(Text-fig. 6; 7, Figs. 6;8;9; 10.)
Dissection. The dissection to show the alimentary canal of Evechinus is made difficult by the large size of the gonads, which tend to obscure the other contents of the body cavity, and also by the extreme thinness of the gut wall Strong mesenteric ligaments attach the intestine to the gonads very firmly and must be previously cut if the intestine is lifted or moved in any way. If they are not cut, the intestine wall gives way and its mass of contents spills out to obscure the dissection.
The great convolution of the alimentary canal, particularly the intestine, makes its course rather difficult to follow. For general laboratory dissection, where only one animal is available with which to demonstrate all systems, it is best to dissect from the adoral surface. By cutting the test around the peristome with old scissors or forceps, the lantern is completely freed and gently tipped so that the stone canal and axial organ may be located and freed. The mesentery holding the oesophagus in place must also be cut. The whole lantern can then be lifted out of the body cavity and placed to one side, while still retaining its connection with the oesophagus (Text-fig. 6). To demonstrate the alimentary canal alone, however, I have found the best method to be that of removing the aboral half of the test piece by piece with strong forceps, leaving until last that part immediately surrounding the apical system. The rectum, stone canal and gonoducts are then carefully severed immediately below the apex. The aboral halves of the gonads must be then removed to reveal the large intestine coiled around the test in undulating dorso-ventral folds. In the five radii the narrower dorso-ventral loops of the stomach may be observed. The oesophagus and rectum may be seen situated in radius III thus giving a reference point for correct orientation (Text-fig. 8). To observe the whole course of the stomach and its attendant siphon, the intestine and the rest of the gonads must be removed (Text-fig. 9). Spilling of the contents of the intestine is unavoidable at this stage but they may soon be removed by gentle washing. Aristotle's lantern must be opened to observe the pharynx. This is best done by removing, with forceps or old scissors, a whole alveolus, and then one jaw from either side of it, at the same time clearing away the accompanying muscles.
The pharynx (PH) is that part of the digestive tube which is enclosed within the lantern (Text-Fig. 7, Fig. 6). It has a diameter of the order of 7 mm and a length corresponding to the height of the lantern—i.e., about 20 mm. Five radial ridges (RR) of connective tissue pass down its sides giving it a pentagonal shape.
About the mouth they become expanded to form five lobes, alternating with the interradial teeth. On both sides of each ridge are a pair of ligaments (LL) the adoral ends of which are fixed to the internal parts of the jaws. Aborally they are attached to the rotulae. Five other shorter pairs (SL) come from the inferior part of the pharynx to pass on to the jaws quite near the teeth.
The pharynx leads into the narrow, much convoluted oesophagus (OE) (diameter ca. 5 mm), which continues upwards along the vertical axis of the animal, together with the axial organ (AO) and stone canal (SC), almost reaching the periproctal region. From there it bends on itself and redescends to the level of the lantern, to pass out horizontally in radius III between the rectum and the first loop of the intestine to meet the wider, thin-walled stomach (ST). Sheets of mesentery unite the oesophagus to the axial organ and to the diverticulum of the stomach. The mesentery is also attached to the test in the apical region, thus suspending the oesophagus with the axial organ and attendant stone canal in the central axis of the animal. In some specimens the oesophagus has a striated appearance due to the presence of rows of pigment passing along it.
The stomach (ST) in fresh specimens is a yellowish-orange colour, and is extensively sacculated. It has been variously described as the “first or inferior spiral” (Lang, 1896; Bonnet, 1925), “direct canal” (Delage and Hérouard, 1903;
Text-fig. 8.—Alimentary System. Aboral View with Aboral Gonad Removed. Abbreviations: AO, axial organ: AP, ampulla; D, diverticulum; FLI, first loop of intestine; FLS, first loop of stomach; G, gonad; INT, intestine; L, lantein: ML, mesenteric ligaments; OE, oesophagus; R, rectum; RAC, radial ambulacral canal; ST, stomach.
Bonnet, 1925), or “first curve of the intestine” (Cuénot, 1948). It continues horizontally in an anticlockwise direction (viewing the animal from the aboral pole) forming a dorso-ventral inflexion in each radius, to lead into the intestine (INT), without any sharp boundary, in interradius 2. This is contrary to the condition in Echinus, as described by Delage and Hérouard (1903), where the slight inflexions of the stomach are interradial. The condition in Evechinus is more similar to that described by Bonnet (1925) for Spharechinus and Paracentrotus, where the internal border of the stomach has a pentagonal aspect while the external border forms a five-rayed star the arms of which ascend in the radial zones along the walls of the test. The stomach of Heliocidaris erythrogramma also has this aspect and is of comparable diameter with that of Evechinus. In the interradial zones the gut is suspended in such a way that the external border falls to the interior of the internal border, held in place by strands of mesentery (ML) securing it to the perignathic girdle. The diameter of the stomach is of the order of 9 mm.
At the junction of the stomach and the oesophagus is a sac-like dilatation, the diverticulum (D), which is said (Cuénot, 1948) to contain a feebly acidic liquid with a diastasic action on albumen and starch. He considers it the principal seat of absorption of the products of digestion.
The end of the oesophagus and the beginning of the intestine are connected by a narrow, cilia-lined tube and with a diameter of between 1 and 2 mm. This is the siphon (SI), or accessory intestine. It lies on the inner side of the stomach and accompanies this organ through all its turns, to finally open into it once more at the base of the inflexion in radius II. It is attached to the stomach by a narrow strand of mesentery, while a further strand links the internal marginal canal (IMC) of the haemal system to its inner side. There is no sign of an accessory siphonal groove such as is found in Arbacia (Cuénot, 1948). Its function has been thought in the past to be the subservence of respiration, which it effects by keeping a stream of fresh water flowing through the gut, thus functioning in much the same way as the accessory intestine of certain worms. (Lang, 1896; Chadwick, 1900; MacBride, 1906). However, Bonnet (1925) has suggested that the siphon serves as a diversion channel for water taken in with the food, passing the water directly to the intestine in which the excrements accumulate, and thus permitting the concentration of diastases in the stomach. This view is supported by Cuénot (1948). It may be that the siphon fulfils both these functions. The internal epithelium of the siphon is well developed and thrown into numerous folds, so that, as Bonnet (1925), suggests “… on ne peut s'empecher de penser que cet organ ne joue pas seulement le rôle d'un conduit servant à laisser passer l'eau extérieure dans la seconde courbure de l'intestine, mais qu'il pourrait bien remplir aussi quelque autre fonction”. He gives, however, no suggestions as to what that function might be.
The intestine (INT) is of larger diameter than the stomach (about 14 mm), but like the stomach, has very thin walls, which in fresh specimens appeal a pinkish-brown colour, in some places quite transparent. On the border between interradius 2 and radius III it turns upwards to return in the opposite direction to that of the stomach (i. e., clockwise, viewing the animal from the aboral pole). This inflexion, and the downward inflexion of the intestine in interradius 2, are held together by a continuous sheet of darkly pigmented mesentery which is continued along the whole internal border of the intestine. The intestine is even more convoluted than the stomach, being reflected down towards the lantern in each interradius, and upwards, overlying the corresponding loop of the stomach, in each radius (Text-fig. 8). This is in contrast to the condition in Echinus where, as described by MacBride (1906), the festoons of the intestine alternate with those of the stomach. In Heliocidaris erythrogramma the intestine follows the same course as in Evechinus but is of rather less diameter. Various names have also been applied to the intestine. Lang (1896) calls it the “superior spiral”, Delage and Hérouard
Text-fig. 9.—Alimentary System. Aboral View of Stomach with Intestine and Gonads Removed. Abbreviations: AP, ampulla; AU, auricula; D, diverticulum; FLI, first loop of intestine; FLS, first loop of stomach; IA, interambulacrum; IMC, internal marginal canal; L, lantern; ML, mesenteric ligament; OE, oesophagus; RAC, radial ambulacral canal; RLS, radial loop of stomach; SI, siphon.
(1903) the “reflected canal”, Bonnet (1925) the “recurrent coil” and “dorsal or second flexure,” and Cuénot (1948) the “second curve of the intestine”.
Arriving at the lateral border of radius III with interradius 3, the intestine is continued without any sharp boundary as the narrower rectum (R). This passes up between the previously mentioned radius and interradius, with gradually decreasing diameter, to the anus, which opens to the exterior from a variable position, usually a little excentric, within the periproct.
A continuous sheet of mesentery runs along the entire internal border of the gut, becoming especially well developed and darkly pigmented along the intestine. On the external border the mesentery is represented by strong mesenteric ligaments (ML) which firmly attach the stomach to the perignathic girdle, the intestine to the overlying gonads, and both coils of the gut to the sides of the test.
In all specimens examined the stomach has contained only a very small quantity of food materials in the process of digestion, while the intestine has always been more or less crammed with excrement in the form of small pellets. Many of the pellets appeared to be surrounded by a case of hyaline material, probably mucin. Lumps of this material were found at the beginning of the intestine in some specimens. It is probable that the internal epithelium cells in this region are specially concerned with the secretion of this material.
The first turn of the alimentary canal is thought (Cuénot, 1948) to correspond to the larval intestine, while the second turn is the result of progressive elongation of the larval rectum.
Food of Evechinus chloroticus
The great volume of the gut contents and the efficiency of the teeth in tearing and grinding food into small pieces, or fine powder in the case of hard objects, makes identification of such material difficult. However, animals have frequently been found holding pieces of the brown seaweed, Carpophyllum maschalocarpum, between their teeth, and all alimentary canals examined contained a large volume of such shredded brown alga, frequently together with green and red algae. The gut also contains much calcareous material, finely powdered and held together in the form of small balls. This would come from the shells of encrusting animals living on the seaweed and possibly also from animals such as tuberculous polychaetes encrusted on stones and rocks. In general it may be said that Evechinus chloroticus feeds on littoral seaweeds and their associated epifauna. One animal was found with a partially eaten leaf in its mouth of Coprosma repens, the common coastal “taupata”, the leaves of which are frequently found floating in the sea near the coast. This is interesting when taken together with Fell's (1952) account of ophiuroids, Pectinura maculata, in Dusky Sound feeding on pollen dropping from beeches (Nothofagus) overhanging the water. The only other record of such a nature is one he cites of a deep sea echinoid in the East Indies which feeds on the leaves of dicotyledonous trees washed out to sea by rivers. The fact that the exclusively marine echinoderms are able to feed on land angiosperms seems rather remarkable. In the case of Evechinus, however, such feeding is probably accidental, for in general the animal appears to exhibit little power of selection, eating almost anything edible with which it comes in contact. In the gut of one animal I found several small pieces of wood and in another a short length of string.
Histology of the alimentary canal (Text-fig. 10, figs. 1–5)
The digestive tube of Evechinus chloroticus consists of the four fundamental layers typical of all echinoids; the external or coelomic epithelium, a muscle layer, a layer of connective tissue, and an internal epithelium.
The pharynx (Text-fig. 10, Fig. 1) is covered externally by a low ciliated epithelium (LEP) which is not continuous with the coelomic epithelium covering the rest of the gut, but forms the internal lining of the lantern coelom. It consists of small cells with conspicuous nuclei. Internal to this is a thin muscle layer of circular fibres (CM). This thin layer is in contrast to the description of Echinus by Bather (1900), where the pharynx is described as being a muscular organ. The connective tissue of the pharynx is very well developed. It appears to form two layers, one within the circular muscle and one outside it. The external layer is confined to the radii, where it forms five pronounced radial ridges (RR). It is to these ridges that the ligament bands uniting the pharynx to the jaws are attached. The connective tissue lying inside the muscle layer is present only in the interradii where it takes the form of five shallow triangles (ICT), the apices of which are directed internally. Bounding the lumen of the pharynx is a high, extensively folded, pseudo-stratified epithelium (IEP) containing numerous gland cells secreting mucin (MU). These are especially abundant in the five radii, in each of which the epithelium forms a deep fold. A thin cuticle (CU) invests the internal edge. Also observed in transverse sections of the pharynx are the five radial vessels (RHV) of the haemal system, running down the outside of each radial ridge. The cross section of the pharynx of Evechinus has a very different form from that of Echinus as figured by Chadwick (1900), where the outline is distinctly five-rayed and where there appear to be no radial ridges.
The external epithelium (CEP) investing the oesophagu (Text-fig. 10, Figs. 2 and 3) is part of the coelomic epithelium covering the remainder of the alimentary canal which is also continued on the internal face of the test and is reflected on all the organs contained within the general body cavity. The cells appear similar
Text-fig. 10.—Histology of the Alimentary Canal. Fig. 1—T.S. pharynx. Fig. 2—T.S. oesophagus. Fig. 3—Portion of wall of oesophagus enlarged. Fig. 4—T.S. stomach. wall. Fig. 5—T.S. siphon. (All measurements expressed in millimetres. Figs. 1–2 drawn to the same scale.) Abbreviations: CEP, coclomic epithelium; CI, connective tissue: CM, circular muscle fibres; CU, cuticle; EMC, external marginal canal; ICT, interradial connective tissue; IEP, internal epithelium; IMC, internal marginal canal; LA, lacuna; LEP, epithelium of lantern coelom; LM, longitudinal muscle fibres; ME, mesentery; MM, muscle layer; MU, mucin; RHV, radial haemal canal; RR, radial ridge of connective tissue; SI, siphon; V, vacuole.
to those constituting the external epithelium of the pharynx. The muscle layer (MM) of the oesophagus is also relatively narrow but rather better developed than in the pharynx. There is an outer layer of circular fibres (CM), with longitudinal fibres (LM) also present, between the circular muscle and the connective tissue. In Echinus an opposite arrangement of the muscle layers of the oesophagus is described by Delage and Hérouard (1903). The connective tissue (CT) is not as thick in the oesophagus as it is in the pharynx and varies in width around the diameter of the oesophagus. It has an open mesh-like structure, forming lacunae (LA), in which the liquids of the haemal system circulate. The folded internal epithelium (IEP) is also of the pseudo-stratified type, as is the whole internal surface of the gut. It also contains numerous mucin-secreting (MU) cells, but these are not localized in any way like those of the pharynx. A strong cuticle (CU) is present on its inner border. The lacunal vessels accompanying the oesophagus (IMC, EMC) and the mesentery (ME) uniting it to the diverticulum and the apical pole are also revealed in cross section.
The muscle layer of the stomach (Text-fig. 10, Fig. 4) is chiefly composed of longitudinal fibres (LM) although a few circular fibres are present. The connective tissue layer is of fairly uniform width with many large lacunal spaces (LA). The internal epithelium is high and extensively folded, with very short cilia present on its inner border. It is extremely vacuolated (V), but no stainable material could be detected in the vacuoles. This vacuolation, and the great development of the lacunae, are in accord with the function of the stomach, which is the main digesting and absorbing region of the alimentary canal.
The histology of the diverticulum is very similar to that of the stomach, the main difference being in the cells of the internal epithelium, which in the diverticulum are crammed with a pink-staining granular material. There is no sign of any special glandular formation in the diverticulum, which, as Bannet points out, is a special glandular formation in the diverticulum, which, as Bonnet points out, is a junction of the oesophagus with the diverticulum a sharp transition could be seen from the dark-stained mucous-containing cells of the oesophagus to those of the diverticulum where practically no mucous is secreted.
The muscle fibres surrounding the siphon (Text-fig. 10, Fig. 5) are mainly circular (CM), and some of them are continued up into the internal mesentery The connective tissue (CT) encloses large lacunae, and varies in width following the folds of the internal epithelium (IEP). This is also of the pseudo-stratified type but is not so vacuolated as that of the stomach, and has a conspicuous granular border. Very short cilia are present on the cells bounding the lumen.
Cross sections of the stomach show the internal and external marginal canals excavated in connective tissue. The internal marginal canal (Text-fig. 10, Fig. 5, IMC) is also surrounded by circular muscle fibres and so is evidently contractile like the internal marginal canal of spatangids.
The wall of the intestine is of much the same structure as the stomach, except that the connective tissue layer is thinner and contains fewer lacunae, while the internal epithelium is lower, less folded, and does not contain so many vacuoles.
The rectum is rather more muscular than the intestine, with circular fibres quite well developed. Longitudinal muscle fibres are also present within the connective tissue of the internal mesentery. The connective tissue layer is thin, containing a few lacunae, while the internal epithelium is higher than in the intestine and quite extensively folded .The cells are rather more vacuolated than one would expect to find in a presumably inactive organ such as the rectum.
Examination of the internal epithelium of the stomach and intestine is made especially difficult because of the great delicacy of this layer and the readiness with which it comes away from the underlying connective tissue. In collections of gut
contents much of the internal epithelium of the gut wall is found mixed with the food materials.
In all references which I have consulted the internal epithelium of the entire alimentary canal of echinoids is described as being ciliated. I have experienced great difficulty in locating any cilia, except on the internal epithelium of the siphon and the stomach. Elsewhere they could not be identified with certainty, even when using an oil immersion objective. I would hesitate to say, therefore, that the entire interior surface of the alimentary canal is ciliated in Evechinus.