215-222 Milano 24-2-1989 Boll. Malacologico 24 (1988) (9-12) | |

Riccardo Cattaneo Vietti* & Ferdinando Boero**

RELATIONSHIPS BETWEEN EOLID (MOLLUSCA, NUDIBRANCHIA) RADULAR MORPHOLOGY AND THEIR CNIDARIAN PREY***

Key words: Nudibranchs; Cnidarians; Radular morphology; Trophic relationships.

Abstract

Eolids, among nudibranchs, usually feed on cnidarians, mostly on hydroids. The assessment of the relations between the morphological characteristics of the prey and the morpho- functional aspects of the radular structure of seventeen families of eolids has been attempted from data available in the literature.

Riassunto

Gli eolidiacei, tra i nudibranchi, predano generalmente cnidari, ed in particolare idrozoi. L’analisi del rapporto tra morfologia radulare e preda presenta, tuttavia, notevoli difficoltà inter- pretative. Specie con radule triseriate, ad esempio, predano indifferentemente sia idroidi tecati che atecati o la stessa preda è attaccata da specie con formule radulari diverse. In questi casi, più che la morfologia della radula è importante il comportamento predatorio della specie, comporta- mento ancor oggi assai poco conosciuto. Una buona convergenza morfologica esiste invece tra le radule delle famiglie che predano, rispettivamente, specie neustoniche ed attiniari.

Acknowledgements

Contributions of the Ministero della Pubblica Istruzione (40% and 60% funds) are gratefully acknowledged. We express our sincere thanks to our friend and collegue Dr. A. Balduzzi for his invaluable assistance and to Prof. M. Sarà for his criticisms.

Introduction

The diet of nudibranch molluscs shows a general tendency of the spe- cies to select a given type of prey. Todd (1981), in a review of nudibranch ecology, distinguished four trophic groups: sponge-grazers (dorids), bryo- zoan-grazers (mainly dorids), hydroid-grazers (eolids) and «miscellaneous» groups, including representatives of all four suborders preying upon other different taxa. Recently Cattaneo Vietti & Balduzzi (in press) studied this

* Istituto di Zoologia dell’Università di Genova, Via Balbi, 5, 16126 Genova, Italy. ** Dipartimento di Biologia dell’Università di Lecce, 73 100 Lecce, Italy. *** Lavoro accettato il 30 aprile 1988.

215 relationship in dorids. Even though eolids feed mostly on hydrozoans and anthozoans (mainly actinians) some of them (e.g. Facelina annulicomis, F.

coronata, Phidiana crassicomis, P. pugnax ) are euryphagous and can attack other opisthobranchs or small invertebrates. Calma glaucoides feeds on teleost eggs, and Favorinus spp. on invertebrate eggs. Some neustonic spe-

cies (e.g. Glaucus atlánticas, Glaucilla spp. and Fiona pinnata ) feed on planktonic cnidarians, molluscs or stalked barnacles. Eolids act as a controlling factor in the development of hydroid populations, being able to completely deplete them, mainly at the end of the seasonal cycles of the species (Barange & al, in press; McLeod & Valiela, 1975). The feeding intensity of an eolid can be high: Tenellia adspersa can destroy up to 100 adult hydranths of Perigonimus megas in 24 hr (Turpaeva, quoted by Roginskaya, 1970). In this paper we aim to point out the relationship between morpholo- gical characters of the prey and of the radular structure in 17 families of eolids, especially those feeding on hydroids. The feeding preferences of actinian-predators were recently studied by Tardy (1969), Waters (1973), Edmunds & al (1974), Moreteau (1977), Hall & al (1982), and Edmunds (1983).

Material and methods

The bulk of data was drawn from the literature: we have used the data reported by Barletta (1976), Behrens (1980), Bouchet & Tardy (1976), Clark (1976), Edmunds & Kress (1969), Farmer (1980), Gosliner (1979), Gosliner & Griffiths (1981), Haefelfinger (1960), Kuzirian (1979), MacDonald & Nybakken (1978; 1980); Miller (1961; 1971; 1977), Ros (1975; 1978), Rudman (1979; 1980; 1981; 1982), Schmekel & Portmann (1982), Salvini-Plawen (1972), Swennen (1961), Tardy (1969), Thompson & Brown (1984), Todd (1981). The data concerned over 130 species which feed upon over 20 families of hydroids, excluding anthozoans and other less important taxa. To facili- tate the interpretation the data were divided according to the families and the classifications proposed by Schmekel & Portmann (1982) and Thompson & Brown (1984) for nudibranchs, and by Bouillon (1985) for hydroids, are adopted. Data were considered from a qualitative point of view (presence/abs- ence of a prey in the diet of every radular group).

216 Results

A large part of the eolids feeds on hydroids (Tab. 1). Also primitive

Notaeolidiidae, with an unusual pluriseriate radula (2.5.1 .5.2.), feeds on athecates hydroids (probably Capitata), according to Vayssiere’s (1905) drawings of the nematocysts found in the cerata. Most of the advanced families of eolids have continued this specialisation on hydroid prey. No strong correlation between radular type (uni-, tri-, and multiseri- ate) and hydroid type exists: eolids with both uniseriate and triseriate radulae were reported to feed on both thecate and athecate hydroids. (Tab.

2 ). The triseriate Eubranchidae seem to prefer thecates whereas the tris- eriate Pleuroprocta (Flabellinidae, Cumanotidae, Pleurolidiidae) tend to feed on athecates. The Facelinidae have a varied and complex diet (some species are euryphagous), but prefer athecates. The Tergipedidae, apart from specialized species as Cuthona nana feeding on Hydractiniidae (Christensen, 1977), Cuthona poritophages and Phestilla spp. feeding on scleractian coral (Rudman, 1979; 1981), shows a tendency to feed on the- cates. The doubtful genus Catriona seems to prefer athecates. The monospecific Fionidae and Calmidae feed, respectively, on a diet range of neustonic species and teleost eggs, whereas the paucispecific psmammophilous family Pseudovermidae preys on the athecate Euphysi- dae and on the actinulid Halammohydridae. Finally Aeolidiidae, Pteraeolidiidae and some Herviellidae prey on actinians.

Table 1 Percent frequences of preys in the diet of aeolid families according to re- ferences listed at pag. 2.

Rad. type Athecata Thecata Eggs Anthozoa Others

Notaeolidiidae multiseriate 100 _ Flabellinidae triseriate 73 25 — — 2 Cumanotidae triseriate 100 _ — — — Pleurolidiidae triseriate 100 — Heteroprocta Glaucidae uniseriate 50 — — — 50 Facelinidae uniseriate 63 25 13 Favorinidae uniseriate 22 22 44 12 Pteraeolididae uniseriate — 100 Flerviellidae uniseriate — 33 — 67 — Aeolidiidae uniseriate — — — 100 — Piseinotecidae uniseriate 50 50 — — — Eubranchidae triseriate 15 85 Pseudovermidae triseriate 100 — — Tergipedidae uniseriate 43 50 — 7 —

Acleioprocta Embletoniidae uniseriate 50 50 — — Fionidae uniseriate 67 — — — 33 Calmidae uniseriate — — 100 — —

217 Acleioprocta Heteroprocta

Clavidae

Hydractiniidae

Bougainvilliidae

Eudendriidae

(D — Capitata indet.

I I I

I CL I I i ro i i Protohydridae ili I

Myriothelidae

Anthomedusae/Athecatae Euphysidae

Corymorphidae

Boreohydridae

Tubulariidae

Halocordylidae

Corynidae

Solanderiidae

Velellidae

Haleciidae

Sertulariidae

Plumulariidae

Leptomedusae/Thecatae

Aglaopheniidae

Campanulariidae

Halammohydridae

Table 2 Food trends of hydroid-feeder eolids according to references listed at pag. 2. 0 = main food # = secondary food • = occasional food

218 Discussion

As already suggested by Nybakken & McDonald (1981), the available data make the correlation between radular shape and diet difficult. The radular patterns do not allow any discrimination between thecate and athecate feeders. Nybakken & McDonald (1981) proposed two different feeding tactics according to radular types: species with uniseriate radulae feed by puncturing the pensare of the prey, then ingesting the coenosarc, while species with triseriate radulae tend to feed directly on naked hyd- ranths or gonophores.

It is possible, however, to find cases in which the differences between triseriate and uniseriate radulae are less clearly defined. Flabellinopsis iodinea, for instance, manipulates the hydranths of Eudendrium ramosum with the lips so as to put them into a suitable position for the jaws to grasp; the hydranths are torn from the stalk as a result of 3 or 4 violent contractions of the body and are then drawn into the mouth by radular action (McBeth, 1971). Cratena peregrina shows a completely different be- haviour to feed on the hydranths of Eudendrium racemosum. The hyd- ranths, in fact, are attacked from one side of their base until all the hyd- ranth body is ingested, the stalk is then cut and also the tentacles pass into the mouth. Flabellinopsis iodinea has a triseriate radula, whereas Cratena peregrina has a monoseriate one. Both feed on hydranths of congeneric spe- cies but adopt two different feeding strategies.

Morever it is apparent that many species feed both on thecates and on athecates, so that the same radular type may be used for preys with diffe- rent features. On the contrary, a strict relationship exists between Aeolidiidae, Pter- aeolidiidae and some Herviellidae reported to prey on actinians: they have a pectinate, broad and uniseriate radula. The tooth of the tergipedid Phes- tilla, feeding on scleractinian corals (Rudman, 1981; 1982a), shows long pointed denticles with the tips all approximately at the same level, perhaps due to morphological convergence with the actinian-feeder genera.

Another good resemblance appears to be between Glaucidae and Fionidae strong cuspidated teeth: both families feed on neustonic species. The apparent lack of homogeneity in many of the data recorded from the literature possibly reflects insufficient observation. The simple record of the species on which a given nudibranch was collected gives only a rough indication about its diet, especially if the feeding technique has not been carefully studied. Other points are anyway relevant in the study of trophic relations be- tween nudibranchs and hydroids.

— The big colonies of some hydroid species are often covered by epi- biotic hydroids of smaller size. These are not easily detectable in situ, but could be the object of predation. The nudibranch should be taken together with its possible prey, the cnidome of the prey should be studied and com- pared with the clepto-cnidome of the nudibranch, to verify if they match.

219 If they don’t, another prey should be searched on. Direct observation of feeding, however, is the definitive way to assess a diet.

— Diets are possibly related with the age of the predator (Todd, 1983). The juveniles, in fact, may begin feeding on small thecate hydranths and, once adult, may pass to the bigger hydranths of athecates. Thecate hyd- roids, besides having smaller hydranths than athecates, generally have also smaller nematocysts, which could be easier to pack in the cnidosac of juvenile nudibranchs. Coryphella pedata, for instance, feeds on athecates when adult, whereas young stages have been recorded feeding on the the- cates Obelia geniculata and Sertularella gayi (Garstang, 1890 quoted by Thompson & Brown, 1984). — Many hydroid species are seasonal, so that the same nudibranch could feed on different species in the different periods of the year. — SStrong differences may be evidenced in the diets of populations of the same species living in far apart areas: Coryphella lineata is reported to feed on Eudendriidae in the Mediterranean, and on Tubulariidae in the Atlantic. — Preys must be identified at specific level. The genus Eudendrium, for instance, comprises species with big nematocysts and species with small ones, some species have a pseudohydrotheca, others have cnidophores. These features could require different specializations of the predators. — The choices of nudibranchs could be influenced by experimental conditions when studies are done in the laboratory. — Some radular types allow a generalist diet, as evidenced by Cattaneo Vietti & Balduzzi (in press) for dorids.

A general outcome of the present review is that the feeding biology of eolid nudibranchs is far from being completely understood. Further approaches to this problem should carefully consider also the biology of the prey species.

220 REFERENCES

Barange M., M. Zabala, J.M. Gilí, T. Riera, in press - A general approach to the «in situ» energy budget of Eudendrium racemosum (Cnidaria, Hydrozoa) in the Western Mediterra- nean.

Barletta G., 1976 - Considerazioni sulla bionomia dei nudibranchi e sulla loro alimentazione. Conchiglie, Milano, 12 (5-6): 117-128.

Behrens D.W., 1980 - Pacific Coast Nudibranchs. Sea Challengers, Los Osos, California. 112 PP- - Bouchet P., J. Tardy, 1976 Faunistique et biogéographie des nudibranches des còtes frangai- ses de l’Atlantique et de la Manche. Ann. Inst, oceanogr. Paris, 52 (2): 205-213.

- Bouillon, J., 1985 Essai de classification des Hydropolypes-Hydroméduses (Hydrozoa-

Cnidaria). Indo-Malayan Zool., 1: 29-243.

Cattaneo Vietti R., A. Balduzzi, in press - Relationship between radular morphology and food in Doridina (Mollusca: Nudibranchia). 9th Int. Malacol. Congr., Edinburgh (1986).

Christensen H., 1977 - Feeding and reproduction in Precuthona peachi (Mollusca Nudibran- chia). Ophelia, 16 (1): 131-142. Clark K.B., 1975 - Nudibranch life cycles in the Northwest Atlantic and their relationship to the ecology of fouling communities. Helgolander wiss. Meeresunters., 27: 28-69.

Edmunds M., 1983 - Advantages of food specificity in Aeolidia papillosa. J. Moll. Stud., 46 (1): 80-81.

Edmunds M., A. Kress, 1969 - On the European species of Eubranchus (Mollusca Opistho-

branchia). J. mar. biol. Ass. U.K., 49 (4): 879-912. Edmunds M., G.W. Potts, R.C. Swinfen, V.L. Waters, 1974 - The feeding preferences of

Aeolidia papillosa (L.) (Mollusca, Nudibranchia). J. mar. biol. Ass. U.K., 54: 939-947. Farmer W.M., 1980 - Sea-slug Gastropods. Farmer Enterprises, pp. 1-177. Gosliner T.M., 1979 - The systematics of the Aeolidacea (Nudibranchia: Mollusca) of the Hawaiian Islands, with descriptions of two new species. Pacific Science, 33 (1): 37-77. Gosliner T.M., R.J. Griffiths, 1981 - Description and revision of some South African Aeoli- dacean Nudibranchia (Mollusca, Gastropoda). Ann. 5. Afr. Mus., 84 (2): 105-150.

Kuzirian A.M., 1979 - Taxonomy and biology of four New England coryphellid nudibranchs

(Gastropoda: Opisthobranchia). /. moll. Stud., 45: 239-261.

Haefelfinger H.R. - 1960 - Catalogue des opisthobranches de la Rade de Villefranche-sur-mer

et ses environs (Alpes Maritimes). Rev. Suisse Zool., (si (3): 323-351.

Hall S.J., C.D. Todd, A. Gordon, 1982 - The effects of ingestive conditioning on the prey (L.) species selection in Aeolidia papillosa (Mollusca: Nudibranchia). J. Anim. Ecol., 51: 907-921.

McBeth J.W., 1971 - Studies on the food of Nudibranchs. Veliger, 14 (2): 158-161. McDonald G.R., J.W. Nybakken, 1978 - Additional notes on the food of some California nudibranchs with a summary of known food habits of California species. Veliger, 21 (1): 110-119.

McDonald G.R., J.W. Nybakken, 1980 - Guide to the nudibranchs of California. American Malacologists, Inc. Florida. 1-72 pp. McLeod P., I. Valiela, 1975 - The effect of density and mutual interference by a predator: a laboratory study of predation by the nudibranch Coryphella rufibranchialis on the hydroid Tubularia larynx. Hydrobiologia, 41 (3-4): 339-346.

Miller M.C., 1961 - Distribution and food of the nudibranchiate mollusca of the South of the

Isle of Man. J. animal ecology, 30 (1): 95-116. Miller M.C., 1971 - Aeolid nudibranchs (Gastropoda: Opisthobranchia) of the families Flabel-

linidae and Eubranchidae from New Zealand waters. Zool. J. Linn. Soc., 50 (4): 311-337. Miller M.C., 1977 - Aeolid nudibranchs (Gastropoda: Opisthobranchia) of the family Tergipe-

didae from New Zealand waters. Zool. J. Linn. Soc., 60 (3): 197-222. Moreteau J.C., 1977 - Etude sur l’alimentation d’Aeolidia papillosa L. Cah. Biol. Mar., 18: 369-383.

- Nybakken J., G. McDonald, 1981 Feeding mechanisms of West American Nudibranchs feeding on Bryozoa, Cnidaria and Ascidiacea, with special respect to the radula. Malacolo- gia, 20 (2): 439-449. Roginskaya I.S., 1970 - Tenellia adspersa, a nudibranch new to the Azov Sea, with notes on its taxonomy and ecology. Malac. Rev., 3: 167-174. Ros J.D., 1975 - Opistobranquios (Gastropoda: Euthyneura) del litoral iberico. Inv. Pesq, Bar- cellona: 39 (2): 269-372.

221 Ros J.D., 1978 - La alimentación y el sustrato en los opistobranquios ibéricos. Oecologia aquati- Barcellona, 3: 153-166. ca , Rudman W.B., 1979 - The ecology and anatomy of a new species of aeolid opisthobranch

mollusc; a predator of the scleractinian coral Porites. Zool. J. Linn. Soc., 65 : 339-350. Rudman W.B., 1980 - Aeolid nudibranch molluscs (Glaucidae) from the Indian Ocean and the

south-west Pacific. Zool. J. Linn. Soc., 68 (2): 139-172. Rudman W.B., 1981 - Further studies on the anatomy and ecology of opisthobranch molluscs

feeding on the scleractinian coral Porites. Zool. J. Linn. Soc., 71 : 373-412. Rudman W.B., 1982 - The taxonomy and biology of further aeolidacean and arminacean nudi-

branch molluscs with symbiotic zooxanthellae. Zool. J. Linn. Soc., 74 : 147-196. Rudman W.B., 1982a - A new species of Phestilla\ the first record of a corallivorous aeolid

nudibranch from tropical America. J. Zool. Lond., 198 : 465-471. Salvini-Plawen L.V., 1972 - Cnidaria as food-sources for marine Invertebrates. Cah. Biol.

Mar., 13 : 385-400.

Schmekel L., A. Portmann, 1982 - Opisthobranchia des Mittelmeeres, Nudibranchia und Saccoglossa. Fauna e Flora del Golfo di Napoli. 40. Springer-Verlag. 410 pp. Swennen C, 1961 - Data on distribution, reproduction and ecology of the nudibranchiate

molluscs occurring in the Netherlands. Neth. J. Sea. Res., 1 (1-2): 191-240.

- Tardy J., 1969 Etude systématique et biologique sur trois espéces d’Aeolidielles des cotes européennes (Gastropodes Nudibranches). Bull. Inst. Ocean. Monaco, 68 (1389): 1-40. Thompson T.E., G. Brown, 1984, Biology of Opisthobranch Molluscs. II. Ray Society, Lon- don, pp. 1-229.

- Todd C.D., 1981 The ecology of nudibranch molluscs. Oceanogr. Mar. Biol. Ann. Rev., 19 : 141-234. Todd C.D., 1983 -Reproductive and trophic ecology of nudibranch molluscs. In: The Mollusca. Academic Press, pp. 225-259. Vayssière A., 1905 - Mollusques nudibranches et marsèniadès. Exp. Antarctique Franc. (1903- 1905). Masson, Paris, pp. 1-51. Waters V.L., 1973 - Food-preference of the nudibranch Aeolidia papillosa and the effect of the

defences of the prey on predation. Veliger, 15 : 174-192.

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