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The Dinoflagellate Genera Brachidinium, Asterodinium, Microceratium and Karenia in the Open SE Pacific Ocean

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The Dinoflagellate Genera Brachidinium, Asterodinium, Microceratium and Karenia in the Open SE Pacific Ocean Algae Volume 21(4): 445-452, 2006 The Dinoflagellate Genera Brachidinium, Asterodinium, Microceratium and Karenia in the Open SE Pacific Ocean Fernando Gómez Station Marine de Wimereux, Université des Sciences et Technologies de Lille, FRE 2816 ELICO CNRS, 28 avenue Foch, BP 80, F-62930 Wimereux, France The morphometry and distribution of the unarmoured dinoflagellates Brachidinium capitatum F.J.R. Taylor, Asterodinium gracile Sournia, Microceratium orstomii Sournia and the toxic species Karenia papilionacea Haywood et Steidinger have been investigated in open waters of the SE Pacific Ocean. The genus Microceratium Sournia is recorded for the first time since the initial description. These taxa showed a high morphological similarity and they may correspond to life stages of a highly versatile single species that is able to project body extensions. Karenia papil- ionacea showed the higher abundance in the surface waters of the more productive areas (the Marquesas Archipelago and the Perú-Chile Current). Brachidinium capitatum and K. papilionacea often co-occurred, predominat- ing B. capitatum in offshore surface waters. Asterodinium gracile was recorded at the bottom of the euphotic zone (down to 210 m depth), with a shallower distribution in more productive areas. Intermediate specimens of Asterodinium-Brachidinium-Karenia, with variable disposition and size of the body extensions were illustrated. Key Words: Asterodinium, Brachidinium, harmful algae bloom, Karenia papilionacea, Microceratium, phytoplankton, SE Pacific Ocean Pitcher and K. bidigitata Haywood et Steidinger and other INTRODUCTION taxa may be conspecific such as K. longicanalis Yang, Hodgkiss et G. Hansen and K. umbella de Salas, Bolch et Most of the species of the genus Gymnodinium Stein Hallegraeff (Yang et al. 2001; Botes et al. 2003; de Salas et were described during the late 1800’s and early 1900’s. al. 2004; Haywood et al. 2004). Very little progress has been made since then and the Among the recently described species, Karenia papil- taxonomic system has therefore remained almost ionacea Haywood et Steidinger showed several peculiar unchanged since the 19th century. Biecheler (1934) using characteristics in cultures with an unusual plasticity and a silver-impregnation method observed for the first time high size variability. In culture, K. papilionacea is also able the apical groove in Gymnodinium. Takayama (1985) to move forward the prominent apical process based on scanning electron microscopy (SEM) showed (Haywood et al. 2004, p. 170). Other close species, K. several types of apical grooves in unarmoured dinofla- bicuneiformis, showed pointed or bulbaceous antapical gellates. Daugbjerg et al. (2000) based on light tips in natural waters that were rounded when the microscopy, SEM, pigment composition and LSU rDNA species is cultured (Haywood et al. 2004, p. 173). The sequences split Gymnodinium into four genera: species of Karenia were described based on abundant Gymnodinium sensu stricto, Akashiwo G. Hansen et materials cultured under optimal conditions for growth Moestrup, Karlodinium J. Larsen and Karenia G. Hansen et that does not reproduce the low turbulence and olig- Moestrup. Since then, the description of new species of otrophic conditions of the open ocean. Consequently lit- Karenia characterized by a short straight apical groove, tle is known on the morphology and the life cycle of with fucoxanthin and lacking peridinin, has proliferated. species such as K. papilionacea under natural conditions. In some cases, a single species has been described under The dinoflagellate Brachidinium capitatum F.J.R. Taylor different names such as K. bicuneiformis Botes, Sym et is a flattened unarmoured taxon easily identifiable by the four radiating elongate antapical extensions, apical *Corresponding author ([email protected]) process, numerous yellow-green chloroplasts and promi- 446 Algae Vol. 21(4), 2006 nent nucleus. However, the partially erroneous descrip- tion by Taylor (1963) based on formalin-preserved speci- mens induced a mysterious character to Brachidinium F.J.R. Taylor. Taylor described Brachidinium as a laterally compressed, with no cingulum or sulcus, non-motile dinoflagellate placed in the order Dinococcales Pascher (coccoid or parasitic dinoflagellates). Sournia (1972b) found more specimens of B. capitatum with variable mor- phology and based on single or a few fixed specimens described two new species: B. taylorii Sournia and B. bre- vipes Sournia. From the same location, Sournia (1972a, b) Fig. 1. Map of the sampling stations during the BIOSOPE cruise described two closely related genera: Asterodinium in the SE Pacific Ocean. Sournia with the species A. gracile Sournia and A. spin- osum Sournia and Microceratium Sournia with the species coasts through the severe oligotrophic waters of the M. orstomii Sournia. Asterodinium differs from South Pacific Gyre (Claustre and Maritorena 2003) pro- Brachidinium on having two elongate extensions radiat- vides the opportunity to investigate the distribution of ing from the hyposome and three extensions from the the brachidinianceans and K. papilionacea under different episome. In comparison with Asterodinium, Microceratium trophic regimes. The present study also investigates the Sournia has only one extension in the episome and two morphometry of Brachidinium capitatum, Karenia papil- extensions in the hyposome. Co-occurring with these ionacea and Asterodinium gracile. Microceratium orstomii records, Sournia found gymnodinioid cells that he con- has been recorded for the first time since the initial sidered close to Brachidinium, illustrating the species description. Intermediate specimens among these gen- recently described as Karenia papilionacea (Sournia 1972b, era, with variable disposition and size of the body exten- p. 157; Haywood et al. 2004, p. 171). Later Sournia (1986, sions are illustrated. The hypothesis of the conspecifity p. 49) with the sentence “il pourrait s’agir ici de stades de of these taxa is reported. développement d’autres dinoflagellés plus notoires” was hypothesizing that the brachidiniaceans, members of the MATERIALS AND METHODS genera Brachidinium, Asterodinium and Microceratium, constitute life stages of more common dinoflagellates. Samples were collected at 12 stations from 5 to 270 m The brachidiniaceans have remained under-investigat- depth during the BIOSOPE (Biogeochemistry and Optics ed during decades. Gómez et al. (2005a, b) based on light South Pacific Experiment) cruise on board R/V L’Atalante and scanning electron microscopy revealed the morpho- from 26 October to 12 December 2004 (Fig. 1). Eighty logical similarities among Brachidinium capitatum, three samples collected by Niskin bottles were preserved Asterodinium gracile and Karenia papilionacea. These three with acidified Lugol’s solution and stored at 5°C. taxa coincided in distinctive morphological characters Samples of 500 mL were concentrated via sedimentation such as the straight apical groove, cingulum-sulcus junc- in glass cylinders. Along 6 days, the top 450 mL of sam- ture, prominent nucleus in the left hyposome, numerous ple was progressively slowly siphoned off with small- yellow-green chloroplasts, among other characters bore tubing. Fifty mL of concentrate representing 500 mL (Gómez et al. 2005b). Consequently the Sournia’s (1986) whole water was settled in composite settling chambers. hypothesis reappeared and the brachidiniaceans may be The entire chamber was scanned at 200× with an IX71 life stages of common coastal species that are able to pro- inverted Olympus microscope equipped with a DP70 ject body extensions. In coastal waters, brachidiniaceans Olympus digital camera and each specimen was pho- with no extensions may be polled as unidentified tographed and measured at 400× with the DP70-BSW gymnodinioid cells under routine microscopical analysis software (Olympus, Tokyo, Japan). or refereed as Karenia brevis-like cells before the descrip- The percentage of surface irradiance at each depth was tion of K. papilionacea (Iizuka 1975; Fraga and Sánchez calculated from underwater PAR (Photosynthetic Active 1985; Nézan 1998). Radiation, 400-700 nm) profile performed by a PNF-300 Within this context, a cruise along a transect of 7500 Profiling Natural Fluorometer sensor (Biospherical Km from the Marquesas Archipelago to the Chilean Instruments, San Diego, U.S.A.). The limit of the euphot- Gómez: Brachidinium, Asterodinium, Microceratium and Karenia 447 shore stations (Figs 3A, B). The highest abundance of K. papilionacea, 12 cells L–1, was recorded at 15 m depth in open waters of the Perú-Chile Current near the Juan Fernández Archipelago and 8 cells L–1 near the Marquesas Archipelago (Fig. 3A). However, in these regions the abundance was higher if the specimens that cannot be strictly ascribed to K. papilionacea are included (Figs 4I, J) Brachidinium and Asterodinium are easily identifiable due to the distinctive body extensions. The cell body of K. papilionacea corresponded to that of Brachidinium lack- ing the extensions, maintaining the distinctive apical Fig. 2. Histograms of the width at the cingulum level of the process, the prominent round to oval nucleus located in records of A. Karenia papilionacea, B. Brachidinium capitatum the left hyposome and the yellow-green pigmentation. and C. Asterodinium gracile. The cell outline of the “standard” K. papilionacea showed a butterfly (Figs 4A-C) or Mexican-hat shape (Figs 4D-F). ic zone corresponds to the depth where PAR is reduced
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