 at the anterior end of segment I travel along the lines A1–A15 and B1–B15 respectively, since segment I will occupy, relative to the wave, the successive positions shown for each of the segments I-XIV on the right of the figure. The motion of the line A1B1 is shown in Text-fig. 3, and this can be compared with the motion of the ligatures seen in the cinematograph record in Pl. I, fig. 2.
It is clear that during the passage of one complete muscular wave over a point situated on the side of the animal’ s body, that point moves forward along an arc which is concave towards the outside of the body. Since the distance moved by the wave relative to the body is equal to one wave-length (λ) and the distance moved by the wave relative to the earth is nl, where n is the number of segments in the wave and l is the length of a segment when it is in contact with the ground, it follows that the distance moved by the body relative to the earth is nl–λ. So long as the wave-length and number of segments constituting the wave are constant the value of I depends on the degree of shortening undergone by the side of a segment when the longitudinal muscles are fully contracted. The greater is the degree of shortening the longer must be the length of a segment during maximum relaxation, and the longer is the distance travelled by the wave (relative to the ground) during the passage of one complete wave. If the body wall of the worm were flexible but not extensible the value of I would be minimal and the maximum rate of progression of the animal would be very much slower, for it would only be equal to the difference between the length of the body and the sum of its constituent wave-lengths. It may be noted that the degree of contraction of the segments in Text-fig. 2 is very much greater than is typical of an actual Nereis: in Plate I, fig. 2, the relative rate of progression of the body to that of the waves is considerably less than that shown in the diagrams in Text-figs. 2 and 4.
The motion of a single parapodium can be followed in Text-fig. 4, wherein the line B1C1 represents one side of segment I. The parapodium is lifted from the ground as it completes its effective stroke and is carried forwards and inwards as the underlying longitudinal muscles contract. The parapodium is carried forwards and outwards as these muscles relax ; it is during the early part of this period of relaxation that the parapodium makes its preparatory stroke. It should be observed that the motive power for this type of locomotion is almost entirely derived from the longitudinal muscles pulling against points d’ appui which are established by the bases of the active parapodia. The adductor muscles of the parapodia probably play a very subordinate role in the propulsion of the animal. It may be recalled that the establishment of points d’ appui by the longitudinally relaxed segments of Nereis is the precise opposite to the condition found in the earthworm (Gray & Lissmann, 1938), where fixation is effected by those segments showing complete longitudinal contraction. Text-fig. 5 shows that this difference accounts for the fact that the earthworm progresses in a direction opposite to that in which the muscular waves pass over the body, whereas Nereis moves in the same direction as the waves. Obviously if no fixation occurred, no progression would be effected.
THE PROGRESSION OF NEREIS THROUGH WATER
The movements executed by Nereis when swimming actively through water are essentially the same as those seen during rapid locomotion over the surface of the ground, although the amplitude, wave-length, and frequency of the undulatory waves passing over the longitudinal muscles are greatly increased, particularly in the anterior region of the body (Pl. I, fig. 4). The details of transition from ambulation to swimming cannot readily be followed by the eye, but cinematograph records show that the change in the form of the muscular waves first occurs at the anterior end of the animal, although the rest of the body is affected very shortly afterwards. (Text-fig. 6). Once this pattern is established it is transmitted anteriorly as during ambulation. Similarly, when a Nereis ceases to swim the return to waves of shorter length and amplitude first begins at the anterior end of the body and then spreads backwards.
The propulsive mechanism of a swimming Nereis can be followed by a consideration of Text-fig. 7, which shows, diagrammatically, the track of a single parapodium, relative to the earth, when a wave (of the same form as that shown in Text-figs. 2 and 4) moves forward, relative to the ground, at the same velocity as it moves over the surface of the body; under these circumstances, of course, the body would remain stationary relative to the ground. It can be seen that, during its effective beat, the parapodium is moving backwards relative to the earth. A movement of this type creates a posteriorly directed flow of water towards the hind end of the animal ; the water is, in fact, driven from regions immediately anterior to the parapodium in the vicinity of a leading surface of a muscular wave and is directed towards regions lying in the vicinity of a trailing surface. This backward current subjects the worm to a forward thrust and under normal circumstances the animal moves forward through the water. As the worm moves forward the track of a parapodium through the water becomes of the type shown in Text-fig. 8. It will be noted that the backward velocity of the parapodium relative to the earth is partly due to its own movements relative to the body of the worm and partly to the effect of the longitudinal muscles of the segment. In a form such as Nephthys the parapodia are probably passive—but they possess, owing to the movements of the underlying longitudinal muscles, a definite propulsive effect.
The efficiency of Nereis, as a swimming organism, is not very great, for the rate of progression of the body through the water is very small compared with the frequency and velocity at which the muscular waves pass over the longitudinal muscles (see Pl. I, fig. 4). If Nereis possessed no parapodia, there can be no doubt that the animal would progress through the water in a direction opposite to that of the muscular waves of the body. It is of some interest to note that if parapodial-like appendages are attached to a cylinder capable of exhibiting undulatory motion (see Gray, 1936), the direction of water flow past the body of the model is opposite to that which occurs in the absence of attached appendages, and to that in which the undulations pass over the cylinder itself.
Little or nothing is known of the mechanism responsible for muscular and parapodial co-ordination in Nereis. Removal of the supra- and suboesophageal ganglia usually initiates, like other violent stimuli, a period of active swimming, after which the animal temporarily loses tone and cannot usually swim for a considerable period of time. N. virens, on the other hand, exhibits prolonged swimming movements when cut into relatively short lengths. Transection of the nerve cord abolishes co-ordination between the two regions of the body, and involves loss of tone by the posterior region, but the movements of each region are normal in type ; removal of several adjacent parapodia does not interfere with the propagation of the parapodial or muscular waves.
After removal of the supra- and suboesophageal ganglia, Nereis displays one reflex which may be of ambulatory significance. Such preparations when left undisturbed usually show little or no spontaneous activity, but if they are subjected to gentle tension by being drawn over a horizontal surface, the parapodia quickly display an active and normal locomotory rhythm; if the preparation is initially active the frequency of the rhythm is increased on applying longitudinal tension.
SUMMARY
Ambulation in Nereis involves two phenomena: (a) the spread, at a rapid rate, of an ambulatory pattern over the segments of the body, the pattern being propagated (during forward progression) from the anterior end of the animal towards the tail; (b) the transmission of this pattern, at a relatively slow rate, in an anterior direction.
During rapid ambulation, the activity of the parapodia is co-ordinated with that of the longitudinal muscles and progression is, largely, attributable to these muscles. Since one side of each segment is fixed to the ground when the underlying longitudinal muscles are fully relaxed, it follows that the animal must progress in the direction in which the muscular waves travel over the body, and not, as in the case of the earthworm, in the opposite direction.
The mechanism of swimming is described.