Tuatara: Volume 22, Issue 3, February 1977

Predators of Sea Anemones

Predators of Sea Anemones

Abstract

A review is presented of literature concerning invertebrate and some vertebrate predators of sea anemones. Several previously unpublished records for New Zealand are given.

Introduction

Invertebrates, particularly the nudibranch Aeolidia papillosa (Boutan, 1898; Fleure and Walton, 1907), pycnogonids (Stephenson, 1928) and starfish (Verwey, 1930), have long been regarded as important or potentially important predators of sea anemones, and actual records are not uncommon for northern hemisphere species (Tables 1, 2).

There appears to be only one previously published record of an invertebrate preying on an anemone in the New Zealand and Australian region, and a few records for vertebrate predators (Table 3). This review therefore aims to encourage more records for these two countries.

Discussion

As predators of sea anemones, Stephenson (1928) cited ‘various fishes, crabs and other crustacea, nudibranchs, starfish, the larger worms [and] pycnogonids’. The relative importance of these predators is still difficult to assess, because of a lack of detailed field studies.

Aeolids have been the most frequently observed predators (Table 1), and Stephenson (1928) thought that these molluscs ‘are no doubt responsible for a good deal of damage’ to actinians in the wild. Fleure and Walton (1907) considered Aeolidia papillosa to be ‘the most formidable enemy sea-anemones possess’, and Harris (1971) suggested that seasonal fluctuations in the numbers of A. papillosa could influence the distribution patterns of its prey, Metridium senile. Certainly, this particular nudibranch exhibits a distinct preference for actinian species such as Actinia equina and Anthopleura elegantissima (Miller, 1961; Waters, 1973; Edmunds, Potts, Swinfen and Waters, 1975), to which it is attracted from some distance (Stehouwer, 1952; Braams and Geelen, 1953), but many more in situ studies, such as Wobber's (1970) observations of Dendronotus iris feeding on Cerianthus sp., are still needed.

The opisthobranch genus Aeolidia is poorly represented in the southern hemisphere, and apparently not at all in Australia or New Zealand (Robson, 1966); however, one might still expect to find a similar invertebrate predator filling the equivalent ecological niche. To date such predators have been largely undetected in this region, and little is known about the food sources of carnivorous opistho-branchs

Table 1. Records of Predation on Anthozoans by Aeolids in the Northern Hemisphere
PREY PREDATOR AUTHORITIES
Actinia equina Aeolidia papillosa Boutan(1898); Stephenson (1928); Braams and Geelen (1953); den Hartog (1961); Miller (1961); Swennen (1961); Bruce, Colman and Jones (1963); Thompson (1964); Edmunds et al. (1974)
Aeolidiella sanguinea Tardy (1969)
Spurilla neapolitana Salvini-Plawen (1972)
Actinia sp. Aeolidia papillosa Fleure and Walton (1907); Eliot (1910)
Actinothoe anguicoma Aeolidiella glauca Tardy (1969)
Aeolidiella sanguinea Tardy (1969)
Aiptasia mutabilis Spurilla neapolitana Salvini-Plawen (1972)
Anemonia sulcata Aeolidia papillosa Miller (1961); Edmunds et al. (1974)
Spurilla neapolitana Salvini-Plawen (1972)
Anthea sp. Aeolidia papillosa Fleure and Wilton (1907); Eliot (1910)
Anthopleura artemisia Aeolidia papillosa Waters (1973)
Anthopleura elegantissima Aeolidia papillosa Francis (1973); Waters (1973); Edmunds et al. (1974)
Hermissenda crassicornis Francis (1973)
Anthopleura nigrescens Herviella sp. nov. Rosin (1969)
Anthopleura xanthogrammica Aeolidia papillosa Waters (1973)
Bunodeopsis sp. Spurilla neapolitana Salvini-Plawen (1972)
Calliactis effoeta Aeolidia papillosa Boutan (1898)
Cerianthus sp. Dendronotus iris Wobber (1970)
Cereus pedunculatus Aeolidia papillosa Boutan (1898); Tardy (1965)
Aeolidiella alderi Tardy (1969)
Aeolidiella glauca Tardy (1965)
Aeolidiella sanguinea Tardy (1965, 1969)
Cerberilla bernadetti Tardy (1965)
Diadumene cincta Aeolidia papillosa Swennen (1961); Tardy (1965)
Aeolidiella alderi Tardy (1969)
Aeolidiella glauca Tardy (1965)
Aeolidiella sanguinea Tardy (1965, 1969)
Cerberilla bernadetti Tardy (1965)
Diadumene luciae Aeolidia papillosa Waters (1973)
Epiactis prolifera Aeolidia papillosa Waters (1973)
Metridium marginatum Aeolidia papillosa Russell (1942)
Metridium senile Aeolidia papillosa Stehouwer (1952); Braams and Geelen (1953); Swennen (1961); Wolter (1967); Harris (1971)
Sagartia elegans Aeolidiella glauca Miller (1961); Bruce, Colman and Jones (1963)
Sagartia troglodytes Aeolidia papillosa Miller (1961); Swennen (1961); Tardy (1965)
Aeolidiella glauca Tardy (1965, 1969)
Aeolidiella sanguinea Tardy (1965, 1969)
Cerberilla bernadetti Tardy (1965)
Sagartia sp. Aeolidiella takanosimensis Salvini-Plawen (1972)
Berghia coerulescens Salvini-Plawen (1972)
Stomphia coccinea Aeolidia papillosa Robson (1961)
Aeolidia glauca Miller (1961)
Tealia coriacea Aeolidia papillosa Waters (1973)
Tealia crassicornis Aeolidia papillosa McMillan (1942); Waters (1973)
Tealia felina Aeolidia papillosa Miller (1961); Swennen (1961)
Table 2. Other Records of Predation on Anthozoans in the Northern Hemisphere *
Prey Predator Authorities
Actinia equina Nymphon gracile (Pycnogonida: Nymphonidae) Wyer and King (1974)
Pycnogonum littorale (Pycnogonida: Pycnogonidae) Bruce, Colman and Jones (1963); Myer and Buckmann (1963); Wyer and King (1974)
Anemonia sulcata Pycnogonum littorale Wyer and King (1974)
Anthopleura elegantissima Calliostoma annulatum (Gastropoda: Trochidae) Francis (1973)
Dermasterias imbricata (Asteroidea: Poraniidae) Mauzey, Birkeland and Dayton (1968)
Epitonium sp. (Gastropoda: Epitoniidae) Francis (1973)
Patiria miniata (Asteroidea: Asterinidae) Francis (1973)
Pycnogonum stearnsi (Pycnogonida: Pycnogonidae) Fry (1965)
Anthopleura xanthogrammica Dermasterias imbricata Mauzey et al. (1968)
Pycnogonum stearnsi Fry (1965)
Calliactis parasitica Crossaster papposus (Asteroidea: Solasteridae) Milligan (1916)
Pycnogonum littorale Wyer and King (1974)
Diadumene sp. Crossaster papposus Hancock (1958)
Edwardsia sp. Platichthys flesus (Pisces: Pleuronectidae) McIntosh (1874)
Epiactis prolifera Dermasterias imbricata Mauzey et al. (1968)
Metridium senile Dermasterias imbricata Mauzey et al. (1968)
Gephyreaster swifti (Asteroidea: Radiasteridae) Mauzey et al. (1968)
Hippasteria spinosa (Asteroidea: Goniasteridae) Mauzey et al. (1968)
Pycnogonum littorale Myer and Buckmann (1963)
Peachia hastata Gadus callarias (Pisces: Gadidae) McIntosh (1874)
Stoichactis helianthus Hermodice carunculata (Polychaeta: Amphinomidae) Lizama and Blanquet (1975)
Stoichactis sp. Acanthaster echinites (Asteroidea: Acanthasteridae) Verwey (1930)
Amphiprion polymnus (Pisces: Pomacentridae) Verwey (1930)
Premnas biaculateus (Pisces: Pomacentridae) Verwey (1930)
Stomphia coccinea Crossaster papposus Mauzey et al. (1968)
Gephyreaster swiftiMauzey et al. (1968)
Tealia coriacea Dermasterias imbricata Mauzey et al. (1968)
Table 3. Records of Predation on Anthozoans in New Zealand
PREY PREDATOR AUTHORITIES
Anthopleura sp. Rhombosolea plebeia (Pisces: Rhombosoleidae) Webb (1973)
Actinia tenebrosa Haustrum haustorium (Gastropoda: Thaisidae) Author's observation
Pleurobranchaea novaezelandiae (Gastropoda: Pleurobranchidae) Ottaway (1977)
Calliactis conchicola Emissola antarctica (Selachii: Galeidae) Author's observation
Cricophorus nutrix Baeolidia major (Gastropoda: Aeolidiidae) Morton and Miller (1968)
Paracalliactis rosea Other anthozoans (unidentified) Emissola antarctica Author's observation
Cheilodactylus macropterus (Pisces: Cheilodactylidae) Godfriaux (1974)
Chrysophrys auratus (Pisces: Sparidae) Godfriaux (1970)
Notothenia microlepidota (Pisces: Nototheniidae) Graham (1939)
Parapercis colias (Pisces: Parapercidae) Graham (1939)
Peltorhampus novaezelandiae (Pisces: Rhombosoleidae) Webb (1973)
Rhombosolea leporina (Pisces: Rhombosoleidae) Webb (1973)
Sphaeroides richei (Pisces: Tetraodontidae) Webb (1973)

here. The note of Morton and Moller (1968), that the aeolid Baeolidia major preys on the anemone Cricophorus nutrix, may have been the first published record of predation on a sea anemone by an invertebrate for these two countries, even though there are over 40 known anthozoan species in New Zealand alone (Parry, 1951). Recently Ottaway (1977) observed that Pleurobranchaea novaezelandiae readily ate the common Actinia tenebrosa during laboratory experiments. A similar opisthobranch, Pleurobranchaea maculata, occurs in Australia, and is known to be ‘a voracious predator of smaller shell-less opisthobranchs’ (Burn, 1966). There is a possibility that P. maculata might also eat anemones.

Few other molluscs have been reported as predators of anemones (Tables 2, 3). Francis (1973) recorded Calliostoma annulatum and Epitonium sp. as predators of Anthopleura elegantissima, but gave no indication of their effect on populations. Fleure and Walton (1907) ‘once noticed Trochus ziziphinus nibbling at the base of an anemone’, and on two occasions I observed Haustrum haustorium to partially eat juvenile Actinia tenebrosa. The two juveniles died as a consequence of the attacks, but it seems unlikely that predation by Haustrum would have any marked effect on Actinia populations.

The polychaete worm Hermodice carunculata is known to be an active predator of Stoichactis helianthus. After a single Hermodice starts feeding on Stoichactis, other worms are attracted to feed on the same anemone. Although it is not known whether the anemones die following such attacks, Hermodice could still affect the local distribution of Stoichactis (Lizama and Blanquet, 1975). A similar situation might exist for pycnogonids. Even though Fry (1965) considered actinians to be the major food source of Pycnogonum stearnsi, it is not known whether predation by sea-spiders would actually kill adult anemones. Stephenson (1928), however, observed that ‘serious results may ensue from such attacks on young or small anemones’, so there is still the possibility that pycnogonids could influence the distribution of some actinian species.

Some starfish are considered to be omnivorous (Feder and Christensen, 1966) and have been observed to eat anemones in an aquarium (Milligan, 1916) and in the sea (Table 2). Verwey (1930) believed that Acanthaster echinites was ‘probably one of the worst enemies of anemones’; however, the first unequivocal indication that actinians can be a significant part of the diet of some asteroids came from the extensive in situ observations of Mauzey, Birkeland and Dayton (1968). They found that, in some habitats, Dermasterias imbricata fed mainly on Epiactis prolifera, and occasionally on Anthopleura xanthogrammica, A. elegantissima, Tealia coriacea and Metridium senile. Other starfish were also seen to eat anemones (Table 2).

Most known vertebrate predators are fish. Over a century ago Peachia hastata had been discovered in cod stomachs, and ‘swarms’ of an Edwardsia species in flounder stomachs (McIntosh, 1874). Even within symbiotic relationships, damselfish sometimes eat the tentacles of their host anemone, Stoichactis (Verwey, 1930). Several New Zealand fish species ingest anemones (Table 3), although from the two detailed records it seems likely that the anemones may have been ingested incidentally along with other prey. Webb (1973) found that an Anthopleura species constituted up to 4.8% of the gut contents of the sand flounder Rhombosolea plebeia, but the cockle Chione stutchburyi is a significant part of the diet of this flounder, and where the study was done Anthopleura aureoradiata is commonly found attached to the cockle (Parry, 1951). Similarly, 40 Calliactis conchicola and several Paracalliactis rosea were seen in the gut contents of 12 gummy sharks, Emmissola antarctica (= Mustelus antarcticus), caught in 100m of water offshore from Kaikoura (Ottaway, personal observation). At Kaikoura, both anemones are epizoic on the carapaces of the spider crab, Leptomithrax longipipes, and C. conchicola is also found on living whelks, Austrofusus glans, and whelk shells occupied by hermit crabs (Hand, 1975). Every anemone found eaten by the gummy sharks was attached to Leptomithrax, but there were Leptomithrax present in the stomachs that did not bear anemones. Since there were no whelks or hermit crabs ingested, with or without anemones, it seems that the sharks were preying on Leptomithrax rather than the anemones.

Other vertebrate predators seem to be few. At one time the French collected anemones and sold them in Bordeaux markets (Rondeletius, quoted in Johnstone, 1846, p. 227). Dicquemare (1773) actually carried out cautious experiments on the toxicity of cooked actinians, feeding them to his cat and himself. He apparently satisfied himself that some species, especially Tealia crassicornis, were palatable, because later he wrote (Dicquemare, 1775): ‘De toutes les efpeces d'anémones de mer, celle-ci m'a paru devoir mériter la préférence pour la table. Lorfqu'on les a fait bouillir un peu fermes, et qu'on les fert pour manger à quelle fauffe on juge àpropos, …’ Even so, Johnston (1846) had reservations about Dicquemare's opinion: ‘The mouth waters at the liquorish description, … but I have not been tempted to test its truth.’ More recently, Martin (1960) reported that cooked Rhodactis howesii was commonly eaten by Samoans, although fatal cases of poisoning were known to occur amongst those natives who had eaten the anemone raw.

Acknowledgements

I am indebted to Dr W. C. Clark, Professor G. A. Knox, Professor M. C. Miller and Mr R. C. Willan for their comments and constructive criticisms of the manuscript at various stages of preparation.

This work was supported by a New Zealand Commonwealth Postgraduate Award.

References

Boutan, L., 1898: Moeurs de l' Eolis papillosa Linné. Archives de zoologie expérimentale et générale Series 3, 6: 28.

Braams, W. G., and Geelen, F. M., 1953: The preference of some nudibranchs for certain coelenterates. Archives néerlandaises de zoologie 10: 241-164.

Bruce, J. R., Colman, J. S., and Jones, N. S. (Editors), 1963: ‘Marine Fauna of the Isle of Man’. Liverpool University Press, Liverpool. 307 pp.

Burn, R., 1966: Port Phillip Survey 1957-1963: Opisthobranchia. Memoirs of the National Museum of Victoria 27: 265-288.

Dicquemare, L'Abbé, 1773: Mémoire pour fervir à l'hiftoire des anemones de mer. Philosophical Transactions of the Royal Society (London) 63: 361-403.

——, 1775: Second mémoire pour fervir à l'hiftoire des anemones de mer. Philosophical Transactions of the Royal Society (London) 65: 207-248.

Edmunds, M., Potts, G. W., Swinfen, R. C., and Waters V. L., 1974: The feeding preferences of Aeolidia papillosa (L.) (Mollusca: Nudibranchia). Journal of the Marine Biological Association of the United Kingdom 54: 939-947.

Eliot, C. N. E., 1910: ‘A Monograph of the British Nudibranchiate Mollusca’. Ray Society, London. 198 pp.

Feder, H., and Christensen, A. M., 1966: Aspects of asteroid biology, pp. 87-127 in Boolootian, R. A. (Ed.), ‘Physiology of Echinodermata’. Interscience, New York. 822 pp.

Fleure, H. J., and Walton, C. L., 1907: Notes on the habits of some sea anemones. Zoologischer Anzeiger 31: 212-220.

Francis, L., 1973: Intraspecific aggression and its effect on the distribution of Anthopleura elegantisima and some related sea anemones. Biological Bulletin Marine Biological Laboratory Woods Hole 144: 73-92.

Fry, W. G., 1965: The feeding mechanisms and preferred foods of three species of Pycnogonida. Bulletin of the British Museum (Natural History) 12: 197-223.

Godfriaux, B. L., 1970: Food of predatory demersal fish in Hauraki Gulf. N.Z. Journal of Marine and Freshwater Research 4: 325-336.

——, 1974: Food of Tarakihi in Western Bay of Plenty and Tasman Bay, New Zealand. N.Z. Journal of Marine and Freshwater Research 8: 111-153.

Graham, D. H., 1939: Food of fishes of Otago Harbour and adjacent seas. Transactions of the Royal Society of N.Z. 68: 421-439.

Hancock, D. A., 1958: Notes on starfish on an Essex oyster bed. Journal of the Marine Biological Association of U.K. 37: 565-589.

Hand, C., 1975: Descriptions of two New Zealand sea anemones (Actiniaria: Hormathiidae). N.Z. Journal of Marine and Freshwater Research 9: 493-507.

Harris, L., 1971: Ecological observations on a New England nudibranch-anemone association. The Echo 4: 22.

Hartog, J. C. den, 1961: Enige aantekeningen over Actinia equina (L.) de Gewone zeeanemoon. De Levende Natuur 64: 280-285.

Hedgpeth, J. W., 1949: Report on the Pycnogonida collected by the Albatross in Japanese waters in 1900 and 1906. Proceedings of the United States National Museum 98: 233-321.

Helfer, H., and Schlottke, E., 1935: ‘Pantopoda’. Akademische Verlagsgesellschaft, Leipzig. 314 pp.

Johnston, G., 1846: ‘A History of British Zoophytes’. Van Voorst, London. 488 pp.

Lizama, J., and Blanquet, R. S., 1975: Predation on sea anemones by the amphinomid polychaete, Hermodice carunculata. Bulletin of Marine Science 25: 442-443.

Martin, E. J., 1960: Observations on the toxic sea anemone, Rhodactis howesii (Coelenterata). Pacific Science 14: 403-407.

Mauzey, K. P., Birkeland, C., and Dayton, P. K., 1968. Feeding behaviour of asteroids and escape responses of their prey in the Puget Sound. Ecology 49: 603-619.

McIntosh, W. C., 1874: On the invertebrate marine fauna and fishes of St. Andrews. Annals and Magazine of Natural History, Series 4, 13: 204-221.

McMillan, N. F., 1942: Food of nudibranchs. Journal of Conchology 21: 237.

Meyer, K., and Bückmann, D., 1963: Die Hautungen des Pantopoden Pycnogonum litorale (Strom). Zoologischer Anzeiger Suppl. bd. 26: 604-609.

Miller, M. C., 1961: Distribution and food of the nudibranchiate Mollusca of the south of the Isle of Man. Journal of Animal Ecology 30: 95-116.

Milligan, H. N., 1916: Asteroids feeding on living sea-anemones. Nature 96: 619-620.

Morton, J. E., and Miller, M. C., 1968: ‘The New Zealand Sea Shore’. Collins, London. 638 pp.

Ottaway, J. R., 1977: Predation on Actinia tenebrosa by Pleurobranchaea novaezelandiae. N.Z. Journal of Marine and Freshwater Research 10. (In press.)

Parry, G., 1951: The Actiniaria of New Zealand: Part I. Records of the Canterbury Museum 6: 83-119.

Robson, E. A., 1961: The swimming response and its pacemaker system in the anemone Stomphia coccinea. Journal of Experimental Biology 38: 685-694.

——, 1966: Swimming in Actiniaria. pp. 333-360 in Rees, W. J. (Ed.), ‘The Cnidaria and their Evolution’. Academic Press, London. 449 pp.

Russell, H. D., 1942: Observations on the feeding of Aeolidia papillosa L. with notes on the hatching of the veligers of Cuthona amoena A. and H. Nautilus 55: 80-82.

Salvini-Plawen, L. V., 1972: Cnidaria as food sources for marine invertebrates. Cahiers de Biologie Marine 13: 385-400.

Stehouwer, E. C., 1952: The preference of the slug Aeolidia papillosa (L.) for the sea-anemone Metridium senile (L.). Archives néerlandaises de zoologie 10: 161-170.

Stephenson, T. A., 1928: ‘The British Sea Anemones’. Vol. I. Ray Society, London. 148 pp.

Swennen, C., 1961: Data on distribution, reproduction and ecology of the nudibranchiate molluscs occurring in the Netherlands. Netherlands Journal of Sea Research 1: 191-240.

Tardy, J., 1965: Description et biologie de Cerberilla bernadetti espèce nouvelle de Gasteropode Nudibranche de la côte atlantique française. Bulletin de l'Institut Océanographique, Monaco 65: 1-22.

——, 1969: Etude systematique et biologique sur trois espèces d'Aeolidielles de côtes européenes (Gasteropodes, Nudibranches). Bulletin de l'Institut Océanographique, Monaco 68: 1-40.

Thompson, T. E., 1964: Grazing and the life cycles of British nudibranchs. pp. 275-297 in Crisp, D. J. (Ed.), ‘Grazing in Terrestrial and Marine Environments’. Blackwell, Oxford. 322 pp.

Verwey, J., 1930: Coral reef studies. 1. The symbiosis between damselfishes and sea anemones in Batavia Bay. Treubia 12: 305-354.

Waters, V. L., 1973: Food-preference of the nudibranch Aeolidia papillosa, and the effect of the defenses of the prey on predation. Veliger 15: 174-192.

Webb. B. F., 1973: Fish populations of the Avon-Heathcote estuary: 3. Gut contents. N.Z. Journal of Marine and Freshwater Research 7: 223-224.

Wobber, D. R., 1970: A report on the feeding of Dendronotus iris on the anthozoan Cerianthus sp. from Monterey Bay, California. Veliger 12: 383-387.

Wolter, H., 1967: Beitrage zur biologie, histologie und sinnesphysiologie (inbesondere der chemorezeption) einiger nudibranchier (Mollusca, Opisthobranchia) der Nordsee. Zeitschrift für Morphologie und Okologie der Tiere 60: 275-337.

Wyer, D., and King, P. E., 1974: Feeding in British littoral pycnogonids. Estuarine and Coastal Marine Studies 2: 177-184.

* Further references to associations of pycnogonids and anthozoans are listed in Helfer and Schlottke (1935), Hedgpeth (1949), and Wyer and King (1974).