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Morphological and Chemical Camouflage of The /. Moll Stud. (1997), 63,431-439 © The Malacological Society of London 1997 MORPHOLOGICAL AND CHEMICAL CAMOUFLAGE OF THE MEDITERRANEAN NUDIBRANCH DISCODORIS INDECORA ON THE SPONGES IRCINIA VARIABILIS AND IRCINIA FASCICULATA Downloaded from https://academic.oup.com/mollus/article/63/3/431/1073528 by guest on 24 September 2021 A. MARIN1*, M.D. LOPEZ BELLUGA1, G. SCOGNAMIGLIO2 and G. CIMINO2 'Departamento de Ecologia e Hidrologia, Facultad de Biologla, Universidad de Murcia, E-30100 Murcia, Spain. 2Consiglio Nazionale delle Ricerche, Istituto per la Chimica di Molecole di Interesse Biologico, 1-80072-Arco Felice (Na), Naples, Italy (Received 15 March 1996; accepted 27 January 1997) ABSTRACT supported by recording the induction of feeding- deterrence in the fresh-water fish Carassius auratus The nudibranch Discodoris indecora shows a perfect and in the marine fish Chromis chromis and Sparus camouflage on its prey, the dictyoceratid sponge auratus. Ircinia variabilis. Shape and colour of the nudibranch are remarkably similar to that of the sponge which is widespread in the shallow waters of the Mediter- ranean Sea. The metabolite pattern of /. variabilis is INTRODUCTION dominated by unusual molecules, the sesterter- penoids palinurin and variabilin, containing 25 In the evolution of opisthobranch gastropods carbons and displaying at the ends a ^-substituted and especially of nudibranchs, the loss of the furan ring and a tetronic acid. However, a chemical shell has been compensated by the develop- polymorphism has been recently described for /. vari- ment of a wide range of defensive mechanisms. abilis. Some specimens contain either palinurin or Some nudibranchs that feed on cnidarians are variabilin whereas others possess a mixture of both known to store nematocysts within cnidophage sestertepenoids. During the study of Mediterranean cells and use them for their own defence sponges, a linear sesterterpenoid related to palinurin (Thompson, 1960; Greenwood & Mariscal, and variabilin was found in Ircinia fasciculata, that from a taxonomic point of view is closely relatedto 1984). Nudibranchs also retain pigments and Ircinia variabilis. Discodoris indecora shows a typical zooxanthellae from the diet, so they may be defence behaviour when it is disturbed, secreting a camouflaged on the food source (Marin & Ros, copious white slime that contains large amounts of 1991). Certain nudibranchs contain repugnant palinurin and variabilin. Most likely the animal is able substances often obtained from dietary to transfer the sponge metabolites from the digestive sponges. Harris (1971) suggested that this glands to mantle glands. Electron micrographs of the 'physiological exchange' fits the classical con- nudibranch mantle showed the presence of unicell- cept of symbiotic association. ular glands characterized by a cylindrical vacuole with a big nucleus on the basis. The glands were con- Many chemical studies have been performed centrated in the most conspicuous tubercles of the on Mediterranean dorid nudibranchs. In almost dorsal mantle. Probably, the sponge metabolites are all cases, the diet of sponges has been proved by stored in these glands. the comparison of the metabolic patterns dis- Comparative chemical analysis of mucous secre- played by the nudibranch-sponge pair (Cimino tions, dorsal tubercles, mantle, foot, digestive glands & Sodano, 1994). Nudibranchs belonging to the and hepatopancreas of D. indecora confirmed this Family Chromodoridae (genus Hypselodoris hypothesis. Palinurin and fasciculation were, of spp., Chromodoris spp and Cadlina spp.) course, present in the digestive glands but they were display very similar morphological features. also found in the mucus and in the mantle sections However, it seems that the genus Hypselodoris enriched by the above described unicellular glands. spp., with the exception of H. orsini (Cimino, The defensive role of palinurin and variabilin, Fontana, Gimenez, Marin, Mollo, Trivellone & strongly suggested by their anatomical location, was Zubia, 1993), select sponges containing fura- nosesquiterpenoids (Garcfa-G6mez, Cimino & • To whom correipcndcnce ihould be jcnL (Fajc 34-68-363963; E- i kk@f) Medina, 1990; Avila, Cimino, Fontana, Gav- 432 A. MARIN, M.D. LOPEZ BELLUGA, G. SCOGNAMIGLIO & G. CIMINO agnin, Ortea & Trivellone, 1991), whereas the Bergh, 1881 in order to: clarify its feeding genus Chromodoris spp. select sponges possess- habits; investigate the transfer of dietary ing diterpenoids (Molinski, Faulkner, He, Van metabolites to mantle glands; place Discodoris Duyne & Clardy, 1986; Gavagnin, Vardaro, indecora in a hypothetical evolutionary Avila, Cimino & Ortea, 1992) and, finally, scenario of dorid nudibranchs. Cadlina species, possessing a more complex radula (Andersen, Pika, Dumdei & Burgoyne, 1993), can eat different kinds of sponges. The transfer of the sponge metabolites from the MATERIALS AND METHODS digestive glands to some dorsal formations Downloaded from https://academic.oup.com/mollus/article/63/3/431/1073528 by guest on 24 September 2021 (Mantle Dermal Formation) has been previ- Collection of molluscs ously suggested (Avila, Cimino, Fontana, Gav- The nudibranch Discodoris indecora was collected on agnin, Ortea & Trivellone, 1991) but only the sponges lrcinia variabihs (Schulze, 1879) and /. recently has it been rigorously proved fasciculata (Pallas, 1766) which were removed from (Fontana, Gim6nez, Marin, Mollo, Cimino, shallow rocks (1-2 m depth) during April to Septem- 1994). In the case of H. orsirti, the transfer of ber 1993 and 1994 in Spain (Mazarr6n and Torre- the dietary components is also accompanied by vieja, Murcia) and Italy (Naples and Taranto). A population of D. indecora was also found upon /. chemical transformation of the extremely reac- fasciculata. Nudibranchs and sponges were frozen as tive main sponge metabolite, scalaradial, first in soon as possible after collection. Some nudibranchs deoxoscalarin and then in 6-ketodeoxoscalaria were disturbed in order to obtain defensive secre- (Cimino, Fontana, Gimdnez, Marin, Mollo, tions. Trivellone & Zubia, 1993). The main biological role of these sponge Transmission electron microscopy metabolites sequestered by chromodorid gastropods is the protection against potential Nudibranchs were narcotized in 7.5% MgCl2 and predators. A more complex habit is shown by pieces of mantle were excised and fixed in for 1 h in Phyllidia species (family Phyllidiidae), analo- cold (1-4°C) 2.5% Millonig's phosphate-buffered glutaraldehyde (pH 7.2-8.2). Fixation was followed gous to chromodorid gastropods, transfer by a 24 h wash in 2.5% NaHCO and then post-fixed sponge compounds to the mantle and into the 3 in 2% OsO4 in 1.25% NaHCO3 for 1 h. The tissues mucus, whereas Dendrodoris spp. is able were dehydrated in an ethanol series and embedded to biosynthesize 'de novo' icthyodeterrent in Epon. Ultrathin sections were stained with uranyl molecules (Cimino, De Rosa, De Stefano, acetate and lead citrate. Sodano & Villani, 1983). Strangely enough, the Mediterranean Doripsilla aereolata contains in its hermaphrodite glands the same mixture of Extraction and isolation of metabolites sesquiterpenoids esters found in Dendrodoris, Frozen animals were carefully dissected to remove but notal metabolites are quite different mantle, foot, digestive gland and reproductive (Okuda, Scheuer, Hochlowski, Walker, & organs. These were extracted with acetone. The Faulkner, 1983). sponges were cut into small pieces and then extracted with acetone. The extraction was repeated three From an evolutionary point of view, dorid times. The solvent was then removed in vacua and the gastropods with notal spicules are situated aqueous residues were extracted with ether and then between non spiculated nudibranchs and the with n-butanol. Each extract was chromatographed ancestral shelled forms. Until now, only a few on silica gel plates (Merck F^) in chloroform- studies have been performed on Mediterranean methanol (95:5). The chromatograms were checked molluscs with notal spicules. Doris verrucosa for fluorescent compounds by exposure under u.v. contains some unusual diacylglycerols, whereas light and furans by spraying with Ehrlich reagent. Peltodoris atromaculata (Bergh, 1880) even Compounds from the crude extract were purified by though its digestive gland contains some silica gel chromatography and structurally elucidated by proton nuclear magnetic resonance ('H-NMR) dietaric polyacetylenes from the sponge Pet- spectrometry. rosia ficiformis, is not able to transfer these compounds to the mantle (Cimino, Gavagnin, Sodano, Puliti, Mattia & Mazzarella, 1988; PaJatabdity and toxicity bwassays Castiello, Cimino, De Rosa, De Stefano & Sodano, 1980). Discodoris indecora is similar to Ichthyotoxicity assays were conducted with the fish Gambusia affinis, Chromis chromis and Spams P. atromaculata, a selective predator of auratus, following the procedure described by sponges. Gunthorpe & Cameron (1987), and using the toxicity We have investigated Discodoris indecora ranking denned by Coll et al. (1982). DEFENCE ALLOMONES OF DISCODORIS INDECORA 433 RESULTS which lies inside the cell (Fig. 2). At the distal tip of the gland, the cytoplasm possesses ovoid Defensive behaviour vacuoles which coalesce towards the cell The body colour of D. indecora is golden- membrane (Fig. 2). In addition, smooth muscle brown with yellow and opaque white pigment fibres pass through and surrounding the con- on the top of many of the mantle tubercles. The nective matrix. mantle is covered
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