Feeding mechanisms and feeding strategies of Atlantic reef corals

J. Zool., Lond. (1975) 176, 527-544

Feeding mechanisms and feeding strategies of Atlantic reef corals

J. B . L E W I S The Belluirs Research Institute of McGill University, St. Jmnes, Barbados, W.I.

A N D

W . S . P R I C E .Marine Sciences Centre, McGill University, Mrontreul, Canada

(Accepted 8 October 1974)

(With 5 plates in the text)

The feeding behaviour of 35 species of Atlantic reef corals was examined in the laboratory and in the field. Observations were made during the day and at night, using freshly hatched brine shrimp nauplii and finely ground, filtered fresh fish as food sources. Three feeding strategies were observed: Group I-feeding by tentacle capture only; Group 11-feeding by entanglement with a mucus net or mucus filaments; Group 11I--feeding by a combination of tentacle capture and mucus filament entanglement. Group I included corals of the families Poritidae and Pocilloporidae which were normally expanded during both day and night. Group I1 included corals of the family Agaricidae which were normally expanded at night and contracted during the day. Group I11 included corals of the other families examined which, with the exception of Dendrogyra cylindrus, were normally expanded only at night.

Feeding responses were elicited by both chemical and tactile stimuli. A preparatory feeding posture was assumed in response to chemical stimuli and consisted of horizontal positioning of the tentacles, elevation of the oral disk to form a cone-like mouth, a wide mouth opening and secretion of mucus by the epidermis of the oral disk. Following the assumption of the preparatory feeding posture, food capture and ingestive movements were elicited by tactile stimuli. However, food capture and ingestive movements were also elicited by chemical stimuli alone in those species which were normally contracted during the day.

While expanded corals captured food with their tentacles or with mucus filaments, contracted corals were able to feed by capturing fine particulate matter with mucus filaments only and thus acted as suspension feeders. By a combination of feeding strategies, reef corals were able to feed both day and night and a wide range of potential food ranging from fine particulate matter to large zooplankton was available to them

Contents

Introduction .. . . Materials and methods . . List of species examined . . . General observations . . Details of feeding behaviour

Group I . . . . Group I1 . . . . Group I11 . . . .

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

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Introduction This study is concerned with the feeding behaviour of corals, involving the oral ingestion

of food and the mechanisms whereby food is obtained in this way. The literature on feeding mechanisms of hermatypic corals has recently Seen reviewed by Muscatine (1973) who considered that corals should be regarded as suspension feeders. Previous work indicates that a number of methods of food capture are used. These include capture by tentacles, entanglement by mucus strands or mesenterial filaments, and feeding by ciliary currents. An attempt is made to assess the relative importance of these various feeding strategies and to relate them to the production of reef corals

A recent paper by Goreau, Goreau & Yonge (1971) has emphasized the current contro- versy over the sources of nutrition of hermatypic corals. Whereas reef corals are generally regarded as feeding principally upon particulate material of animal origin (Yonge, 1930; Goreau, Goreau & Yonge, 1971 ; Muscatine, 19731, food sources other than particulate material, such as dissolved organic matter and nutrients translocated from the zooxanthellae, have been considered by Stephens (1962), Franzisket (1969), Lewis, D. H. & Smith (1971), and others. Di Salvo (1973) and Sorokin (1973a, b) have shown that bacteria may be taken up by corals. Johannes, Coles & Kuenzel (1970) have concluded that the supply of zooplankton in tropical waters is too poor to supply the total nutritional needs of reef corals and that alternative sources are required. These considerations have been discussed by Goreau, Goreau & Yonge (1971) who, while noting that feeding mechanisms vary considerably, concluded that reef corals are essentially heterotrophic in their nutrition. If this is so, then the feeding mechanisms of corals deserve re-examination in detail in order to determine the efficiency of food capture and the potential sources of food.

In the few species of ahermatypic corals which have been examined, the tentacles with their nematocysts were the chief organs of capture (Carlgren, 1905; Boschma, 1925). Among the hermatypic corals as well, the tentacles were regarded as being the most important organs of food capture by Yonge (1930) who examined more than 40 genera of Pacific corals. Similarly, Abe (1938) emphasized the importance of the tentacles in the feeding behaviour of some fifteen species from Palao. Price (1973) observed that tentacle capture was common in Atlantic reef corals.

However, mucus secreted by the oral disk was found to play an important part in the entanglement and capture of zooplankton in Fungia (Duerden, 1906), in Manicina (Meandra) areolata (Yonge, 1935), and in corals from Palao (Abe, 1938). Yonge (1930) found that corals with small polyps depended less on tentacles than on mucus strands or filaments for the capture of zooplankton, and Goreau (1 956) considered mucus important for trapping particulate material in many species of Jamaican corals. Price (1973) also noted the importance of mucus for food capture in Atlantic reef corals.

Mesenterial filaments, extruded through the mouth or body wall, were observed to capture zooplankton by Isophyllia (Carpenter, 1910), by Montastrea (Orbicella) annularis (Vaughan, 1912), by some genera of Pacific corals (Yonge, 1930) and by Mussa angulosa (Goreau, 1956).

Observations on capture of food by ciliary currents on the oral disk indicated that these currents normally had a cleansing function but could, under some circumstances, reverse and transport food towards the mouth. Ciliary reversal was observed occasionally in Isophyllia by Carpenter (1 9 lo), in Manicina (Meandra) areolata by Vaughan (19 12), in Pacific corals with reduced tentacles by Yonge (1930), and in corals from Palao by Abe

FEEDING O F ATLANTIC REEF CORALS 529

(1938). Yonge (1935) later was unable to find ciliary reversal in Manicina (Meandra) areolata.

Materials and methods The investigation was carried out at the Bellairs Research Institute of McGill University in

Barbados, West Indies. Most of the species studied were collected from a fringing reef off the west coast of the island. Observations were made during both clay and night, in the laboratory and in the field.

In order to observe feeding behaviour in the laboratory a fish homogenate and live brine shrimp nauplii (Artemiu sp.) were offered as food. The fish homogenate was prepared by grinding up fresh fish in sea water, centrifuging, filtering and finally mixing with a little finely ground Alcian Blue. Alcian Blue is a specific stain for mucopolysaccharides (Pearse, 1935) and stained mucus strands darkly.

All corals examined in the laboratory were carried from the field in buckets of water without exposing them to the air and placed in running sea water aquaria. The observations of feeding behaviour was completed within 24 h in most cases. Feeding behaviour was observed through a Wild M-5 stereoscopic microscope with illumination through a blue filter during the day and a red filter (Nikon R-60) at night. Laboratory photographs were taken with a Nikon F attached to the Wild M-5 microscope. During observations in the laboratory colonies were held in glass finger bowls holding 350 ml of water.

Live brine shrimp nauplii were offered as food in the field by means of a 25 ml plastic syringe and feeding was observed with a hand magnifying lens. Field observations were carried out with the aid of SCUBA diving gear. Underwater photographs were taken with a Nikonos I1 with a 28 mm f/3.5 lens coupled with close up rings and a Braun electronic flash. Night observations were carried out with the aid of underwater hand lanterns and ]helmet lights.

List of species examined Family Astrocoenidae

Family Pocilloporidae 1.

2. 3. M . decatis (Lyman).

4. Acropora palmata Lamarck. 5. A . cer vicornis Lamarck.

6. 7. 8.

9.

Stephanocoenia michelinii Milne Edwards and Haime.

Madrucis mirabilis (Duchassaing and Michelotti).

Family Acroporidae

Family Agariciidae Agaricia agaricites (Linnaeus), forma agaricites and forma purpurea. A . lamarcki Milne Edwards and Haime. Helioseris cucullata (Ellis and Solander).

Siderustrea siderea (Ellis and Solander). Family Siderastreidae

10. S. radians (Pallas).

1 1 . Porites astreoides Lesueur. 12. P. porites (Pallas). 13. P. furcata Lamarck. 14. P. divaricata Lesueur.

Family Poritidae

530 J. B. LEWIS AND W. S . PRICE

Family Faviidae 1 5. Favia fragum (Esper) . 16. Diploria clivosa (Ellis and Solander). 17. D. strigosa (Dana). 18. D. labyrinthiformis (Linnaeus). 19. Manicina areolata (Linnaeus). 20. Colpophyllia natans (Muller). 21. 22. M. cavernma (Linnaeus).

23. Meandrina meandrites (Linnaeus). 24. 25. 26. Dendrogyra cylindrus Ehrenberg.

27. Mussa angulosa (Pallas). 28. Scolymia lacera (Pallas). 29. Isophyllia sinuosa (Ellis and Solander). 30. I. multijlora Verrill. 3 1. Isophyllastrea rigida (Dana). 32. 33. 34. M. ferox Wells.

Family Caryophyllidae 35. Eusmilia fastigiata (Pallas).

Montastrea annularis (Ellis and Solander).

Family Meandrinidae

Dichocoenia stokesi Milne Edwards and Haime. D. stellaris Milne Edwards and Haime.

Family Mussidae

Mycetophyllia lamarckiana Milne Edwards and Haime. M. danaana Milne Edwards and Haime.

General observations Our observations, and those of other authors, lead us to consider that there is a sequence

of events which constitutes the feeding behaviour of corals. Expansion of the polyp, especially of the tentacles, is one of the prerequisites for feeding in corals. Most Atlantic reef corals are fully expanded at night but a few species are normally expanded during the day as well. Those which we found consistently expanded during the day were two species of Madracis, four species of Porites and Dendrogyra cylindrus. Other species were observed expanded at times during the day and as Goreau (1956) observed, some colonies of most species can be found expanded during daylight. Those species which we frequently observed to be expanded during the day included Diploria clivosa, Montastrea cavernosa, Siderastrea siderea, S. radians, Acropora cervicornis and Stephanocoenia michelinii.

While the degree of expansion of the polyps varied between species and within the same corallum, maximum expansion could be elicited by the addition of either brine shrimp or fish homogenate in the water in the laboratory. Maximum expansion consisted of horizontal and vertical positioning of the tentacles, elevation of the oral disk to form a cone-like mouth, a wide mouth opening, and production of mucus by the epidermis of the oral disk. This may be termed a preparatory feeding posture and is similar to the behaviour described in sea anemones by McFarlane (1970) and Williams (1972), and in corals by Mariscal & Lenhoff (1968) and Abe (1938). The preparatory feeding postures were similar

FEEDING O F ATLANTIC REEF CORALS 53 1

for all species examined and are shown for Porites porites, JWontastrea cavernosa, Madracis mirabilis, Diploria labyrinthiformis, Meandrina meandrites and Eusmilia jastigiata in Plate I, (a)-(f). Preparatory feeding postures in Siderastrea siderea, Acropora palmata and Agaricia lamarcki are shown in Plate 11, (a)-(c).

Mucus was produced in the mouth and by the epidermis of the oral disk in all the species examined. The amount of mucus varied from a dense net in Montastrea annularis (Plate V(f)) and Mussa angulosa, thick strands and filaments in Diploria strigosa and Colpophyllia natans (Plate V(c)), to small patches in Porites porites (Plate II(f)). Mucus was broken up by ciliary currents in the laboratory and by water turbulence in the field to form fine threads and filaments lying along the septa1 ridges or attached to the mouth.

Following the assumption of the preparatory feeding posture, food capture and ingestive movements were elicited by tactile stimuli. The presence of fine particulate food in the immediate vicinity of the mouth caused further expansion of the mouth, tentacle contractions, mucus production and subsequently, in all but the families Poritidae and Pocillo- poridae, ingestion of mucus filaments. A tactile stimulus caused by contact of brine shrimp with the tentacles caused rapid tentacle contraction, contraction of the oral disk and a folding towards the mouth of the tentacles holding captured prey.

Our observations further revealed that there was a feeding response elicited by chemical stimuli alone in those species which were not normally expanded during the day. In contracted species, there was no assumption of the preparatory feeding posture during daylight in response to a chemical stimulus. Instead, ingestive movements, elicited by the fish homogenate, began with mouth opening and mucus production. The mucus was formed into a loose net or filaments and was sucked into the mouth. Capture and ingestive movements by mucus filaments and mucus nets were observed in all species which were not normally expanded during the day.

Our field observations confirmed that food capture was accomplished by mucus filaments as well as by tentacles. At night most expanded species readily caught zooplankton with their tentacles. Mucus strings or long mucus filaments were also observed at night, attached to the oral disk or extruded from the mouth. These filaments were swept about by water turbulence and entangled fine particulate material as well as larger zooplankton. Such filaments were periodically drawn back into the mouth.

During the day when most polyps were not expanded, mucus filaments were also observed in the field. Fine particulate matter was trapped in the filaments and eventually ingested.

While we observed feeding behaviour involving the tentacles or by mucus strands in all species examined, two mechanisms reported by other authors were not normally observed in the field or under our experimental conditions. These were feeding involving ciliary reversal alone and feeding by means of mesenterial filaments. In our view neither of these forms of behaviour is as important as tentacle or mucus strand feeding. Arguments in support of this view are presented in the Discussion.

Feeding behaviour, then, consisted of preparatory feeding activity followed by tentacular feeding or mucus capture and ingestion. The species examined can be divided into three groups depending upon the predominant feeding strategies employed : (I) corals feeding primarily by tentacle activity; (11) corals feeding primarily by a mucus net or filaments, i.e. suspension feeders, and (111) corals using a combination of tentacles and suspension feeding. The details of these strategies are described in the following sections.

532 J . B . LEWIS AND W. S . PRICE

PLATE 1. Preparatory feeding posture. (a) Poriies poriies (Pallas), lab. photo. x 7. (b) Madrucis mirabilis (Duchassaing and Michelotti), field photo. x 6. (c) Meandrina meandrites (Linnaeus), field photo. x 3. (d) Mont- astrea cavernosa (Ellis and Solander), field photo. x 3. (e) Eusmilia fastigiata (Pallas), field photo. Y 3. (f) Dbloria lubyrinthiformis (Linnaeus), field photo. x 3.

F E E D I N G O F ATLANTIC R E E F CORALS 533

PLATE 11. (a) Acroporu pulmutu (Lamarck). Preparatory feeding posture, field photo. x 6. (b) Aguriciu lumurcki (Milne Edwards and Haime). Preparatory feeding posture, field photo. x 3. (c) Siderastreu sidereu (Ellis and Solander). Preparatory feeding posture, lab. photo. x 6. (d) Montustreu cuvernosu (Linnaeus). Preparatory feeding posture with elongate sweeper tentacles, field photo. x 2. (e) A,guriciu uguricites (Linnaeus). Elongate sweeper tentacles, field photo. x 6. (f) Porites porftes (Pallas). Loose, particulate material on surface of corallum, lab. photo. x6.

534 J . B. LEWIS AND W . S . PRICE

Details of feeding behaviour Group I

Group I is comprised of six species feeding primarily by tentacle capture : Porites porites, P. astreoides, P. divaricata, P. furcata, Madracis mirabilis and M . decactis.

Polyps of all six species were expanded both day and night in the laboratory and in the field. In the preparatory feeding posture (Plate I(a), (b)) the polyp column was raised well above the calyx. The mouth was open, rounded, and the oral disk itself was convex. The tentacles were short but fully extended horizontally. Strong ciliary currents were directed off the oral disk and down the column walls. Mucus was produced in the mouth but mucus strands were rarely observed.

In the Poritidae the tentacles responded rapidly to the addition of brine shrimp in the field and in the laboratory. Prey was captured by contact with the tentacle tips. Each tentacle partly contracted and all tentacles folded inward towards the mouth. At the same time the oral disk sank to form a concave cup. The prey was thus held beneath the tentacles, the mouth opened wide and turned towards the tentacle holding the prey. Finally, the brine shrimp were stuffed into the mouth by the tentacles or were entangled in mucus and sucked into the stomodeum.

In Madracis mirabilis (Plate I(b) and M. decactis the tips of the tentacles were inflated into pronounced bulbs which were heavily armed with nematocysts. Strong ciliary currents were observed directed away from the mouth off the oral disk and out between the tentacles. Clockwise currents circulated around the column wall. Very little mucus was produced and mucus strands were observed rarely.

Upon the addition of brine shrimp in the field and in the laboratory, there was rapid excitation of the tentacles which lashed about in the vicinity of the prey. Brine shrimp were caught by the tentacle tips and one or several tentacles with entrapped prey immediately turned inward towards the mouth. The tentacles were wrapped around the prey, the polyp was partly withdrawn into the calyx and the mouth opened wide. Prey was stuffed into the mouth or released on the oral disk where it was caught in mucus and drawn into the stomodeum.

Although in the laboratory a homogenate of ground fish added in the vicinity of the mouth increased the sensitivity of the tentacles in all six species, the fine particulate material offered was not ingested without the assistance of the tentacles. Most stained particles remained suspended in the water or remained on the oral disks and were moved about by ciliary currents. Mucus strands were rarely formed or taken into the mouth. Plate Il(f) shows loose scattered particles on the surface of Porites porites. However, mucus may at times cover the whole colony of this and other species (Lewis, 1973; Coles & Strathmann, 1973).

Group II Group I1 is comprised of those species which are primarily suspension feeders. It

includes Agaricia agaricites, A. lamarcki and Helioseris cucullata. Polyps of all three species expanded in the dark only. In the preparatory feeding posture

the polyp was raised well above the septa1 ridges, the circular mouth was open slightly and the rudimentary tentacles were prominent (Plate II(b)). Strong ciliary currents flowed away from the mouth towards the edge of the disk. The epidermis produced a copious


flow of mucus which in laboratory-maintained colonies often appeared as a continuous layer or net raised slightly above the surface of the polyp.

Upon the addition of fish homogenate at night, in the laboratory, the mouth opened wide and the mucus net was dispersed by ciliary currents and came to lie in strands along the septal ridges. The mouth became elevated as a cone or was elongated and slit-like. The stomodeum was exposed and the mouth everted to form a lip. Feeding commenced as mucus strands were drawn into the mouth. No reversal of ciliary currents towards the mouth was observed on the disk but ciliary currents directed away from the mouth were present during feeding. Contractions of the oral disk caused the tentacles to withdraw.

Brine shrimp were only occasionally observed to be captured directly by tentacles in the laboratory. Brine shrimp released in the vicinity of the polyps in the field were immediately entangled in the mucus strands and sucked into the mouth. After the mucus strands with entangled food became completely ingested, the polyps withdrew into the calyx, the mouth closed and feeding stopped. Fine particulate mateirial which settled on the polyps in the field was caught in mucus and ingested. Thick mucus cords were also observed to capture particulate material in the field.

Although the rudimentary tentacles did not appear to be functional in the capture of food, enlarged or extended “sweeper” tentacles were observed in the field on a few occasions. Such tentacles, often 4-6 mm in length (Plate II(e)), were highly reactive, waved and lashed about and caught large zooplankton readily.

During the day the polyps of all three species were partially or wholly withdrawn. Tentacles were not expanded and there was little expansion of the oral disk above the calyx. The mouth was normally closed. There were strong ciliary currents directed away from the mouth and mucus filaments were formed and swept across the corallum.

Upon addition of fish homogenate during the day ciliary currents increased in activity, the mouth opened and mucus strings formed on the oral disk and along the septal ridges. Shortly after the opening of the mouth the mucus strings with entangled particles were drawn into the mouth and upon completion of ingestion the mouth closed. Mucus strings being drawn into the mouth are shown for Agaricia lamarcki (Plate III(a)) and for A. agaricites in Plate III(b).

Brine shrimp offered during the day were occasionally caught in the mucus strands and sucked into the mouth. However, it was evident that zooplankton was not captured by the mucus filaments as readily during the day as at night.

Group 111 Corals of this group used both tentacles and mucus nets to capture and ingest food. It

includes the following species : Favia fragum, Diploria clivosa, D. strigosa, D. labyrinthiformis, Manicina areolata, Colpophyllia natans, Montastrea annularis, M . cavernosa, Stephanocoenia michellinii, Acropora palmata, A. cervicornis, Siderastrea siderea, S. radians, Dichocoenia stokesi, D. stellaris, Mussa angulosa, Scolymia lacera, Isophyllia sinuosa, I. multifora, Isophyllastrea rigida, Mycetophyllia lamarckiana, M . ferox, M . danaana, Eusmilia fastigiata, Meandrina meandrites and Dendrogyra cylindrus.

A11 the corals in this group showed similar feeding behaviour. [n the preparatory feeding posture at night the tentacles were fully expanded horizontally or vertically and a broad oral disk was exposed. The mouth was partially open, raised in a cone, and was slit-like

536 J . B . LEWIS AND W. S . PRICE

PLATE 111. Ingestion of mucus filaments. (a) Aguriciu lumurcki (Milne Edwards and Haime), lab. photo. x 7. (b) Aguriciu agarkites (Linnaeus), lab. photo. x 6. (c) Montustreu annularis (Ellis and Solander), lab. photo. x 6. (d) Dichocoeniu stokesi (Milne Edwards and Haime), lab. photo. x 3. (e) Siderastrea radians (Pallas), lab. photo. x 12. (f) Stephunocoeniu michelinii (Milne Edwards and Haime), lab. photo. x 7.

FEEDING OF ATLANTIC REEF CORAL,S 537

and everted to form a grooved lip. There were strong ciliary currents directed away from the mouth, across the oral disk and up to the septal ridges between the tentacles. Mucus was produced in the mouth and on the oral disk and this wais broken up into strands which, at least in the laboratory, lay along the septal ridges. E'articulate material trapped in mucus was observed in the field in all species and is shown for Diploria strigosa in Plate

Upon the addition of fish homogenate at night in the laboratory, the mouth gaped open and the mucus strands lying on the oral disk and along the septal ridges were drawn into the mouth. At the same time the tentacles became highly active, waving about and under- going periodic contractions.

The addition of brine shrimp at night caused the tentacles to wave about. Upon con- tacting the brine shrimp they caught and held the prey, turned towards the mouth and folded inward and downward. The oral disk contracted and caused movement of the tissue on the septal ridges inward towards the mouth. The tentacles then lay adjacent to the mouth and were covered with a fold of tissue (shown for Scolymia lacera in Plate V(b)) similar to the lip described by Reimer (1971) for Palythocz. The mouth bent towards the tentacles holding the prey. The prey was then either deposited on the oral disk in the mucus strands or the tentacles were stuffed into the gaping mouth and sucked off into the stomodeum.

In both Siderastrea siderea and S. radians the expanded tentacles occurred in three concentric cycles. The inner and middle cycles were bifurcate and all tentacles were very short in comparison with other species (Plate II(c)). In the preparatory feeding posture the tentacles were held erect and the epidermis produced a copious flow of mucus which formed a loose net. In the field most colonies contained a loose aggregate of particulate material bound together by mucus and lying in the polyps (Plate IV(a)).

The addition of brine shrimp nauplii at night elicited rather weak responses and in- effective prey capture by the tentacles in both species of Siderastrea. Most of the brine shrimp escaped capture. Ingestive movements consisted of contraction of the oral disk, extension of the mouth, bending of the mouth towards the tentacles and folding inwards of the tentacles. Prey ingestion was also aided by a flow of mucus into the mouth. Brine shrimp were readily caught in mucus nets and ingested without the aid of tentacles.

Two species of the family Acroporidae, Acropora palmata and A. cervicornis, were examined. Neither species expanded well in the laboratory during either day or night and polyps in the fully expanded preparatory feeding posture: were not observed. However, our field observations confirmed that brine shrimp were ireadily caught by the tentacles. Mucus strands being drawn into the mouth were observed in the field, and in the laboratory mucus ingestion occurred after the addition of fish homogenate. Colones with partially expanded polyps are shown in Plate II(a).

Thus, although we have limited observations of feeding in Acroporida it is likely that both species belong to Group 111 and feed by a combination of tentacle capture and mucus filaments.

The tentacles of M. cavernosa were larger than in the species considered above. The feeding posture has been described by Lehman & Porter (1973) and is shown in Plate I(d). Because of the large size of the polyps of M. cavernma the capture of zooplankton in the field was readily observed. Strands of mucus extruded from the mouth were seen to trap particulate material both day and night and to be drawn into the mouth.

Vb).

538 J. B. LEWIS A N D W . S . P R I C E

PLATE IV. (a) Siderastrea sidera (Ellis and Solander). Particulate material on surface of corallum, field photo. P 3. (b) Mycetophyllia danaana (Milne Edwards and Haime). Ingestion of mucus filaments, field photo. x 2. (c) Manicim areolata (Linnaeus). Ingestion of mucus filaments, lab. photo. x 3. (d) Favia frugum (Esper). Ingestion of mucus filaments, lab. photo. x 6 . (e) Meandrina meandrites (Linnaeus). Mucus strand with attached particles, field photo x3. (f) Diploria labyrinthiformis (Linnaeus). Ingestion of mucus filaments, lab. photo. x 10.

F E E D I N G O F A T L A N T I C R E E F C0RAL.S 539

PLATE V. (a) Coipophylliu nutuns (Miiller). Interlocking tentacles, field photo. x 1. (b) Diploriu strigosu (Dana), Particulate material on surface of corallum, field photo. x 1. (c) Coipophyl'Ziu nutuns (Miiller). Ingestion of mucus. filaments and extratentacular lip or fold, lab. photo. x 3. (d) Mussu unguloaa (Pallas). Ingestion of mucus filaments, lab. photo. x 2. (e) Scolymiu luceru (Pallas). Extratentacular lip or fold, larb. photo. x 2. (f) Montustreu unnuluris (Ellis and Solander). Ingestion of mucus net, lab. photo. x 7.

540 J . B . LEWIS AND W . S . PRICE

Elongate “sweeper” tentacles were often observed in this species (Plate II(d)). Such tentacles were up to 90 mm in length, highly flexible and active and were able to catch and hold brine shrimp nauplii at any point along their length. Similar elongate, threadlike tentacles have been reported in the red coral, Corallium rubrum by Abel (1970).

Three species of Group I11 were distinguished by having very long and active tentacles. While mucus feeding was also observed it was apparent that Eusmilia fastigiata, Meandrina meandrites and Dendrogyra cylindrus made very efficient use of their tentacles for prey capture. Dendrogyra and Meandrina corallites are nearly completely covered with long, well-armed tentacles, while in Eusmilia the tentacles are fewer but highly elongate and active. Dendrogyra was expanded both day and night while Eusmilia and Meandrina expanded readily only at night.

In the preparatory feeding posture in all three species the tentacles were held nearly horizontal, exposing a broad oral disk. The mouth was open and raised on a conical peristome. Ciliary currents were directed across the oral disk towards the tentacles and mucus strands were formed on the disk and septal ridges. Ciliary currents were also present along the tentacles, directed distally. Meandrina and Eusmilia in preparatory feeding postures are shown in Plate I(c), (e).

Upon the addition of fish homogenate at night in the laboratory, above the oral disk the tentacles become highly active and twisted and lashed about. The mouth opened wider, exposing an everted pharynx and forming a pronounced lip. Mucus strands were drawn into the mouth from the oral disk and septal ridges.

Upon the addition of brine shrimp in the laboratory and in the field, the tentacles writhed vigorously in the vicinity of the prey. The tentacles of each species were able to trap prey along their whole length and act individually. The tentacles were then turned towards the mouth, the oral disk contracted and food was either stuffed into the mouth or deposited in mucus on the oral disk. After the food was ingested the mouth partially closed and the polyps assumed the preparatory feeding posture again.

During the day the polyps of both species were withdrawn and only the tips of the tentacles were exposed. Upon the addition of fish homogenate the mouth opened and mucus strands were slowly sucked in. Mucus filaments, laden with particulate material, were frequently observed in Dendrogyra and Meandrina (Plate IV(e)) in the field. Such filaments were periodically sucked into the mouth at night and during the day.

Discussion Our observations indicate that there were two primary mechanisms in Atlantic reef

corals whereby particulate food was obtained. These were by tentacle capture and by suspension feeding with a mucus net or filaments. Both mechanisms were observed in the laboratory and in the field.

In Group I, the Poritidae and Pocilloporidae, tentacle feeding was most important. Although mucus was produced in the vicinity of the mouth and mucus was important in the actual ingestion of the prey, there was no evidence that a mucus net was used for prey capture.

Both families of Group I were distinguished by having tentacles expanded for feeding during the day as well as at night. Thus, although Group I was dependent upon a single feeding strategy, food capture could take place continuously and feeding efficiency was thereby increased.


In Group 11, the Agaricidae, feeding by a mucus net was most important. Although live zooplankton was occasionally captured by tentacles and elongate sweeper tentacles have been observed in one species, the short rudimentary tentacles of this group prevented effective tentacle prey capture. As with Group I, one feeding mechanism was utilized but mucus nets were produced both day and night and hence feeding could take place continuously.

In Group 111, it appeared that tentacle and mucus filament capture occurred at night while most species were suspension feeders during the day. All species had relatively long active tentacles with the exception of the Siderastereidae. In both S. siderea and S. radians the tentacles were short and mucus production was more: abundant than in the rest of Group 111. Thus the Siderastereidae may be regarded as transitional between Groups I1 and 111. Tentacle capture does occur but was not very effective and was compensated for by the efficiency of mucus net capture.

Among Group I11 only Dendrogyra was consistently expanded both day and night and was characterized by long and very active tentacles. Prey capture by the tentacles was rapid and efficient. A mucus secretion aided ingestive inovenients in the mouth and pharynx both day and night.

Our observations for all species suggest that there were two levels of response to feeding stimuli in corals. The two responses, the adoption of a preparatory feeding posture and the capture/ingestive movements, appeared to be separate and were similar to feeding behaviour described for the sea anemone Tealia by McFarlane (1970), for the sea nettle C'hrysaora by Loeb & Blanquet ('1973), for the zooanthiid Palythoa by Reimer (1971), and for hermatypic corals by Mariscal & Lenhoff (1968) and Lehman & Porter (1973). In all cases a chemical stimulus was needed to evoke a preparatory feeding posture and a tactile stimulus triggered a series of subsequent feeding reactions. Goreau (1956) and Muscatine (1 973) considered that normal feeding response in corals was usually elicited by a combination of chemical and tactile stimuli.

Feeding movements in response to chemical stimuli are obviously important not only in initiating mucus net capture but in establishing the preparatory feeding posture. A number of authors have found that reef corals are extremely sensitive to amino acids or meat extracts in the surrounding water. Mariscal (1971) and Mariscal & Lenhoff (1968) have shown that the response of Cyphaster and several other species of Pacific reef corals to live prey and to extracts of amino acids, consisted of a wide mouth opening and sharp contractions of the tentacles. In experiments using live prey, tentacle contractions and prey capture preceded the response of mouth opening. Lehman & Porter (1973) found that a number of amino acids on filter paper would evoke feeding responses in the Caribbean coral Montastrea cavernosa and that there was a separation of oral and tentacular responses. Abe (1938) found that mouth opening and other feeding responses were elicited by meat tissue extracts. It is likely that the occasioiial daytime expansion of many species of corals is due to the presence of food in the wateir (Goreau, 1956; Taylor, 1973).

Our field observations support the view that food capture by tentacles and mucus filaments are both important aspects of feeding behaviour in Atlantic reef corals. Natural zooplankton and brine shrimp nauplii were readily captured by expanded tentacles of most species. Mucus nets and filaments were also observed in the field in all species with the exception of the Families Poritidae and Pocilloporidale. Particulate matter and zooplankton were caught in the nets and mucus was sucked into the mouth.

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

The production of copious amounts of mucus by reef corals has been reported by a number of authors (Johannes, 1967; Lewis, 1973; Marshall, 1969; Coles & Strathmann, 1973). Johannes (1967) observed mucus streaming from heads of Porites in the Pacific while Coles & Strathmann (1973) described mucus secreted from Porites and Acropora as forming diffuse, transparent strands which contained particulate material. Thus it is evident that the formation of mucus nets and filaments normally occurs in the field and that this mucus traps particulate material.

The ability of reef corals to feed by a mucus net or filaments greatly increases the potential food sources available to them. Goreau (1956) has emphasized the importance of fine particulate material as potential food for reef corals. Jorgensen (1 966) considers that mucus suspension feeders are able to efficiently retain particles down to less than 1 pm and has stated that in most suspension feeders, feeding goes on more or less continuously. Thus the suspension feeding abilities of many reef corals provides an answer to the theoretical difficulties raised by Johannes et al. (1970) in regard to the poverty o f zooplankton in tropical waters available to corals. Not only zooplankton but a wide range of suspended particulate material is available to feeding corals. This view also supports the conclusion of Sorokin (1973a, b) that corals consume bacterioplankton.

Although we have no direct information on the amount of suspended material over the reefs in Barbados, Glynn (1973) has shown that the flux of suspended matter, primarily detrital in nature, was an order of magnitude higher than plankton on reefs in Puerto Rico. This suggests that a significant potential food source exists for reef corals in addition to zooplankton. While the productivity of Barbados waters is low (Beers et al., 1968) sub- stantial standing crops of zooplankton are present throughout the year (Calef & Grice, 1967; Lewis & Fish, 1969).

Mucus secretion serves two purposes in feeding. In tentacle feeding forms the captured prey is stuffed into the mouth or pushed into mucus on the oral disk and subsequently sucked into the stomodeum. In suspension feeders the mucus net is the primary method o f prey capture.

Because of our failure to observe corals feeding routinely by means of mesenterial filaments we do not consider this method of feeding as important as tentacle and suspension feeding. Previous reports of the use of mesenterial filaments for capturing and extra- coelenteric digestion have been in connection with large particles of food on the oral disk (Carpenter, 1910; Vaughan, 1912; Yonge, 1930; Goreau, 1956). While capture of live food by mesenterial filaments was observed in the laboratory this form of behaviour occurred only in damaged specimens, in specimens which had been held in the laboratory for several days, or when large particles of food were placed on the oral disk. Extrusion of the mesenterial filaments has already been shown to occur in corals subjected to pollution or adverse conditions (Lewis, 1971), and Lang (1970) has described the use of filaments as aggressive weapons in a number of corals.

Finally, we did not observe any cases in which there was a reversal of ciliary currents on the oral disk which directed food towards the mouth. Indeed, ciliary currents travelling in the normal direction, away from the mouth,were frequently observed during the process of ingestion. Furthermore, because of strong water turbulence prevailing on coral reefs it is difficult to perceive how the weak currents caused by ciliary action on the oral disk can transport food material in a directional manner. As Yonge (1973) has suggested, observations of supposed ciliary currents directed towards the mouth can be explained

F E E D I N G O F ATLANTIC R E E F CORALS 543

on the basis of mucus strings pulled along by cilia lining the stomodeum. Nevertheless, reversal of ciliary currents has been reported by Yonge (1930) in Fungia and other genera in the Pacific.

Our study was supported by a grant from the National Research Council of Canada. We are grateful to Messrs Michael Lands and Bruce Ott for technical assistance and to Dr Finn Sander for making laboratory facilities available. We also thank Dr Henry Reiswig and Dr Carol Lalli for their helpful comments on the manuscript.

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Feeding mechanisms and feeding strategies of Atlantic reef corals