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  1. Molluscs Associated with Living Tropical Corals1 MICHAEL G. HADFIELD Pacific Biomedical Research Center, University of Hawaii Honolulu, Hawaii 96822 INTRODUCTION Of the many thousands of molluscan species which are restricted in their dis- tributions to shallow-water, tropical habitats, few can be shown to have a direct or obligatory association with living corals. For the remainder, a coral reef provides a major type of habitat in which the molluscs are living lives comparable to those of molluscs on temperate shores: they are detritivores, herbivores and carnivores, microphagous or macrophagous, whose life cycles are adapted to the temperatures and food webs of tropical reef ecosystems. In this paper I wish to discuss species with direct and obligatory associations with living corals. The purpose of such a survey is to assess the types of interactions which occur between corals and mol- luscs, to indicate where knowledge is scant, and to recommend directions for future research. Frequently one encounters molluscan groups which are only generally coelen- terate-specific; that is, members of one family will prey on scleractinians, hydro- corals, alcyonaceans, zooanthiniarians, gorgonians, and antipatharians. For this reason, the molluscan associates of these non-scleractinians are included in the ensuing discussion. This inclusion leads to some discussion of better studied, non-tropical forms where, due to their distributions nearer the large temperate research laboratories, more and enlightening information is available. I have been able to find good examples of active mollusc-coral associations in the three molluscan classes, Gastropoda, Lamellibranchia, and Aplacophora. For sake of convenience, and because such a series may indicate evolutionary tenden- cies, I have divided the associations into four classes. These are: (I) Predatory and parasitic molluscs, all of which presumably survive by eating the flesh of living corals; (II) Molluscs which bore into living coral, using the coral skeleton as a re- fuge while obtaining their energy from material suspended in sea water which they collect by filtration; (III) Epizoic molluscs which cling to the outer surfaces of living coral and obtain their food by filtration; and, (IV) Molluscs which serve as sub- strata for corals. As will become apparent, several problems arise in such a classifi- cation. Many species fall into the shadows of the outline either because their actual food is unknown, or, as in the case of Fungiacava (discussed below), their 1 Paper presented at a Symposium on "Animal associates on coral reefs", International Symposium on Indo-Pacific Tropical Reef Biology, Guam and Palau, June 23-July 5, 1974. Micronesica 12(1): 133-148. 1976 (June).

  2. Micronesica 134 habits overlap the categories. The major problem in classifying the coral-associated molluscs by nature of relationship is that too little knowledge is available. The massive conchological literature is replete with citations of species being "found with," or "associated with," or "on," some cnidarian. Many such citations have entered the literature as verifications of predation. As will be noted in the follow- ing discussion, too often the exact habits of many of these molluscs are yet to be learned. Other reviews relevant to the present topic are those of Graham ('1955), Rees (1967), Robertson (1970a), Salvini-Plawen (1972), and Yonge (1974). As indicated by their titles, none of these reviews addresses the topic as I do here and few pose basic questions concerning the biology or evolution of mollusc-coral interactions. All are valuable because of their tabulations, their discussions and their biblio- graphies. THE ASSOCIATIONS (I) Predatory and Parasitic Molluscs. Except for a few forms (Fungia, for example), it is generally very difficult to define what an "individual" is in a coral (see, for instance, papers in Boardman et al., 1973). Thus, a strict distinction between "parasite" and "predator" be- comes meaningless. Is an animal which regularly crops some polyps from a coral head, but does not kill the entire head, a parasite or a predator? This debate is best exemplified in studies of the two prosobranch gastropod families Corallio- philidae and Architectonicidae. Coralliophilids are snails presumably related to the muricids which live either next to or buried in living corals. The precise food and method of feeding are not known for most species. Ward (1965) found mucus, nematocysts and zooxan- thellae in the gut of Coralliophila abbreviata which, like other members of the genus, lives in permanent sites immediately adjacent to the living portions of scleractinians. Ward maintains that C. abbreviata contributes to the weakening and destruction of Montipora colonies in Barbados, while Robertson (1970a) suggests that all coral- liophilids are, " . . . well adapted parasites, injuring their hosts slightly." Yonge (1974) says, however, "There is no question of parasitism, feeding is by way of a delicate proboscis which probably seizes animal matter carried by cilia over the surface of the coral." It should be added at this point that simple analysis of gut contents of coral associated animals may not always indicate what their primary food source is. This is true for a variety of reasons, among which are: (1) coral tissue is generally soft and when masticated by teeth or radulae and partially digested by enzymes it is extremely difficult to identify (see Bosch, 1965, for instance); (2) corals are pro- bably constantly sloughing off moribund zooxanthellae and discharged nematocysts which will likely be carried off in the mucus sheets; and, (3) coral mucus alone may provide a food source for a number of marine organisms (Clausade, 1971; Knudsen,

  3. Vol. 12. June 1976 135 1967; Patton, 1972; Richman, 1973). A gut filled with unidentified material, nematocysts and zooxanthellae might thus simply result from a coral mucus diet. Magi/us and Leptoconchus, two other coralliophilid genera, live embedded in Jiving corals such as Goniastraea, Acropora and the hydrocoral Millepora. Their protoconchs are deeply buried in the coral skeleton and the snails live in tubes extending to the surface of the coral colony. What they eat and how they obtain it are yet unknown. The Architectonicidae are mesogastropods presumed to be related to the cerithiids. They live among and feed on scleractinians and zoanthids, exhibiting a high degree of prey-species specificity. Robertson (1967) and Robertson et al. (1970) have summarized most of the available information on interactions between architectonicid snails and their coral hosts. The results indicate that neither Heliacus, which feeds on zoanthids, nor Philippia, different species of which feed on zoanthids or the stony coral Porites, kill off their host colonies. The motility of the architectonicid snails is sufficient to allow their movement from coral colony to coral colony should they be "complete" predators. Life cycle studies become particularly interesting in regard to such specialized predators as the coralliophilids and architectonicids. Robertson (1964), Robertson et al. (1970) and Scheltema (1971) have established that architectonicids have very long-term pelagic larvae, probably approaching six months for some species. Schel- tema (1971) has, in fact, traced potential trans-Atlantic dispersal in Philippia krebsii. With such long larval periods and great potential displacement, it would seem critical that such species be able to locate a requisite prey as they near the end of their larval period. Robertson et al. (1970), however, claimed that larvae of Philippia radiata will settle readily in clean dishes and then quickly attain a state of "arrested growth" which was interpreted as a "searching phase," during which the appropriate prey is found. Contrary indications are present in data obtained in my laboratory in Hawaii by Dale B. Bonar, a former graduate student here. Study- ing larvae of P. radiata taken from near-shore plankton hauls off Oahu, Hawaii, Bonar found that metamorphosis occurred much more readily in the presence of living Porites. Nine out of ten larvae placed in bowls with living Porites lobata had metamorphosed within two days; not until seven days in culture did larvae without coral begin to metamorphose. Bonar found, in addition, that growth of the teleoconch was strictly dependent on the presence of coral and that culture conditions were strongly influential in determining metamorphosis. Larvae with teleoconch diameters of 1.68-1.70 mm would metamorphose but never grow; larvae with teleoconchs ranging from 1. 70 to a maximum 1. 77 mm did demonstrate teleoconch growth in the presence of living coral. One animal, reared successfully · in the lab, began laying eggs at a shell diameter of 7.2 mm less than three months after it had metamorphosed. Other common predators of corals and sea anemones include the wentletraps or epitoniid snails. An Hawaiian species, Epitonium ulu, lives on and eats the solitary scleractinian Fungia scutaria. E. ulu was briefly discussed by Bosch (1965),

  4. Micronesica 136 who reported a very rapid growth rate from settling to reproductive size (1.65 cm) in two to three weeks. Eric Guinther of the Hawaiian Institute of Marine Biology has made other interesting observations on E. ulu (personal communication). He notes that the snails apparently never crawl directly on the flesh of the coral, but rather move about tl1e inverted basal area of the coral on a grid of secreted mucous strands which are cemented to the coral skeleton. Small tissue lesions occur on infested Fungia, and E. ulu guts contain zooxanthellae, nematocysts and pink tissue, indicating that predation (parasitism?) does occur (Bosch, 1965). Other prosobranch coral predators have been reported among diverse groups, including two species of the muricid genus Drupa (subgenus Drupe/la), summarized by Robertson (1970a), and the archaeogastropod Calliostoma javanicum. The latter species has been reported to feed on the stony corals Mussa and Agaricia (Glynn, 1973, cites a Yale University doctoral thesis by J. Lang as a source of this information). This observation provides an interesting example of a trochid gastropod feeding in a carnivorous manner. The group is predominantly herbivo- rous; could C. javanicum be living on the zooxanthellae alone? (See addendum). A final prosobranch group which lives entirely as predators or symbionts of hard and soft corals is the mesogastropod family Ovulidae. Most of the species in this family feed on octocorals, but some are specialized to live on scleractinians and hydrocorals. The degree to which ovulids utilize the cnidarian substrates for food is variable. Thus, Simnia spelta eats away the flesh of its host, the gorgonian Eunice/la stricta, and incorporates the gorgonian pigment into its own shell (Theodor, 1967). Neosimnia implicata apparently harms its host, Leptogorgia, very little, eating instead the mucus secreted by the gorgonian and the organic materials trap- ped in the mucus (Patton, 1972). Cyphoma gibbosum is known to eat the flesh of Plexaura homomalla, Gorgonia sp., and other gorgonians in the Caribbean (Kinzie, 1970, 1974). There are fascinating details available in the literature concerning the mimicry of ovulids with their various hosts (Adams, 1968; Fox and Wilkie, 1970; Patton, 1972; Theodor, 1967; Thiriot-Quievreux, 1967). A very important group of cnidarivores is found in the gastropod subclass Nudibranchia. At least one family, the Tritoniidae, are specialists for preying on Alcyonacea, Gorgonacea, Madreporaria and hydrocorals. eats Alcyonium digitatum in British waters (Rees, 1967), and T. bayeri has been found feeding on Briareum asbestinum and Pseudopterogorgia sp. in Florida (Marcus and Marcus, 1967). Several aeolid species also eat various reef coelenterates, among them are the Hawaiian Pteraeolidia ianthina which lives on, mimics and probably eats the octocoral Sarcothelia edmondsoni, and two species of the genus Phestilla which feed on Scleractinia. Phestilla sibogae which devours Porites compressa has been under investigation in my laboratory in Hawaii for the past five years (Hadfield and Karlson, 1969; Hadfield, 1972; Bonar arid Hadfield, 1974). This species is highly adapted to life on a specific prey; it lives upon the coral, eats it, and lays its eggs on bared parts of the coral skeleton. Larvae of P. sibogae are Tritonia hombergi

  5. Vol. 12. June 1976 137 induced to settle and complete their metamporphosis into young nudibranchs by a substance released from the coral into sea water. The only non-gastropod molluscs which are known to live as predators or parasites of hard and soft corals are the neomeniomorph aplacophorans. Salvini- Plawen (1972) has summarized the available knowledge concerning solenogastre- cnidarian associations. Most such associations involve gorgonians or alcyonaceans, the cnidarians serving as both substratum and prey for the neomeniomorphs. Few of these associations have been reported from shallow tropical waters. (Il) Molluscs Which Bore into Corals. Members of this group do not, in general, feed on the coral into which they bore. Rather, they use the living coral skeleton as a growing refuge and they take their food by filtration from the overlying sea. Their deleterious effects thus will be restricted to weakening the coral skeleton and competing with the corals for suspended food. Most molluscan representatives in this category are bivalves, although some of the coralliophilid gastropods may have similar habits. Most boring bivalves are found to belong to the family Mytilidae. Gohar and Soliman (1963a) list three species of the genus Lithophaga which they found infesting living madreporarians in the Red Sea. Gerlach (1961) found Lithodomus sp. boring into live con1l in the Maldive Islands, and a series of papers by Gareau et al. (1969, 1970, 1972) has provided a very comprehensive picture of the biology of Fungiacava eilatensis, a mytilid which lives commensally with species of Fungia. Gohar and Soliman (1963a, 1963b) and Soliman (1969) have raised the very interesting point that boring bivalves and gastropods which inhabit living coral face a very different problem from those molluscs which bore into non-living substrata; namely, they must continually bore outward, not inward, in order to escape being sealed off in their burrows by growth of the coral. Fungiacava is indeed an interesting animal. Totally committed to its com- mensal existence, it occupies burrows in living fungiids in only very restricted locali- ties, principally in the northern Gulf of Eilat (Gareau et al., 1969). The relation- ship between mollusc and coral has been clearly established by the studies men- tioned above. The mollusc lives within the coral skeleton and its opening to the outer world is via the coelenteron of the coral. The bivalve extends its siphons into the coelenteron of the coral to collect detrital material, phytoplankton, and exuded zooxanthellae for its own nutrition (Gareau et al., 1970). Another bivalve which lives in craters which it excavates in living coral is the pectinacean Pedum spondyloideum. Yonge (1967) reports that Pedum attaches with byssus to living coral when young and becomes progressively encased as the coral grows. Pedum, like the Lithophaga species mentioned above, is a filter feeder. The tridacnid clams form a more-or-less continuous series extending from forms which are found lying about on the reef flat (Hippopus hippous), to others which nestle amongst living coral (Tridacna maxima, T. fossor), and finally, to Tridacna crocea which is frequently found buried in living heads of Porites and other massive corals (Yonge, 1936; Otter, 1937). T. crocea bores mechanically by

  6. ... w 00 Table 1. Molluscs Associated with Living Tropical Corals* Mollusc "Host" Nature of Association Locale Source Gastropoda Prosobranchia Archaeogastropoda Trochidae 1. Calliostoma javanicum Mus,a angulosa (S) & Agaricia spp. (S) Lang, 1970; cited by Glynn, 1973 Predatory; produces small lesions on coral Caribbean Mesogastropoda Cerithiacea Architectonicidae 2. Architectonica perspectiva 3. Heliacus bicanaliculatus 4. H. cy/indricus Seychelles Gulf of California Bahamas British Honduras Netherlands Antilles Hawaii Hawaii Hawaii Maldives Hawaii Hawaii Taylor, 1968 Robertson, 1967 "zoanthids" (Z) Zoanthus danai (Z) Palythoa caribaeorum (Z) P. mammillosa (Z) Zoanthus pulchellus (Z) Palythoa vestitus (Z) Zoanthus confertus (Z) Zoanthus confertus (Z) Palythoa tuberculosa (Z) P. vestitus (Z) Palythoa vestitus (Z) & Zoanthus confertus (Z) Porites lobata (S) "Probably predatory" "symbiotic" ::: ~- 0 I; "' ;:;· I» Robertson, 1967 "symbiotic" Robertson, 1967 Robertson, 1967 Robertson, 1967 Robertson, 1967 Robertson, 1967 Robertson, 1967 "symbiotic" "symbiotic" "symbiotic" "symbiotic" "symbiotic" "symbiotic" 5. H. discoideus sterkii 6. H. implexus 7. H. mighelsi 8. H. trochoides 9. H. variegatus Robertson, 1970b; Robertson, et al, 1970 Hawaii Predatory 10. Phi/ippia radiata Ptenoglossa Epitoniidae (Scalidae) 11. Amaea sp. 12. Epitonium billeeana 13. Epitonium costulatum 14. E. ulu Robertson, 1965 Robertson, 1970a Roi:J.ertson, 1963, 1970a Bosch, 1965 Robertson, 1970a Robertson, 1965 Robertson, 1970a Maldives Gulf of California S. W. Philippines Hawaii "associated" "associated" "associated'' Predatory; produces lesions on coral "associated" "associated" Tubastraea aurea (S) Tubastraea tenuilame/losa (S) Fungia sp. (S) Fungia scutaria (S) Ceylon and Maldives Maldives Palythoa sp. (Z) Tubastraea aurea (S) 15. Epitonium sp. 1 16. Epitonium sp. 2

  7. Table 1. (continued) Cypraeacea Ovulidae "soft corals" (A?) "soft corals" (A?) gorgonians (G) Plexaura homomalla (G) Briareum asbestinum (G) "branching alcyonarians" (G?) stony corals (S) Sarcophyton (A) Leptogorgia virgulata (G) Allopora californica (H) Solenosmilia variabilis (S) "associated" "associated" Predatory Predatory Predatory Predatory Predatory Predatory "associated" ''associated" "associated" S. W. Ceylon S. W. Ceylon Puerto Rico West Indies Caribbean Puerto Rico Tropical Eastern Pacific D'Asaro, 1969 Tropical Pacific North Carolina California N. W. Cuba Robertson, 1965 Robertson, 1965 Ghiselin & Wilson, 1966 Kinzie, 1974 Ciereszko et al, 1974 Ghiselin & Wilson, 1966 17. Calpurnus lacteus 18. C. verrucosus 19. Cyphoma gibbosum 20. 21. 22. Ovula ovum 23. Neosimnia implicata 24. Pedicularia californica 25. Pedicularia decussata C. signatum Je1111eria pustulata Vicente, 1966; Yonge, 1974 Field, 1949 Fox & Wilkie, 1970 Dall, 1889; cited by Robertson, 1970a Hedley, 1903 and Berry, 1946; cited by Robertson, 1970a Rees, 1967 < - .... i:: ::, ~ Stylasterine hydrocorals (H), gorgonians (G), "madrepores" (S) 26. Pedicularia sp. !'-' "associated" ? CD - °' Alcyonium digitatum (A) & Eunicella verrucosa (G) Eunicella stricta (G) & Lophogorgia sarmeulosa (G) "associated" Britain 27. Simnia patula \C) --.I 28. S. spelta Predatory Mediterranean Theodor, 1967 Neogastropoda Muricacea Muricidae Porites sp. (S), Stylophora sp. (S) & Seriatopora sp. (S) Montipora spp. (S) Acropora sp. (S) Pocillopora sp. (S) Pocillopora sp. (S) & Porites compressa (S) 29. Drupa (Drupe/la) cornus "associated" Micronesia Demond, 1957 "on" "on" "on" Predatory Cocos-Keeling Island Cook Islands Maldives Hawaii Maes, 1967 Robertson, 1970a Robertson, 1970a Fankboner, cited by Robertson, 1970a - .... \C)

  8. - .p. 0 Table 1. (continued) ··Host" Mollusc Nature of Association Locale Source 30. Drupa (Drupe/la) rugosa Coralliophilidae 31. Coralliophila abbreviata "exclusively stony corals" (S) "associated" Demond, 1957 Micronesia Montastrea annularis (S) Acropora palmata (S) Diploria clivosa (S) Favia fragum (S) gorgonians (G) Acropora palmata (S) & Diploria clivosa (S) Acropora (S) & Montipora (S) Palythoa sp. (Z) Predatory "on" "on" "with" "associated" "associated" Ward, 1965 Robertson, 1970a Robertson, 1970a Robertson, 1970a Abbott, 1958 Robertson, 1970a West Indies Bahamas Bahamas British Honduras Bahamas Bahamas 32. C. caribaea 33. C. erosa 34. C. sugimotonis "lives on" "associated," presum- ably predatory "on" "on" "on" "on" "preferred" Cocos-Keeling Islands Ceylon & Maldives Maes, 1967 Robertson, 1965 35. C. violacea Porites (S) Porites (S) Porites (S) Porites (S) Porites (S), Poci/lopora (S), Stylophora (S), & Seratiopora (S) Porites (S), Pocillopora (S), Stylophora (S), & Seratiopora (S) Seriatopora (S) Pocillopora spp. (S) Pocillopora (S) Poci/lopora (S) Cocos-Keeling Micronesia Clipperton Island Maldive Islands W. Indian Ocean Maes, 1967 Demond, 1957 Hertlein & Allison, 1960 Robertson, 1970a Taylor, 1971 ~ r, ... 0 "' n~ Pl C, ,,,_ 36. C. costularis "preferred" W. Indian Ocean Taylor, 1971 37. Quoyula madreporarum "attached" "attached" "embedded in" "on branches and in clefts" Madagascar Cocos-Keeling Clipperton Island Maldives, New Caledonia, Fiji, Cook Islands, Pacific Mexico & Nicaragua Micronesia Maes, 1967, cited in Robertson, 1970a Hertlein & Allison, 1960 Robertson, 1970a Montipora (S), Pocillopora (S) & Sty/ophora (S) Pocillopora, Seriatopora, Stylophora, & Porites (all, S) Porites nigrescens (S) "large reef Alcyonacea of the western Pacific" (A) "with" Demond, 1957 . Taylor, 1968 Bayer, 1961; cited in Rees, 1967 38. Q. monodonta "with" Micronesia Demond, 1957 "with" "embedded in, with no communication to out- side" Seychelles 39. Rapa rapa W. Pacific

  9. Table 1. (continued) Opisthobranchia Nudibranchia Arminacea Arminidae 40. Armina sp. Pbyllididae 41. Phyllidia bourgini Dendronotacea Tritoniidae 42. Tritonia bayeri - "corals" (?) Predatory Salvini-Plawen, 1972 Madagascar Acropora (S) & millipores (H) Predatory Vicente, 1966 Biscayne Bay, Florida Briareum asbestinum (S) & Pseudopterogorgia sp. (S) Sarcothe/ia edmondsoni (A) Predatory Marcus & Marcus, 1967 Probably T. bayeri Predatory Hawaii R. Kinzie, personal communication Rees, 1967 Marcus & Marcus, 1967 Alcyonium digitatum (A) Gorgonacea (G) 43. T. hombergi 44. T. pickensii Predatory "on," probably preda- tory Predatory Predatory England Gulf of California -< ?-- - ..... i: ~ - 0\ !'-' 45. T. striata 46. T. wellsi Paralcyonium elegans (A) Leptogorgia virgulata (G) ? North Carolina Salvini-Plawen, 1972 Patton, 1972 Aeolidacea Cuthonidae \0 _, 47. Phestilla melanobrachia Tubastraea aurea (S) & Dendrophyllia (S) Porites compressa (S) Porites /obata & P. compressa (S) Predatory Hawaii, etc. Harris, 1971 Predatory Predatory Hawaii, etc. Hawaii, etc. Harris, 1971 personal observation 48. P. sibogae Pteraeolididae E. A. Kay, Univ. of Hawaii, personal communication personal observation Gohar & Abul-Ela, 1957 Sarcothe/ia edmondsoni (A) Predatory Hawaii 49. Pteraeolidia ianthina 50. 51. Phyllodesmium xeniae ? "small aeolid" Porites compressa (S) Xenia umbellata (A) & H eteroxenia fuscescens (A) Predatory Predatory Hawaii Red Sea Aplacophora Neomeniomorpha numerous species - octocorals (mainly G ?) Predatory see Salvini-Plawen, 1972 world wide ""' -

  10. - N Table 1. (continued) -I>- Mollusc "Host" Locale Source NaJure of Association Lamellibranchia Anisomyaria Mytilacea Mytilidae 52. Fungiacava eilatensis 53. Lithodomus sp. 54. Lithophaga lima 55. L. cumingiana 56. L. hanleyana Pteriacea Pteriidae 57. Electroma sp. 58. Pteria colymbus 59. Pteria sp. Pectinacea Pectinidae 60. Pedum spondyloideum Ostreacea Ostreidae 61. Ostrea sandvicensis Heterodonta Cardiacea Tridacnidae 62. Tridacna crocea Gulf of Eilat Maldive Island Red Sea Red Sea Red Sea Goreau et al, 1969 Gerlach, 1961 Gohar & Soliman, 1963a Gohar & Soliman, 1963a Gohar & Soliman, 1963a Fungia scutaria (S) live coral (S) Montipora lanuginosa (S) Stylophora f[abellata (S) Favia stelligera (S) & other spp. (S) Bores into skeleton Endo-symbiotic Bores into skeleton Bores into skeleton Bores into skeleton Kay & Switzer, 1974 Patton, 1972 Rees, 1967 Fanning Island North Carolina ? Acropora (S) Leptogorgia virgulata (S) antipatharians (Ap) Externally attached Attaches to Attaches to ~ Ef 0 t::l (1) "' o· p, Yonge, 1967 Porites sp. (S) Encased by coral growth New Britain Kay & Switzer, 1974 Acropora (S) & Stylophora (S) Fanning Island Attaches to Tropical Pacific Yonge, 1936; personal observations Porites (S) & other massive (S) spp. Boring in living skeleton Taxodonta Arcacea Arcidae 63. Barbatia decussata Fanning Island Kay & Switzer, 1974 Porites (S) Externally attached * Table 1 demonstrates, to the extent currently possible, which molluscs are associated with which cnidarian species or genera. The items listed under "Nature of Association", show most clearly how little is actually known about the nature of these associations. The letters fol- lowing the named cinidarians in the second column indicate to which cinidarian order each genus or species belongs, as follows: A, Alcyonacea; Ap, Antipatharia; G, Gorgonacea; H, Hydrocorallina; S, Scleratinia; Z, Zoanthinaria.

  11. Vol. 12. June 1976 143 the grinding action of the thickened shell hinge. Yonge (1936) maintains that this species never settles directly on iive coral, but it is frequently seen so surrounded by live coral that this might be questioned. (Ill) Molluscs Which Live Epizoically on Coral. Certain pteriid and ostreid bivalves are frequently found attached by their byssus to the surfaces of living hard or soft corals. Most notable are those species of Pteria which are almost invariably found attached to gorgonians and anti- patharians (Field, 1949; Rees, 1967; Patton, 1972). Patton reports that the byssal attachment of Pteria colymbus to the coenenchyme of Leptogorgia virgulata may cause the flesh of the gorgonian to fall away exposing the axial skeleton to fouling by the settlement of sessile organisms. Kay and Switzer (1974) report on three bivalve species which they found as- sociated with living stony corals at Fanning Island. Electroma sp. was associated with Acropora, Ostrea sandvicensis with Stylophora, and Barbatia decussata with Porites. Questions arise concerning the nature of these attached filter feeders and their "hosts," such as, are the relationships species-specific? The presumed advantage to the bivalve is that they select settling sites which are raised well above the rubble or sand surrounding the coral, a position assured by the elongate, branching cnidari- ans upon which they live. Vermetid gastropods, also filter feeders, are frequently seen growing on Indo- Pacific Scleractinia, but the relationship is not specific (Gerlach, 1961, and personal observations). (IV) Molluscs Which Serve as Substrata for Corals. While small coral colonies may be found on the shells of many molluscs, this category was constructed mainly to encompass the abundant vermetid gastropods which are found with their tubes projecting from coral heads throughout the tro- pical Pacific. The association appears rather non-specific, although in certain locales some species of corals are never seen without vermetids. For instance; most Porites lobata heads which I have observed in Hawaii contain the vermetid Petaloconchus keenae (Hadfield et al., 1972), and in Palau all of the Dendropoma maximum which I saw were buried in living Porites. A recent paper by Hughes and Lewis (1974) discusses other aspects of the biology of D. maximum. The im- portance of vermetid shells as settling sites for corals recolonizing areas such as those decimated by Acanthaster or pollution is potentially great. Carried to its logical conclusion, this category must include those symbioses wherein the mollusc serves as requisite host for coral. Such is the situation in the biology of the solitary corals Heteropsammia and Heterocyathus which always settle on the empty shells of certain snails. The shells of the snails are also used as refuges by the bivalve Jousseaumiella and the sipunculan Aspidosiphon (Bouvier, 1894; Bourne, 1906).

  12. 144 Micronesica CONCLUSIONS Altogether, I have summarized data on nearly 80 molluscan species which, in some manner, make their life on or in living corals or by eating them (Table 1). Trends are seen; certain groups are specialized coral carnivores, others use the growing skeleton for a refuge wherein they can grow and feed by filtration. Certain groups remain enigmatic in that their positive association with certain corals is known but the nature of their association is not. The fact that coral. mucus and the debris which it collects forms the major food for several species is important in the energy transfers which occur on coral reefs. Numerous questions arise in any discussion such as this one. Some of the more important ones are the following. How do settling larvae find the specific coral on which they will live and then survive the protective mechanisms of the coral? In fact, life cycle data are absent for nearly all of the species cited in this survey. What are the effects of the unusual and bizarre chemicals synthesized by corals on their molluscan associates (see Ciereszko and Karns, 1973)? Do they orient the molluscs in their specificity toward their prey/hosts? Do they repel certain molluscs from otherwise potential hosts? C. M. Yonge (1963) noted, "thanks no doubt to the presence of nematocysts, corals are little affected by predators." This seems hardly to be true in light of presently accumulating information. Not only do prosobranchs, nudibranchs and aplacophorans eat corals, but members of several other molluscan groups are capable of residing on the surfaces of coral. Much evidence is also accumulating about predation on corals by fish, echinoderms and polychaete worms. A leading ques- tion is, how are the nematocyst toxins avoided, both while the motile animal is crawling on the coral surface and during ingestion of coral flesh? Robertson (1963, 1970a, 1970b, 1970c), Salvini-Plawen (1972) and others suggest two primary answers. First, mucus must play a definite role in defense against nematocysts. It may act simply as a thickened, viscous cushion which the nematocyst threa~s either cannot penetrate or lose their penetrating velocity in passing through. Mucus may also have a specific neutralizing effect on the chemicals which compose nematocyst toxins. It has also been noted by the above-named authors that cuticular coverings or linings are present about the mouths and anterior digestive tracts of most cnidari- vores. These cuticular layers no doubt deflect the nematocyst threads and impede their penetration into susceptible tissues. Ward (1965) suggests that a salivary gland secretion "desensitizes" nematocysts ingested by Coralliophila abbreviata. As mentioned above, Epitonium ulu apparently never crawls directly on the flesh of its host Fungia scutaria but moves about it on a grid of mucous threads. An important and barely touched aspect of mollusc-coral associations is a truly ecological examination of them. Some associations are obviously so well established through long evolutionary time that they exist in all locales where potential hosts can exist; such is true of the gorgonian-ovulid associations. In many instances, however, the host may have a wide range of distribution while the molluscan predator/symbiont will occur with the host in only a few selected areas.

  13. Vol. 12. June 1976 145 The outstanding example here is the limited range of Fungiacava eilatensis as com- pared to that of its host Fungia scutaria (Goreau et al., 1969). Kay and Switzer (1974) have noted discontinuities in the distribution of molluscan species in the lagoon of Fanning Island. Interestingly, they list some of the bivalves which hang onto the branches of live corals as occurring with the corals in less turbid areas of the lagoon and being absent from the still-present "hosts" in the areas of cloudier water. In summary, I must admit to having barely touched the surface of the fascinat- ting assemblage which can be labelled, "Molluscs Associated with Living Tropical Corals." A major problem exists in assessing the true nature of most such associa- tions. This is partly reflected in confusing use of terms, although I see little value in arguing the meaning of "symbiont" vs. "commensal" vs. "associate" until much more information is available on the biological aspects of these associations. Let us hope that with the appearance of more and better tropical shore marine labora- tories, the true nature of these associations will be revealed and that, even more importantly, they will be placed into the larger picture of coral reef ecology, pro- ductivity, longevity and geology. Acknowledgments My sincere thanks and appreciation go to Dr. E. Alison Kay for her thoughtful discussions, the papers she made available and for allowing me the use of a type- script of a talk she gave to the Malacological Society of London. Dr. Robert A. Kinzie III read the manuscript and made numerous and valuable suggestions, as did Ms. Marilyn F. Dunlap; to both of them, my sincere thanks. Some of the studies referred to in this paper were supported by NSF Grant GB-36702. Travel expenses to attend the Guam-Palau symposium were partially paid from a fund provided to the Western Society of Naturalists by Dr. and Mrs. Henry Lee. REFERENCES CITED Abbott, R. T. 1958. The marine molluscs of Grand Cayman Island, British West Indies. Academy of Natural Sciences of Philadelphia Monograph 11, vii+138 p. Adams, R. O. 1968. The color variation of Neosimnia (Mollusca, Gastropoda) with notes on the natural history. Master of Science Thesis, Florida State University (ref. provided by R. A. Kinzie). Boardman, R. S., A.H. Cheetham, and W. A. Oliver, Jr. (eds.) 1973. Animal Colonies, Devel- opment and Function Through Time. Dowden, Hutchinson and Ross, Inc. Stroudsburg, Penn. 603 p. Bonar, D., and M. G. Hadfield. 1974. Metamorphosis of the marine gastropod Phestilla sibogae. I. Light and electron microscopic analysis of larval and metamorphic stages. J. Exp. Mar. Biol. Ecol. 16: 227-255. Bosch, H.F. 1965. A gastropod parasite of solitary corals in Hawaii. Pac. Sci. 19(2): 267- 268.

  14. Micronesica 146 Bourne, G. C. 1906. Report of Jousseaumia, a new genus of eulamellibranchs commensal with the corals Heterocyathus and Heteropsammia, collected by Professor Herdman in Ceylon. Rep. Pearl Oyster Fish. Ceylon 5: 243-266. Bouvier, M. E. L. 1894. A new instance of commensalism: Association of worms of the genus Aspidosiphon with madreporarian polyps and a bivalve mollusk. Ann. Mag. Nat. Hist. 14(6): 312-314. Ciereszko, L. S., and T. K. B. Karns. 1973. Biochemistry of coral reef coelenterates. In O. A. Jones and R. Endean (eds.), Biology and Geology of Coral Reefs. Vol. II. Biology I. Academic Press, p. 182-202. Cierezsko, L. S., P. A. Steudler, and F. J. Schmitz. 1974. The sterol composition in the study of predator-prey pairs of coral reef organisms. Two new marine sterols. Abstract of con- tributed papers, International Symposium on Inda-Pacific Tropical Reef Biology, June- July, 1974. Clausade, M. 1971. Colonisation d'un Milieu Alveolaire Recifal par la Faune Vagile: Intro- duction I'Etude Experimentale. Tethys, suppl. I : 137-140. D'Asaro, C. N. 1969. The egg capsules of Jenneria pustulata (Lightfoot, 1786) with notes on spawning in the laboratory. Veliger 11 : 182-184. Demond, J. 1957. Micronesian reef-associated gastropods. Pac. Sci. 11: 275-341. Field, L. R. 1949. Sea anemones ·and corals of Beaufort, North Carolina. Bull: Duke Univ. Mar. Stn., No. 5, 39 p. Fox, D. L., and D. W. Wilkie. 1970. Somatic and skeletally fixed carotenoids of the purple hydrocoral, Allopora ca!ifornica. Comp. Biochem. Physiol. 36: 49-60. Gerlach, S. A. 1961. The tropical coral reef as a biotope. Atoll Res. Bull. No. 80: 1-6. Ghiselin, M.T., and B. R. Wilson. 1966. On the anatomy, natural history, and reproduction of Cyphoma, a marine prosobranch gastropod. Bull. Mar. Sci. 16(1): 132-141. Glynn, P. W. 1973. Aspects of the ecology of coral reefs in the Western Atlantic region. In 0. A. Jones and R. Endean (eds.), Biology and Geology of Coral Reefs. Vol. II: Biology I. Academic Press, p. 271-324. Gohar, H. A. F., and I. A. Abut-Ela. 1957. On a new nudibranch (Phy!lodesmium xeniae). Publ. Mar. Biol. Stn. Al Ghardaqa 9: 131-144. Gohar, H. A. F., and G. N. Soliman. 1963a. On three mytilid species boring in living corals. Pub!. Mar. Biol. Stn. Al Ghardaqa 12: 65-98. ----. 1963b. On the biology of three coralliophilids boring in living corals. Pub!. Mar. Biol. Stn. Al Ghardaqa 12: 99-126. Goreau, T. F., N. I. Goreau, T. Soot-Ryen, and C. M. Yonge. 1969. On a new commensal mytilid (Mollusca: Bivalvia) opening into the coelenteron of Fungia scutaria (Coelenterata). J. Zoo!., Lond. 158: 171-195. Goreau, T. F., N. I. Goreau, C. M. Yonge, and Y. Neumann. 1970. On feeding and nutrition in Fungiacava eilatensis (Bivalvia, Mytilidae), a commensal living in fungiid corals. J. Zoo!., Land. 160: 159-172. Goreau, T. F., N. I. Goreau, and C. M. Yonge. 1972. On the mode of boring in Fungiacava eilatensis (Bivalvia: Mytilidae). J. Zoo!., Lond. 166: 55-60. Graham, A. 1955. Molluscan diets. Proc. Malac. Soc. Land. 31: 144-159. Hadfield, M. G. 1972. Flexibility in larval life patterns. Amer. Zoo!. 12(4): 72L Hadfield, M. G., and R.H. Karlson. 1969. Externally induced metamorphosis in a marine gastropod. Amer. Zoo!. 9(4): 1122. Hadfield, M. G., E. A. Kay, M. U. Gillette, and M. C. Lloyd. 1972. The Vermetidae (Mollusca: Gastropoda) of the Hawaiian Islands. Mar. Biol. 12(1): 81-98. Harris, L. G. 1971. Nudibranch associations as symbioses. In T. C. Cheng (ed.), Aspects of the Biology of Symbiosis. University Park Press, p. 77-90. Hertlein, L. G., and E. C. Allison. 1960. Gastropods from Clipperton Island. Veliger 3: 13-16. ,,

  15. Vol. 12. June 1976 147 l{ughes, R. N., and A.H. Lewis. 1974. On the spatial distribution, feeding and reproduction of the vermetid gastropod Dendropoma maximum. J. Zool., Lond. 172: 531-547. Kay, E. A., and M. F. Switzer. 1974. Molluscan distribution patterns in Fanning Island Lagoon and a comparison of the mollusks of the lagoon and the seaward reets. Pac. Sci. 28(3): 275-295. Kinzie, R. A. m. 1970. The ecology of the gorgonians (Cnidaria: Octocorallia) of Discovery Bay, Jamaica. Ph.D. thesis, Yale University. Part II, 37 p. - · 1974. Plexaura homomalla: the biology and ecology of a harvestable marine resource. In F. M. Bayer and A. J. Weinheimer (eds.), Prostaglandins from Plexaura homomalla: Ecology, Utilization and Conservation of a Major Medical Marine Resource. Studies in Tropical Oceanography No. 12, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami. University of Miami Press, Coral Gables, Florida. p. 22-38. Knudsen, J. W. 1967. Trapezia and Tetralia (Decapoda, Brachyura, Xanthidae) as obligate ectoparasites of pocilloporid and acroporid corals.. Pac. Sci. 21: 51-57. Maes, V. O. 1967. The littoral marine molluscs of Cocos-Keeling Islands (Indian Ocean). Proc. Acad. Nat. Sci. Philadelphia, 119: 93-217. Marcus, E., and E. Marcus. 1967. American Opisthobranch Mollusks. Studies in Tropical Oceanography. No. 6. Institute of Marine Sciences. University of Miami. 256 p. Otter, G. W. 1937. Rock-destroying organisms in relation to coral reefs. Scient. Rep. Gt. Barrier Reef Exped., 1928-29, 1(12): 323-352. Patton, W. K. 1972. Studies on the animal symbionts of the gorgonian coral, Leptogorgia virgu- lata (Lamarck). Bull. Mar. Sci. 22(2): 419-431. Rees, W. J. 1967. A brief survey of the symbiotic associations of Cnidaria with Mollusca. Proc. Malac. Soc. Lond. 37: 213-231. Richman, S. 1973. The rate of mucus production by corals and its significance as an energy source for coral reef copepods. Abstracts of Papers, 36th Ann. Meet. Am. Soc. Limn. and Ocean., Inc., Salt Lake City, Utah. June 11-14, 1973. Robertson, R. 1963. Wentletraps (Epitoniidae) feeding on sea anemones and corals. Proc. Malac. Soc. Lond. 35(2 and 3): 51-63. ---. 1964. Dispersal and wastage of larval Philippia krebsii (Gastropoda: Architectoni- cidae) in the North Atlantic. Proc. Acad. Nat. Sci. Philadelphia 116(1): 1-27. ---. 1965. Coelenterate-associated prosobranch gastropods. Annual Reports for 1965 of the American Malacological Union. p. 6-8. ---. 1967. Heliacus (Gastropoda: Architectonicidae) symbiotic with zoanthiniaria (Coel- enterata). Science 156(3772): 246-248. ---. 1970a. Review of the predators and parasites of stony corals, with special reference to symbiotic prosobranch gastropods. Pac. Sci. 24(1): 43-54. ---. 1970b. The feeding, larval dispersal, and metamorphosis of Philippia (Gastropoda: Architectonicidae). Pac. Sci. 24(1): 55-65. 1970c. Systematics of Indo-Pacific Philippia (Psi/axis), architectonicid gastropods with eggs and young in the umbilicus. Pac. Sci. 24(1): 66-83. Robertson, R., R. S. Scheltema, and F. W. Adams. 1970. The feeding, larval dispersal, and meta- morphosis of Philippia (Gastropoda: Architectonicidae). Pac. Sci. 24(1): 55-65. Salvini-Plawen, L. V. 1972. Cnidaria as food sources for marine invertebrates. Cah. Biol. Mar. 13: 385-400. Scheltema, R. S. 1971. Larval dispersal as a means of genetic exchange between geographically separated populations of shallow-water benthic marine gastropods. Biol. Bull. 140(2): 284-322. Soliman, G. N. 1969. Ecological aspects of some coral-boring gastropods and bivalves of the Northwestern Red Sea. Am. Zoo!. 9: 887-894. Taylor, J. D. 1968. Coral reef and associated invertebrate communities (mainly molluscan) around Mahe, Seychelles. Phil. Trans. Roy. Soc. Lond. (B) 254: 129-206. ---. 1971. Reef associated molluscan assemblages in the Western Indian Ocean. Syrop.

  16. 148 Micronesica Zoo!. Soc. Lond. 28: 501-534. Theodor, J. 1967. Contribution a l'etude des Gorgones (VI): la denudation des branches de gorgones par des mollusques predateurs. Vie et Milieu (A) 18: 73-78. Thiriot-Quievreux, C. 1967. Observations sur le developpement larvaire et postlarvaire de Simnia spelta Linne (Gasteropode: Cypraeidae). Vie et Milieu (A) 18: 143-151. Vicente, N. 1966. Contribution a l'etude des gasteropodes opisthobranches de la region de Tulear. Recueil des Travaux, Station Marine Endoume-Marseille, suppl. 5(3): 87-131. Ward, J. 1965. The digestive tract and its relation to feeding habits in the stenoglossan proso- branch Coralliophila abbreviata (Lamark). Canad. J. Zoo!. 43: 447-464. , Yonge, C. M. 1936. Mode of life, feeding, digestion and symbiosis with zooxanthellae in the Tridacnidae. Scient. Rep. Gt. Barrier Reef Exped., 1928-29, 1: 283-321. ---. 1963. The biology of coral reefs. In F. S. Russell (ed.), Advances in Marine Biology. Volume 1. Academic Press, N.Y. p. 209-260. ---. 1967. Observations on Pedum spondyloideum (Chemnitz) Gmelin, a scallop associated with reef-building corals. Proc. Malac. Soc. Lond. 37: 311-323. ---. 1974. Coral reefs and molluscs. Trans. Roy. Soc. Edinburgh 69(7): 147-166. ADDENDUM Alan C. Miller [1972. "Observations on the associations and feeding of six species of prosobranch gastropods on anthozoans in Discovery Bay, Jamaica." The Echo (Western Malacological Society). 5: 35-36.] reports undigested zooxan- thellae in feces of Calliostoma javanicum which had been feeding on coral and Frank E. Perron [1975. "Carnivorous Calliostoma from the northeastern Pacific." The Veliger. 18: 52-54.] notes that several other Calliostoma species feed on hy- droids. I must agree with Perron that members of this genus are predators.