Observations on the Mechanism of Feeding in the Suctorian Podophrya

Most Suctoria catch their prey by means of tentacles, to the tips of which the prey adheres. The contents of the prey then pass up the tentacles into the body of the captor. It is the purpose of this paper to present additional data bearing on this process of feeding.

The tentacles of a suctorian are described as consisting of two concentric tubes (Collin, 1912), the walls of which unite at the distal end. The wall of the outer tube appears to originate in and to be continuous with some component of the body surface of the suctorian (Noble, 1932). The inner tube projects inwards from the tentacle for a short distance into the cytoplasm, and ends abruptly. During feeding the contents of the prey pass through the inner tube. These relations are illustrated in Text-fig. 1, reproduced from Noble’s paper (Noble, 1932). Possibly the space between the two tubes, which is continuous with the ectoplasm of the suctorian, is occupied by gelated protoplasm having considerable structural rigidity. The elongated shape could not be maintained without some rigidity, and the disintegration of suctorian tentacles under the influence of high hydrostatic pressure (Kitching & Pease, 1939) suggests the collapse of a gel structure. According to Kormos (1938) the tentacles emerge through holes in the cuticle of the suctorian.

The tentacles terminate, at their distal ends, either in a knob or in an open funnel. Capture of prey is attributed by some authors to the development of a sudden suction. However, according to Konnos (1938) tentacles with open funnels are incapable of capturing five prey; he attributes capture to a stickiness of the knob.

There is evidence to suggest that the body of the prey may be subject to some digestive influence while the suctorian is feeding upon it. Iziumov (1947) coloured the ciliate Glaucoma with congo red and then offered it to the suctorian Tokophrya infusionum. A change in colour, indicating increased acidity, was observed in the prey in the region where the tentacles of the suctorian were attached. He also observed the dissolution of grains of paramylum in a captured Chilomonas.

The mechanism of the suction of Suctoria has provoked much speculation. Early work is summarized in Collin’s fine monograph (Collin, 1912), which contains full references. Collin rejected the idea that material flows along the tentacles of the suctorian because of the hydrostatic pressure within the body of the prey; but this explanation has more recently been reaffirmed by Pestel (1931). Collin (1912) considered that the pressure required would be too great, and believed that the liquid contents of the prey were driven along by peristalsis of the inner tube of the tentacle. Other authors refer to suction but do not explain it. Kahl (1931) rejected suction on the grounds that it would involve an expansion of the surface, which he was unable to believe in.

Podophrya sp. was used in this work. I have not seen any cysts, but this species resembles P. colliniRoot (1915) in appearance and type of prey captured. It was originally found in a pond in the University grounds, and was maintained in culture. Podophrya has a pear-shaped or spheroidal body, which is attached to the substrate by a stalk. The tentacles are bom on all parts of the body surface, and are swollen at the tips (see Pl. 10). The body surface is normally smooth in outline and free from dents or wrinkles. However, some specimens cultured in 10 % sea water were wrinkled.

Podophrya sp. was cultured in closed glass dishes and grown on silk threads as already described (Kitching, 1951). The culture medium was Bristol tap water, or for certain experiments 5 or 10 % sea water, to which was added a small quantity of a culture containing Paramecium caudatum and Colpidium as food. In the case of cultures of Podophrya in dilute sea water, the ciliates were also grown in sea water of the same dilution.

Observations were carried out on cultures 5–11 days old. Silk threads carrying the Podophrya were mounted on a slide in a drop of fluid from the culture. Except when micromanipulation was required they were covered with a cover-glass; the latter rested on two small pieces of well-washed filter paper which facilitated irrigation. For all observations and experiments the material was irrigated frequently from a pipette with medium from the culture dish to prevent any possibility of a change in the concentration of solutes.

Photographs were taken with a Leica microscope camera. Measurements were made with a screw micrometer eyepiece. A de Fonbrune micromanipulator was used for some experiments. The body volume and surface area of the Podophrya were calculated as those of a prolate spheroid from measurements of the major and minor axes.

The tentacles of the Podophrya normally remained motionless and extended. When a suitable ciliate collided with the Podophrya, the tentacles which the ciliate happened to touch at the tip adhered to it. Adhesion of tentacles only occurred with certain ciliates—for instance, Paramecium caudatum, P. aurelia and Colpidium sp., but not Spirostomum, Euplotes or Vorticella. When the prey was caught by one or more tentacles its swimming movements sometimes caused it to rotate and twist the adherent tentacles into a rope-like spiral, and then it often escaped. In other cases its movements merely brought it into contact with the tips of other tentacles, which also adhered. There were no bending movements of tentacles towards the prey.

The process of feeding is illustrated in Pls. 10 and 11. After a few minutes many or all of the cilia of the prey stopped beating. At this time also the body surface of the Podophrya in some cases became wrinkled (Pl. 11, figs. B2–5 and C2), although this did not always happen. Some or all of the adherent tentacles then became shorter and stouter, and material from within the prey was seen to flow along these into the Podophrya. Granules derived from the prey were often seen to enter the Podophrya and to traverse the outer part of the body in sequence as though still in a confined channel. The rate of output of the contractile vacuole of the Podophrya increased considerably. The body of the Podophrya increased in volume, and during this process any dents or wrinkles which had previously developed in the surface became smoothed out. The prey usually shrank in the region where the tentacles of the Podophrya were attached to it. This is illustrated in Pl. 10, in which the anterior end of the Colpidium is seen to diminish progressively. The contractile vacuole, visible in figs. A2–A5, provides a fixed point in the Colpidium which facilitates a comparison of these photographs with one another. In some cases, particularly in Paramecium, a local excavation was formed in the surface in the region where the Podophrya was attached (Pl. 11, fig. D).

Paramecium is very much larger than Podophrya, and superficially it often appeared little affected when it was finally released by the Podophrya. Its contractile vacuoles continued to operate throughout the process of feeding, and in several cases it was seen to swim away some minutes after its release. Colpidium, which is much smaller than Paramecium, was normally cytolysed. At first its contractile vacuole continued to beat regularly, and damage appeared to be purely local. Later the Colpidium, much depleted in size, rounded up. The granules within collected to that side of the spherical remnant to which the tentacles of the Podophrya were attached (Pl. 10, figs. A6–8). The rest of the Colpidium became much vacuolated. Finally, the contractile vacuole stopped, and there was no sign of life. The passage of material up the tentacles of the Podophrya ceased, and the dead Colpidium vfzs released.

Observations were made of the time after capture at which the cilia in different parts of Paramecium stopped. P. caudatum and P. aurelia were used. Usually the Paramecium was caught by its anterior end, and in this case the cilia of the anterior end stopped first. The region of stoppage then extended along the Paramecium until it reached the posterior end. In a few cases observations were obtained of Paramecium caught by the posterior end. The cilia of the posterior end stopped first, and the area of stoppage extended progressively towards the anterior end. It should be mentioned that, whatever part of the Paramecium was held by the Podophrya, the tuft of cilia at the tip of the posterior end always appeared to be inactive, and the gullet cilia always continued to beat for much longer than any of the others. Examples of these results are illustrated in Text-fig. 2.

Wrinkling of the pellicle of Podophrya was often observed a few minutes after the Podophrya had captured a Paramecium caudatum, P. aurelia or Colpidium sp. The wrinkles occurred in any part of the body surface, and often took the form of a deep cup-shaped depression (Pl. 11, fig. C2). Wrinkling occurred equally strongly in experiments in which the prospective prey had been transferred by centrifuging to some of the culture medium in which the Podophrya had been living; this was done to eliminate any possibility that the medium introduced with the prey might be responsible for wrinkling, as, for instance, by an osmotic effect. Wrinkling was never seen to occur in any unfed Podophrya adjacent to the one under observation.

Wrinkling of the body surface might be ascribed either to a loss of volume of the body or to an expansion of the body surface or to both. The disappearance of the wrinkles is presumably due to the uptake of material from the prey. It seemed therefore that perhaps on those occasions when there is no wrinkling the uptake of food keeps pace with the process—whatever it may be—by which wrinkling is produced. Accordingly, a comparison was made between the occurrence and persistence of wrinkles in Podophrya fed on normal and on partially dehydrated prey. The experiments of the three kinds to be described were suitably interspersed in time.

(a) Podophrya in tap-water culture were fed on Colpidium cultured in tap water. Out of twenty-three experiments strong wrinkling was observed in ten cases, a slight departure from the normal smoothness of outline in seven, and no change in six. Wrinkling, when it occurred, began within 2 or 3 min. and normally the body surface was smooth again in 6–12 min. after the capture of the prey. In two exceptional cases wrinkling persisted until 17 and 40 min. after the capture.

(b) Podophrya cultured in 10 % sea water were fed on Colpidium which had just been transferred by centrifuging to 10 % sea water. The prey was much shrunk in these experiments. Out of eleven experiments strong wrinkling of the surface of the Podophrya occurred in all cases, beginning in from 1 to 7 min. from the time of capture. The wrinkles disappeared after the following times: 38 min., 97 min.,⁠. In the remaining four experiments the observations were terminated with wrinkles still remaining after hr. In these various experiments no food was seen passing up the tentacles for about the first hour, but later the prey filled out and food particles were seen streaming into the Podophrya.

(c) Podophrya cultured in 10 % sea water were fed on Colpidium cultured in or adapted to 10 % sea water. Out of twelve cases wrinkling occurred in six, and the body of the Podophrya remained smooth in six. Wrinkling began in from 1 to 4 min., and had disappeared in from 6 to 22 min. after capture of the prey.

Clearly no difference was found between Podophrya cultured in tap water when fed on Colpidium cultured in tap water and Podophrya cultured in 10 % sea water when fed on Colpidium cultured in 10 % sea water. However, when Podophrya cultured in 10 % sea water was fed on Colpidium only just transferred to 10 % sea water the wrinkling was universal and much prolonged, and the uptake of food was greatly postponed. This conclusion is supported by observations of Podophrya feeding on Paramecium.

The use of partially dehydrated prey provided an opportunity for studying the phenomenon of wrinkling without the complications due to the subsequent uptake of food. It was already known that an unfed Podophrya is only capable of a quite limited swelling by osmosis, unless it happens already to be wrinkled, although it can be caused to shrink greatly by a hypertonic solution (Kitching, 1951). This suggested that an expansion of the body surface of pellicle might be important in permitting the great swelling which occurs during feeding. Experiments were therefore carried out to determine the change in distensibility of the body which takes place during the wrinkling process. A comparison was made between the capacity for osmotic swelling on transfer from 10 % sea water to tap water of unfed Podophrya and of Podophrya which had been fed on partially dehydrated prey (as described above) but from which the prey had been removed with a microneedle when wrinkling had developed. Because some Podophrya cultured in 10 % sea water were found in any case to be wrinkled, unwrinkled Podophrya were carefully selected. The results are shown in Table 1. The increase in surface area was much greater in those Podophrya in which wrinkling had been induced by the capture of prey. Agitation of an unfed Podophrya with a microneedle to an extent consider ably greater than that normally caused by prey did not produce any wrinkling or increase in surface area.

Finally, the process of wrinkling was studied by a comparison of photographs taken at intervals of a few minutes or less during the early stages of feeding. This was done in the hope of determining whether any diminution of body volume is associated with wrinkling, and in order to compare the size of the body when the wrinkles were just disappearing with the original size; this comparison would indicate any increase in surface area due to wrinkling. Examples of the photographs are shown in Pl. 11, and tracings obtained by projection from negatives are given in Text-fig. 3.

The photographs shown in Pl. 11, figs. B1–5 and C1–3, are of normal Podophrya cultured in tap water and fed on normal prey. In series B two Podophrya are attached to one Colpidium. One of these shows strong wrinkling, which in this case persisted until the prey was practically consumed. The other Podophrya did not wrinkle, but appears to have obtained most of the food. It is clear from the photographs that the wrinkling involved an increase in the area of the body surface. It should be mentioned that wrinkling was in no way confined to cases in which two Podophrya were attached to the same prey. It was frequently seen when the prey was not shared. This is illustrated in series C. Here the wrinkling merely took the form of a small cup-shaped depression, which soon filled up. In view of the increase in the surface during wrinkling it is not possible to decide whether or not a change of volume also occurred. The small volume of a depression such as that shown in C2 or seen in early stages of wrinkling in other cases would be compensated by an insignificantly small extension of the overall outline of the body. On the other hand, in all cases in which wrinkling became strongly marked there was also a considerable extension of the outlined area. This is illustrated in Text-fig. 3, in which the outline is given for Podophrya (a) immediately after capture of the prey, (b) at the time of greatest wrinkling, (c) when the wrinkles were on the point of disappearance. The third condition was obtained either in the normal course of feeding, or (for some Podophrya in 5 % sea water) by osmotic swelling. In either case the outlines show that at the moment of disappearance of the wrinkles the body was much larger than it had been originally. They confirm that the surface of the body expands during wrinkling.

Observations were made of the rate of increase in body volume of Podophrya during feeding. The results are shown in Text-fig. 4. Points are plotted only for those measurements taken when the body surface was smooth in outline. The number of tentacles attached to the prey is also given in each case, although it must be realized that the uptake of food does not necessarily occur through all the tentacles attached.

The observations of Iziumov (1947), already outlined, strongly suggest that some digestive action takes place within the prey itself. The progressive stoppage of cilia from the region of attachment of the Podophrya outwards, and the local destruction of the prey in this region, fit in with this hypothesis, although other explanations are possible. However, this digestive action must be very localized. For instance, it does not normally stop the contractile vacuole of the prey until late in the feeding process.

External digestion implies that digestive material or juice, however small in quantity, must pass from the Podophrya into the prey. There is as yet no direct evidence for this. Although it might be tempting to ascribe the wrinkling of the Podophrya, which often follows soon after the capture of prey, to an injection of digestive juice into the prey, the evidence presented does not warrant any such supposition. I cannot either confirm or deny this possibility. Actually the quantity of material might be exceedingly small; sufficient might be present at the tips of the tentacles.

The wrinkling of the body surface of Podophrya which often occurs within a few minutes of capture of prey is due to an expansion or growth of the body surface. At the least this expansion enables the Podophrya to accommodate a considerable volume of food. The expansion no doubt occurs even when no wrinkles are seen, wrinkling being prevented by the simultaneous uptake of food.

Does expansion of the body surface merely permit the uptake of food by the action of some other force, or does it represent a mechanism of active suction? The difference of pressure necessary to drive liquid food material along the tentacles of the Podophrya can be estimated very roughly, on certain not unreasonable assumptions, by the use of Poiseuille’s formula. The rate of swelling of the Podophrya cannot be regarded as an accurate measure of the rate of uptake of food, since it is possible (Kitching, 1938, p. 414) that water derived from the food is removed by the extra activity of the contractile vacuole which is associated with feeding.

Rudzinska & Chambers (1951) have estimated that in the suctorian Tokophrya infusionum this increased activity accounts for a very large proportion of the liquid ingested. In Podophrya (Kitching, unpublished data) the extra activity amounts usually to 3–6μ³/sec., or, say, 20,000μ³/hr. The rate of swelling of the body may also be estimated as not more than 20,000μ³/hr. The viscosity of the material flowing along the tentacles is not known and is difficult to estimate. If we grant the claim of Fetter (1926) that the viscosity of the endoplasm of Paramecium is about 8000 times that of water, it is necessary to assume a digestion or structural breakdown before this material could pass along the tentacles. It must be remembered that with a material as complex as protoplasm the ‘viscosity’ is likely to depend on the method and conditions of measurement. On the assumption that the viscosity of this material under the conditions in question is twice that of water, that the length of the tentacles is 25 μ, that the internal diameter of the inner tube is between and 1 μ, and that three tentacles are functional, a difference of pressure between about 1 and 0·1 cm. water would be required. This estimate is exceedingly rough, and would be seriously affected by any error in the estimate of the internal diameter of the inner tube of the tentacles, which is in any case only a guess. The hydrostatic pressure within the ciliate Spirostomum ambiguum has been estimated by Picken (1936) as 3–7 cm. of water, although this value must also be regarded as very rough. It seems very possible, provided that any structural viscosity of the protoplasm consumed is destroyed, that the hydrostatic pressure of the prey might be sufficient to account for the passage of material along the tentacles of the Podophrya. It is assumed that there is little if any positive pressure within the latter. However, the rate of uptake of food does not diminish during the later stages of feeding, so that it would be necessary to assume that the tone of the body surface of the prey was maintained. A more serious objection is the observation, illustrated in Collin’s monograph (Collin, 1912), that Choanophrya infundibulifera can draw in particles of food from a distance. Only suction could account for this. If suction is admitted in one case, it is difficult to reject it in other cases, for which it would clearly provide the most reHable mechanism of feeding. However, the evidence presented in this paper does not provide any information as to whether a negative pressure is in fact achieved in Podophrya. Suction might well be effected by an expansion of the body surface, so long as there is some resistance to a collapse of the body wall inwards. Wrinkling of the surface would then represent a failure of that resistance to prevent local inward collapse, due perhaps to delay in liquefaction of the protoplasm of the prey at the point of attachment of the tentacles. The necessary resistance to inward collapse might be provided by a gelated layer underneath the plasma membrane of the Podophrya. Another interesting problem is set by the expansion of the cuticle which must also take place. Growth of the body surface presumably also occurs during the process of internal budding which occurs in this species.

I am indebted to Prof. J. E. Harris for valuable suggestions and criticisms, and to Mr E. Livingstone for maintaining a steady supply of excellent cultures.