On the Feeding Mechanism of the Copepods, Calanus Finmarchicus and Diaptomus Gracilis

In 1925, Storch and Pfisterer described at great length the feeding mechanism of the freshwater copepod, Diaptomus gracilis. They maintained that food was filtered from a current produced by the activities of the head swimming limbs. Their analysis of the mechanics of this process appeared to me inaccurate so that I decided to re-investigate the problem.

I examined first Calanus finmarchicus, a form so similar to Diaptomus that I assumed its feeding mechanism would be essentially the same. My observations, however, on the actual currents produced were totally different from those described by Storch and Pfisterer and I decided to obtain Diaptomus gracilis itself. This I obtained through the kindness of Mr R. Gurney and I found that its feeding mechanism and the currents it produced agreed closely with those of Calanus.

My observations agree with those of Storch and Pfisterer in that I describe food particles as being retained by the maxilla from a current which is caused to pass through it. I agree further that this feeding current results from the swimming activities of the anterior limbs. It is the swimming current that I consider these workers have described inaccurately and this is of vital importance to their argument, as their analysis of the mechanics of the process depends primarily on its correct interpretation.

Part of the observations on Calanus were made while occupying the table of the Royal Microscopical Society at the Marine Biological Laboratory at Plymouth.

The currents produced by the copepods were observed under the microscope by placing coloured starch grains in the water in which they were swimming.

The movements of the limbs are so rapid that it is impossible to analyse them by ordinary methods. Storch and Pfisterer (1925, p. 347) estimate a frequency of 300 beats a minute for the movements of the head swimming limbs of Diaptomus. In the specimens I observed, a rough estimate was 1000 a minute. I succeeded, however, in observing them with complete accuracy by using a stroboscopic source of illumination for the microscope.

The source of light, an ordinary “opalite” bulb, was placed behind a rotating disc which was pierced at equal distances by narrow radial slits whose width could be adjusted. The disc was 9 inches in diameter and was pierced at the edge by four slits about $112$ inches long. The best results were obtained when the slits were about $14$ inch wide. The disc was rotated by a motor whose speed could be controlled by a variable resistance.

The copepod was placed in a compressorium in a small drop of water, as deep as possible, to allow complete and unhindered movements of the limbs. It was then focussed under the microscope and the disc caused to rotate at gradually increasing speed. At first only irregular images of the animal were obtained, but, as the frequency of the flashes of light gradually approached that of the limb movements, the limbs appeared to move regularly and, for a copepod, very slowly. By increasing the speed still further I found it possible to obtain an image of the limbs apparently moving as slowly as desired. At the critical point, when the frequency of the light coincided with that of the limbs, the latter appeared to stand still, but never quite still. I assume that this means that the limb movement is never absolutely regular. By increasing the speed of rotation beyond the critical point the limbs appeared to move slowly but in the reverse direction. In making observations care has to be taken that the real direction of movement is being observed and not the reverse. This was extremely important in studying the movement of the maxilliped whose tip describes a rotary movement. It is, however, quite easy to settle whether the correct movement is being studied, because, in this case, a slight diminution in the frequency of the light makes the limbs move apparently faster, while if it is the reversed movement, the limbs appear to move more slowly or else reverse their apparent motion.

By placing the source of light so that only half is covered by the rotating disc, it is possible to obtain the field of the microscope illuminated, on the one side, by continuous light, and on the other, by intermittent light. In this way I have viewed a copepod with the limbs of one side moving at their normal speed while those on the opposite side appeared to move extremely slowly. This is of great use in studying such a form as a copepod whose movements are apt to be spasmodic. By shifting the slide from the stroboscopic to the continuous half of the field it can be settled at once whether or not the copepod is moving normally.

The main points in the anatomy of Diaptomus and Calanus relevant to a description of their feeding mechanism may be summarised briefly.

Motion through the water is of three types: (1) a sudden rapid jerk forwards, produced by the activity of the trunk swimming limbs, (2) a series of much smaller jerks produced by spasmodic irregular movements, and (3) a steady and comparatively slow forward movement resulting from continuous and rapid vibrations of the antennae, mandibular palps, maxillules and maxillipeds. The first type serves as a means of escape, the second is probably a means to counteract a tendency to sink while the third type produces the feeding current.

The uniramous antennules project laterally and act as balancers.

The biramous antennae project ventro-laterally just in front and to the sides of the large upper lip or labrum (see Text-figs. 1 and 5). The exopodites curve laterally and then dorsally close against the body. The endopodite projects ventrally at an angle of about 30° to the sagittal plane. The endopodites and basal part of the exopodites are armed with long setae spread out in a ventro-lateral fan. The exopodite terminates in a group of three long dorsally directed setae.

The mandibules are wedged in between the distinctly bifid lower lip and the massive upper lip, being slightly overhung by the latter. The biramous mandibular palps project ventro-laterally and carry a fan of setae spread out over the same angle as that of the endopodite of the antenna. These setae are shorter than those of the antenna. The maxillules arise nearer the sagittal plane than the more anterior limbs. Their main axes project antero-ventrally overhanging slightly the mandibules. Both endopodites and exopodites terminate in long setae which, however, are shorter than those of the mandibular palps. Those of the endopodite project directly ventrally and slightly medially, those of the exopodite project in the same direction as those of the mandibular palp. The maxillule is armed medially with three endites, a powerful toothed basal endite projecting obliquely forwards to the split in the lower lip and two distal endites which project forwards, their terminal setae lying across the mouth. On the outer side of the maxillule there is an exite armed with very long slender setae. The most ventral of these project laterally and then curve round posteriorly and extend as far back as the first pair of trunk swimming feet. The more dorsal, that is those next the body wall, project almost directly posteriorly. A section of the fan of setae thus formed would extend over an arc of a quarter of a circle.

The maxillae are short uniramous limbs projecting ventro-anteriorly. They comprise eight joints bearing long plumose setae which extend forwards to the mouth. They thus form the walls of a median wedge-shaped space with the mouth at its apex (see Text-figs. 2 and 5).

The maxillipeds are cylindrical uniramous limbs arising close behind the maxillae. In the living form it is difficult, with continuous light, to see them apart from the maxillae. Each consists of a very short basal joint, followed by two comparatively long joints of doubtful homology and (finally) a short flexible setose portion of five joints. The first long joint lies close against the maxilla and reaches as far as its tip. The remainder of the limb then stretches ventro-anteriorly and laterally, the setae spreading out in a fan close underneath the tips of the maxillules.

The trunk swimming limbs extend obliquely forwards, the apex of the anterior pair reaching as far as the mouth. They converge to a point slightly nearer the body than the tips of the maxillae.

The figures in Storch and Pfisterer’s paper are incorrect in several important details. The setae of the maxillulary exite are figured in a parasagittal plane. The maxillipeds are too short and project inwards instead of outwards and the swimming trunk limbs reach only as far as the maxillae instead of the mouth.

This arrangement of limbs results in two spaces of importance in the feeding mechanism (see Text-figs. 2 and 5). The first of these is the filter chamber between the maxillae, the walls of which are the maxillae, the roof is the body wall, and the floor the tips of the anterior trunk swimming limbs. The floor is complete laterally except for a small split occurring between the trunk limbs and the ventral setae of the maxillae. Anteriorly this space is closed by the large upper lip. Its only entrance is posteriorly between the maxillipeds and the first pair of swimming trunk limbs. The second of these spaces, which I call the suction chamber, is bounded medially by the maxillae and laterally by the setae of the maxillulary exite.

The essential points in the feeding mechanism of Diaptomus according to Storch and Pfisterer may be briefly summarised as follows :

The activity of the swimming limbs produces a powerful antero-posterior current which runs close against the ventral side of the body. This does not agree with “eine langsame, gleichmässige, gleitende Vorwärtsbewegung” (p. 338). A powerful current passing directly posteriorly means that a considerable amount of water passes backwards and hence the body causing this must pass forwards with considerable speed.

They point out, and lay considerable stress on the fact, that the head swimming limbs diminish in length posteriorly. Each limb produces the maximum movement of water at its tip. The mandibular palp being shorter than the antenna produces its maximum effect nearer the body wall. “So setzt also die Tätigkeit der drei Gliedmassenpaare eine verh ä ltnismässig hohe Wasserschicht in Bewegung, und zwar in der Weise, dass je das folgende Gliedmassenpaar die bewegte Wasserschicht näher an den Kôrper heranträgt.” (p. 351.) That is, each limb draws the current produced by the limb in front, nearer the body wall. They do not attempt to explain the mechanics of this process, which I believe to be erroneous, but which is, however, essential to their analysis of the feeding mechanism.

Assuming, as do Storch and Pfisterer that the limbs move synchronously, the speed of the tip of a limb will depend on the length of that limb and the arc through which the limb swings in one vibration. Storch and Pfisterer do not consider the latter factor, and, presumably, assume that each limb moved through the same arc. In this case the speeds of the tips of the limbs are directly proportional to the lengths of the limbs. The tip of the antenna moves faster than that of the mandibular palp, and the latter faster than the maxillule. Hence the movement of the tip of the mandibular palp can have no effect on the layer of water set in motion by the tip of the antenna because it will be moving more slowly than the latter. If the mandibular palp moved over a much greater arc in one vibration than did the antenna it would move faster, in which case it might conceivably draw some of the water set in motion by the antenna nearer to the body. Actually, however, this is not so. The mandibular palp and maxillule both appear to move over the same arc while the antenna moves through a much larger angle. Hence the layer of water set in motion by the tip of the antenna moves much faster than that forced backwards by either mandibular palp or maxillule.

According to Storch and Pfisterer then, the swimming current is drawn close to the body by the swimming limbs. This is further enhanced by the maxillulary exite. They say (p. 351) that because of its dorso-ventral axis of rotation, and because it lies close against the body wall it is especially adapted to increase still further the moving layer of water and draw it nearer to the body wall. The same criticism applies here as above. Being very close to the body wall its speed of movement through the water is very slow compared with the tip of the antenna and it can have no effect whatever in drawing the current closer to the body wall.

The current having been drawn close to the surface of the body passes backwards on either side, through the space between the forwardly projecting maxilla and the backward exite of the maxillule. The shape and arrangement of the latter, according to Storch and Pfisterer (p. 352), indicate that its function must be to confine the moving layer of water, thus preventing it spreading out too quickly and so losing force. From this it might be concluded that the maxillulary exite was a comparatively rigid plate. Actually the setae are very fine structures, rigid only at their bases and whip-like at their extremities. If the exite did move backwards and forwards as these workers maintain, the pressure on the setae would force them outwards. They certainly could not act as a barrier confining a stream of water which, as Storch and Pfisterer emphasise, is of considerable strength.

This powerful backward current will suck water into it from still regions. Such a region occurs only, according to Storch and Pfisterer (p. 353), between the basal endite of the maxillule on the outside and the tips of the maxillary setae on the inside. Why this position is chosen to the exclusion of others is not stated. Water is therefore sucked from this region into the backwardly flowing stream and to replace it water passes through the maxillary setae from the anterior part of the filter space. This results in a region of low pressure close behind the mouth which, in its turn, sucks water forwards from behind and, to supply this, water from the ventral part of the swimming stream is sucked into the filter space behind the maxillipeds (Storch and Pfisterer, Fig. 11).

Particles carried on the stream of water drawn in in this way are retained in the filter space, sucked forwards and eventually filtered off by the maxillary setae. They are then combed off by the proximal endite of the maxillule and pushed forwards on to the mandibles.

With regard to the maxillipeds Storch and Pfisterer state “Die Maxillipeden bewegen sich nur in einer sehr geringen Amplitude von hinten aussen nach vorne innen und umgekehrt” (p. 347), but can offer no explanation of their function (P-355).

The description and mechanical analysis of the feeding mechanisms as given by Storch and Pfisterer thus depend on two critical points, the production of a powerful antero-posterior swimming current by the head swimming limbs, and the suction of that current closer to the body by the more posterior of those limbs. The latter I have shown is mechanically impossible. The former rests on an inaccurate observation as no such current exists.

In a ventral or dorsal view of either Calanus or Diaptomus swimming slowly through the water, there can be seen, very readily, two large swirls¹, one on either side of the body in the angle between the antennule and the axis of the body (see Text-fig. 3). The centres of the swirls are indefinite but occur usually in Calanus about the middle of the total length of the body, and in Diaptomus further forwards. They rotate in such a way that the water nearest the body moves backwards. They are continuous underneath the body so that, in side view, a marked swirl is obvious ventrally (see Text-fig. 4). Dorsally also there is a swirl, but this is much less marked than ventrally. The copepod thus moves steadily forwards in the middle of a vortex of moving water, which may be termed the “swimming vortex.” A certain amount of water is drawn into the vortex from in front, and a certain amount passes out posteriorly, and this represents the motive force of the copepod when swimming in this fashion. However, the drift towards the body anteriorly is not very marked when compared with such a form as Hemimysis where water streams towards the head from all directions, and is thrown out posteriorly in a powerful swimming stream.

A second smaller vortex occurs inside the swimming vortex, rotating in the opposite direction. In a ventral view it can be seen as two swirls at the sides of the anterior ends of the suction chambers. In side view it cannot be seen in the median plane as it is interrupted by the forwardly projecting swimming trunk limbs, but a little to one side it can be seen to extend forwards between the maxillae to the bases of the anterior swimming limbs and then pass ventrally and backwards. This vortex is the “feeding vortex.” It cannot be traced over the dorsal side of the body.

The inner part of the swimming vortex probably represents the “powerful antero-posterior current” described by Storch and Pfisterer for Diaptomus. It is certainly powerful but it is a vortex and this accounts for the fact that the copepod moves forwards comparatively slowly. According to Storch and Pfisterer, a considerable amount of water is transported in an antero-posterior direction, and in order to take its place the body would have to move forward with corresponding speed. If, however, the water which moves backwards at the level of the tips of the swimming limbs, the level at which the velocity must be greatest, moves at the same high speed which Storch and Pfisterer describe, but is part of a vertical movement, there is comparatively very little actual transport in an antero-posterior direction and hence the body moves slowly forward. The energy of the limbs is expended, not on transporting water backwards, but in maintaining a vortical movement in the water and very little energy is required for this. This may account for the extreme rapidity of the limb movement. They have very little resistance to overcome, simply the viscous drag on the vortex, and hence are able to vibrate at a speed which is very considerable for a Crustacean limb.

The feeding swirl represents the suction through the maxilla described for Diaptomus.

The swimming vortex results from the vibrations of the antennae, mandibular palps, and distal part of the maxillules. The feeding vortex is a necessary resultant of the swimming vortex, but is increased by the activities of the maxillulary exite and maxillipeds. This was demonstrated clearly in a specimen of Calanus which was nearly dead. All its limbs had ceased moving except the antennae and mandibular palps, and the antennules had not flexed backwards as happens when a copepod dies. The swimming vortex was almost as large as normal and there was a very pronounced feeding vortex. This does not agree with Storch and Pfisterer’s account of Diaptomus which regards the maxillule as of vital importance in producing the feeding current.

When Calanus and Diaptomus are swimming slowly forwards the frequency of the head swimming limb movements is remarkably but not absolutely constant. In the other types of movement the limbs move irregularly, and hence their vibrations cannot be analysed stroboscopically. It is the steady forward motion which results in the feeding current and that is the type analysed here.

The maxilla shows no rhythmical movement. For the greater part of the time it remains still, but if the mouth becomes congested with food particles, the maxillae may be flexed ventrally throwing the accumulated food away from the body into the swimming swirl.

The maxillipeds, maxillules, mandibular palps and antennae vibrate regularly, in the case of Diaptomus at the rate of about 1000 times a minute and in the case of Calanus about 600 times a minute. Their movements are synchronous but not in the same phase, as apparently Storch and Pfisterer assumed. They exhibit a marked metachromial rhythm of the type shown in other Crustacea such as Chiro-cephalus or Nebalia (Cannon 1927, 1928), that is, each limb commences its back stroke just before the limb immediately anterior to it. The phase differences are such that the maxilliped commences its back stroke (outward movement) just after the antenna commences its forward stroke, so that these two limbs move almost in opposite phase. The phase difference between mandibular palp and maxillule is very small. The back strokes of antennae, mandibular palps and maxillules are faster than their fore strokes. The tip of the maxilliped exhibits a rotary movement in an obliquely frontal plane (see Text-fig. 5) such that the outward part of the rotation (backward stroke) is faster than the inward part. The movements of these limbs are represented graphically in Text-fig. 6.

The antennae move through by far the greatest arc. The innermost setae of the endopodite, at the end of the back stroke, reach the tips of the maxillules. The range of movement decreases in the more dorso-lateral setae. This results from the fact that, as the endopodite moves backwards the exopodite swings forward. The former moves practically in a straight line sloping posteriorly towards the sagittal plane. The tip of the exopodite rotates in an ellipse passing nearer to the sagittal plane on its forward stroke (Text-fig. 5).

It is difficult to say what is the meaning of the recurved exopodite. It may function in assisting the feeding swirl but it also may serve to diminish the centrifugal drag on the base of the limb. The tissues of a copepod must be relatively heavy compared with water, especially in such forms as Diaptomus and Calanus which reduce their total specific gravity by the production of a drop of light oil. Consequently the mass of the moving limb must be considerable. The position of the exopodite does not reduce the inertia of the limb but it shifts the centre of gravity almost to the axis of rotation, and this must diminish the centrifugal drag on the body.

The mandibular palps and maxillules move backwards and forwards in a parasagittal plane over a comparatively small arc.

The swimming swirl is produced by these three limbs, and, of these, the antennae are the most effective. The feeding swirl results primarily from the swimming swirl. This can be best understood by considering the path of a jet of water when squirted into a volume of still water. If, from a cylindrical jet, a small mass of water is suddenly expelled it does not move forwards as a moving cylinder of fluid but spreads out into the form of a vortex, and this is the more marked the greater the velocity of the moving jet (Text-fig. 7, a). Considering two points, one just inside the cylinder of fluid immediately it has left the nozzle, and another point just outside in the still water, there will be marked discontinuity between the velocities at these two points and discontinuity in velocity in a fluid leads to vorticity. Or again, the viscous drag of the moving cylinder immediately it has left the nozzle, will drag in still water from behind while the viscous resistance at the front end of the cylinder will flatten it out and these two effects together will produce the vortex.

If now, instead of a simple jet, an annular cylindrical jet is considered, the same reasoning applies. The moving water will tend to spread out. It will move outwards from the axis of the jet but, at the same time, it will spread inwards and so produce an inner vortex (Text-fig. 7,b).

This latter type of jet is produced by the steadily swimming copepod. The head swimming limbs move at greatest speed at their tips while their bases, being attached to the body, are stationary. Their setae spread out in fans extending almost half way round the body. The result is that they produce a moving layer of water in the form of half an annular jet (Text-fig. 7, c). This spreads outwards as the swimming swirl but at the same time spreads inwards and produces the feeding swirl.

In the copepod there is an additional effect which increases this vortex production. In the annular jet there is a continuous supply of water being forced through the nozzle. In the copepod this supply comes from the spaces between the swimming limbs. As the antenna moves backwards it obliterates the space between it and the mandibular palp and forces out the water into the swirls. On extending forwards this space is opened out and water must pass in again. It will not pass in from the tip of the limb to any great extent as water in this region is moving rapidly backwards. There is, however, a slight tendency foi water to pass in, for if particles are watched passing over the tips of the swimming limbs they are seen to pass slightly inwards towards the base of the limbs but are immediately thrown out again on the backstroke. The main mass of water will naturally be sucked in from the bases of the limbs where the water is relatively still. That is, a region of low pressure must exist at the bases of the swimming limbs. This will suck in water partly from in front (Text-fig. 5) and partly from behind. The latter suction will serve to increase the feeding swirl.

The action of the maxillulary exite and maxilliped is to force part of the feeding swirl through the comb of filter setae on the maxillae. The two limbs co-operate. The maxilliped sucks water into the filter chamber while the maxillulary exite sucks it out of this chamber through the maxillary setae.

The movement of the maxillipeds has already been described (p. 139). On their outward stroke the setae on the distal joints spread out into a fan, so that a suction is produced in a ventro-lateral direction. The maxillipeds lie just underneath the splits between the tips of the trunk swimming limbs and the maxillae (Text-fig. 2). Hence the suction must extend into the filter chamber and draw in water from behind.

Just after the maxillipeds have finished their outward stroke the maxillules commence to move forwards (Text-fig. 6). The maxillulary exites, at the end of their back stroke lie flat against the outer faces of the maxillae, thus diminishing, and at the same time closing the suction chamber between them and the maxillae. On their forward stroke they simply tend to enlarge this space and so produce in it a region of low pressure. The extent of this suction can be seen from the curvature of the setae as the exite moves forwards (Text-fig. 8). The suction effect of the setae is increased by their armature of setules. These project laterally from the outer faces of the setae so that, on the outward movement of the exite they spread out and fill up the inter-setal gaps, while on the inward movement they collapse and allow the escape of water through the setae (Text-fig. 8). The maxillipeds and maxillules thus work together. The former sucks water into the filter chamber and this is immediately followed by a suction of the maxillule which draws water through the maxillary setae. In the back stroke of the exite the setae spread out and sweep the water backwards into the swimming swirl.

In the backwards and forwards motion of the maxillule the setae on its exite, which project at right angles to the axis of the limb, move through the same angle as the limb itself. The tips of the setae thus move in a dorso-ventral direction. This, combined with their in and out motion resulting from the suction activity of the exite, results in the tips of the setae moving in a flattened ellipse lying close against the ventro-lateral body wall (Text-fig. 5). The tips of the exites thus beat towards the posterior opening of the filter chamber. Thus, while the anterior part of the maxillulary exite is producing suction in the suction and filter chambers, the posterior whip-like ends are actively sweeping particles into the latter.

Small particles sucked into the filter chamber are deposited on the setae of the maxillae. These are heavily armed on their inner faces with laterally projecting setules so that the whole limb forms an efficient filter (Text-fig. 2).

Particles so filtered, if they happen to be deposited near the anterior end of the chamber are scraped off, as Storch and Pfisterer (p. 354) point out, by the endites of the maxillule and passed directly forwards on to the mandibles. In addition, however, there are several long setae which arise on the basal joints of the maxillipeds and project forwards on to the inner faces of the maxillae. These scrape particles off the hinder parts of the filter plates and push it forwards on to the maxillules. The maxilla is thus brushed clean on both its inner and outer faces.