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Feeding Behaviour of Paracentrotus Lividus in the Presence of Caulerpa

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Feeding Behaviour of Paracentrotus Lividus in the Presence of Caulerpa OCEANOLOGICA ACTA- VOL. 19- W 3-4 ~ -----~- Caulerpa taxifolia Feeding behaviour of Paracentrotus lividus Paracentrotus lividus Caulerpenyne in the presence of Caulerpa taxifolia Caulerpa taxifolia Paracentrotus lividus introduced in the Mediterranean Sea Caulerpényne Rodolphe LEMÉE a, Charles-François BOUDOURESQUE b, Julie GOBERT b, Pascale MALESTROIT b, Xavier MARI a, Alexandre MEINESZ a, Valérie MENAGER b and Sandrine RUITTON b a CNRS EP 75, Laboratoire Environnement Marin Littoral, Faculté des Sciences, Parc Valrose, 06108 Nice Cedex 2, France. b CNRS EP 75, Laboratoire de Biologie Marine et d'Écologie du Benthos, Faculté des Sciences de Luminy, 13288 Marseille Cedex 9, France. Received 30/03/95, in revised form 07/11/95, accepted 14/11/95. ABSTRACT Experiments in aquaria have shown that the feeding behaviour of the sea urchin Paracentrotus lividus in presence of the green alga Caulerpa taxifolia varies during the year. In sommer, the alga is strongly avoided and is not consumed. In winter and spring, although the alga is only moderately appreciated, its consomp­ tion is significant, but it is hardly or not at ali absorbed. These results are confir­ med by content analysis of the digestive tract of P. lividus sampled in situ in an area colonized by C. taxifolia. The sea urchins' feeding behaviour is linked to the presence of toxic and repellent secondary metabolites of C. taxifolia, caulerpe­ nyne in particular. RÉSUMÉ Comportement alimentaire de l'oursin Paracentrotus lividus en présence de Caulerpa taxifolia introduite en Méditerranée. Des expériences en aquarium montrent que le comportement alimentaire de l'oursin Paracentrotus lividus en présence de l'algue verte Caulerpa taxifolia varie au cours de l'année. En été, l'algue est fortement évitée et n'est pas consommée. En hiver et au printemps, bien que moyennement appréciée, l'algue est consommée de façon significative mais elle est peu ou pas absorbée. Ces résultats sont confirmés par les analyses du contenu du tube digestif de P. lividus prélevé in situ dans une zone colonisée par C. taxifolia. Le comportement ali­ mentaire des oursins est lié à la présence des métabolites secondaires toxiques et répulsifs de C. taxifolia, et en particulier à celle de la caulerpényne. Oceanologica Acta, 1996, 19, 3-4, 245-253. INTRODUCTION 80 % of the benthic vegetation over an area of several hec­ tares (Meinesz et al., 1993). In certain stations that have The tropical alga Caulerpa taxifolia (Vahl) C. Agardh been invaded for several years, it bas thus become the (Chlorophyta, Ulvophyceae, Caulerpales) was introduced major plant food resource. Because of the invasive nature into the Mediterranean Sea in 1984 (Meinesz and Hesse, of this introduced species, its impact on the fauna and flora 1991 ). lts rapid expansion on a variety of substrates and of the Mediterranean requires investigation. across a wide depth range bas been noted (Meinesz et al., 1993). In tropical regions the development of C. taxifolia is Caulerpa taxifolia is now in competition with benthic not invasive, whereas in the Mediterranean this alga can plants. A decrease of the biomass and diversity of algae form extremely dense beds and may account for more than has been observed, particularly among the hard substrate 245 R. LEMÉE et al. sciaphilic and photophilic communities (Boudouresque et Consomption and absorbtion rates of Caulerpa taxifolia al., 1992; Verlaque and Fritayre, 1994). Similarly, changes in the structure of Posidonia oceanica (L.) Delile beds Experiments were carried out in spring (March, April and have been recorded (Villele and Verlaque, 1994). The sitt­ May) and summer (July) 1994. The duration of the experi­ ing of the substrate engendered by the dense beds of ments varied from one to four weeks. Ten sea urchins were C. taxifolia cause major alterations in the composition of placed in each aquarium, in the presence of a single alga. the invertebrate fauna. Sorne Molluscs are more abondant, The control algae used as food were Cystoseira compressa while the numbers and diversity of several Crustaceans (Esper) Gerloff and Nizmuddin or Halopte ris scoparia (L.) have declined (Bellan-Santini et al., 1994 ). The first fin­ Sauvageau (ex Stypocaulon scoparium (L.) Kützing). The dings from investigations of the fish fauna show that inva­ overall mass of each alga was weighed and made up to sion of the sea bottom by C. taxifolia alters the structure of 50 g (wet weight) every day to estimate the sea urchins' the populations (Francour et al., 1994 ). daily food intake. This quantity of plant matter in each aquarium was non-limiting. The wet weight of plants was The species of the genus Caulerpa have developed an effi­ measured after standardized centrifugation. For the calcu­ cient strategy against grazers and epiphytes by synthesi­ lation of food intake, aquaria containing the algae without zing toxic or repellent secondary metabolites (Norris and the presence of echinoderms were used to deduce the Fenical, 1982; Capon et al., 1983; Faulkner, 1984; Paul variations in mass due to the growth or decay of algae. For and Fenical, 1986). Evidence has been provided of the pre­ each of the three species, a dw/ww conversion rate was sence of numerous terpenes in C. taxifolia introduced into established giving the following results: 11 % for C. taxifo­ the Mediterranean (Guerierro et al., 1992 and 1993). To lia, 16 % for C. compressa and 29 % for H. scoparia. In determine whether these metabolites do in fact have a each aquarium, the faeces were collected, dried (70 oc for repellent effect on Mediterranean grazers, we investigated 24 h) and weighed. In control experiments, 10 sea urchins the feeding behaviour of the common sea urchin Paracen­ were kept without algae to quantify the faeces deposited in trotus lividus (Lamarck, 1816) in the presence of C. taxi­ total absence of food. The absorbtion rate corresponds to joUa. This sea urchin is one of the main Mediterranean her­ the percentage of material ingested which penetrates the bivores, and its selective grazing pressure bas a strong intestinal wall. It is estimated by means of the following influence on the structure of benthic phytocenoses (Ver­ formula: laque, 1987). Consequently, P. lividus feeding behaviour when faced with a C. taxifolia-based diet is weil worth TA= ((Mi- Mr)*100)*Mi-1 investigation. TA = absorbtion rate; W e have measured the consomption and absorbtion rate of Mi = dry weight ingested; C. taxifolia and also determined the situation of this alga Mr = dry weight defecated. among the food preferences of P. lividus. The results of these in vitro experiments are compared with those con­ We have also studied ingestion of C. taxifolia previously ceming the feeding behaviour of P. lividus in situ. cultivated for a month in aquarium conditions and inges­ tion of C. taxifolia and Cystoseira compressa previously subjected to a lethal thermal shock (40 °C). These experi­ ments were carried out in summer. MATERIALS AND METHODS The situation of Caulerpa taxifolia among the food pre­ For the aquarium experiments, we used 20 to 30 dm3 tanks ferences of Paracentrotus lividus equipped with an air diffuser and an internai filter. A fra­ med grid was placed 2 cm above the bottom of the aquaria Experiments were carried out in summer, winter and spring to prevent the sea urchins from reingesting their own from summer 1992 to spring 1994. Five sea urchins were faeces (Knoepffler-Peguy et al., 1987). The artificial sea placed in each aquarium, and were exposed to two plants, water (Instant Ocean sea salt) was renewed at three-day one of which was al ways C. taxifolia. The quantity of plant intervals. The sea water temperatures of the aquaria, the matter in each aquarium was non-limiting (75 g wet weight diameter and the site of sampling of sea urchins are given per plant and per aquarium) and was checked daily to in Table 1. C. taxifolia thalli were always sampled at Cap avoid any imbalance in the resources available for the sea Martin (Alpes Maritimes, France). urchins. The wet weight of plants was measured after stan- Table 1 Temperatures of aquaria sea water, diameters and sites of sampling of sea urchins used in the feeding behaviour experiments. Experiments Sea water temperatures Diameters of sea urchins Site of sampling of sea urchins Absorbtion rate Spring: 13 to 17 oc 45 to48 mm Samena (Bouches-du-Rhône) Summer: 19 to 21 oc Food preferences Winter: 12 to 16 oc 40to54 mm Samena (Bouches-du-Rhône) Spring: 18 to 20 °C Banyuls (Pyrénées-orientales) Summer: 21 to 25 oc 246 FEEDING BY P. UV/DUS ON C. TAXIFOLIA dardized centrifugation. Each experiment lasted five days, RESULTS which is longer than the time necessary to renew the diges­ tive content of sea urchins under normal feeding conditions Consomption rate and absorbtion rate (Frantzis, 1992; Kempf, 1962; Nédélec, 1982). The autho­ rities of the plants used in the food preference experiments In spring (Fig. 1), C. taxifolia was both poorly consumed are given in Table 2. (26 mg/d/indiv.) and poorly absorbed (2 %) by P. lividus. To determine the feeding behaviour of P. lividus in pre­ sence of C. taxifolia, we have confronted this alga with dif­ 150 ferent plants according to their situation among the food .-. SPRING .,; •0 SUMMER preferences of the sea urchins. For instance, the most stron­ =6 125 gly preferred species are Rissoella verruculosa, Cystoseira :a= amantacea var. stricta and Dictyota dichotoma; the mode­ Cb rately preferred species are Corallina elongata, Codium .s lOO fragile and Jania rubens and the avoided plants are Aspa­ ~ ragopsis armata, Codium bursa and Ceramium clavulatum ë 75 .5!= (Knoepffler-Peguy et al., 1987; Odile et al., 1988; Rico, Q. 1989; San Martin, 1987). With regard to Posidonia ocea­ s::s nica, a species moderately preferred by P.
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