STUDIES IN ANIMAL LOCOMOTION

STUDIES IN ANIMAL LOCOMOTION VIII. THE KINETICS OF LOCOMOTION OF NEREIS DIVERSICOLOR BY J. GRAY Zoological Laboratory, Cambridge (Received 30 March 1938) (With One Plate and Eight Text-figures) 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 welldefined 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 parapodial 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 establish-

io J. GRAY ment 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 ^^s^^- 1 \. > ' ' ' ' j "' '."'~ 'L'"''" 'i 'U"fr 3 > r s~ s~ s~ S'/S' A s~ \-\s~ /* s i-^a K^ /'.«\ \ \ V./' \ \ \ \ w \. v y\ s N.X >-.'-^> '>-\ }s\ 'S V.v r 1 ~ 1 ~ 1" 1 ~ 1 ~ 1" 1 ~ 1 ~ 1"I\~I"i" 1 ~yj~ ' r r r v r r r r ^\ r r r y Y Text-fig. 1. DiagramshowingthestartofslowanibulationinTVereu. \Vt* Note the rapid spread ( ) of the ambulatory pattern over the whole body from head to tail and the movement of this pattern from tail to head at a much slower rate ( ). 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 (PI. 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 4

Studies in Animal Locomotion 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 PI. 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 - Direction of motion of wave II Text-fig. 2. Diagram illustrating the motion relative to the ground of two points A^ and B lt on opposite sides of the body of a Nereis, when a complete ambulatory wave of longitudinal contraction passes over the longitudinal muscles of the body. The wave, as shown, consists of fourteen segments and the muscular cycle is therefore conveniently divided into fourteen phases. Since each segment attaches itself to the ground when in the fully extended state, the wave advances (relative to the ground) a distance equal to fourteen times the length of a fully extended segment during the passage of the wave. The advance of the wave, relative to the ground, is shown by the points on the base line WI-WIJ : the advance (relative to the ground) of the points A t and B lt situated on the front edge of segment I, is shown by the dotted lines A t A u and B^ B lt respectively. 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 {W^-W^) (relative to the

12 J. GRAY earth) equal to fourteen times the length (/) of a fully relaxed segment (-BiQ). During the same period the points A 1 and B x at the anterior end of segment I travel along the lines A x -A u and Bj-B u respectively, since segment I will occupy, relative to the wave, the successive positions shown for each of the segments I-XTV on the right of the figure. The motion of the line A 1 B 1 is shown in Text-fig. 3, and this can be compared with the motion of the ligatures seen in the cinematograph record in PI. 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 (A) and the distance moved by the wave relative to the earth is nl, where n is the number of segments in the wave and / Text-fig. 3. Track of the line A 1 B 1 in Text-fig. 2 during the passage of one complete muscular wave. Note that the tracks of the threads shown in PI. I, fig. a are of the same type. 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 A. So long as the wave-length and number of segments constituting the wave are constant the value of / 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 / 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.

Studies in Animal Locomotion Direction of movement of wavt Text-fig. 4. Diagram illustrating the motion, relative to the ground, of one side of a segment, with its parapodium, when one complete ambulatory wave of longitudinal activity passes over the body of Nereis. The dotted lines show the motion of the points Ax, B t and C x during the passage over the body of a wave, identical in form with that shown in Text-fig. 2. The preparatory stroke (shown occurring at the nth phase in the cycle) occurs when the longitudinal muscles begin to extend in length after relaxation from a period of active contraction; this phase occurs on the leading surface of the wave. - Dn-octWa of movem«l of wavt relative to tie bead of tiio uima] A 1 ' 1 «,. *$ '; ' i ' \ i /// i \ -\ \ h i V 1 «-Direction of movement of wiv, relauve to the head of the aiisul -*Dlr«tkHi of movement of animal relative to tie (r«nd \ J\ 6 \ --, \WrT-\ N ) j / j! ' * f r- / /.- ' / / (, 5 4 3 2 1 4- DixMtwn of mottbttt of wava rtlativc to the bmd of the "ht1fl v-dirvctioa of moysment of «n±m*j rdrtivt to the grtraod c J/ 1/ ) } ' f 1 s * s 1 / / / 1 / 1 -I./ / / j' t' Text-fig. 5. Digrams showing that the relationship between the direction of motion of a bilaterally contractile worm, and that in which waves of longitudinal contraction pass over the body, depends on whether the body is attached to the ground during periods of maximum longitudinal contraction or during periods of maximum longitudinal elongation. In A no attachment is effected, the centre of gravity (CG) of the worm remaining stationary; no progression occurs. In B the worm is attached to the ground by the posterior edge of each fully contracted segment. Note that the body moves in a direction opposite to that in which the waves of contraction pass over the body. In C attachment is effected by the posterior edge of each fully relaxed segment. Note that the body moves, relative to the ground, in the same direction' as that of the waves relative to the head of the animal. In all three figures the direction, velocity, and form of the waves relative to the body are identically the same. The movement of each segment relative to the earth is shown by the lines and the movements of the points d'appui by the lines

14 J. GRAY The motion of a single parapodium can be followed in Text-fig. 4, wherein the line Bx Cx 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 (PI. 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 that of swimming.' 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 Textfigs. 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

Studies in Animal Locomotion 15 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. Direction of movement of wive Text-fig. 7. Diagram showing the movement (relative to the ground) of a parapodium and of individual points (A, B and C) on the surface of a wave when the wave moves forward (relative to the ground) at the same velocity as it moves over the surface of the body. The dotted line shows the track of the point B, situated on the posterior edge of segment XIV; the line H 1- shows the track of point A on segment XIV. The track of a parapodium on segment I is also shown. Note that the parapodium, when executing its effective stroke, is travelling towards the hind end of the body and backwards relative to the ground; this motion causes aflowof water from the leading surface of the wave towards the trailing surface and so subjects the body to a forward propulsive force. 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 PI. 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 con-

16 J. GRAY siderable 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 Direction of motion of worm IS Text-fig. 8. Diagram showing the type of movement, relative to the ground, of a single parapodium when a Nereis is swimming forwards in water during the passage of two complete waves over the segment. Note that during the effective stroke (e.g. positions 8, 9, 10) the parapodium is moving backwards relative both to the ground and to the muscular wave. The two upper dotted line* show the track of the corresponding point on the other side of the body. 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 1. 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. 2. During rapid ambulation, the activity of the parapodia is co-ordinated with that of the longitudinal muscles and progression is, largely, attributable to these

JOURNAL OF EXPERIMENTAL BIOLOGY, XVI, i. PLATE T GRAY. STUDIES IN ANIMAL LOCOMOTION (pp. 1 1

Studies in Animal Locomotion 17 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. 3. The mechanism of swimming is described. REFERENCES FOXON, G. E. H. (1936). Ann. Mag. nat. Hist. (10), 18, 403. GRAY, J. (1936). J. exp. Biol., 13, 192. GRAY, J. & LISSMANN, H. W. (1938). J. exp. Biol., 15, 506. EXPLANATION OF PLATE I Fig. 1. Photograph (by Mr D. P. Wilson, Marine Laboratory, Plymouth) of Nereis diverticolor creeping from right to left. Note the variation in the length of the parapodial waves and the correlation between these waves and those seen on the dorsal blood vessel, the active parapodia being situated on each of the leading surfaces of the muscular waves. Scale: 1 in. Fig. 2. Successive cinema-photographs of an actively creeping Nereis diversicolor moving from right to left. The movement of the transverse axis of a segment can be followed by observing the movements of the three transverse threads attached to the body. Note that each point moves forward when the underlying longitudinal muscles are contracted or contracting and is at rest when these muscles are relaxed. Scale: 1 cm. Fig. 3. Transition from ambulation to swimming in Nereis virens. Note that the anterior end of the body shows typical swimming waves, while the posterior end still displays typical ambulatory waves of short wave-length and smaller amplitude. Fig. 4. Successive cinema-photographs of Nereis diversicolor swimming from right to left. Note the slow rate of progression of the animal through the water compared to the speed of movement of the waves (indicated by numerals) relative either to the body or to the ground. Scale: 1 in. JEB -XVli