J. Zool., Lond. (1976) 178, 77-89

Patterns of ciliary currents in Atlantic reef corals and their functional significance

J. B. LEWIS A N D W. S. PRICE Bellairs Research Institute of McGiN University, St. James, Barbados, W. I. and the

Marine Sciences Centre, McGiN University, Montreal, Canada

(Accepted 10 June 2975)

(With 5 figures in the text)

Patterns of ciliary currents of 35 species of Atlantic reef corals are described and compared with currents of Pacific corals. Observations were made during the day and at night, during feeding and without food. There is a basic pattern of ciliary currents common to both Atlantic and Pacific species. In all but the family Agaricidae currents flow off the oral disk and up or out between the tentacles. In the centre of the disk region currents flow towards the mouth or the peristome. On the polyp stalk or column there was considerable variation between species in both Atlantic and Pacific forms. In some species currents flow downwards toward the coenosarc while in others, current pass up the stalk towards the tentacles.

In the Atlantic Agaricidae there may be an inward flow towards the mouth, an outward flow or a unidirectional flow across the corallum. The patterns of flow depend upon the state of contraction of the polyps or the shape and proximity of adjacent polyps.

No ciliary current reversal was observed in Atlantic species. Ciliary currents are functional as a cleansing mechanism and facilitated the ability of mucus nets and strands to gather particles.

Contents

Introduction . . . . . . . . . . . . Materials and methods . . . . . . . . . . Observations . . . . . . . . . . . .

Family Poritidae . . . . . . . . . . Family Pocilloporidae . . . . . . .. Family Caryophyllidae . . . . . . . . Families Faviidae and Meandrinidae . . . . Families Siderastreidae and Astrocoenidae . . Family Agaricidae . . . . . . . . . . Family Mussidae . . . . . . .. . . Family Acroporidae . . . . . . . . ..

Discussion . . . . . . . . . . . . .. References . . . . . . . . . . . . ..

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Introduction In an earlier account of feeding mechanisms (Lewis & Price, 1975) the view was

developed that Atlantic reef corals can act as suspension feeders by means of a mucus net, in addition to capturing zooplankton with their tentacles. Nevertheless, ciliary currents were regarded by previous authors (Vaughan, 1912; Yonge, 1930; Abe, 1938) as being important for food capture, especially in species with reduced tentacles. Ciliary currents

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on the oral disk of corals are generally considered to function primarily as cleansing mechanisms (Yonge, 1930) and in most of the species examined the currents flow away from the mouth and off the disk. However, in a few species, under certain conditions, the direction of the flow may be reversed and the currents are thought to cause transport of particles on the surface towards the mouth.

The purpose of this paper is to re-examine the role of ciliary currents, especially in suspension feeding strategies, and to compare the patterns of ciliary currents on polyps of Atlantic reef corals with those of Pacific corals previously described by Yonge (1930).

Materials and methods The details of the collection of living corals and the methods of examination have been reported

previously (Lewis & Price, 1975). The investigation was carried out at the Bellairs Research Institute of McGill University in Barbados, West Indies.

In order to observe ciliary currents in the laboratory a stained fish homogenate and colloidal graphite were used as tracers. The fish homogenate was prepared by grinding up a little fresh fish in sea water, centrifuging, filtering and finally mixing with a little finely ground Alcian Blue. A graphite suspension was prepared by vigorously shaking a small amount of colloidal graphite (Aquadag) in sea water. It was necessary to stir the graphite from time to time to keep the particles in suspension.

Each of the 35 species of corals listed by Lewis & Price (1975) was examined for ciliary currents in the laboratory. Colonies were examined during the day and at night, during feeding and without food.

0 bservations Family Poritidae

Regular patterns of ciliary currents were observed in all the four species of Politidae examined, Porites porites, P . astreoides, P . divaricata and P . furcata. In the laboratory, ciliary currents on the oral disks of expanded polyps were directed away from the mouth and swept particles of stained fish homogenate or colloidal graphite off the oral disk and out between the tentacles (Fig. l(a)). Orally directed currents were present on the cone- shaped peristome and carried particles through the open mouth to the stomodeum. When the mouth was closed, the orally directed currents on the peristome were less pronounced but converged and forced particles upwards and back upon the oral disk (Fig. l(b)).

Currents were also present on the tentacles of expanded polyps of all four species. These were directed distally near the tips. At the bases of the tentacles, currents flowed around each tentacle and transported particles off the edge of the polyp surface where they were entrained by strong, downwardly directed currents of the polyp stalk or column. The currents of the stalk carried particles toward the base of each polyp and converged between the bases of adjacent polyps. The stalk currents caused small-scale turbulence and up- welling which lifted particles off the surface. Circular currents were also present around the base of each polyp and these transported free particles across the surface of the corallum.

On the surface of contracted polyps, ciliary currents were directed away from the mouth. With the tentacles turned inward and the oral disk constricted to draw part of the stalk epithelium over the calyx, the downwardly directed currents of the stalk and those at the base of the tentacles drove particles off the polyp surface (Fig. l(b)). Turbulence

CILIARY CURRENTS I N ATLANTIC REEF CORALS 19

M

FIG. 1. Patterns of ciliary currents and formation of mucus filaments. (a) Porites porites (Pallas), expanded polyp x I 1 . (b) Porites porites (Pallas), contracted polyp x 1 1 . (c) Eusrnilia fustigiata (Pallas), expanded polyp x 1.5. (d) Mussu ungulosa (Pallas), expanded polyp x 1.5. (e) Favia frugum (Esper), expanded polyp x 9. (f) CoZpophyI/ia nutuns (Muller), expanded polyp x 2.

m-mouth, t-tentacle, mf-mucus filament, c-column.

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occurred around the circumference of each polyp, where the currents of adjacent polyps converged.

Although mucus production and the formation of mucus filaments are not as common in the Poritidae as in other families (Lewis & Price, 1975), nevertheless mucus filaments which were formed were caught in the turbulent area between adjacent contracted polyps. The converging currents rolled up filaments into bundles which trapped particles driven off the polyp surface (Fig. l(a), (b)).

In Pacific species of the family Poritidae, Yonge (1930) has described the pattern of ciliary currents in expanded polyps of Porites solida. They are identical to the currents of Atlantic Poritidae except that the stalk currents flow upward.

Family Pocilloporidae In expanded polyps of the two species of the family Pocilloporidae examined, Madracis

mirabilis and M . decactis, ciliary currents were identical to those of the Poritidae except that the currents of the polyp stalk were directed upward, not downward, in a clockwise, spiral motion (Fig. 3(d)). In contracted polyps, currents on the oral disk were directed outward and converged with the upward directed stalk currents around the periphery of the polyps. Mucus filaments were seldom observed in either species. Yonge (1930) found that ciliary currents flowed off the oral disk in Pocillopora bulbosa and up the stalk. Rapid currents carried particles across the surface of the corallum.

Family Caryophyllidae In Eusmilia fastigiata the pattern of ciliary currents is similar to that found in the

Pocilloporidae except that the flow is upward on the edge zone or theca in expanded polyps (Fig. l(c)). In contracted polyps, with the tentacles withdrawn, the flow is outward from the mouth and up the theca. Thus mucus is caught in filaments around the rim of the calyx in the area of turbulence where the currents meet. Yonge (1930) reported that the ciliary currents of Caryophyllia smithii from the Pacific were not well developed. Currents carried particles off the oral disk, out between the tentacles and down the column (Carlgren, 1905).

Families Faviidae and Meandrinidae All the meandrine forms of the two families Faviidae and Meandrinidae had similar

patterns of ciliary currents. The species examined were Diploria clivosa, D . strigosa, D. labyrinthformis, Manicina areolata, Colpophyllia natans, Meandrina meandrites and Dendrogyra cylindrus.

The typical pattern of currents on expanded polyps is shown in Fig. l(f) for Colpophyllia natans. Particles on the oral disk were carried outward away from the mouth, over and out between the tentacles. There were also distally directed currents on the tentacles. In the mouth region there were orally directed currents on the peristome which transported particles down into the stomodeum.

In the interpolypal region currents flowed away from the polyp centre but strong currents along the mid line of the interpolyp coenosarc caused turbulence, upwelling and often an apparent flow reversal. Currents flowing inward between adjacent interpolyp ridges were reported by Price (1973).

CILIARY CURRENTS IN ATLANTIC REEF CORALS 81

In contracted polyps there was a current flow away from the mouth and along the oral valleys. Currents pass upwards toward the mid line of the interpolypal ridges in two tracts. This is shown for Diploria strigosa in Fig. 2(b). During contraction the coenosarc of the

( b )

FIG. 2. Patterns of ciliary currents and formation of mucus filaments. (a) Favia fragurn (Esper), contracted

m-mouth, t-tentacle, mf-mucus filament. polyp x 11.5. (b) Diploria sfrigosa (Dana), contracted polyp x 2.5.

ridge moves downward to form a lip over the contracted tentacles. One tract of ciliary currents flows directly upwards toward the mid line where it meets the current from the opposite side. The second tract of currents is directed over the septa1 ridges but angled upward. The convergence of currents along the mid line of the interpolyp ridges causes

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turbulence and upwelling and it is along this line that mucus filaments collect in strands and bundles (Fig. 2(b)).

A number of Pacific meandrine forms have been described by Yonge (1930). Ciliary reversal was observed in species of Merulina and Tridacophyllia where tentacles are small. In all cases, however, material was removed from the oral disk by outwardly directed currents. Yonge also noted that a great deal of waste material in meandrine forms was collected in the centre of the interpolypal ridges.

In the non-meandrine species of the families Faviidae and Meandrinidae ciliary currents on the oral disks were directed outward in expanded polyps. Particles were transported off the disks and out between the tentacles in Favia fragum (Fig. l(e)), Montastrea annularis, M . cavernosa and Dichocoeniu stokesi. There were orally directed currents on the peristome. On the stalk, particles were transported upwards toward the tentacles in M . annularis and Favia fragum but downwards in the other species.

The stalk currents were very marked in contracted polyps of all four species. Two separate tracts could be observed which transported particles inwards toward the disk region or down the column. These are shown for Favia fragum in Fig. 2(a). One set of currents flowed along the grooves between the ridges over the primary septa and was directed towards the tentacles. The second tract of currents was directed transversely from the edge of each groove and up over the ridges toward the centre. Because these transverse currents flowed at an angle up the ridges there was a net transport of particles towards the tentacles and disk region.

Strong currents were also observed at the bases of polyp stalks, in the grooves between each polyp. These flowed around each stalk and transported particles across the surface of the coralum.

On the oral disk of contracted polyps of F. fragum ciliary currents flowing in the normal direction away from the mouth met the incoming currents from the grooves and ridges. Turbulence occurred around the outside of the ring of tentacles and it was at the base of the tentacles that bundles of mucus filaments accumulated and trapped particulate matter. In M . cavernosa however, the current flow was directed away from the disk region of completely contracted polyps. The stalk tissue covered the calyx completely and the downwardly directed currents carried particles to the interpolyp spaces. This is shown in Fig. 3(e)).

Yonge (1930) described the pattern of ciliary currents in Favia pallida from the Pacific. The general arrangement of currents is the same as for F. fragum except that currents on the stalk were directed downward rather than upward as in the Atlantic species.

Families Siderastreidae and Astrocoenidae Stephanocoenia michelini and the two species of the family Siderastreidae examined,

Siderastrea siderea and S. radians, had identical patterns of ciliary currents. In the laboratory all species produced considerable quantities of mucus and consequently ciliary currents were difficult to observe. Currents on the oral disks of expanded polyps were directed away from the mouth, past the tentacles and converged with similar currents from adjacent polyps in the interpolypal region (Fig. 3(a)). Turbulence occurred around the periphery of each polyp and particles were transported across the corallum by strong currents in the grooves between polyps. Orally directed currents were present on the peristome and there were distally directed currents on the short tentacles.

83 ClLlARY CURRENTS IN ATLANTIC REEF CORALS

( a )

( e l ( C )

FIG. 3. Patterns of ciliary currents and formation of mucus filaments. (a) Siderastrea siderea (Ellis and Solander), expanded polyp x 30. (b) Helioserus cucullafa (Ellis and Solander), contracted polyps x 6. (c) Agaricia agaricires (Linnaeus), polyps in varying stages of contraction x 3. (d) Mudracis mirabilis (Duchassaing and Michelotti), expanded polyp x 18. (e) Montastrea cavernom (Ellis and Solander), contracted polyp x 6.

m-mouth, t-tentacle. mf-mucus filament, c-column.

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In contracted polyps the currents were identical to those on expanded tissue. Mucus filaments accumulated between polyps in the region of current convergence (Fig. 3(a)). Vaughan (1912) considered that particles were drawn into the mouth of S. radians exclusively by ciliary action but we found no evidence of ciliary reversal in either species.

Family Agaricidae Patterns of ciliary currents in the Agaricidae were more variable than in the other

families examined. While the basic pattern for individual polyps in Agaricia ugaricites, A. Zamarcki and Helioseris cucuZZata was similar to other groups, the shape of coralla resulted in modifications.

Ciliary currents on an expanded polyp of A. agaricites are shown in Fig. 5(c). Two tracts were observed which carried particles away from the mouth and up the septal ridges. Currents flowing directly away from the mouth occurred along the ridges of the secondary septa. Currents directed laterally were found on the ridges of the primary septa and passed up the ridges to meet in the centre line. Particles were thus lifted off the surface of the ridges but the net transport was outwards away from the mouth. In Fig. 5(a) currents flowing away from the mouth are shown for A. lamarcki and in Fig. 5(b) currents meeting along the interpolyp ridges are illustrated for the same species.

Because of the irregularity in shapes of coralla in the Agaricidae the pattern of currents on an individual polyp was influenced by the adjacent polyp and by the proximity of the polyps to the edge of the colony. In Fig. 4(a) a modified flow is shown for a plate-shaped colony of contracted A . agaricites. In three adjacent polyps, curients flowed in two directions, toward and away from the mouths. Currents flow over the septal ridges and down into the calyxes of the polyps. Particles were also carried away from the mouths, over the septal ridges and into the calyxes of adjacent polyps. Similarly, there were currents which flowed between the mouths of the second and third polyps along a valley connecting the three.

In Helioserus cucullata there was a similar current flow across the corallum. This is shown in Fig. 3(b). Currents on the oral disk flow away from the mouth but because of the overhang of the upper calyx wall the flow is turned back to flow parallel to the lower limb. The asymmetric shape of the calyx thus causes a net flow towards the edge of the corallum.

In Fig. 4(b) directional transport across three adjacent polyps is shown for A. lamarcki. There was some flow between polyps and turbulence in the mouth region but this was masked by the strong currents across the interpolyp ridges.

As a consequence of the variability of current pattern in the agaricids there was an irregular distribution of mucus filaments. Thus, while bundles of filaments were common around the periphery of polyps, filaments were also found stietched across several adjacent POIYPS.

Current patterns were also influenced by the degree of expansion of polyps in the family Agaricidae. In fully expanded polyps the “normal” pattern was exhibited. As the polyps became further contracted, however, the disk tissue area became smaller, the stalk tissue lying over the interseptal spaces became broader and covered most of the calyx. This caused currents on the surface to flow in the opposite direction. The sequence of varying degrees of contraction in A . agaricites is shown jn Fig. 3(c). Since polyps of all three species of the Agaricidae were seldom observed fully expanded, currents were frequently observed flowing towards the mouth.

C I L I A R Y C U R R E N T S IN A T L A N T I C R E E F C O R A L S 85

( b )

FIG. 4. Patterns of ciliary currents. (a) Agaricia agaricires (Linnaeus), contracted polyps x 7.5. (b) Agaricia

m-mouth, t-tentacle. lumarcki (Milne Edwards and Hairne), partially contracted polyp x 7.5.

Yonge (1930, 1973) has described in detail the ciliary currents of Pacific Agaricidae. Because of their short tentacles he regarded the ciliary currents as being of considerable importance for food gathering. No ciliary reversal was observed in Pacific species. There

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‘ b )

FIG. 5. Patterns of ciliary currents. (a) Aguriciu lamurcki (Milne Edwards and Haime), partially contracted polyp x 20. (b) Agariciu lamurcki (Milne Edwards and Haime), section of corallum showing interpolyp space x 25. (c) Aguriciu uguricites (Linnaeus), expanded polyp x 6.

m-mouth, t-tentacle.

CILIARY C U R R E N T S IN ATLANTIC R E E F CORALS 87

are some similarities in currents of Atlantic and Pacific forms although in the Pacific genus Coeloseris currents transported all particles toward the mouth. Cleansing may possibly be also the result of water movements in this typical shore-living coral (Yonge, 1930).

Family Mussidae In the two species of the Mussidae which have separated calyxes, Mussa angulosa and

Scolymia lacera, the patterns of ciliary currents are identical. There are inwardly directed currents on the peristome and outwardly directed currents on the oral disk of expanded polyps. Currents on the oral disk pass out through the tentacles and flow downwards on the column. At the base of the stalk currents are directed upwards. The ciliary current pattern of Mussa angulosa is shown in Fig. l(d).

In contracted individuals the column wall is pulled inward to form a lip which covers the tentacles and a portion of the oral disk. The downwardly directed currents of the stalk flow outward off the surface of the polyp and are met at the edge of upwardly directed currents at the base of the stalk. Turbulence occurs at the edge of the polyp surface and mucus filaments are held and bound into strands around the polyp circumference (Fig. l(d)) in both contracted and expanded polyps.

Six other species of the family Mussidae, Isophyllia sinuosa, I. multijlora, Isophyllastrea rigida, Mycetophyllia lamarckiana, M . danaana and M . ferox were examined. In the three species of Mycetophyllia ciliary currents were similar to those of the meandrine corals of the families Faviidae and Meandrinidae. Currents were directed away from the mouth in both expanded and contracted polyps and mucus strands were concentrated in the spaces between polyps. In the two species of Isophyllia and Isophyllastrea rigida currents were similar to those of Mussu angulosa.

A number of species of Mussidae from the Pacific were examined by Yonge (1930). He found that ciliary currents flowed away from the mouth across the oral disk, up the inner side of the tentacles and down the outer side. In some species currents were directed down the column but in others they flowed upward.

Family Acroporidae As has been previously reported (Price, 1973; Lewis & Price, 1975) polyps of the two

species of Acroporjdae, Acropora palmata and Acropora cervicornis, were seldom observed fully expanded. In partially expanded polyps ciliary currents were directed away from the mouth, down the stalk but up the cylindrical corallites. In contracted polyps, currents flow off the oral disk. Mucus filaments are thus concentrated around the periphery of the cylindrical corallite. Weakly developed currents carry material around the base of each corallite across the corallum. The pattern of currents in four genera of Pacific Acroporidae were found to be similar by Yonge (1930). Expansion of polyps was incomplete but currents carried material off the oral disk and down the column. Transport of particles was more efficient in Acropora hebes than in other species.

Discussion This survey has indicated that there is a basic pattern of ciliary currents common to both

Atlantic and Pacific reef corals. In all but the family Agaricidae, the pattern on the oral disk is identical in all species. Currents flow away from the mouth toward the edge of the polyp and up or out between the tentacles. In the centre of the disk region currents flow

88 J . B. LEWIS A N D W . S. PRICE

towards the mouth on the peristome. During feeding strong currents draw material down into the stomodeum. At the bases of the columns there are currents which flow around each polyp and along the interpolyp spaces to transport particles across the corallum.

The consequence of these general patterns is that particles settling on the oral disk of all corals are carried off the polyp and swept into the interpolyp spaces. Currents at the base of the polyps serve to prevent accumulation of material on the coenosarc. Thus the views of Yonge (1973) and Abe (1938) that ciliary currents are involved in cleansing are supported by the observations on both Atlantic and Pacific corals.

On the polyp stalk or column there is considerable variation between species in both Atlantic and Pacific forms. In some species curients flow downwards towaid the coenosarc while in others currents pass up the stalk and up the outer edge of the tentacles. In species of Montastrea (Atlantic), for example, stalk currents flow upward in M . annularis and downward in M . cavernosa, while in the Pacific corals differences in flow direction were found by Yonge (1930) in two species of Poritidae. On the tentacles themselves, currents at the tips appear to be directed distally in Atlantic corals. Yonge (1930) however, found currents flowing upward on the inside of tentacles and downward on the outside of some Pacific species.

In Pacific corals, reversal of ciliary currents was observed by Yonge (1930) in the Fungiidae except in F. achniformis, now Heliofungia actiniformis, Wells, which has extremely long tentacles, and in some meandrine corals. This reversal occurred in species in which there were reduced tentacles. We did not observe any cases of ciliary reversal in Atlantic corals. Vaughan (1912) however, observed ciliary reversal in the Atlantic coral Municina (Meandra) areolata but this was not confirmed by Yonge (1935). We conclude, therefore, that ciliary reversal is not needed to assist food capture in Atlantic reef corals.

Nevertheless, current flow towards the mouth was frequently observed. In both Atlantic and Pacific forms in which stalk currents flow upward, particles are transported toward the mouth when the tentacles are folded inward. This was noted by Yonge (1930) in Psam- mocera stellata and other species in the Pacific. Current flow towards the mouth also occurs in Atlantic species in which, during contraction of the polyps, the column wall closes over the disk. Thus in Montastrea annuluris and Favia fragurn currents flowing up the polyp column in expanded specimens, flow inward towards the mouth in contracted polyps.

Comparisons of the family Agaricidae from the Atlantic and Pacific reveal a number of apparent differences. Yonge (1930) found that in certain species of Pacific Agaricidae where the tentacles are reduced or are lacking, ciliary currents were always directed towards the mouth. He regarded this as a case of specialization for feeding.

In Atlantic agaricids, the general pattern of current flow away from the mouth was not always observed in either expanded or contracted polyps. On the same colony there may be an inward flow towards the mouth, an outward flow and a unidirectional flow across the corallum. The pattern of the flow depends upon the state of contraction of the polyps or the shape and proximity of adjacent polyps.

We have also shown that the dual tracts of ciliary currents found in Pacific agaricids are present in Atlantic agaricids and in other families as well. These dual currents are found on the columns of stalked polyps and'may result in orally directed ciliary flow when polyps are contracted. The dual tracks found on all agaricids may be analagous to the column currents of stalked species. Indeed, complete polyp expansion is difficult .to observe in agaricids and in the observations of Abe (1938) and Yonge (1973) the calyxes of the

CILIARY C U R R E N T S IN A T L A N T I C R E E F CORALS 89

polyps appear to be covered mostly by stalk tissue. According to Hyman (1940) in some corals the column can close over the oral disk during contraction as in anemones. In others the polyp simply withdraws into the calyx.

The general current pattern for Atlantic species, and presumably for Pacific corals, has an important effect upon the accumulation of mucus. In both expanded and contracted species there is an area of turbulence either around the periphery of the calyx or in the interpolyp spaces. In these areas mucus filaments are concentrated and particles driven off the oral disk or lifted from the coenosarc are collected upon the filaments. These filaments may then be ingested (Lewis & Price, 1975). The significance of the ciliary currents in feeding is that they facilitate the ability of the mucus nets and filaments to gather particles and are functional in coral suspension feeding strategies.

Thus mucus binding may serve as a cleaning mechanism when the mucus filaments are carried off by wave action, or as a feeding strategy when mucus filaments are ingested. Whether or not mucus strands are ingested or are carried away into the water column, will depend upon the degree of water turbulence and current velocity. Recent work by Johannes (1967), Coles & Strathmann (1973), Marshall (1969), and Benson & Muscatine (1974) have emphasized the contribution that coial mucus may make to detritus over a reef. Ingestion of filaments occurs when a feeding response is elicited by tactile or chemical stimuli (Lewis & Price, 1975).

This work was supported by a grant in aid of research from the National Research Council of Canada.

R E F E R E N C E S Abe, N. (1938). Feeding behaviour and the nematocyst of Fungia and 15 other species of corals. Palao trop. biol.

Benson, A. A. & Muscatine, L. (1974). Wax in coral mucus: Energy transfer from corals to reef fishes. Limnol.

Carlgren, 0. (1905). Uber die bedeutung der flimmerbewegung fur den nakrungtransport bei den actiniarien und

Coles, S. L. & Strathmann, R. (1973). Observations on coral mucus “flocs” and their potential trophic significance.

Hyman, L. H. (1940). The Invertebrates 1. Protozoa through Ctenophora. New York and London: McGraw-Hill

Johannes, R. E. (1967). Ecology of organic aggregates in the vicinity of a coral reef. Limnol. Oceanogr. 12: 189-195. Lewis, J. B. & Price, W. S. (1975). Feeding mechanisms and feeding strategies of Atlantic reef corals. J. Zool.,

Marshall, N. (1969). Notes on mucus and zooxanthellae discharged from reef corals. In Symp. Corals and Coral

Price, W. S. (1973). Aspects of feeding behaviour of West Indian reef corals. MSc. thesis: McGill University. Vaughan, T. W. (1912). Studies of the geology and of the Madreporaria of the Bahamas and of Southern Florida.

Yonge, C. M. (1930). Studies on the physiology of corals. I. Feeding mechanisms and food. Scient. Rep. Gr.

Yonge, C . M. (1935). Studies on the biology of Tortugas corals. I. Observations on Meandra areolata Linn. Pap.

Yonge, C. M. (1973). The nature of reef building (hermatypic) corals. Bull. mar. Sci. 23: 1-55.

Stn Stud. 1: 469-52 I .

Oceanogr. 19: 810-814.

madreporarien. Biol. Zbl. 25: 308-322.

Limnol. Oceanogr. 18: 673-678.

Book Co. Ltd.

Lond. 176: 527-544.

Reefs: 59-65. Cochin, India: Mar. Biol. Assoc.

Y6. Carnegie Instn Wash. 11: 153-162.

Barrier Reef Exped. 1: 13-57.

Tortugas Lab. 29: 199-208,