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Potentially Toxic Epiphytic Dinoflagellate Assemblages on Macroalgae in the NW Mediterranean

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Potentially Toxic Epiphytic Dinoflagellate Assemblages on Macroalgae in the NW Mediterranean AQUATIC MICROBIAL ECOLOGY Vol. 26: 51–60, 2001 Published October 26 Aquat Microb Ecol Potentially toxic epiphytic dinoflagellate assemblages on macroalgae in the NW Mediterranean Magda Vila*, Esther Garcés, Mercedes Masó Institut de Ciències del Mar, Passeig Marítim de la Barceloneta, 37–49, 08003 Barcelona, Catalonia, Spain ABSTRACT: A potentially toxic epiphytic dinoflagellate assemblage on macroalgae was studied for 1 yr in a shallow protected rocky habitat in Palamós (Costa Brava, NW Mediterranean). The assem- blage was monitored on 4 macroalgae: Corallina elongata (Rhodophyceae), Dictyota dichotoma, Dilo- phus fasciola and Halopteris scoparia (Phaeophyceae). The dominant dinoflagellates were Ostreop- sis sp., and the accompanying species were Coolia monotis and Prorocentrum lima. The diatom Coscinodiscus sp. was an abundant component of the assemblage. Ostreopsis followed the same sea- sonal pattern on the 4 macroalgae selected. Substrate was not significantly different for the dinofla- gellate assemblages. Ostreopsis was present both in the water column and in the sand concomitant with maximal cell densities on macroalgae. Small-scale sampling revealed that all the epiphytic organisms prefer slightly shaken habitats. While Ostreopsis sp. prefers shaken to slightly shaken waters, Coolia monotis prefers slightly shaken to calm ones. The dinoflagellate assemblage follows a clear seasonal pattern, achieving maximum cell concentration during spring and summer without significant relative changes in the species composition. The epiphytic assemblage was widespread along the Catalan coast and Majorca, although dinoflagellates were found to be more abundant in the Costa Brava. In Corsica, diatoms dominated the assemblage, whereas Ostreopsis sp. was a minor component. KEY WORDS: Ostreopsis · Coolia monotis · Prorocentrum lima · Benthic dinoflagellates · Ciguatera fish poisoning Resale or republication not permitted without written consent of the publisher INTRODUCTION gellates) are eaten by herbivorous fish, which then become toxic. Thus, the toxins are biologically concen- Epiphytic (in close association with macroalgae) and trated within the food chain (Steidinger & Baden 1984). benthic (in coral rubble, sand and detritus) dinofla- A dinoflagellate assemblage in the genera Gam- gellates are relevant because the species Gambierdis- bierdiscus, Ostreopsis, Coolia, Prorocentrum and cus toxicus causes ciguatera (Yasumoto et al. 1977, Amphidinium (Ballantine et al. 1985, Carlson & Tindall Adachi & Fukuyo 1979). Ciguatera, or ciguatera fish 1985, Bomber & Aikman 1989, Bourdeau et al. 1995, poisoning, is a human disease caused by the ingestion Faust 1995) has also been reported in ciguatera- of contaminated marine finfish from tropical and sub- endemic areas. In particular, Prorocentrum lima, P. tropical regions, which results in gastrointestinal and concavum, Ostreopsis siamensis and O. ovata have neurological disorders and sometimes death. Polyether been implicated in ciguatera fish poisoning based on toxins (ciguatoxins and maitotoxins, among others) distribution, toxicity to mice and the presence of a fat- that are produced by marine epiphytic dinoflagellates soluble toxic fraction (Yasumoto et al. 1980, Nakajima (Steidinger 1983) may cause these symptoms. Macro- et al. 1981). These organisms form epiphytic communi- algae (and epiphytic assemblages of harmful dinofla- ties associated with coral reefs, or rather with macro- algae attached to coral surfaces. These assemblages *E-mail: [email protected] may vary in species composition and cell concentration © Inter-Research 2001 52 Aquat Microb Ecol 26: 51–60, 2001 between sites (Tindall & Morton 1998). The mixed 48º association of toxic dinoflagellates may contribute to the polymorphism of the clinical features of ciguatera N (Yasumoto et al. 1987). 44º Ostreopsidaceae species are widespread in most epi- phytic and benthic dinoflagellate communities from 40º 18 ciguatera-endemic regions of the world (35° N to 15 14 35° S). Thus, the geographic distribution of Ostreopsis 16 36º 17 siamensis, O. lenticularis and O. ovata is similar to that of Gambierdiscus toxicus (Tindall & Morton 1998), with 2 notable exceptions: O. siamensis and O. ovata 6º 4º 0º 4º 6º 8º 12º have been reported in the Mediterranean Sea (Taylor 1979, Tognetto et al. 1995). Nevertheless, data are limited on the incidence of Ostreopsis in the waters of 1 the Mediterranean Sea and on the magnitude of po- 2 3 tentially toxic epiphytic dinoflagellate assemblage Sampling site 4 attached to macroalgae. 5 42º In this study, we quantified epiphytic dinoflagellate 6 8 7 9 assemblages on the Catalan coast, NW Mediterranean. 10 The potentially toxic epiphytic dinoflagellate assem- 12 11 blage associated with macroalgae was examined dur- ing an annual cycle in a rocky habitat. In addition, small-scale spatial variability and middle-scale spatial 13 N distribution were analysed to shed some light on the epiphytic dinoflagellate assemblages in the NW 41º Mediterranean. 2º 3º The dominant dinoflagellate Ostreopsis sp. could not Fig. 1. Study area and stations sampled. 1: Cala Garbet; 2: be assigned to any described species. Thus, a brief de- Portlligat; 3: Canyelles Grosses; 4: Cala Portitxol; 5: Cala scription of the species with scanning electron mi- Pedrosa; 6: La Foradada; 7: Palamós (sampling site); 8: Gran crophotographs is included for further considerations. de Palamós; 9: Cala Canyet; 10: Santa Cristina d’Aro; 11: El Xuclador; 12: Sant Pol de Mar; 13: Vallcarca; 14: Riu Sènia; 15: Deià; 16: Cala Fornells; 17: Portals Vells; 18: Campomoro; 1–14 in Catalonia; 15–17 in Majorca; 18 in Corsica MATERIAL AND METHODS Sampling sites. Epiphytic dinoflagellates on selected The main macroalgae analysed were Corallina elon- macroalgae (Rhodophyceae and Phaeophyceae) were gata (Rhodophyceae), Dictyota dichotoma, Dilophus quantified for 1 yr (July 1997 to July 1998). The sampled fasciola and Halopteris scoparia (Phaeophyceae). C. macroalgae grow in multispecies assemblages attached elongata is present throughout the year; thus, we have to stones in the infralittoral. Macroalgal specimens (in studied the seasonal patterns in this macroalga. In triplicate) were collected weekly at 20 to 40 cm depths addition, other macroalgae were collected sporadi- during summer (July and August 1997) and monthly cally, mainly during the cold season, when the 4 target during the rest of the year. The sampling site was a species were very scarce. The additional macroalgae shallow protected rocky habitat in Palamós (Catalan sampled were Jania corniculata, Pterocladia capil- sea, NW Mediterranean). During the summers of 1997 lacea, Laurencia gr. obtusa, Rissoella verruculosa, and 1998, a more extensive study was carried out. Four- Ceramium ciliatum, Peyssonnelia squamaria (Rhodo- teen stations were sampled, mainly along the Costa phyceae), Dictyopteris membranacea, Padina pavon- Brava (northern Catalan coast) and in 2 other Mediter- ica (Phaeophyceae) and Ulva sp. (Chlorophyceae). ranean areas (Majorca and Corsica) (Fig. 1). Surface water (0.5 m) and sediment samples were Sampling methods. A subsample (15 to 20 g fresh collected in 150 and 50 ml bottles and preserved with weight [FW]) was carefully cut and placed with tweez- formaldehyde (1% final concentration) for dinoflagel- ers in a small glass bottle containing 10 ml of formalde- late examination. Nutrient samples were taken and hyde-filtered seawater. Since the macroalgae commu- frozen immediately and analysed for nitrate, nitrite, nity is dynamic and the species composition varies ammonia, phosphate and silicate as described by throughout the year, at every sampling date the avail- Grasshoff et al. (1983). Temperature and salinity were able macroalgae were taken to cover the annual cycle. measured. Vila et al.: Epiphytic dinoflagellates in the Mediterranean Sea 53 Once in the laboratory, macroalgae bottles were pore PC polycarbonate membrane filter (Costar, shaken vigorously for 1 min to dislodge the epiphytic Europe Ltd, Badhoevedorp). Samples were washed in organisms. Macroalgae were removed and the sample distilled water and dehydrated in an ethanol series (30, was settled for 6 h in 10 ml counting chambers. An 50, 70, 80, 90, 100%) at 4°C, critical point dried with appropriate area of the chamber was then scanned CO2 and examined under a Hitachi S-570 scanning (Throndsen 1995) for epiphytic organism counting at electron microscope (Nissei Sangyo Co. Ltd, Tokyo; 63 to 200× magnification using a Leica-Leitz DM-IL modified from Faust et al. 1996). inverted microscope (Leica Mikroskopie und Systeme GmbH, Wetzlar). Samples were examined and counted for epiphytic microalgal species. When high densities RESULTS of organisms were found in the sample, only a sub- sample was examined. Macroalgae were processed for Taxonomy of the epiphytic assemblages fresh weight (FW) and dry weight (DW) measure- ments. DW was measured after the macroalgae were Natural populations of benthic dinoflagellates and dried in an oven at 60°C. FW and DW were highly diatoms formed a mucilaginous matrix on the macroal- correlated (regression analysis, r2 > 0.98). Thus, we gal thallus and aggregated therein (Fig. 2A,B). Cells worked with FW, as is usual in other studies. One-way remained motile within the matrix and loosely linked ANOVA was performed to test differences between to macroalgae, as revealed by light microscopy. When the 4 macroalgae for each epiphyte dinoflagellate the epiphyte assemblage was dense, the brownish
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