UNIVERSIDAD COMPLUTENSE DE MADRID FACULTAD DE CIENCIAS BIOLÓGICAS TESIS DOCTORAL MEMORIA PARA OPTAR AL GRADO DE DOCTOR PRESENTADA POR Fernando Gómez Pérez DIRECTOR: María Blanca Pérez Uz Madrid, 2015 © Fernando Gómez Pérez, 2007 Diversidad y biogeografía de dinoflagelados marinos : notas en la taxonomía de algunos de los grupos menos conocidos Departamento de Microbiología III Diversidad y biogeografia de dinoflagelados marinos Notas en la de les grupos de aigunos conocîdos ^6 i'- ,-■. y i f f 'fiS - "Una de las creaciones mas prodigiosas de la Naturaleza, de las que mas sublimes encantos enderran para el contemplador del Universe y mas elevan el espiritu a las serenas y etéreas esferas del In fin ite , es, sin duda, la de eses misterieses seres dim inutes, larges sigles ignerades de la humanidad, y aun hey tetalm ente inadvertides para la inmensa mayena de las gentes que per metives varies no auxilian su defidente vista cen el pederese auxilie del micrescepie" Carus Falcon, 1903 A m i madre Agradecimientos Mi agradecimiento a Fidel Echevarria y Carlos M. Garcia per darme la oportunidad de analizar mis primeras muestras de fitoplancton y a Manuel Varela per las primeras guias de identificacion. Hervé Claustre me ha proporcionado muestras del Méditerranée y del Pacifice Sur. En Japon, Ken Furuya me prepercieno excelentes muestras y me die la m ayor estabilidad laberal hast a ahera, 20 meses sin cambiar de laberaterie. De Yukie Nagahama aprendi técnicas de micrescepia y Yasuwe Fukuye cempartio cenmige su bibliegrafia sebre dinoflagelados. De regreso a Eurepa, Sami Seuissi me perm itio continuar estudiande el fitoplancton. Diez ahes tras de mi licenciatura, Blanca Pérez Uz me ha facilitade cempletar la tesis doctoral que tantas limitaciones me ha creado estes ahes. Indice Agradecimientos 1. Introducciôn a les dinoflagelados 1.1 Historia de las investigaciones sobre dinoflagelados 1.1.1 Observaciones pre-microscôpicas.................................................................. 8 1.1.2 Primeras observaciones microscôpicas......................................................... 10 1.1.3 De Cilioflagellata a Dinofiageliata..................................................................19 1.1.4 Los dinoflagelados en Espana........................................................................29 1.1.5 La biologia molecular en la ultima década.....................................................43 1.2 cQué son los dinoflagelados? 1.2.1 Células môviles 1.2.1.1 Flagelo transversal y orientaciôn........................................................ 46 1.2.1.2 Flagelo longitudinal y desplazamiento..................................... 48 1.2.2 El dinocarion 1.2.2.1 Ultraestructura..................................................................................... 49 1.2.2.2 Bioluminiscencia................................................................................... 51 1.2.3 Cloroplastos 1.2.3.1 Ultraestructura y tipos......................................................................... 51 1.2.3.2 RuBisCO................................................................................................ 52 1.2.4 Consecuencias ecologicas derivadas de su ultraestructura........................ 53 2. Objetivos.........................................................................................................................55 3. Resultados (Articulos) 3.1 Diversidad y biogeografia 3.1.1. cCuàntas especies? Gomez, F. 2005. A list of dinoflagellates in the world oceans. Acta Botanica Croatica 64, 129-212............................................................................................57 3.1.2. Biogeografia Gomez, F., 2003. Checklist of Mediterranean free-living dinoflagellates. Botanica Marina 46, 215-242............................................................................142 Gomez, F. y Boicenco, L., 2004. An annotated checklist of dinoflagellates in the Black Sea. Hydrobiologia 517, 43-59.....................................................170 Gomez, F., 2006. Endemic and Indo-Pacific plankton in the Mediterranean Sea: A study based on dinoflagellate records. Journal o f Biogeography 33, 261- 270.......................................................................................................................187 3.2 Taxonomia y distribuciôn de dinoflagelados poco conocîdos 3.2.1 Brachidinium, Asterodinîum, Microceratium Gômez, F., 2003. New records of Asterodinium Sournia (Brachldiniales, Dinophyceae). Nova Hedwigia 77, 331-340.....................................................198 Gômez, F. y Claustre, H., 2003. The qems Asterodinium (Dinophyceae) as a possible biological Indicator of warming in the Western Mediterranean Sea. Journal o f the Marine Biological Association of United Kingdom 83, 173- 174......................................................................................................................208 Gômez, F., Yoshimatsu, S. y Furuya, K., 2005. Morphology of Brachidinium capitatum F.J.R. Taylor (Brachidiniales, Dinophyceae) collected from the western Pacific Ocean. Cryptogamie Aigoiogie 26, 165-175....................210 Gômez, F., Nagahama, Y., Takayama, H. & Furuya, K., 2005. Is Karenia a synonym of Asterodinium-Brachidinlum? (Gymnodiniales, Dinophyceae). Acta Botanica Croatica 64, 263-274................................................................221 Gômez, F., 2006. The Dinoflagellate Genera Brachidinium, Asterodinium, Microceratium and Karenia in the Open SE Pacific Ocean. Aigae 21, 445- 452...................................................................................................................... 233 Gômez, F., 2007. Observations on a distinctive H-shaped dinoflagellate. An example of the projection of body extensions in gymnodinioid cells. Acta Botanica Croatica 66, aceptado.............................................................. 241 3.2.2 Ceratoperidinium Gômez, F. y Abboud-Abi Saab, M., 2003. Records of Ceratoperidinium Margalef (Dinophyceae) from the Mediterranean Sea. Vie et Milieu 53, 43-46.................................................................................................................. 251 Gômez, F., Nagahama, Y., Fukuyo, Y. y Furuya, K., 2004. Observations on Ceratoperidinium (Dinophyceae). Phycoiogia 43, 416-421........................255 3.2.3 Gynogonadinium gen. prov. Gômez, F. Gynogonadinium aequatoriale, gen. et sp. nov. a new dinoflagellate from the open western Equatorial Pacific. Aigae, enviado..............................262 3.2.4. Noctilucales: Scaphodinium, Petalodinium, Leptodiscus, Spatulodinium, Kofoidinium, Pomatodinium. Gômez, F. y Furuya, K., 2004. New records of Scaphodinium mirabile (Dinophyceae), an unnoticed dinoflagellate in the Pacific Ocean. Phycological Research 52, 13-16......................................................................274 Gômez, F. y Furuya, K., 2005. Leptodiscaceans (Noctilucales, Dinophyceae) from the Pacific Ocean: First records of Petalodinium and Leptodiscus beyond the Mediterranean Sea. European Journal o f Protistology 41, 231-239...............................................................................................................278 Gomez, F. y Furuya, K. 2007, Kofoidinium, Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. European Journal of Protistology 43, aceptado................................................ 287 Gomez, F. y Souissi, S. On the ecology and unusual life cycle of the dinoflagellate Spatulodinium pseudonoctiiuca in the NE English Channel. Comptes Rendus Biologies, enviado................................................................. 297 3.2.5. Dinophysiales: Histioneis Gomez, F., 2005. Histioneis (Dinophysiales, Dinophyceae) from the western Pacific Ocean. Botanica Marina 48, 421-425.....................................309 Gomez, F., 2007. Synonymy and biogeography of the dinoflagellate genus Histioneis (Dinophysiales, Dinophyceae). Revista de Biologia Tropical 55, aceptado..............................................................................................................314 4. Discusion 4.1. Diversidad y biogeografia 4.1.1. dCuantas especies?....................................................................................... 340 4.1.2. Biogeografia..................................................................................................345 4.2. Taxonomia y distribution de dinoflagelados poco conocidos 4.2.1. Brachidinium, Asterodinium, Microceratium...............................................353 4.2.2. Ceratoperidinium...........................................................................................355 4.2.3. Gynogonadinium gen. prov..........................................................................355 4.2.4. Noctilucales: Scaphodinium, Petalodinium, Leptodiscus, Spatulodinium, Kofoidinium, Pomatodinium..............................................356 4.2.5. Dinophysiales: Histioneis............................................................................. 357 5. Conclusiones.................................................................................................................358 6. Bibliografia.................................................................................................................... 360 1. Introducciôn a les dinoflagelados 1.1 Historia de las investigaciones sobre dinoflagelados 1.1.1. Observaciones pre-microscôpicas Los dinoflagelados han sido conocidos desde siempre. Segûn algunas teonas los primeros hominidos comenzaron a consumir mariscos caracterizados por altos contenidos en acidos grasos poli-insaturados y eso permitio el desarrollo del cerebro humano (Broadhurst et al., 1998). Algunas especies de dinoflagelados producen toxinas que se acumulan en mariscos y peces. Asi que estos primeros hominidos ya sufrieron las consecuencias de estos primeros contactos con los dinoflagelados. Las grandes proliferaciones de dinoflagelados, en su mayor parte asociadas con especies tôxicas, son capaces de producir coloraciones del agua. Este fenômeno, conocido comùnmente como mareas rojas, ha recibido multitud de nombres en la bibliografia cientifica como proliferaciones o floraciones algales nocivas (en inglés como Harmful Algal Blooms o su acrônimo "HAB") (Ochoa et al., 2003). Aunque es comùn referir como primer ejemplo de mareas rojas a la primera de las plagas que azotaron Egipto en tiempos de Moisés cuando "las aguas del Nilo se transformaron en sangre..." (Éxodo 7: 19-21; 1491 a.C.), ese ejemplo es muy dudoso que estuviese asociado con dinoflagelados porque las mareas rojas de dinoflagelados son poco frecuentes en aguas fluviales. Anos mas tarde, los israelitas ahadieron el marisco en su lista de alimentes prohibidos, alejandoles de los problèmes causados por los dinoflagelados (Deuteronomio 14: 9-10, ~1451 a.C.). Los antiguos griegos atribuian las mareas rojas a la furia de Neptuno. En la Edad Media se hablaba de la 'purga de mar' como una purificaciôn de los fondes marinos y muchas otras teorias aparecieron hasta finales del siglo XIX (Sobrino, 1918; Kofoid y Swezy, 1921). En la sabiduria popular aparecian reglas como evitar comer mariscos en los meses que no tuvieran la letra "r", es decir entre mayo y agosto, cuando los dinoflagelados suelen alcanzar sus mayores abundancias. No es posible diferenciar a simple vista el marisco contaminado, asi que las intoxicaciones han continuado, sobre todo en islas tropicales donde el marisco es casi la ùnica fuente de protemas. Ademàs de las mareas rojas, otro fenômeno visible asociado con los dinoflagelados es la bioluminiscencia. Las primeras referencias conocidas aparecen en el Mediterraneo (Aniximenes, 500 a.C.; Aristoteles, 350 a.C.; Titus Livius, 215 a.C.; revisado en Harvey, 1957). En las noches mas oscuras durante el verano se veian pequenos destellos luminosos en los rompeolas y las estelas de los barcos dejaban un rastro de luz tenue. Este fenômeno es mas llamativo en aguas tropicales como en la Bahia Fosforescente de Puerto Rico o el Fire Lake en Bahamas, pero la presiôn turistica terminé por a Itéra r las comunidades de dinoflagelados. En el 77 a.C. el naturaliste griego Plinio describe 'fuegos que aparecen repentinamente en las aguas'. La palabra griega "pyrrhos" (=fuego, llama) séria dos milenios mas tarde usada para nombrar a los dinoflagelados como Pyrrhophyta (Pascher, 1914). En la novela '20.000 léguas de vlaje submarino' escrita por Julio Verne en 1869, el capitan Nemo a bordo del 'Nautilus' describiô en su paso por el Indico: "Era un 'mar de leche', una balsa de agua que brillaba en la oscurldad...deblda a la presencla de mirfadas de Infusorlos". Recientemente se publicô por primera vez una imagen de satélite de un ^mllky sea' con mas de 250 Km. de longitud (Miller et al., 2005). En este caso se trataba de bioluminiscencia y no del color bianco asociado con la proliferaciôn de aigunos cocolitofôridos. A menor escala la bioluminiscencia es un fenômeno comün en mares tropicales, especialmente en el Océano Indico, Goifo Pérsico y el Mar del Sur de la China. Los marinos describen como unos 'discos' o 'ruedas' brillantes se desplazan a ras de las aguas (Herring y Horsman, 1985). En el Océano Pacffico LIngulodInlum (=Gonyaulax) polyedra tiende a agruparse y migrar verticalmente formando circulas luminosos de centenares de metros de diametro. No han faltado interpretaciones sobre el origen de estas luces como bases submarinas de OVNIs (Ribera, 1966). Desde un punto de vista ecolôgico, la bioluminiscencia en dinoflagelados se ha interpretado como un mecanismo que les permite reducir la presiôn de sus depredadores. En la noche cuando el dinoflagelado détecta vibraciones de un posible depredador que se a ce rca, generalmente un copépodo, produce un destello que llama la atenciôn de un segundo depredador. Pequehos peces se acercan a la fuente de luz que esta delatando la presencia de un copépodo para depredarlo. Los copépodos 'saben' que ese destello révéla su posiciôn ante sus depredadores y se alejan rapidamente sin atacar al dinoflagelado. El minûsculo dinoflagelado bioluminiscente no es de interés para los peces y ha eliminado a su depredador directo (Buskey y Swift, 1983). Los dinoflagelados son responsables de barreras de coral de miles de kilômetros observables incluso desde el espacio. En un contexto de incremento de niveles de diôxido de carbono, las zooxantelas, unos dinoflagelados simbiôticos en invertebrados marinos (esponjas, anémonas, gasterôpodos, turbelarios, etc.) y especialmente en pôlipos {Symbiodinium spp.) son de una extrema importancia en el ciclo del carbono a través de la formacion de los arrecifes de coral (Marshall, 1996). 1.1.2. Primeras observaciones microscôpicas^ Aunque las grandes concentraciones de dinoflagelados puedan ser visibles al ojo humano, individualmente las células al ser menores de 1 milimetro, no son visibles a simple vista. Algunas especies bioluminiscentes como Noctiluca, Pyrocystis o Leptodiscus alcanzan diametros de hasta dos milimetros, siendo visibles al ojo humano, aunque no lo suficiente como para distinguir su morfologia. Desde antiguo, el pulido de crista les permitia fabricar rudimentarias lentes que apenas alcanzaban una magnificaciôn de 10 aumentos. A finales del siglo XVI comienzan a fabricarse lentes de mayor calidad, principalmente por artesanos holandeses como Z. Janssen (~1588-~1632) o J. Lipperhey (1579- 1619) que en aquel tiempo eran simplemente usadas en espectaculos. Galileo Galilei (1564-1642) conociô de la existencia de esas lentes y en 1609 las utilizô en un rudimentario 'Occhiolino', combinando una lente côncava y convexa para observa r los ojos de una mosca. Francesco Fontana (1580-1656) en Napoles usana las primeras lentes convergentes en 1618. En 1619, el holandés Cornelius Drebbel (1572-1633) présenté uno de estos primeros microscopios en Londres y en 1625 Johannes Faber (1574-1629) establece el término microscopio (derivado del griego: m/cros=pequeho y skopien=ver, observer). El fiiôsofo italiano Petrus Borellus remarcaba que el microscopio séria util para investigar los misterios de la naturaleza. En 1665, Robert Hooke (1635-1703) con un microscopio de 30 aumentos describiô unas 'celdillas' en el corcho en su Micrographia Illustrata. Dos siglos después esas 'celdillas' recibirfan el nombre de células. Antony van Leeuwenhoek (1632-1723) fabricô un microscopio que podia alcanzar hasta 270 aumentos y ayudado de una supuesta prodigiosa agudeza visual describe entre ̂ Una revision historica de la descripciôn de los primeros dinoflagelados puede encontrarse en Kofoid y Swezy (1921), Taylor (1980a) y Taylor (1987). Mi gratitud a M.O. Soyer-Gobillard (CNRS, Banyuls), M. Sandrine (Biblioteca, Banyuls) y P. Assmy (AWI-Bremerhaven) por la bibliografia y datos biogrâficos de autores. 10 1674-1716 sus observaciones de animalcules, traducidas como ''living atoms" o ' l it t le animais" en sus cartas a la Royal Society de Londres. Sus cartas constituyen la primera descripciôn de protista s. Van Leeuwenhoek incluiria las primeras descripciones de frûstulas de diatomeas en 1702, sin aparentemente ningùn dinoflagelado. Entre las especies de dinoflagelados mas accesibles estana Noctiluca, que por su gran tamano y bioluminiscencia llamaba la atenciôn a esos primeros observadores en las costas europeas y la especie epicontinental Ceratium hirundinelia, muy comùn en los embalses europeos. No esta claro quien fue el primer observador de Noctiluca con un microscopio. El yerno de Daniel Defoe, Henry Baker (1698-1774), incluyô un capitulo titulado "Of luminous water insects" en su libro Employment for the Microscope publicado en 1753. Baker cita una carta donde Joseph Sparshall describe que observé un animalcule de las costas de Norfolk (Mar del Norte) que emitia luz al ser agitado. Sparshall observé el 'insecto luminoso' con un microscopio y préparé una ilustracién para el libro de Baker, pero que al parecer no llego a tiempo a la imprenta (segun Harvey, 1957). Fueron muchos otros los observadores de la bioluminiscencia de Noctiluca en las costas atlanticas europeas, por ejemplo J.B. Leroy en 1754, J. Baster en 1957, P. Forsskal en 1762 o M. Rigaut en 1765, pero sin ilustrarla. La primera ilustracién de Noctiluca a partir de una observacién microscépica aparecena en el libro de Martinus Slabber (1740-1835) publicado en 18 partes entre 1769 y 1778. Este holandés aficionado a la zoologia, publica en 1771 su plancha V III, dibujada por P.M. Brasser y él mismo (Fig. 1), donde i lustra una Noctiluca. Fig. 1. Noctiluca, primer dinoflagelado ilustrado T # - (Slabber, 1771). Aigunos observadores de la época como Louis Joblot (1645-1723) en 1718 i lustra ban a los infusorios con formas monstruosas o satiricas y eso resta ba credibilidad a la existencia de esos organismos. A partir de 1753 en botanica y 1758 en zoologia se comenzé a utilizar la nomenclatura binomial propuesta por Cari von Linneus (1707-1778). Linneo, un botanico con poca confianza en las posibilidades del microscopio, no incluyé ninguno de los que él llamaba 'animales invisibles' hasta la edicién X del Systema Naturae en 1758, incluyéndolos en la 11 clase Vermes y en su ultimo orden, con el ambiguo nombre de Zoophyta. En la edicion X II en 1767, los pocos géneros de protistas que Linneo incluyô recibian nombres como Chaos, reflejando su desconfianza hacia esos 'animales invisibles' que se empezaban a describir. En 1753, Martin Ledermüller introduce el término 'animales de infusiones' para todos estos pequenos organismos que aparecian en infusiones. El término sena latinizado como Infusoria por H.A. Wrisberg en 1763. En 1818 aparecena el término Protozoa utilizado por primera vez por Goldfuss (1818) y aparecerian con caracter de reino: Protozoa por Owen (1859), Regnum Primigenum (Protoctista) por Hogg (1860) y Protista por Haeckel (1866) (revisado por Rothschild, 1989). En 1762 P. Forsskal (1732-1763) habia usado 'medusa noctiluca' para referirse a Noctiluca. Slabber en 1771 usa el nombre de 'medusa marina'. 'Noctiluca' ya existia para designar a otros organismos con capacidad de brillar en la oscuridad y un anélido marino, actualmente Nereis, habia recibido el nombre de 'Noctiluca marina' en el Systema Naturae de Linneo (1758). El primer nombre genérico de un dinoflagelado pudo ser Gleba, propuesto para Noctiluca en 1791 por J.G. Bruguière (1749-1798). Segûn Bütschli (1880-1882, p. 1031) Bruguière habia reproducido las figuras de Slabber (1771). Sin embargo, ya por aquel entonces el género Gieba estaba previamente ocupado y era un homônimo posterior de moluscos descritos pôstumamente en 1776 por Forsskal. El género Gieba de Bruguière no era binomial y nunca estuvo en uso. Al igual que Slabber (1771), Macartney observé Noctiluca en el Mar de Norte y en 1810 propuso el nombre Medusa scintiilans. En 1815, L. Oken (1779-1851), se refiere a Noctiluca como Siabberia, dedicando el género a M. Slabber, pero sin utilizar la nomenclatura binominal. En 1816, Lamarck (1744-1828) créa el epiteto miliaris y utiliza Noctiluca como género inspirandose en 'Noctiluque' que aparecia en un manuscrite de M. Suriray (1769-1846). En 1836, Suriray describe formalmente Noctiluca miliaris, a partir de una comunicacién fechada en 1810. Ehrenberg (1834) en su 'Das Leuchten des Meeres' propone Mammaria scintiilans para referirse a Noctiluca. El nombre Mammaria ya aparecfa listado por O.F. Müller en 1776/1777 y quedé en desuso. Otros epitetos aparecerian para describir a Noctiluca, considerando que se trataba de diferentes especies en cada océano. Busch (1851) propone Noctiluca puntata y Giglioli (1870) Noctiluca omogenea y N. pacifica. En la actualidad se acepta una sola especie como Noctiluca scintiilans 12 (Macartney 1810) Kofoid 1920 (Sournia, 1984). Noctiluca scintiilans présenta pequehas variaciones geograficas. Asi por ejemplo N. scintiilans no présenta bioluminiscencia en el Pacifico norte y solo en el sudeste asiatico proliféra la 'green Noctiluca’ que présenta unos flagelados endosimbiontes que nadan libremente dentro de la célula (Finlayson, 1826). Noctiluca no présenta la morfologia ti'pica de un dinoflagelado y se mantuvo alejado de los dinoflagelados en el grupo Cystoflagellata desde Haeckel (1873) hasta Kofoid (1920). Hoy en dia aun no esta clara su posiciôn filogenética debido a la falta de informacion de secuencias de ADN de otras Noctilucales. El primer dinoflagelado con las caracteristicas tipicas de este grupo fue publicado por el danés Otto Friedrich Müller (1730-1784) y descrito siguiendo las réglas de Linneo en su obra pôstuma Animalcula Infusoria junto con otras 300 especies de infusorios que él consideraba como un tipo de gusanos (O.F. Müller, 1786). Entre sus infusorios se encontraban los dinoflagelados epicontinentales: Bursaria {Ceratium) hirundinelia y Vorticella {Perldinium) cincta, cuyas diagnosis ya se publicaron en 1773 y Cercaria {Ceratium) tripos, una especie marina listada en 1776/1777 (ilustrada en 1781, p. 206). O.F. Müller no ilustro ningùn flagelo, pero describe una fila de pequenos cilios alrededor de la célula en su observacién del movimiento de Cercaria {Ceratium) tripos: "Motus ientus ope forte ciliorum fubtus conditorum". Las denominaciones Bursaria y Vorticella son actualmente géneros de ciliados y Cercaria no fue incluida en los trabajos posteriores de Ehrenberg, siendo un término usado para las larvas acuaticas de trematodos. 13 22 -JtdT / / Fig. 2. liustradones de los primeros dinoflagelados descritos tras Noctiluca por O.F. Müller (1786). En 1793, Franz Paula von Schrank (1747-1835) describe Ceratium pieuroceras y C. tetraceras, siendo el primer género de dinoflagelados aun vigente. En 1802 tamblén describe Ceratium macroceras. Esas especies son sinonimas de Ceratium (Bursaria) hirundinelia, muy comùn en los embalses europeos y previamente descrito por O.F. Müller. En 1830, Gustav Adolph MIchaelis (1798-1848) demostraba que los infusorlos podian producir bioluminiscencia en las aguas del puerto de Kiel. Ademas del ya conocido Cercaria (Ceratium) tripos, MIchaelis I lustra bajo el nombre de Cercaria sp. y Ceratium sp., las especies que poco después serian Prorocentrum micans Ehrenberg 1834, Perldinium (=Ceratium) fusus Ehrenberg 1834 y un ^Voivox', un Protoperidinium que podna corresponder a Perldinium divergens Ehrenberg 1841 y que recibiria el nombre Perldinium michaelis Ehrenberg 1840/1841. Después otro Perldinium michaelis Stein 1883 aparecia, quizas en referenda a especimenes que aparecen en la parte central de su plancha y que podnan corresponder a Perldinium steinii Jorgensen 1899. Michaelis ilustraba sus especimenes de Ceratium tripos con très flagelos (Fig. 3). El 'filamento motor' vibraba barriendo un area conica y Michaelis lo interprété como si hubiese varios flagelos posteriores. Esta fue la primera ilustracién de un flagelo en dinoflagelados. 14 . Fig. 3. Plancha publicada por Michaelis (1830) donde se ilustran per primera vez el flagelo de los dinoflagelados, aunque erroneamente, como 3 flagelos longitudinales. También aparecen por primera vez los géneros Protoperidinium y Prorocentrum y la especie Ceratium fusus. 15 Christian Gottfried Ehrenberg (1795-1876) en torno a 1830/1832 erigiô los géneros Peridinium y Glenodinium, agrupandolos en la familia Peridinaea. También describiô el dinoflagelado epicontinental Peridinium fuscum que después séria la especie tipo del género Gymnodinium en Stein (1878, p. 89) y el género Dinophysis en 1834/1840. Sin embargo, Ehrenberg no relacionô a Dinophysis, con los dinoflagelados que habia descrito. Las fechas de las descripciones de sus especies varian en la bibliografia: unas veces se cita la fecha de presentaciones orales, otras la publicaciôn de la diagnosis y otras la publicacion de las ilustraciones. En estos primeros nombres de dinoflagelados aparecia el término griego 'dino, dinium' (=rotaciôn, giro) que hacia referencia al caracteristico movimiento de los dinoflagelados rotando sobre su eje longitudinal y desplazandose en una trayectoria hélicoïdal. Nada tiene que ver con 'dino' en dinosaurio que viene del griego 'din-o' o 'dein-o' (=terrible, monstruoso). En Sorrento, Ehrenberg describiô Prorocentrum iima como Cryptomonas iima dentro del grupo de las criptoficeas. Ehrenberg (1838/1840) observé microfésiles y en su 'xanthidia' estaba describiendo un Peridinium fésil. A partir de fésiles también describe el género Actiniscus, que Schütt en 1891 encontraria vivo en el plancton. En 1850, el geélogo Mantell (1790-1852) habia descrito ilustrado Spiniferites, hoy en dia reconocido como la forma fésil de Gonyauiax. Estudios previos revelaban que estos organismos microscépicos eran mas simples en su organizacién que los animales superiores. Sin embargo a Ehrenberg le sorprendié la complejidad de los infusorios y présenté su monografia Die Infusoriensthierchen ais volikommene Organismen antes de que Schwann y Schleiden formulasen la teoria celular por separado en 1838-1839. Con este titulo de 'Los pequehos animales infusorios como organismos completos', Ehrenberg consideraba a los infusorios como animales en miniatura. Asi por ejemplo, los cromatéforos eran o varios, el nùcleo era la préstata y las vacuolas eran estémagos. A pesar de disponer de un buen microscopio, no parecia tener confianza en lo que observaba con grandes magnificaciones y sus estudios se limitaban a un màximo de 300 aumentos. Al no observer detalles internos de la célula, Ehrenberg continué con la idea intuitive de animales en miniatura, lo que obstaculizaba que aceptara las teorias évolutives que en 1859 Charles Darwin (1809-1882) présenté en The origin o f species by means o f natural selection. 16 Félix Dujardin (1801-1860) en 1834 fue el primero en rebelarse contra esta idea de 'pequehos animales' al demostrar que el citoplasma de los foraminiferos no era pluricelular. Dujardin divide a esos 'animales unicelulares' en funciôn de su tipo de locomociôn, Infusoria para especies provistas de flagelos o cilios y Rhizopoda para los que se desplazaban por otro medio, por ejemplo con pseudôpodos. Sin embargo la influencia de Ehrenberg era tan grande que sus ideas se mantendnan varias décadas mas, lo que no contribuyô al avance de la protistologia con independencia de la zoologia (Sokin, 2001). Por ejemplo todavia en 1891, J. Pelletan consideraba a las diatomeas como organismos pluricelulares. Dujardin (1841) describe Oxyrrhis marina, que es ahora considerado un dinoflagelado primitivo (Gao y Li, 1986). Dujardin al igual que Ehrenberg seguia viendo una fila de pequehos cilios alrededor del cingulo de los dinoflagelados (Fig. 4). Fig. 4. Ceratium tripos con una fila de cilios en el cingulo segùn Dujardin (1841). En 1845, Johannes Müller (1801-1858) introducia en Helgoland a sus estudiantes como Ernst Haeckel (1834-1919) en el estudio de los organismos microscépicos pelagicos. J. Müller fabricé una finisima malla que recogia lo que él denominaba 'Auftrieb'. En 1855 entre sus descripciones de radiolarios incluyé a Thalassicoila, que podria estar cercano a Physematium atianticum Meyen (1834). En Messina y Niza, J. Müller habia observado un infusorio bioluminiscente en sus muestras de zooplancton, con el aspecto de una Noctiluca sin apéndice y que se consideraba la forma enquistada de Noctiluca, pero en realidad debia ser Pyrocystis. Por aquel entonces, la bioluminiscencia que llamaba la atencién a los navegantes en aguas abiertas de mares tropicales se atribuia a Noctiluca. Sin embargo, en la mayor parte de los casos se debia a Pyrocystis, ya que Noctiluca suele ser mas comùn en las zonas costeras mas eutréficas. Quizas las primeras descripciones de Pyrocystis fueron las especies Mammaria adspersa von Tilesius (1814) 0 Physematium atianticum Meyen (1834), pero las ilustraciones no son suficientemente detalladas. Estos infusorios bioluminiscentes o 17 ^Infusionsthierchen' en mares calidos (Gilbert, 1819; Baird, 1830) muy probablemente se trataban de Pyrocystis pseudonoctiiuca. A partir de observaciones durante la expedicion cientifica del Challenger (1873-76) que habia circunnavegado el globo, John Murray en C. Wyville Thomson (1876) describia Pyrocystis pseudonoctiiuca y P. fusiformis, aunque inicialmente como diatomeas. En 1885, Murray incluiria las ilustraciones y discutia sobre la posiciôn sistematica de Pyrocystis como un infusorio. Segun Murray (1885), los rudimentarios analisis quimicos mostraban la existencia de silice. La pared de dinosporina que caracteriza a los quistes vegetativos de Pyrocystis era el origen de la confusion sobre su sistematica. En 1890, Haeckel incluiria el género Pyrocystis citado por J. Murray como un dinoflagelado y en 1891 lo redescribiria como Murracystis. Ahos mas tarde, la observacion de estados de vida con células que se asemejaban a Gonyauiax en el interior de los quistes de Pyrocystis llevô a Kofoid y Swezy (1921) a relacionarlo con ese grupo de dinoflagelados, confirmado recientemente mediante biologia molecular. En 1859 dos discipulos de J. Müller, Edouard Claparède (1832-1871) y Johannes Lachmann (1832-1860), publicaron sus observaciones de protistas en Bergen. Describieron el género Amphidinium, establecieron Prorocentrum como un dinoflagelado y llamaron la atenciôn sobre la formacion de quistes en dinoflagelados. Claparède y Lachmann (1858-61) dividieron a los infusorios en cuatro ôrdenes e incluyeron los dinoflagelados en Cilioflagellata. Aün se interpretaba el flagelo transversal como una fila de cilios y los dinoflagelados eran por tan to intermedios entre los ciliados y los flagelados. Los términos Ciliata y Flagellata habian aparecido recientemente con Perty y Cohn en 1852 y 1853, respectivamente. Los avances fueron escasos durante las dos décadas siguientes. Ehrenberg y sus ideas de animales en miniatura seguian teniendo una gran influencia. Los dinoflagelados se consideraban estadios embrionarios de anélidos Nereidos y eso influyô por ejemplo en la descripciôn de género Gonyauiax como una larva de un anélido (Diesing, 1866). Polykrikos, con varios nûcleos y varios pares de flagelos, fue inicialmente considerado como la larva de un turbelario pelagico, en 1873 como un ciliado por Bütschli y en 1881 Bergh lo asociaria con los dinoflagelados. En 1875 J. Warming (1841-1924) demostrô que la teca de los dinoflagelados estaba compuesta de celulosa. Warming considéré a los dinoflagelados como plantas, intermedios entre las diatomeas y las desmidiaceas. 18 Otro factor que no contribuia al avance de los estudios de dinoflagelados era la falta de microscopios. A partir de 1847 Carl Zeiss (1816-1888) comienza a fabricar microscopios en Jena, perfeccionandolos con la asistencia de E. Abbe (1840-1905) y 0. Schott (1851-1935). En 1866, Zeiss habia vendido 1000 microscopios que empezaban a llegar a los microbiologos de la época. En 1868, Filippo Pacini (1812-1883), descubridor de agente causante del côlera, diseho y mando construir un microscopio invertido, que ya eran utilizados para observar reacciones quimicas. Brandt (1881) describe las zooxantelas {Zooxanthella spp. / Symbiodinium spp.) como protistas simbiontes en radiolarios coloniales y pôlipos. Bergh (1881) describiô Dipiopsaiis, Protoceratium y Protoperidinium y dividiô el orden Cilioflagellata en dos familias, la Adinida que incluia Prorocentrum, y la Dinifera. Esta ultima la dividiô en subfamilies, Dinophyida, con Dinophysis y Amphidinium, Peridinida, para Peridinium y especies relacionadas, Gymnodinida para Gymnodinium, Hemidinium y Polykrikos. Amphidinium permanecio aun por aigunos anos lejos de Gymnodinium en las clasificaciones. 1.1.3. De Cilioflagellata a Dinofiageliata El aho 1883 fue clave debido a los trabajos de Friedrich Ritter von Stein (1818-1885), Georges Pouchet (1833-1894), Georg Klebs (1857-1913) y Paul Gourret (1859-1903). 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I il I î I iii i! % s y u a 8 s 2) & ü u - - g g .=c g .Uh =I -o :S ^ g 1 2 , ; q g S g a % o o oiiiiiii iiiiis 11 S 5 S S S 5 5 3 5 S £ S 3 5 3 5 £ 5 - ? . 3 . s £ i * R 3 3 3 3 _3 3 3 "3 3 3 0 3 0î i g s s H S S ï g g g i i l l i l i ' - ' l l l c @ s gi'a a a a a a a i* a a a a a a V a a a ̂ y a g a a a oo j\0 — - M S ' I a y ’3 — , c - go u £0 ^ *13 ^ il _ % ^ e2 I 1 v5 . y !! - g i IIcdS 00 3 3 O'1̂ % 8 i ! « ^ VO i II a 3 00 3 as il u 73 00 p C 51 X S 4= •M ^ 00 ;p I r ~0 0 0 \ 0 —•sc s D s o s c i s o s c \ c \ o ( ~ ' t ~ ' t > t ^ t ^ t ~ ~ t o t ^ t ^ r ^ e x > y z 0 0 o o o o o o o o o c o c o o o o o o o o o o o o o o o o o o o o o o o o o o ACTA BOT. CROAT. 64 (1), 2005 179 107 gômez F. g Cû o ca "9 ao O O O O O O O ' O O O '—' — — ' —' —' '—t '—I —'0\0v 0\ Os 0 \ ïîa % I î III I I * " * Iî :t % i I i l i •2 -2 .2 III o $ I i I II ï - i g ■? ji & a % ^ a; 5: a: a: — fS m Tj- 1/1 \o O 8 8 O o S 00 O' o 8 8 8 5 oc ig I I 8 I P! iil I PU I < 8 £> §. I < 2 3 ! (N 1 ; j u ON 0 \ s — H II l2 :S U V PU 'O •a B" -s ai îl ilI a I I îl Z % 1- II I I IÏg: fi' II >< -a O' o 2 S ï I II II %- %- su Su %- 0" » —I C4 m ^ Tt O o O o o O O O O O O O VI v o r ^ o o o o — 1 cu 003 oi I o K m O' 8 NO I I s w s M — II — Ô PSI a 15 I— m > , O' I cd 1 Ü ii ii IIsu O' it :3 S g 2 1 a I bq m 00 O' — Ü £ Si 'z Su> cm so o « « il - Z -C io o II UIt if u ,2i ll H Î1 I m ___ oo m oo oo I §1 itH —' |g II I" II Ti lm Q <3 i:W /] c/3 — « I- Qi P 3 I = C/3 c 1Î « X ^0Û — JÎI 5 £ 5 5 5 S S S « S 5 S S ~ 5 S S S S S â ; S S S S 5 S s' t l ' l I' 1 1 II ' il­l s a O & Hlu;11 ON o — (N Cl 'It IT) 'O r— ooono—' (Nci't-'ONOr' N C / r - ' r - ' r - r - - r - r — r— t-- r-~ oo oc o o o o o c o o o o o o O O O O O O O O 03 o o o o o o o o o o 0 0 O ' O — ' ( N C l T t o o 0 0 O ' O ' O ' O ' O 'o o o o o o o ACTA BOT. CROAT. 64(1), 2005 189 117 gô m ez F. g CQ U) Q C/n 00 V 5 CN 3d ON cS PU OjO 00 "z O O 190 ACTA BOT. CROAT. 64 (1), 2005 118 FREE-LIVING MARINE DINOFLAGELLATES O _ T W O ^ 5 2 8 "5 O(N U5 OO —' Z ) C 3 -J5 ̂I MlUP S 3" g 3 « V3 % -E O If. OO c/3 8 e ll c ? Pi ^i f I & § (N O II> I ■ÿ ® ■ a ll ii a Ü §> s I I I i| 11 Î!r- ’ i l Ü îl Îî3 -g 11 vo . 2 I" c Tt I!S S I 3 O', ON 1 Iig; 'e■§ V «U l Q,&2I 3 go Osen00 Os i pû i % s 5 ‘C •3 s .EISË 2 Î g •u < 1s 1 § • i •5 C a N O ON ‘n' 2 O & -E & NO S i o2OO O n 13 m 2 2 « - " E ,ë r-x (/: oo J ON ^ .2 S ùO I I Ou CL ü g 2 00 %'S % Oc l l ï l ON ii On' I l ^ U I 2 s u 1 1 'y ~ S, -r- : # (J Ô îi IIs 5 2 a a akj üj üj 1HP Ii il H i?§ # E 35 Ii 'Il II :s 2 Ii 1 5 c ^ îiIIi|? -J E: 2I c/); II NC O II 0 - u 11 R s 00 oîî jËo.'; ■C = 1 3 J < J? s -u % q\ t - ~ J.2 :ss IIHI I | £ g. •S S S al %a c%) s A,(k, a. û. o NO CN CN 00 à 5 " ï il •E « 11 I «C5 (U i l l | i “ l ' O iIL %, Uo 03 03 ACTA BOT. CROAT. 64 (1), 2005 191 119 gô m ez F. CO ON -a CQ % co «n % % Q 192 ACTA BOT. CROAT. 64 (1), 2005 120 I FREE-LIVING MARINE DINOFLAGELLATES g cu o .3 § 3 -2 < * c I I -i I I ! I _i M — OÜ•y S E 11 III i J111a , - , 5 l i t 1 - i i 00 iii I Q Q Q Q Q Q ^ 9 Q Q QQ QQQ Q Q Q O O m ACTA BOT. CROAT. 64 (1), 2005 193 121 gômez F. g Î5JÜ ta Q w -^2: ;c3 tW P3 ca o —nOnO ^ nOnOOnnONO 194 ACTA BOT. CROAT. 64 (1), 2005 122 FREE-LIVING MARINE DINOFLAGELLATES I I CQ Z 1 I l l s ! I f Î n o z C CQ I Î ipz 2: 2 g g 2 N8 üilil IÏ’ i l - °2 -■ & S = I l'î <3 I î iliiilillliliiltili 1 1 J 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 J 1 1 1 J 1 1 i 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 U I . Q , c u , û , Q , o . Q , C L , a , û , c , i i , a , a , Q , D , û , Q , Q . a , c . Q , Q - Q , a , a , a , a , a . N o r ^ o o o N O —'C 'i c o 'tm v o r 'O O O N O — « N r 'N 't i n N o r ^ o o o 'O — r)ir)iD»o>n>n'vO\ovo \o\o\o\o\o\o\o r-- r i fN C4 (N o G s 3ë1I13 Q u 1(C % 3518 T3TD f a1Ïi : 1 i 2 CT\ o 6 à N g :=55? Q X ■5 2 oc i ■a rr •o X CQ5l , 2 2 2cs5 5 G 1 .3 c . | .s •S 2 i s IS :sâi73 isk. 2 2 g. g. g. g.3a aaa g g g 3 p g CL (L !L CL CLIT)\o 00 O' o(N r i n Cl CN cc m m cc m cc ' s i ' « —« ; n x r ~ o o O ' 0 —'«N cn rt o o m x r ' - o o O ' O s T-' — r-i rsi r-i — n A \^v T—I WV S./V ' ' W oo oo O ' O ' O '"g 'rt P7 Tf ' ^ r t ' T t ' H 208 ACTA BOT. CROAT. 64 (1), 2005 136 FREE-LIVING MARINE DINOFLAGELLATES 2 I g < S I § -2 II O ' c 11 o' ii iII 11 II 3 a ij II I II /i X 00 O' O —O w o o o o o o — — /l iTi >/l wi >/l 2- Ç oc x ; 3 a a a ACTA BOT. CROAT. 64 (1), 2005 209 137 gôm ez F. I n 'O t 2 o III I S l T3< 3 il il a rt5 X & a 2 % S 2 k l i ii % : •S 3 5 k îii >1 a f i■iH 5 s i 0 1 I è' 1 I I 005 _ i ï U 5 I O' œ 1 i % i a - s i l i l a o î^1=2 OO oo "â 2 2 t ) u f I l l k 'il 2-3 = 5 2 a E a e I I il I! s | -% O ' OO s —, _ Ci. W O ' i l à |£ 1CT' 00 il! § 1 I îi JI ^ 5 2 a m 1 1 rt :#.3 g i 1 1 1 a i d ! »H 5S ü > ■g ■§ o C2 O m M OO D oo i l s i ï ê oo o n 0\ O ' O ' 3 -5 G L. L. 3 1 ! ” i II 11 C a a l i s i l S 5 5 IIIIII I I î ip a a O' o — r ' i m' r t ’ i / i x r ' - c i o O ' O'— r'4 f N r < i ç N ( N r / r N | ( N t N 0 4 r n un in ui un V) VI un /i —' (N rn 7j- m m m m un un un un 'X r~ 00 rn m m un un u-i 210 ACTA BOT. CROAT. 64 (1), 2005 138 FREE-LIVING MARINE DINOFLAGELLATES g i I 1 1 1 I e l i 2 o - ? I I 13 i .} i |i i f I00 n O' § J ill I III il I l i , I ill:” 3 :3 ilill liBlllilliI I I I I I I â a* a'a’a-iC O' CD —l o i m - r t - r t ’ u i t n ' o t ^ o o o ' O n »H ml/n ^ l/n «—I l/l r t g § e m ( 2 OS go 0 0 : s s 'B , 8 7 3 1 3 < A g 80 0 X • 2 .tn o \ o c/5 1 . 1 i s 1 s # 11 c/5 0 <3 %) I 1 î i 2 o o . 1 . 1 J %, Q s g < < 212 140 ACTA BOT. CROAT. 64(1), 2005 3.1. Diversidad y biogeografia: 3.1.2. Biogeografia Gomez, F., 2003. Checklist of Mediterranean free-living dinoflagellates. Botanica Marina 46, 215-242. Gômez, F. y Boicenco, L., 2004. An annotated checklist of dinoflagellates in the Black Sea. Hydrobioiogia 517, 43-59. Gomez, F., 2006. Endemic and Indo-Pacific plankton in the Mediterranean Sea: A study based on dinoflagellate records. Journal o f Biogeography 33, 261-270. 141 ts o ta n ic a M a n n a v o l . 4 o , zuuj, p p . z i 3 - z 4 Z (W zuuj o y w a i t e r a e u r u y i e r • B e n in • iN e w Y o rk Checklist of Mediterranean Free-living Dinoflagellates F. Gomez D epartm ent of Aquatic Biosciences. The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657. Japan, fernando.gomez@fitopiancton.com A n an n o ta ted checklist of the free-living dinoflagellates (D inophyceae) o f the M ed ite rran ean Sea, based on lite ra tu re records, is given. The d istribu tion o f 673 species in 9 M ed ite rranean sub-basins is rep o rted . The num ber o f taxa am ong the sub-basins was as follows: L igurian (496 species), B alear-P rovençal (360), A d ri­ atic (322), Tyrrhenian (284), Ion ian (283), L evantine (268), A egean (182), A lboran (179) and A lgerian Seas (151). Introduction T he oligotrophic conditions in the M editerranean Sea could favour the richness of dinoflagellates, typical organism s of oligotrophic waters. Intensive studies have been m ade by Jorgensen (1920, 1923), Schiller (1931-37) (A dria tic Sea), Pavillard (1 9 0 p l9 3 7 ) (G ulf o f L ions and M onaco), H alim (I960) (V illefranche and A lexandria), R am pi (1939-1969) (L igurian Sea) and M argalef (1945- 1995) (Spanish coasts). H ow ever a catalogue of the d inoflagellate species recorded is no t available. The aims of this study are to provide a checklist of the species from each sub-basin and to evaluate the species richness o f dinoflagellates in the M edi­ te rran ean Sea based on a com pilation of published data. Material and Methods This study is based on literatu re records of free-living dinoflagellates (Table I), g rouped in the m ain sub­ basins o f the M edite rranean Sea (Fig. 1). References used for the e laboration of this checklist, bu t not cited in the text, checklist o r notes are listed in the A ppen­ dix. Species with their nom enclatural authorities are arranged alphabetically in each o rd er according to the classification proposed by C hrétiennot-D inet et al. (1993) with the following m odifications: the gen­ era Parahistioneis and Phalacroma have been added to the D inophysaceae; Balechina Loeblich et Loe- blich III, Plectodinium B iecheler and the recently erected genera A kash iw o G. H ansen et M oestrup, Karenia G. H ansen et M oestrup and Karlodinium J. L arsen have been added to the G ym nodiniaceae; Proterythropsis Kofoid et Swezy in K ofoid has been added to the W arnowiaceae; Pavillardinium De-Toni has been added to the O xytoxaceae; Exuviella C ienkow ski has been added to the P rorocentraceae; M ysticella C arbonell-M oore has been added to the Podolam padaceae; Calcigonellum D eflandre. Cal- cionellum D efrandre, Pentapharsodinium Indelicato et Loeblich III and Preperidinium M angin have been added to the Peridiniaceae. Synonyms have been tracked dow n and relocated in o rder to avoid duplicate entries. Synonyms, which have no t been quoted in the w orld lite ra tu re during the last decades, are not reported . Because of space lim itation, no t all the references repo rting each species for each area have been included. O nly when a taxon is repo rted in less than 3 of the 9 M edite r­ ranean sub-basins considered, is the source of the record reported . Exceptionally, also in 3 of the M editerranean sub-basins w hen the num ber o f cita­ tions was low (< 5). In som e cases, these scarcely re ­ p o rted taxa can be considered as m isidentifica tions o r unreliable records, recently described species o r rare species. The results o f this study depend on the valid identification by the au tho rs o f each reference. In m ost o f the cases, the re are no t photographs o r fig­ ures of the taxa and the verification of the records is difficult. R ecords of unarm oured cells should be con­ sidered cautiously due to the difficulties o f their identification. M ost o f these doubtfu l records are in the studies by Skolka et al. (1986) for the L ibyan w a­ ters and/or Innam orati et al. (1986,1989 a,b) for the L igurian Sea. M any species o f the ra re genera His- tioneis and H eterodinium , m ainly rep o rted by R am pi (1939-1969) and H alim (1960), w ere n o t. fu rthe r recorded after the ir first description. For recently de­ scribed taxa, the geographical d istribution is still un ­ know n beyond the type locality (e.g., som e calcare­ ous dinoflagellates). Parasitic (except D issodinium pseudolunula Swift ex E lb rach ter et D rebes) and sym biotic species (i.e., Sym biod in ium F reuden tha l) have been excluded. F reshw ater species have been excluded [e.g., Peridiniella catenata (L evander) Balech, P. danica (Paulsen) O kolodkov et D odge, etc]. Som etim es these species are rep o rted from off­ shore w aters especially in sub-basins such as the A driatic o r A egean Seas. Taxa only rep o rted from the identification of cysts have been excluded except 142 mailto:fernando.gomez@fitopiancton.com 216 F. Gômez Table I. References considered for each M editerranean sub-basin (references from the Appendix are excluded). Alb Arg Bal Tyr Lig Ion A dr Aeg Lev 13 52 4 3 12 21 3 59 1-2 33 56 8 -9 6 14-18 149 10 73-74 40 56 87-88 24 19 49 151 20 82-83 46 100 127 34 23 51 22 126 65-66 119 47 27-30 57-58 50 81 60 32 61-64 71-72 83 68-69 38-39 75-77 141 85-86 96-99 54-55 84 150 106-107 101-105 58 89-93 163-167 126 115-116 70 116 173-176 118 95 125 - 120-122 108-113 129-140 168-169 117 160-161 171-172 128 143-144 146-148 151 162 177-178 45“N 401̂ 35"N 3(TN iourian Baiaar Provençal TyrrfMwtlan Algerian Alboran Ionian Levantine -5’ W 0“ 5”E 10» E 15'E 20» E Fig. 1. Map of the M editerranean sub-basins. 25» E 30» E 35» E w hen live cells have germ inated from cysts (Ci- m iniello et al. 2000, D ’O nofrio et al. 1999, M eier et al. 2002): Results M editerranean free-living planktonic dinoflagellates w ere rep resen ted by 673 species w ith 604 and 480 species reported in the w estern and eastern basins respectively (Table II). The L igurian (74% ), Balear- P rovençal (53 % ). A dria tic (48 % ), Tyrrhenian = Io n ­ ian (42% ) and L evantine (40% ) Seas showed the highest num ber of species w hereas the A egean (27% ), A lboran (26% ) and A lgerian (22% ) Seas show ed the lowest num ber of species. Acknowledgements I acknow ledge the financial support by the Spanish M inistry o f Science and Technology and by the E u ro ­ pean Com m ission (ICB2-CT-2001-80002). I thank for the helpful com m ents and suggestions by four re ­ viewers and the Editor. This checklist has been m ade possible w ith the collaboration of m any colleagues supplying less accessible literature. Accepted 22 December 2002. 143 \_necKUSi ui ivicuiierrancan ircc-iiving uinuiiagcuaies z,i / Table 11. List of taxa and their distribution. Dinophyceae West et Fritsch 1927 Alb Alg Bal Tyr Lig Ion A dr Aeg Lev Reference no. Actiniscales Sournia 1984 Actiniscaceae Kiitzing 1844 A chradina Lohmann 1903 A ch rad ina p u k h ra Lohmann + + 76,116 Actiniscus E hrenberg 1843 Actin iscus pentasterias (Ehrenberg) Ehrenberg + + + + Brachydiniales Loeblich 111 ex Sournia 1984 Brachydiniaceae Sournia 1972 Asterodinium Sournia 1972 A ste rod in ium gracile Somnm^ + + + 1 , 5 7 A ste rod in ium Ubanum A h h o u d -A h i Saah^ + + 2,57,58 Brachydinium F.J.R. Taylor^ B rachyd in ium capitatum F.J.R. Taylor + + + + B rachyd in ium ta y lo rii Sournia + 102 D esm om onadales Pascher 1914 Desm ocapsaceae Pascher 1914 Desmocapsa Pascher 1914 Desmocapsa gelatinosa Pascher^ + + 75,76,77.145 H aplodiniaceae Lindem ann 1928 H aplod in ium Klebs 1912 H a p lo d in iu m antjoliense Klebs'* + 75 Dinococcales Pascher 1914 G loeodiniaceae Pascher ex Schiller 1937 Gloeodinium Klebs 1912 G lo e o d in ium m arin u m Bouquahem ^ + + 12,103,160 Thoracosphaeraceae Schiller 1930 Thoracosphaera K am ptner 1927 Thoracosphaera he im ii (Lohm ann) Kamptner* + + + + + + Dinophysales Lindem ann 1928 Citharistaceae Kofoid et Skogsberg 1928 Citharistes Stein 1883 Citharistes apsteini Schiitt + 81 Citharistes regius S tein + + + D inophysaceae Stein 1883 Am phisolenia Stein 1883 A m ph iso len ia bidentata Schroder + + + + + + + + + A m ph iso len ia bispinosa Kofoid + 29 A m ph iso len ia b re v ica u d a K o io id + 91,139 A m phiso len ia clavipes Kofoid + 1,86 A m ph iso len ia com planata Kofoid et Skogsberg + 91 A m ph iso len ia extensa Kofoid + + + 33,80,90 A m ph iso len ia g lob ife ra Stein + + + + + + + + + A m ph iso len ia in fla ta M n n a y e tV ^ \ t t in g + + 91,105 A m ph iso len ia lem m erm anni Kofoid + 40,46 Am phiso len iapa laeo thero ides Kofoid + 91 A m ph iso len ia pa lm ata Stein + + + + + A m ph iso len ia quadrisp ina K o fo id + 1,86*^" A m ph iso len ia rectangulata Kofoid + + 148,168 A m ph iso len ia sigma Halim^ + 66 A m ph iso len ia spimdosa K o fo id + + + + + + + A m ph iso len ia truncata Kofoid et M ichener + + + + + Dinophysis E hrenberg 1839 ( - Phalacrom a Stein 1883 pa rtim .) D inophys is acum inata C laparède et Lachmann** + + + + + + + + + D inophys is acuta Ehrenberg^ + + + + + + + + D inophys is alata Jorgensen'** + + + + + D inophysis am andula (Balech) Sournia" + + + + + + D inophys is apicata (Kofoid et Skogsberg) + 125 A be vel Balech D inophysis apicu lata M eunier'- + 91 D inophys is biceps Schiller + + 138,145 144 z lô h Cjomez Table II. (continued) Dinophyceae West et Fritsch 1927 Alb Alg Bal Tyr Lig Ion A dr Aeg Lev Reference no. Dinophysis caudata Saville-Kenl + + + + + + + + + Dinophysis circumsuta (Karsten) Balech + + + + + + Dinophysis dentata Schiller + + 77,145.175 Dinophysis diegensis Kofoid'-^ + + + 76,168,175 D inophysis exigua Kofoid et Skogsberg + 81 Dinophysis fo r t i i Pavillard''* + + + + + + + Dinophysis hastcita Stein'* + + + + + + + + Dinophysis irregu laris (Lebour) Balech + 175 Dinophysis m inuta (Cleve) Balech + 150 Dinophysis in itra (Schütt) Abé vel Balech'* + + + + + + + + Dinophysis monacantha Kofoid et Skogsberg + 95 Dinophysis ovum Schü tt'' + + + + + + + + Dinophysis parva Schiller'** + + + + Dinophysis punctata Jorgensen + + + + Dinophysis pus illa Jorgensen + + 76,115 Dinophysis recurva Kofoid et Skogsberg"* + + + + + + + Dinophysis rete Sournia^" + 173,175 Dinophysis rotundatum Claparède et Lachmann + + + + + + + + + Dinophysis saccidus Stein-' + + + + + + + + + Dinophysis schilleri Sournia^^ + + + + Dinophysis schroederi Pavillard + + + + + + + Dinophysis schuettii Murray et Whitting-^ + + + + + + + + Dinophysis s im ilis Kofoid et Skogsberg-'* + + 81,122.168 Dinophysis sphaerica Stein + + + + + + + + + Dinophysis spinosa Rampi + + + + + Dinophysis tripos G ourret + + + + + + + + + Dinophysis iiracantha Stein + + + + + + + H istione is Stein 1883 (= P arah istione is Kofoid et Skogsberg \ 92 'ipa rtim .) H istioneis alata Rampi + 136 Histioneis bernhard ii Rampi + 140 Histioneis cerasus Bohm + 10 Histioneis depressa Schiller + + + + Histioneis detonii Rampi^* + 136 Histioneis elegans Halim + 64 Histioneis expansa Rampi + 136 Histioneis fa o u z ii Halim + 64,140 Histioneis frag ilis Bohm in Schiller + 149 Histioneis gubernans Schütt + + 130,140,176 Histioneis h ippoperoides Kofoid et Michener + 81 Histioneis hya lina Kofoid et Michener + + 81.149 Histioneis im bricata Halim + 64 Histioneis inclinata Kofoid et Michener + + + 47,136,149 Histioneis isselii Forti + + 51,141 Histioneis joergensenii Schiller + + + + + Histioneis k o fo id ii Forti et Issel +. . + 50,95,141 Histioneis ligusiica Rampi + 133,136 Histioneis long ico llis Kofoid + + + + Histioneis marchesonii Rampi + + 34,133 Histioneis oxypteris Schiller + + 140,145 Histioneis p a v illa rd ii Rampi + 129 Histioneis ram p ii Halim + 64 Histioneis remora Stein + + 81,122 Histioneis robusta Rampi + 140 Histioneis speciosa Rampi + 140 Histioneis subcarinata Rampi + + 99,136 Histioneis sublongicollis Halim + 64 Histioneis variah ilis Schiller + + + Histioneis v illa franca Halim + 64 Histioneis vouckii Schiller + + + 145 LtiecKiisi oi Meaiierranean iree-iivmg amoiiageiiaies Z iv Table II. (continued) D inophyceae West ei Fritsch 1927 Alb Alg Bal Tyr Lig Ion A dr Aeg Lev Reference no. Ornithacercus francescae (M urray et Whitting) + 4 4 Balech-* O rn ithoce ra is geniculatus Dangeard + + 4 Ornithacercus heteroporiis Kofoid + + + + + 4 4 Ornithacercus m agnificus Stein + + + + + + 4 4 4 Ornithacercus quadratus Schütt^’* + + + + 4 4 4 Ornithacercus splendidus Schütt^* + + + 4 Ornithacercus stein ii Schiitt emend. Kofoid et + 4 4 Skogsberg-** Ornithacercus th u n iii (Schmidt) Kofoid et Skogsberg + + 33,115 P arah is tione is Kofoid et Skogsberg 1928 { -H is t io n e is Stein 1883 partim .) Parahistioneis acutifann is Rampi + 136 Parahistioneis karstenii (Kofoid et Michener) + 129 Kofoid et Skogsberg'** Parahistioneis mediterranea Schiller + + 4 Parahistioneis para fo rm is Kofoid et Skogsberg + 4 81,136 Parahistioneis sphueraidea Rampi + 4 73,136 Parahistioneis varians Bdhm in Schiller 4 10 P ha la c ro m a Stein 1883 { - D inophys is Ehrenberg 1839 pa rtim .) Phalacrom a acutum (Schiitt) Pavillard" + + 4 + 4 Phalacrom a argus Stein + + + + + 4 4 Phalacrom a b ipa rtitiun Kofoid et Skogsberg + 99 Phalacrom a cuneus Schiitt + + + + + 4 4 Phalacrom a doryphoriun Stein + + + + + + 4 4 Phalacrom a expulsum (Kofoid et Michener) Kofoid + + 64,69,99 et Skogsberg'- Phalacroma favus Kofoid et Michener + + + + 4 4 Phalacrom a nasutum S tein" + + + + + + Phalacrom a operculatum Stein + + + 4 Phalacrom a ovatum (Claparède et Lachmann) + + + + + + 4 Jorgensen Phalacrom a parvu lum (Schiitt) Jorgensen + + + + + 4 4 4 4 Phalacroma porod ictyum Stein + + + 4 4 Phalacrom a praetextum Kofoid et M ichener + 95 Phalacrom a pu lche llum Lebour + + + + 4 4 4 Phalacrom a striatum Kofoid + 4 4 80,125,173, 175 Triposo len ia Kofoid 1906 Triposolenia b icorn is Kofoid + + + 4 4 4 Triposolenia longicorn is Kofoid + 76 Triposolenia truncata Kofoid + + + 4 4 4 Oxyphysaceae Sournia 1984 O xyphysis Kofoid 1926 Oxyphysis oxytoxoides Kofoid + + 4 4 - . - X V - ; . Gymnodiniales Lemmermann 1910 : - ' 4 - .T -. ' Gymnodiniaceae Lankester 1885 A k a sh iw o G. Hansen et M oestrup 2000 A kash iw o sanguinea (Hirasaka) G. Hansen et + + + + 4 4 4 4 M oestrup" A m p h id in iu m Claparède et Lachmann 1885 A m p h id in iu m acutissimum Schiller + + + 4 4 A m p h id in iu m acutum Lohmann + 4 4 A m p h id in iu m carterae H ulburt + 4 1,168 A m p h id in iu m conns Schiller + 4 77,145 A m p h id in iu m cras.sum L ohm ann" + + + 4 4 4 A m p h id in iu m cucurbitella Kofoid et Swezy 4 149 A m p h id in iu m curvatum Schiller + 4 4 A m p h id in iu m extensum Wulff + 4 75,76,149 A m p h id in iu m flagellans Schiller + 4 4 146 Z2U F. Gomez Table II. (continued) Dinophyceae West et Fritsch 1927 Alb Alg Bal Tyr Lig Ion A dr Aeg Lev Reference no. A m ph id in ium glaucum Conrad 4 76 A m ph id in iu m globosum Schroder + 4 4 4 4 A m ph id in iu m hya linum Entz 4 4 77,149 A m ph id in iu m in fla tum Kofoid + 127 A m ph id in iu m kesslitzi Schiller 4 4 4 A m p h id in iu m lacustn fonne Schiller'* + 4 4 A m p h id in iu m lanceolatum Schroder 4 4 4 A m ph id in iu m latum Lebour + 4 4 A m p h id in iu m lissac Schiller 4 4 76,77,175 A m p h id in iu m ocean ia im Lohmann 4 4 75,149 A m ph id in iu m operculatum Claparède et Lachm ann" + + 4 145,177 A m ph id in ium ovoideum (Lemm erm ann) 4 76 Lemmermann A m ph id in iu m pe lluc idum H erdm an 4 76 A m ph id in ium roseolum (Schmarda) Schiller 4 149 A m ph id in iu m schroederi Schiller" + 4 4 4 A m ph id in iu m sphenoides W ulff" 4 4 76,149 A m ph id in iu m stigmatum Schiller 4 4 4 A m ph id in iu m turbo Kofoid et Swezy 4 4 77.81 A m ph id in iu m vasculum Kofoid et Swezy 4 149 A m ph id in iu m vigrense Woloszynska 4 76 B a lech ina Loeblich et Loeblich III 1966 Balechina coerulea (Dogiel) F.J.R. Taylor 4 4 76,149 Balechina m arianae F.J.R. Taylor^* 4 160 C och lod in ium Schiitt 1896 C ochlodin ium achrom aticum Lebour + 4 76,102 Cochlod in ium adria ticum Schiller 4 4 77.145 C ochlodin ium b rand tii Wulff + + 4 4 4 C ochlodin ium c itron Kofoid et Swezy 4 149 Cochlod in ium consrrictum (Schiitt) Lemmermann + 4 81,147 Cochlod in ium fa u re i Kofoid et Swezy 4 81 C ochlodin ium geminatum (Schiitt) Schiitt + 147 C ochlod in ium he lix (Pouchet) Lemmermann'" + 4 4 Cochlod in ium po lyk riko ide s Margalef"*- 4 143 C ochlodin ium pu lche llum Lebour + 4 4 Cochlod in ium pupa Lebour + 101,102 C ochlodin ium strangulatum (Schiitt) Schütt 4 4 4 Cochlod in iiun turb ineum Kofoid et Swezy 4 149 Cochodin ium schuettii Kofoid et Swezy 4 141,145 G ym nod in ium Stein 1878 emend. G. Flansen et Moestrup G ym nod in ium achrom aticum Lebour + 34,99 G ym nod in ium agile Kofoid et Swezy 4 4 76,149 G ym nod in ium ag ilifo rm e Schiller + 4 4 4 G ym nod in ium n/hn/n/n L indem ann" 4 76 G ym nod in ium am phora Kofoid et Swezy 4 76 G ym nod in ium arcticum Wulff + 4 4 4 G ym nod in ium attenuatum Kofoid et Swezy 4 4 76,149 G ym nod in ium auratum Kofoid et Swezy 4 4 76,149 G ym nod in ium aureolum (H ulburt) G. H ansen" + 4 4 4 4 G ym nod in ium aureum Kofoid et Swezy + 4 101,149 G ym nod in ium baccatum Balech + 34 G ym nod in ium b iconicum Schiller + 4 4 4 G ym nod in ium canus Kofoid et Swezy 4 4 86,149 G ym nod in ium caput Schiller 4 4 4 4 76,145,149 G ym nod in ium carinatum Schilling + 127 G ym nod in ium catenatum G raham " •** + + 13,56 G ym nod in ium cinctum Kofoid et Swezy 4 76 G ym nod in ium conicum Kofoid et Swezy" 4 4 22,149 G ym nod in ium c o rii Schiller 4 4 4 4 G ym nod in ium costatum Kofoid et Swezy + 99 147 U i iV icuiLC i i a i f c u i i i i c c - u v : i i ^ Table 11. (continued) D inophyceae West e/Fritsch 1927 Alb Alg Bal Tyr Lig Ion A dr Aeg Lev Reference no. G ym nod in ium cucumis Schütt + + + 4 G ym nod in ium dip loconus Schütt + + 4 G ym nod in ium dissim ile Kofoid et Swezy + 4 76,149 G ym nod in ium elongatum H ope + 4 144,149 G ym nod in ium flavum Kofoid et Swezy + 4 76,81 G ym nod innun fu lv u n i Kofoid et Swezy 4 149 G ym nod in ium fuscum (Ehrenberg) Stein + + 4 G ym nod in ium galeaeforme M atzenauer 4 81 G ym nod in ium gelbum Kofoid 4 81 G ym nod in ium gibberum Schiller + + 4 4 G ym nod in ium gleha Schütt + + 76,147 G ym nod in ium gracile Bergh 4 149 G ym nod in ium gram m aticum (Pouchet) Kofoid et + + 4 4 Swezy^* G ym nod in ium heterostriatum Kofoid et Swezy" + + 4 4 G ym nod in ium im p iid icum (Fraga et Bravo) + + + 4 4 4 G. H ansen et M oestrup" G ym nod in ium incertum H erdm an + 76 G ym nod in ium incisum Kofoid et Swezy + 76 G ym nod in ium lachm annii Saville-Kent + 75 G ym nod in ium lineatum Kofoid et Swezy 4 149 G ym nod in ium lira Kofoid et Swezy + 76 G ym nod in ium lohm ann ii Paulsen 4 4 40,149 G ym nod in ium maguelonnense Biecheler*® + 4 9,149 G ym nod in ium m arinum Saville-Kent + 4 4 G ym nod in ium m in o r Lebour + 4 4 21,22,76 G ym nod in ium m itra tum Schiller + 76 G ym nod in ium m ultilineatum Kofoid et Swezy + 76 G ym nod in ium m ultis tria tum Kofoid et Swezy + 4 81,168 G ym nod in ium najadeum Schiller + + 4 4 G ym nod in ium nanum Schiller + + 75,76,77,102 G ym nod in ium neapolitanum Schiller + + + 4 4 G ym nod in ium opressum Conrad + + 75,76,102 G ym nod in ium ostenfeldii Schiller 4 4 75,76,145 G ym nod in ium ovulum Kofoid et Swezy 4 75,76 G ym nod in ium paulsenii Schiller 4 4 4 G ym nod in ium pu lche llum J. Larsen** + + 23,171 G ym nod in ium pu lchrum Schiller 4 4 G ym nod in ium punctatum Pouchet 4 75,76 G ym nod in ium pygmaeum Lebour 4 76 G ym nod in ium ravcnescens Kofoid et Swezy 4 76 G ym nod in ium rotundatum Klebs + 4 4 4 G ym nod in ium rubrocinctum Lebour 4 76 G ym nod in ium scopulosum Kofoid et Swezy 4 76 G ym nod in ium semidivisum Schiller 4 4 75,76,77,145 G ym nod in ium sim plex (Lohm ann) Kofoid et Swezy" + 4 4 4 4 G ym nod in ium situla Kofoid et Swezy 4 1 4 9 — G ym nod in ium sphaericum Calkins 4 149 G ym nod in ium sphaeroideum Kofoid 4 4 75,149 G ym nod in ium sulcatum Kofoid et Swezy 4 76 G ym nod in ium translucens Kofoid et Swezy 4 75 G ym nod in ium tridentatum Schiller 4 149 G ym nod in ium variabile H erdm an + 4 4 75,76,77,102, 149 G ym nod in ium vestific ii Schütt*^ + + 76,147 G ym nod in ium vouk ii Schiller + + + G ym nod in ium w u lff ii Schiller + + 77,149 G y ro d in iu m Kofoid et Swezy 1921 emend. G. H ansen et Moestrup (= G ym nod in ium Stein IS IS pa rtim .) G yrod in iu m acutum (Schün) K o fo id et Swezy + + + 148 z z / r. uoniez Table II. (continued) Dinophyceae West et Fritsch 1927 Alb Alg Bal Tyr Lig Ion A dr Aeg Lev Reference no. G yrod in ium b iconicum Kofoid et Swezy 4 149 G yrod in ium conicum Schiller 4 145 G yrod in ium contortum (Schiitt) Kofoid et Swezy** 4 4 4 4 4 G yrod in ium corsicum Paulmier, Berland, Billard et 4 4 4 Nezan G yrod inu im crassum (Pouchet) Kofoid et Swezy 4 4 4 G yrod in ium cuneatum Kofoid et Swezy 4 75 G yrod in ium fissum (Levander) Kofoid et Swezy*" 4 127 G yrod in ium fus ifo rm e Kofoid et Swezy + 4 4 4 4 4 4 G yrod in ium glaebum Hulburt 4 4 4 G yrod in ium herbaceum Kofoid et Swezy. 4 4 4 G yrod in iu fn lachryma (M eunier) Kofoid et Swezy** 4 4 4 4 G yrod in ium longum (Lohmann) Kofoid et Swezy 4 4 75,101 G yrod in ium nasutum (Wulff) Schiller 4 149 G yrod in ium ochraceum Kofoid et Swezy 4 4 77,145 G yrod in ium ovatum (G ourret) Kofoid et Swezy 4 4 60,81 G yrod in ium ovum (Schiitt) Kofoid et Swezy 4 4 144,145,147, 166 G yrod in ium parvu lum (Schiitt) Kofoid et Swezy 4 4 4 G yrod in ium pe lluc idum (Wulff) Schiller 4 4 4 G yrod in ium pepo (Schiitt) Kofoid et Swezy** 4 4 4 G yrod in ium pingue (Schiitt) Kofoid et Swezy** 4 4 4 4 G yrod in ium rubricaudatum Kofoid et Swezy 4 76 G yrod in ium spirale (Bergh) Kofoid et Swezy 4 4 4 4 4 4 G yrod in ium varians (Wulff) Schiller 4 4 Karenia G. Hansen et M oestrup 2000 Kfl/enifl èrcv/s (Davis) G. Hansen et Moestrup** + + 59.81 Karlodinium J. Larsen 2000 K arlod in ium m icrum (Leadbeater el Dodge) + 1 J. Larsen*'* Katodinium Fott 1857 ( - Massartia Conrad 1926) Katod in ium glaucum (L e b o m ) LoehUch + + + K atod in ium tubulatum (Rampi) Sournia** + 140 Plectodinium Biecheler 1934*^ Plectodinium nucleovolvatum Biecheler + + + + Pseliodinium Sournia 1972 Fseliod in iiun vaubanii Sournia 4 + + 4 4 4 Torodinium Kofoid et Swezy 1921 Torodin ium robustum Kofoid et Swezy 4 4 4 4 4 4 Zbro/fmiH/n teredo (Pouchet) Kofoid et Swezy** 4 4 4 4 2,118,145,146 Polykrikaceae Kofoid et Swezy 1921 Pheopolykrikos Chatton emend. M atsuoka et Fukuyo 1986 Pheopolykrikos beauchampii Chatton 4 24 Pheopolykrikos hartm annii {Z im m erm ann ) + 177 M atsuoka et Fukuyo Polykrikos Biitschli 1873 P olykrikos k o fo id ii ChaWon 4 4 4 4 4 Polykrikos sch w a rtz iiB ü isd û i 4 4 4 4 Ptychodiscaceae Lemmermann 1899 Ptychodiscus Stein 1883 Ptychodiscm noctiluca Stein*'* 4 4 123,137 Warnowiaceae Lindemann 1928 Erythropsidinium PC. Silva 1960 ( - Erythropsis Hertwig 1884) £r>t/?rop5id/mu/« ngde (Hertwig) P.C. Silva** 4 4 33,147 E ryth rops id in ium m in o r (Kofoid et Swezy) PC. Silva 4 101,102 E ryth rops id in ium p a v illa rd ii {K o fo id et Swezy ) 4 4 61,120 PC. Silva** Greuetodinium Loeblich III 1980 (= Leucopsis G reuet 1968) 149 cnecKiisi OI Meaiierranean iree-iiving ainoiiageiiaies Table II. (continued) Dinophyceae West et Fritsch 1927 A lb Alg Bal Tyr Lig Ion A dr Aeg Lev Reference no. G reuetodin ium cy lind ricum (G reuet) Loeblich II I" 4 62 JSematodinium Kofoid et Swezy 1921 (= Pouchetia Schütt 1895) N em atod in ium arn ia tum (Dogiel) Kofoid et Swezy** + 4 38,76,93 N em atod in ium torpedo Kofoid et Swezy + 4 81,102 Proterythropsis Kofoid et Swezy in Kofoid Proterythropsis crassicaudata Kofoid et Swezy + 101,102 W am owia Lindemann 1928 {-P ouchetia Schütt) W arnowia compacta (Schütt) Schiller + 147 W arnowia d o h rn ii Z im m erm ann + 4 101,177 W arnowia fusus (Schütt) Lindemann + 4 4 4 4 W arnowia ju n o (Schütt) Schiller + 4 101,147 W arnowia maculata (Kofoid et Swezy) Lindemann + 101 W arnowia polyphem us (Pouchet) Schiller + 4 120,149 W arnowia pu lchra Schiller 4 4 4 61,145 W arnowia rosea (Pouchet) Schiller + 4 49,121 W arnowia violescens Kofoid et Swezy 4 81 Noctilucales H aeckel 1894 Kofoidiniaceae Taylor 1976 Cymbodinium Cachon et Cachon 1967 C ym bodin ium elegans Cachon et Cachon 4 16 Kofoidinium Pavillard 1928 K o fo id in iu m p a v illa rd ii Cachon et Cachon*'* 4 17 K o fo id in iu m splendens Cachon et Cachon 4 4 1,17 K o fo id in iu m velelloides Pavillard + + 4 4 4 4 4 Pomatodinium Cachon et Cachon 1966 Pom atodin ium im patiens Cachon et Cachon + 4 15,99 Spatulodinium Cachon et Cachon 1968 S patu lod in iian pseudonoctiluca (Pouchet) Cachon et 4 4 18,173,175 Cachon ex Loeblich et Loeblich III Leptodiscaceae Kofoid 1916 Cachonodinium Loeblich 111 1980 Cachonodiniurn caudatum (Cachon et Cachon) 4 18 Loeblich 111™ Craspedotella Kofoid 1905 Craspedotella p ileo lus Kofoid 4 17 Leptodiscus Hertwig 1877 (= Pratjetella Lohmann 1920) Leptodiscus medusoides Hertwig"** + 4 4 18,70,99,171 Leptophyllus Cachon et Cachon 1964 { - Abedinium Loeblich et Loeblich 111 1966) Leptophyllus dasypus Cachon et Cachon™ 4 14 Petalodinium Cachon et Cachon 1969 Petalodinium po rce lio Cachon et Cachon 4 18 Scaphodinium M argalef (= Leptospathium Cachon et Cachon 1964) Scaphodinium m irab ile Margalef** + + 4 4 Noctilucaceae Kent 1881 Noctiluca Suriray ex Lam arck 1816 N octiluca scintillons (M acartney) Kofoid + + + 4 4 4 4 4 4 Protodiniferaceae Kofoid et Swezy 1921 Pronoctiluca Fabre-Dom ergue 1889 P ronoctiluca pelagica Fabre-Dom ergue + 4 4 Pronoctiluca rostra ta F.J.R. Taylor*" 4 1 Pronoctiluca sp in ifera (Lohm ann) Schiller + 4 4 4 Oxyrrhinales Sournia 1984 O xyrrhinaceae Sournia 1984 Oxyrrhis Dujardin 1841 O xyrrh is m arina Dujardin + + 4 4 4 Peridiniales Haeckel 1894 A mphidom ataceae Sournia 1984 150 Zz4 F. Gômez Table II. (continued) Dinophyceae West et Fritsch 1927 Alb Alg Bal Tyr Lig Ion A dr Aeg L i Amphidoma Stein 1883 ( = Pavillardinium Dc-Toni 1936 partim ., Murrayella Kofoid 1907) A m phidom a caudata HaildaF^ + + + A m ph idom a elongata Kofoid et Swezy + A m ph idom a nucula Stein'^ + + Ceratiaceae Kofoid 1907 Ceratium Schrank 1793 Ceraiium arietinum Cleve + + + + + + + 4 4 Ceratium azoricum Cleve + + + + + 4 4 Ceratium belone Cleve + + + + + + 4 4 Ceratium hreve (Ostenfeld et Schmidt) Schroder + + 4 4 Ceratium h ru n e llii Rampi^’ + Ceratium huceros (Zacharias) Schiller + + + + + + + 4 4 Ceratium candelahrum (Ehrenberg) Stein + + + + + + + 4 4 Ceratium carriense G ourret + + + + + + + 4 4 Ceratium claviger Kofoid^* + + + Ceratium coarctatum Pavillard + + + + + 4 4 Ceratium concilians Jorgensen + + + + + + 4 4 Ceratium co iito rtum (G ourret) Cleve + + + + + + + 4 4 Ceratitim contrarium (G ourret) Pavillard^^ + + + + + + + 4 4 Ceratium decliiia tum (Karsten) Jorgensen + + + + + + + 4 4 Ceratium deflextim (Kofoid) Jorgensen + + + 4 Ceratium denticulatum (Jorgensen) Paulsen^” + + 4 Ceratium d ig ita tum Schütt + + + + + 4 4 Ceratium egyptiacum Halim*' 4 Ceratitim euarcuatum Jôrgensen*- + + +■ + + + + 4 4 Ceraiium extensum (G ourret) Cleve^^ + + 4- + + + + 4 4 Ceratiutn fa lca tifo rm e Jorgensen + + + + 4 Ceratium falcatum (Kofoid) Jorgensen + + + + + + 4 4 Ceiatium fiirc a (Ehrenberg) Claparède et Lachmann + + + + + + + 4 4 Ceratium fusus (Ehrenberg) Dujardin + + + + + + + 4 4 Ceratium geniculattim (Lemm erm ann) Cleve + + + + Ceratiutrt g ibberum G ourret + + + + + + 4 4 Ceratium gravidum G ourret + •f + + + + 4 4 Ceratium hexacanthum G ourret + + + + + + 4 4 Ceratiutrt h o rrid u m (Cleve) Gran*"* + + + + + + 4 4 Ceratium iiic isum (Karsten) Jorgensen + + + + + 4 4 Ceratium in fla tiu n (Kofoid) Jorgensen + + + + + + 4 4 Ceratiutrt k o fo id ii Jorgensen + + + + + + 4 4 Ceratium lim tdus (G ourret ex Pouchet) G ourret + + + + + + + 4 4 Ceratium lineatutn (Ehrenberg) Cleve + + + Ceratiutrt lo tig iros trum G ourret + + + + + + + 4 4 Ceratium longissim iim (Schroder) Kofoid + + + + 4 4 4 Ceratium lunu la (Schimper ex Karsten) Jorgensen + + + + 4 4 Ceratiutn macroceros (Ehrenberg) Cleve + + + + + + 4 4 4 Ceratium massiliense (G ourret) Karsten + + + + + + 4 4 4 Ceratiutn m inutum Jorgensen + + + 4 Ceratium paradoxides Cleve*^^ + + 4 4 Ceratium p a v illa rd i l Jorgensen + + + + + + 4 4 4 CeraVMtn pentagonum G ourret + + + + + + 4 4 4 Ceratiutn p la tycorne Daday + + + + + + 4 4 4 Cerati.um praeo longutn (Lemm erm ann) + + + + Kofoid ex Jorgensen Ceratium pu lche llum Schroder + + + + + 4 4 4 Ceratium ratiipes Cleve + + + + + 4 4 4 Ceratiutn reflexutn Cleve 4 Cerati.um schroeteri Schroder + + 4 4 Cerati.um setaceum Jorgensen + + + + + + 4 4 Ceratium strictum (O kam ura et Nishikawa) Kofoid + + + + 4 4 4 Cerati.um sytnm etricutn Pavillard + + + + + + 4 4 4 Cerati.utn tenue (Ostenfeld et Schmidt) Jorgensen^'’ + + + + 4 149 3 3 ^ 8 134 82,119.168 1,65.86 150 151 cnecRiisi 01 Meüiierranean iree-iiving ainoiiageiiaies z z j Table II. (continued) Dinophyceae West et Fritsch 1927 Alb Alg Bal Tyr Lig Ion A dr A eg Lev Reference no. Ceratium teres Kofoid + 4 4 4 4 4 4 4 4 Ceratium trichoceros (Ehrenberg) Kofoid + 4 4 4 4 4 4 4 4 Ceratium tripos (Millier) Schiller 4 4 4 4 4 4 4 4 4 Ceratium volans Cleve^^ 4 4 4 4 4 4 4 4 Ceratium vu ltu r Cleve 4 4 4 4 4 4 4 4 Ceratocorythaceae Lindem ann 1928 CeratocorysSiQiw 1883 Ceratocorys armata (Schiitt) Kofoid Ceratocorys gou rre tii Paulsen Ceratocorys ho rrida Stein Cladopyxidaceae Poche 1913 Cladopyxis Stein 1883 (= Micracanthodinium Deflandre 1937 p a rtim .) C ladopyxis hrachio lata Stein C ladopyxis caryophyllum (Kofoid) Pavillard*"^ C ladopyxis quadrisp ina Pavillard*^ C ladopyxis spinosa (Kofoid) Schiller^ Falaeophalacroma Schiller 1928 Palaeophalacroma un ic inctum Schiller^' Palaeophalacroma verrucosum Schiller Crypthecodiniaceae Biecheler ex Chatton 1952 Crypthecodinium Biecheler 1938 C rypthecodin ium cohn ii (Seligo) Chatton'^^ G oniodomataceae Lindem ann 1928 G oniodoma Stein 1883 (= Triadinium D odge 1981, = Heteraulacus Diesing 1850 partim .) G oniodom a acum inatum (Ehrenberg) Stein^^ G oniodom a sphaericum Murray et Whitting'^'* Pyrodinium Plate 1906 P yrod in ium bahamense Plate'^'’ Gonyaulacaceae Lindem ann 1928 Alexandrium Halim emend. Balech 1989 ( - Protogonyaulax F.J.R. Taylor 1976) 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 64,168 40 A lexand rium andersonii Balech 4 27 A lexandrium balechii (Steidinger) Balech 4 4 110,156 A lexandrium catenella (W hedon et Kofoid) Balech 4 4 4 4 A lexand rium compressum (Fukuyo, Yoshida et 4 20 Inoue) Balech Ale.xandrium concavum (G aarder) Balech 4 30 A lexandrium foedum Balech 4 6,30 A lexandrium insuetum Balech 4 30 A lexandrium kutnerae (Balech) Balech 4 30 A lexandrium le d Balech 4 4 30 A lexandrium m arga le fii Balech 4 4 30 A lexand rium m inutum Halim^^ 4 4 4 4 4 4 A lexand rium ostenfeldii (Paulsen) Balech et Tangen^’ 4 4 Alexandrium pseudogonyaulax{B i&cheleT) A- V “ ■ 20:30,7 L " ' Horiguchi ex Kita et Fukuyo A lexandrium tamarense (Lebour) Balech 4 4 4 4 4 4 4 A lexandrium ta y lo rii Balech 4 4 4 A m ylax Meunier 1910 ( - Gonyaulax Diesing 1866 partim .) A m y la x biixus (Balech) Dodge"^* 4 1 A m y la x triacantha (Jorgensen) Sournia-’̂ 4 87 Gonyaulax Diesing 1866 ( - Am ylax M eunier 1910 p a rtim .) G onyau lax a fricana Schiller 4 4 4 76,138,145 G onyaulax birostris Stein 4 4 4 4 4 4 4 G onyaulax hrevisulcatum Dangeard 4 4 33,76,100,119 G onyau lax diegensis Kofoid'"" 4 4 4 4 4 4 G onyaulax digitale (Pouchet) Kofoid'"' 4 4 4 4 4 4 4 4 4 152 Z lb F. Gomez Table 11. (continued) Dinophyceae West et Fritsch 1927 Alb Alg Bal Tyr Lig Ion Adr Aeg Lev Reference no. G onyaulax elegans Rampi 4- 138 G onyaulax frag ilis (Schütt) Kofoid + + + 4 4 4 G onyaulax g lyptorhynchus Murray et Whitting'"^ + 95 G onyaulax gracilis Schiller + 4 52,167 G onyaulax h ig lile y ii Murray et W hitting"" 114 Gonyaulax hyalina Ostenfeld et Schmidt 4 4 138,173,174, 175 Gonyaulax ligustica Rampi + 4 118,138 Gonyaulax k o fo id ii Pavillard"*^ + 4 4 + 4 4 4 G onyaulax m inuta Kofoid et Michener'"-^ + 4- 4 4 4 Gonyaulax monacantha Pavillard + + + 4- 4 4 4 4 4 Gonyaulax monospina Rampi 4 4 20,138,167 G onyaulax orientalis Lindemann 4 76 G onyaulax ovalis Schiller'"^ + 4- 4 4 G onyau laxpacifica Kofoid'"^ + + + 4- 4 4 4 4 G onyaulaxpo lygram ina Stein + + + 4- 4 4 4 4 4 Gonyaulax rostrata Dangeard + 168 Gonyaulax rotundata Rampi 4 4 22,138 Gonyaulax rugosum Wailes"" 4 114,149 Gonyaulax scrippsae Kofoid + 4- 4 4 4 Gonyaulax sphaeroidea Kofoid 4 135 Gonyaulax spinifera (Claparède et Lachmann) + + + 4- 4 4 4 4 4 Diesing"" Gonyaulax tro ttii Rampi 4 138 Gonyaulax turhynei Murray et Whitting + 4 4 4 4 G onyaulax unicorn is Lebour 4 64,76 G onyaulax verior Sournia'"" + + 4- 4 4 4 4 Lingulodinium Wall emend. Dodge 1989 L ingu lod in ium in iln e ri (Murray et Whitting) Dodge' '" 4 86 L ingu lod in ium polyedra (Stein) D odge"' + + + 4- 4 4 4 4 4 Protoceratium Bergh 1881 (= Gonyaulax Diesing 1866/?a/7//?i.) Protoceratium areolatuin Kofoid + + 4 4 Protoceratium pepo Kofoid et Michener 4 138 Protoceratium reticulatum (Claparède et + + + 4- 4 4 4 4 4 Lachmann) Bütschli"^ Protoceratium spinulosum (M urray et + + 4 Whitting) Schiller Heterodiniaceae Lindemann 1928 Heterodinium Kofoid 1906 H eterod in ium agassizii Kofoid 4 125 H eterodin ium balechii Rampi + 4 138,168 H eterodin ium crassipes Schiller 4 145 H eterod in ium debeauxii Rampi 4 131 Heterod in ium dispar Kofoid et Adamson + 4 34,99,138 Heterod in ium doma (Murray et Whitting) Kofoid 4 131 H eterod in ium dub iun i Rampi 4 131 Heterod in ium fides Kofoid 4 1 H eterod in ium g lobosiim Kofoid 4 124,125,131 Heterod in ium graham ii Rampi 4 64,138 H eterod in ium inaequale Kofoid"^ + 4 64,121 Heterod in ium k o fo id ii Pavillard + 4 4 90,122,145 Heterod in ium laticeps Léger 4 90 Heterod in ium le iorhynchum (M urray et Wliitting) + 4- 4 4 Kofoid H eterod in ium mediterraneum Pavillard + 4 4 4 H eterodin ium m iln e ri (M urray et Whitting) Kofoid + 4 4 64,124,129, 175 H eterod in ium m inutum Kofoid et Michener + 4 34,81 H eterod in ium rnurray i Kofoid 4 49,64,131,139 H eterod in ium rigdenae Kofoid 4 1 153 Checklist ot Mediterranean tree-living dmoilagellates ZZ / Table II. (continued) Dinophyceae West et Fritsch 1927 Alb Alg Bal Tyr Lig Ion A dr Aeg Lev Reference no. Heterod in ium scrippsi K ofoid '" + 4 4 64,89,90,91, 124,175 Heterod in ium sinistrurn Kofoid et Adamson"-'' 4 1 H eterod in ium whittingae Kofoid 4 91,92,124, 125,139 Ostreopsidaceae Lindemann 1928 Coolia Meunier 1919 { - Ostreopsis J. Schmidt 1901 partim .) Coolia m onotis M eunier"^ + 4 4 4 Ostreopsis J. Schmidt 1901 Ostreopsis ovata Fukuyo 4 162 Ostreopsis siamensis J. Schmidt 4 4 151,161 Oxytoxaceae Lindemann 1928 Centrodinium Kofoid 1907 (= Pavillardinium De-Toni 1936p a rtim .,Murrayella Kofoid 1907partim .) Centrodin ium b iconicum (M urray et Whitting) 4 4 81,138 FJ.R. Taylor"' C entrodin ium coniplanatum (Cleve) Kofoid + 4 4 C entrodin ium elongatum Kofoid + 33 C entrodin ium eminens Bohm 4 4 91,138,175 C entrodin ium interm edium Pavillard + 4 4 C entrodin ium m axim um Pavillard + + 4 4 Centrodin ium p a v illa rd ii F.J.R. Taylor"* + + 4 4 4 4 C entrodin ium splendidum (Rampi) F.J.R. Taylor"^ 4 131,138 Corythodinium Loeblich et Loeblich III 1966 (= Oxytoxum Stein 1883pa rtim .) C orythod in ium belgicae (M eunier) F.J.R. Taylor"" 4 4 76,81.114 C orythod in ium compressum (Kofoid) F.J.R. Taylor + + 4 C orythod in ium com tric tum (Stein) F.J.R. Taylor + + + 4 4 4 4 4 4 C orythod in ium cristatum (Kofoid) F.J.R. Taylor 4 4 4 Corythod in ium curvicaudatum (Kofoid) F.J.R. Taylor 4 168 C orythod in ium diploconus (Stein) F.J.R. Taylor + 4 4 64,88,175 Corythod in ium elegans (Pavillard) F.J.R. Taylor 4 4 4 4 4 C orythod in ium fren g u e llii (Rampi) F.J.R. Taylor 4 4 4 138,168,175 C orythod in ium reticulatum (Stein) Loeblich et + 4 4 4 4 4 4 4 Loeblich III C orythod in ium tessellatum (Stein) Loeblich et + + 4 4 4 4 4 4 4 Loeblich III Oxytoxum Stein 1883 Oxytoxum aceratum Rampi 4 138 O xytoxum adriaticum Schiller 4 4 4 4 O xytoxum areolatum Rampi 4 4 4 22,68,131 O xytoxum b ru n e llii Rampi'"" 4 4 4 64,74,118,138 O xytoxum caudatum Schiller 4 4 4 4 O.xytoxum corondtu in Schiller 4 4 4 140,145,175 O xytoxum crassum Schiller 4 4 4 4 O xytoxum cribosum Stein 4 1 4 0 "- O.xytoxum curvatum (Kofoid) Kofoid'^' 4 4 4 4 O xytoxum depressum Schiller 4 4 4 4 O xytoxum elongatum Wood 4 81 O.xytoxum gladio lus Stein + 4 4 4 4 Oxyto.xum globosum Schiller'-- 4 4 4 4 O xytoxum laticeps Schiller 4 4 4 4 4 O xytoxum longiceps Schiller'"^ + 4 4 4 4 4 4 4 Oxyto.xum longum Schiller + 4 4 4 O.xytoxum m ilne ri Murray et Whitting'-" + 4 4 4 4 4 4 Oxyto.xum m inutum Rampi 4 4 4 4 4 Oxyto.xum obesum Rampi 4 140 O xytoxum ob liquum Schiller 4 4 4 Oxyto.xum ovale Schiller'^-'' + 4 4 4 4 4 4 154 228 F. Gômez Table II. (continued) Dinophyceae West et Fritsch 1927 Alb Alg Bal Tyr Lig Ion A dr Aeg Lev Reference no. O xytoxum parvum Schiller'" 4 4 4 4 4 O xytoxum punctu latum R am pi'" 4 4 55,138 O xytoxum radiosum Rampi 4 131,138 O xytoxum ram p ii Sournia'-* 4 4 29,140 O xytoxum scolopax Stein + 4- 4 4 4 4 4 4 4 Oxyto.xum sphaeroideum Stein + 4 4 4 4 4 4 O.xytoxum spinosum Rampi 4 64,131 O xytoxum subulatum Kofoid 4 4 4 29,91,105 O xytoxum turbo Kofoid 4 4 4 O.xytoxum variabile Schiller'-" 4 4 4 4 4 4 4 Oxyto.xum viride Schiller 4 4 4 4 4 Pavillardinium De-Toni 1936 (= Amphidoma Stein 1883 partim ., Murrayella Kofoid 1907) P avillard in ium ovale (Pavillard) De-Toni"" Schuertiella Balech 1988 (= Gonyaulax Diesing 1866 partim ., Oxytoxum Stein 1883 p a rtim .) Schuettiella m itra (Schütt) B alech"' Peridiniaceae Ehrenberg 1828 Calcigonellum Deflandre 1948 Calcigonellum in fu la Deflandre emend. Montresor'^^ Calciodinellum Deflandre 1947 Calciod inellum levan linw n Meier, Janofske et W illem s'" C alciod inellum operosum D eflandre '" D iplopelta Stein ex Jorgensen 1912 (= Dissodium Abé 1941 partim .) D ip lope lta bomba Stein ex Jorgensen"" D ip lope lta symmetrica Pavillard'-" D iplopsalis Bergh 1881 (= Dissodium A bé 1941 partim .) D ip lopsa lis len tic iila B e rg h '" D iplopsalopsis M eunier emend. Balech 1988 DiplopsalopsLs o rb icu laris (Paulsen) M eunier'" Diplopsalopsis latipeltata Balech et Borgese Kryptoperidinium Lindemann 1924 { - Glenodinium Ehrenberg 1837partim .) K ryp tope rid in ium fo liaceum (Stein) L indem ann '" Oblea Balech ex Loeblich et Loeblich I I I 1966 Oblea rotunda (Balech) Balech ex S ourn ia '" Pentapharsodinium Indélicate et Loeblich I I I 1986 ( - Peridinium Ehrenberg 1831 partim .) Pentapharsodinium tyrrhen icum (Balech) M ontresor, Zingone et Marino'"" Peridinium Ehrenberg 1831'"' Perid in ium quinquecorne Abé'"^ Preperidinium Man gin 1913 {= D iplopeltopsis Pavillard 1913, Zygabikodinium Loeblich et Loeblich 1111970) Preperid in ium m eunieri (Pavillard) Elbrachter'"-' Protoperidinium Bergh emend. Balech 1974'"' {= Peridinium Ehrenberg 1831 partim ., Minuscula Lebour 1925) 29,123 39 106 39 150 28.144 32,149 6,111 Pro toperid in ium abei (Paulsen) Balech'"" 4 4 4 4 4 4 P ro toperid in ium anthonyi (Fauré-Fremiet) Balech 4 76 Pro toperid in ium bipes (Paulsen) Balech'"^ 4 4 4 4 4 4 4 Pro toperid in ium bispinum (Schiller) Balech'"" 4 4 4 4 4 P ro toperid in ium brevipes (Paulsen) Balech 4 4 4 Pro toperid in ium b roch ii (Kofoid et Swezy) Balech 4 4 4 4 4 4 4 4 4 P ro toperid in ium bu lla (M eunier) Balech 4 76 P ro toperid in ium cerasus (Paulsen) Balech 4 4 4 4 4 4 4 4 P ro toperid in ium claudicans (Paulsen) Balech 4 4 4 4 4 4 4 155 »_necKiisi oi ivieuuerranean iree-iivmg uinoiiageiiaies Table II. (continued) Dinophyceae West et Fritsch 1927 Alb Alg Bal Tyr Lig Ion A dr Aeg Lev Reference no. Pro toperid in ium conicoides (Paulsen) Balech 4 40 P ro toperid in ium conicum (G ran) Balech + 4 4 4 4 4 4 4 4 P ro toperid in ium crassipes (Kofoid) Balech'"^ 4 4 4 4 4 4 4 4 P ro toperid in ium curvipes (Ostenfeld) Balech'"* + 4 4 4 4 P ro toperid in ium deficiens (M eunier) Balech 4 86 P ro toperid in ium depressum (Bailey) Balech + 4 4 4 4 4 4 4 4 P ro toperid in ium diabolus (Cleve) Balech'"" + 4 4 4 4 4 4 4 4 P ro toperid in ium divergens (Ehrenberg) Balech + 4 4 4 4 4 4 4 4 P ro toperid in ium elegans (Cleve) Balech 4 4 4 P ro toperid in ium excentricum (Paulsen) Balech 4 4 4 P ro toperid in ium exiguipes (Mangin ex Halim) Dodge 4 40 Pro toperid in ium fim b ria tu m (Meunier) Balech 4 76 P ro toperid in ium fin it im u m Balech'"" 4 4 4 4 4 P ro toperid in ium globulus (Stein) Balech'"' + 4 4 4 4 4 4 4 4 P ro toperid in ium grande (Kofoid) Balech + 4 4 4 4 4 4 P ro toperid in ium g ran ii (Ostenfeld) Balech 4 4 4 4 4 4 4 4 4 P ro toperid in ium heteracanthum (Dangeard) Balech 4 4 77,99 P ro toperid in ium h irob is (A bé) Balech 4 4 1,144 P ro toperid in ium inclina tum (Balech) Balech 4 99 P ro toperid in ium in fla tum (Okamura) Balech 4 4 4 4 4 4 Pro toperid in ium latisp inum (Mangin) Balech 4 4 4 4 P ro toperid in ium leonis (Pavillard) Balech 4 4 4 4 4 4 4 4 P ro toperid in ium ligusticum (Rampi) Balech 4 138 P ro toperid in ium maranense Tolomio 4 163,165 P ro toperid in ium marielebourae (Paulsen) Balech 4 4 4 4 4 P ro toperid in ium mediterraneum (Kofoid) Balech 4 4 4 4 4 4 4 4 4 P ro toperid in ium m inutum (Kofoid) Loeblich III 4 4 4 4 4 P ro toperid in ium mite (Pavillard) Balech 4 4 4 4 4 P ro toperid in ium n ipponicum (Abé) Balech'"- 4 4 40,150 P ro toperid in ium nudum (M eunier) Balech'"' 4 98,99 P ro toperid in ium oblongum (Aurivillius) 4 4 4 4 4 4 Parke et Dodge P ro toperid in ium obtiisum (Karsten) Parke et Dodge 4 150 P ro toperid in ium oceanicum (Vanhoffen) Balech 4 4 4 4 4 4 4 4 4 P ro toperid in ium ovifo rm e (Dangeard ) Balech 4 4 4 4 P ro toperid in ium ovum (Schiller) Balech 4 4 4 4 4 4 4 P ro toperid in ium p a llidum (Ostenfeld) Balech 4 4 4 4 4 4 4 4 P ro toperid in ium parthenopes Zingone et M ontresor 4 178 P ro toperid in ium pedunculatum (Schiitt) Balech 4 4 4 4 4 4 P ro toperid in ium pe lluc idum (Schiitt) Balech 4 4 4 4 4 4 4 4 P ro toperid in ium pentagonum (G ran) Balech 4 4 4 4 4 4 4 4 P ro toperid in ium punctu la tum (Paulsen) Balech 4 4 4 4 4 4 4 P ro toperid in ium pyrifo rm e (Paulsen) Balech 4 4 4 4 4 4 4 4 4 P ro toperid in ium quarnerense (Schroder) Balech 4 4 4 4 4 4 4 P ro toperid in ium sch ille ri (Paulsen) Balech 4 4 4 P ro toperid in ium sim ulum (Paulsen) Balech 4 4 4 4 P ro toperid in ium sinaicum (M atzenauer) Balech 4 4 76 ,77;'149 P ro toperid in ium so lid icorne (Mangin) Balech'"" 4 4 4 4 4 P ro toperid in ium sphaericum (Murray et Whitting) 4 4 4 4 4 4 Balech P ro toperid in ium sphaeroides (Dangeard) Balech'"" 4 4 4 P ro toperid in ium sphaeroideum (Mangin) Balech'"" 4 149 P ro toperid in ium ste in ii (Jorgensen) Balech 4 4 4 4 4 4 4 4 4 Pro toperid in ium subinerme (Paulsen) Loeblich III 4 4 4 4 4 4 4 P ro toperid in ium thorianun i (Paulsen) Balech 4 4 4 4 P ro toperid in ium tregoubo ffii (Halim) Balech'"" 4 63,64 P ro toperid in ium tristy lum (Stein) Balech 4 4 4 76,168,175 P ro toperid in ium tubum (Schiller) Balech 4 4 4 4 P ro toperid in ium tum idum (O kam ura) Balech 4 4 4 P ro toperid in ium variegatum (Peters) Balech 4 127 P ro toperid in ium wiesneri (Schiller) Balech'"^ 4 4 4 156 zJU F. Gômez Table II. (continued) Dinophyceae West et Fritsch 1927 Alb Alg Bal Tyr Lig Ion A dr Aeg Lev Reference no. Scrippsiella Balech ex Loeblich III 1965’"* Scrippsiella lachrymosa Lewis + 39,112 Scrippsiella precaria M ontresor et Zingone + 109 Scrippsiella ram on ii M ontresor + 39,108 Scrippsiella rotunda Lewis + 39,117 Scrippsiella sp in ifera Honsell et Cabrini 4 72 Scrippsiella troclio idea (Stein) Balech ex + + + + + 4 4 4 4 Loeblich III’"" Podolampadaceae Lindemann 1928 Blepharocysta E hrenberg 1873 Blepharocysta herm osilla i Carbonell-M oore + 19 Blepharocysta paulsenii Schiller + + 4 4 Blepharocysta splendor-m aris (Ehrenberg) Stein + + + + 4 M ysticella Carbonell-M oore 1994 M ysticella striata (Schiitt) Carbonell-M oore"’" + 132 Podolam pas Stein 1883 Podolanipas bipes Stein + + + + + 4 4 4 4 Podolampas curvatus Schiller + 4 76,145 Podolampas elegans Schiitt + + + + + 4 4 4 4 Podolampas palm ipes Stein + + + + + 4 4 4 4 Podolampas spin ifera O kam ura’"’ + + + + + 4 4 4 4 Pyrophacaceae Lindem ann 1928 lyrophacus Stein 1883 Pyrophacus horo log ium Stein emend. Wall et Dale + + + + + 4 4 4 4 Pyrophacus ste in ii (Schiller) Wall et Dale + + + 4 4 4 Pyrophacus vancampoac (Rossignol) Wall et D ale’"- + 96,160 Peridiniales incertae sedis Ceratoperidinium M argalef tuc Loeblich III 1980 Ceratoperid in ium mediterraneum Abboud-Abi Saab’"" 4 2 Ceratoperid in ium yeye Margalef ex Loeblich III’"" + 4 1,99,169 Fragilidium Balech ex Loeblich III 1965 (= Helgolandicum von Stosch 1869, Goniodoma Stein 1883 partim .) F rag ilid ium fissile Balech + 6 Heterocapsa Stein 1883 (= Cachonina Loeblich III 1968) Heterocapsa lanceolata Iwataki et Fukuyo'"^ 4 126 Heterocapsa n ie i (Loeblich III) Morrill et -f 4 4 Loeblich III’"" Heterocapsa rotundata (Lohmann) G. H ansen’"" + + 4 4 Heterocapsa triquetra (Ehrenberg) Stein + + 4 4 4 Micracanthodinium D eflandre 1937 (= Cladopyxis Slein 1HS3 pa rtim .) M icracanthodin ium bacillife rum (Schiller) + 4 20,140 D eflandre’"'' M icracan thod in ium clayton ii (Holmes) Dodge'"* ' 4 4 22,140 M icracanthodin ium setiferum (Lohmann) Deflandre'"" + + 4 4 4 Spiraulax Kofoid 1911 ( - Gonyaulax Diesing IS66 pa rtim .) Spiraulax jo l l if fe i (M urray et Whitting) Kofoid + + + 4 4 4 4 Prorocentrales Lemmermann 1910 Prorocentraceae Stein 1883 Exuviella Cienkowski 1881'"" E xuv ie lla aperta Schiller’’’ + 4 4 77,145,168 Mesoporos Li Hick 1937 (= Porella Schiller 1928) M esoporos g lobulus (Schiller) Lillick + + + 4 4 4 M esoporos pe rfo ra tiis (G ran) Lillick + + + + 4 4 4 4 4 Prorocentrum Ehrenberg 1834'^"(= Exuviella Cienkowski 1881) P rorocen trum aporum (Schiller) Dodge + + + 4 4 4 4 157 ViiCLKUbi u i ivicuiicrraiicaii iicc-iiv iiig u iiiu iia^cuaics Table 11. (continued) Dinophyceae West et Fritsch 1927 Alb Alg Bal Tyr Lig Ion Adr Aeg Lev Reference no. Prorocentrum ba lticum (Lohm ann) Loeblich III + + + + 4 4 4 Prorocentrum belizeanum Faust + + 151 Prorocentrum cassubicum (Woloszynska) Dodge + 4 75,76,83 Prorocentrum compressum (Bailey) A bé ex Dodge'^" + + + + + + 4 4 4 Prorocentrum concavum Fukuyo + + 151 Prorocentrum cordatum (Ostenfeld) Dodge'^'* '^" + + + + 4 4 4 Prorocentrum dactylus (Stein) Dodge + + + + 4 Prorocentrum dentaturn Stein'^" + + + + + 4 4 4 Prorocentrum emarginatum Fukuyo + 172 Prorocentrum gracile Schütt’’^ + + + + + 4 4 Prorocentrum lim a (Ehrenberg) Dodge + + + + + 4 4 Prorocentrum m axim um (G ourret) Schiller’"̂* + + + + 4 P rorocentrum m icans Ehrenberg'^" + + + + + + 4 4 4 P rorocentrum m in im um (Pavillard) Schiller'"'" + + + + 4 4 Prorocentrum nanum Schiller'*" + + 4 P rorocentrum nux PuigseiA'er et Zingone + 128 P rorocentrum ovum (Schiller) Dogde + + + 4 4 P rorocentrum rostratum Stein + + + 4 4 P rorocentrum rotundatum Schiller'*' + + + + + 4 4 4 P rorocentrum scutellum Schroder'*^ + + + + + + 4 4 4 P rorocentrum triestinum Schiller + + + + + 4 4 4 P rorocentrum vag inu lum (Stein) Dodge'*" + + + + 4 4 4 P rorocentrum venetum Tolomio et Cavolo'*^ 4 164 Protaspidales Loeblich III 1970 Entomosigmataceae C hatton 1952 Entomosigma Schiller 1925 Entom osigm a pe rid in io ides Schiller'*" + + 4 75,76,145 Pyrocy.stales Apstein 1909 Pyrocystaceae (Schiitt) Lem m erm ann 1899 Dissodinium Klebs in Pascher emend. Elbrachter et D rebes 1978'*" D issod in ium pseudolunula Swift ex E lbrachter et D rebes'* ' + + + + 4 4 4 Pyrocystis Murray ex H aeckel 1890’*" (= Gymnodinium Stein 1883 partim ., Dissodinium Klebs in Pascher emend. Elbrachter et D rebes 1978p a rtim .) Pyrocystis acuta Kofoid + 76,125 Pyrocystis elegans Pavillard + + + + + 4 4 4 Pyrocystis fus ifo rm is (Wyville-l'homson ex Haeckel) + + + + + 4 4 4 Blackman'** Pyrocystis gerbau ltii Pavillard'*" + + + Pyrocystis hamulus Cleve + + + 4 4 Pyrocystis m arga le fii Léger'"" + + 91,104 Pyrocystis m in im a (M atzenauer) Schiller'"' + + 4 4 Pyrocystis noctiluca M urray ex Schiitt'"' + + + + 4 4 Pyrocystis ohtusa P av illa rd ' + + + 4 4 4 4 Pyrocystis robusta Kofoid + + + 4 4 4 Dinoflagellates of uncertain identification A dinim onas Schiller 1928 A d in im onas ov ifo rm e Schiller'"" + 4 4 4 Archaeosphaerodiniopsis Ram pi 1943 Archaeosphaerodiniopsis verrucosa Rampi'"'* + 135 Pachydinium Pavillard 1915 Pachydinium m editerraneum Pavillard'"" + + 4 158 L ô l r. uomez N otes R eported in the Western M editerranean Sea by Gômez and Claustre (2003). These records assigned to Astero- ciin ium gracile Sournia presented morphological dif­ ferences with respect the type species. Asterodin ium lihanum Abboud-Abi Saab requires a more detailed description. The type species Brachyd in ium capitatum F.J.R. Taylor (Taylor 1963) was replaced by B rach id in iuw capitatum FJ.R. Taylor due to an etymological error (Taylor 1967). Sournia ( 1973 p. 5) reported that the correction is invalid. R are dinoflagellate epiphytic on Rhodophyceae (see Sournia 1986. p. 36). R are and insufficiently described taxon (Sournia 1986, p. 36). According to Taylor (1976 p. 190), the cysts were report­ ed by Margalef et al. (1954). G loeodinium Klebs and H em id in ium Stein have been considered as the immo­ bile and mobile stage respectively of the life cycle of the same taxa (see Sournia 1986 p. 67). The continental species, H em id in ium nasuturn Stein and others, are re­ ported in the M editerranean waters (e.g., Schiller 1935-1937. p. 89-92, Vilicic et al. 2002). Syracosphaera lie im ii Lohmann. Ib is taxon was previ­ ously considered to be a coccolithophorid and has been scarcely reported in dinoflagellate checklists (see Tan- gen el al. 1982). This taxon resembles Am phiso len ia spinulosa Kofoid and A m phiso len ia mozambica Sournia. This taxon presents synonyms as Dinophysis borealis Paulsen, D. lachm anni Paulsen, D. boehm ii Paulsen or D. skagii Paulsen. D inophysis dens Pavillard. The orthographical similarity of Dinophysis alata Jo r­ gensen, D inophysis alata Bohm and Dinophysis alata (Wood) Balech is confusing. Vilièic et al. (2002) report­ ed D inophysis alata (Wood) Balech. D inophysis amygdala Balech, Phalacrorna ovum Schiitt. non Dinophysis ovum Schiitt. This taxon resembles Phalacroma ovatum (Claparède et Lachmann) Jorgensen. D inophysis caudata var. diegensis Kofoid. D inophysis intermedia Pavillard, Dinophysis laevis Pouchet. Phalacrom a odiosum Pavillard. Phalacrom a m itra Schiitt, Phalacroma rapa Stein. Pha­ lacrom a dolichopteryg ium Murray et Whitting. Non Phalacroma ovum Schiitt. D inophysis in fund ibu la Schiller. D inophysis lenticida Pavillard. D inophysis reticulata (Kofoid) Balech. D inophysis acuminata f. ren ifo rm is Pavillard. D. p a v il­ la rd ii Schroder, D. ren ifo rm is (Pavillard) Kofoid et Skogsberg, D. ventrecta Schiller. D inophysis .sphaeroidea (Schiller) Balech. D inophysis uracantha Schiitt, non Dinophysis uracan- tha Stein. D inophysis sphaerica Pavillard A possible variety of Histioneis depressa Schiller (Tay­ lor 1976, p. 44). Ornithocercus carolinae Kofoid, Histiones francescae M urray et Whitting. Ornithocercus assim ilis Jorgensen, O. galea (Pouchet) Abé. '* Histioneis splendida Murray et Whitting. Ornithocercus serratus Kofoid, O. orb icu la tus Kofoid et Michener. Histioneis karstenii Kofoid et Michener. D inophysis acutoides Balech, Phalacrom a acutum Pavillard. Phalacroma stenopterygium Jorgensen. Pseudophalacroma nasutum (Stein) Jorgensen, D in o ­ physis nasuta (Stein) Parke et Dixon. G ym nod in ium sanguineurn H irasaka, G. splendens Lebour. A m p h id in iu m phaeocysticola Lebour has been consid­ ered as a synonym of A . crassum Lohmann. However this synonymy is debatable (Elbrachter 1979). A m p h id in iu m lacustre Stein, A. schroederi Schiller and A. lacustrifo rm is Schiller are often considered as syn­ onyms. Typically fresh and brackish water species. A m p h id in iu m klebsii Kofoid et Swezy. "* Considered as a synonym of A m p h id in iu m lac iis tri- fo rn ie Schiller by Dodge (1982 p. 72). G ym nod in ium fHum Lebour. Taylor (1976 p. 114) reported this taxon from the Liguri­ an Sea. Non C ochlod in ium he lix Kofoid et Swezy (= Cochlo- din ium helicoides Lebour). Confusion possible between C och lod in ium p o ly - kriko ides Margalef ( - C. heterolobatum Silva) and G ym nod in ium im pudicum (Fraga et Bravo) G. Hansen et M oestrup (see Cho eta l. 2001). G ym nod in ium a lbu lum Lindemann and G. sim plex (Lohmann) Kofoid et Swezy may be synonyms. •*•* The North European taxon, G yrod in iu m aureo lum Hulburt sensu Braarud et Heimdal, is a synonym of Karenia m ik im o to i (Miyake et Kominami ex O da) G. Hansen et M oestrup (= G ym nod in ium nagasakiense Takayama et Adachi) (Hansen et al. 2000). See also Note 51. According to Bolch and Reynolds (2002) o ther taxa that also produce microreticulate cysts such as G ym no­ d in ium no lle ri Ellegaard et M oestrup and G. m icrore tic- ulatum Bolch et Hallegraeff are present in the Tyrrhen­ ian and A driatic Seas based on the cysts reported by M ontresor et al. (1998) and Rubino et al. (2000). T ie records of G ym nod in ium catenatum G raham by Carrada et a i (1991), Giacobbe et a i (1995) and Labib (1997) are considered as G. im pudicum (Fraga et B ra­ vo) G. Hansen et Moestrup. G ym nod in ium conicum Kofoid et Swezy (= G. v ir id is Lebour) is considered as a synonym of G yrod in iu m viridescens Kofoid et Swezy. Non G yrod in iu m conicum Schiller. ■** G ym nod in ium puncta tum var. grarnm aticum Pouchet. G ym nod in ium rhom hoides Schiitt, G. hya linum Lebour (= G. luc idum Ballantine in Parke et Dixon). G yro d in i- uni striatissimum (H ulburt) G. Hansen et M oestrup has been considered as a synonym until the redescription of G. heterostriatum Kofoid et Swezy by E lbrachter (1994). Tliis brackish waters taxon appears associated with Karenia m ik im o to i (M iyake et Kominami ex O da) G. Hansen et M oestrup (see also Notes 44 and 51). According to Faust and Gulledge (2002) this taxon was recorded in the Tyrrhenian Sea by C arrada et a l (1991). Confusion possible with species of the complex K aren ia 159 v_necKiisi OI ivieauerranean iree-iivmg umoiiageiiaies z j j m ik im o to i (Miyake et Kominami ex O da) G. Hansen et Moestrup. G ym nod in ium pu lche llum is distinguished from K. m ik im o to i by the sigmoid apical groove. See also Note 44. This taxon resembles K atod in ium glaucum (Lebour) Loeblich III. G yrod in ium op inum (Schiitt) Lebour. G yrod in ium dom inans Hulburt. " lac rym a" (= tear-drop) should be the correct epithet of this taxon. G ym nod in ium spirale var. pepo Schiitt. G ym nod in ium spirale \a r.p in g u is Schiitt. "* G ym nodin ium hreve Davis, Ptychodiscus brevis (Davis) Steidinger. Reported as G ym nod in ium galatheanum Braarfid (= G yrod in ium galatheanum (B raarud) Taylor sensu Taylor). More recently this taxon, unless G ym nod in ium galatheanum Braarud sensu Kite et Dodge, is consid­ ered as a synonym of K a rlo d in iu m m icrum (Leadbeater et Dodge) J.Larsen (Daugbjerg etal. 2000). Massartia glauca (Lebour) Schiller, G yrod in ium g lau­ cum (Lebour) Kofoid et Swezy, G ym nod in ium m inutum Lebour, Massartia m inuta (Lebour) Conrad et Kuf- ferath, Massartia tubidata Rampi. Massartia tubulata Rampi. Related to the genus G yrod in ium Kofoid et Swezy ac­ cording to Sournia (1986, p. 57). G ym nodin ium teredo Pouchet. Ptychodiscus in fla tus Pavillard, P. carinatus Kofoid. Erythropsis agilis Hertwig. Probably several species are reported as E. agile (Hertwig) PC Silva according to Elbrachter (1979). Elbrachter (1979) considered this taxon as a synonym of E. agile (Hertwig) P.C. Silva. To the best of my knowledge, never reported after the initial description by G reuet (1968b). "* Pouchetia armata Dogiel, Pouchetia maculata Kofoid et Swezy. K o fo id in ium lebourae (Pavillard) Taylor ( - G ym no­ d in ium lebourae Pavillard). ™ Originally described from the Ligurian Sea as Lepto- d in ium caudatum Cachon et Cachon. " Pratjetella medusoides (Hertwig) Loeblich et Loeblich III. Doubtful taxon (Sournia 1986, p. 53). " A bed in ium dasypus (Cachon et Cachon) Loeblich et Loeblich III. Reported from the Ligurian Sea as Leptospathium nav- icu la Cachon et Cachon-Enjumet (1964) after the de­ scription by M argalef (1963). Balkis (2000) reported this taxon frona the M armara Sea. Resembles Prùnôctiluca acuta (Lohm ann) Schiller. O xytoxum m arga le fii Rampi, O xytoxum to n o llii Rampi. M urrayella spinosa Kofoid, P avilla rd in ium spinosum (Kofoid) Taylor ex Sournia, A m ph idom a spinosa (Ko­ foid) Kofoid et Michener, G onyaulax rouch ii Rampi. " This taxon resembles Ceratium incisum (Karsten) Jo r­ gensen. '* Ceratium buceros f. claviger (Kofoid) Schiller, Ceratium h o rridum f. claviger (Kofoid) Sournia. Also reported as Ceratium trichoceros var. contrarium (G ourret) Schiller. *" Ceratium h o rridum var. lenticu latum Jorgensen, C. buceros f. denticulatum (Jorgensen) Schiller. Reported as Ceratium pu lche llum t eupulchellum by Ghazzawi (1939) in the Canal of Suez. This taxon re­ sembles C. tripos var. pu lche llum (Schroder) Lopez, see Sournia (1967). *' Ceratium arcuatum (G ourret) Pavillard, C. tripos var. arcuatum G ourret. non C. arcuatum Cleve. *" Ceratium fusus var. extensum Gourret. C. tripos var. ho rridum Cleve, but C. tenue (Ostenfeld et Schmidt) Jorgensen, C. in term edium (Jorgensen) Jor­ gensen and C. buceros (Zacharias) Schiller have not been considered as synonyms. *" This taxon resembles Ceratium lim u lus (G ourret ex Pouchet) G ourret. *" C. tenuissimum Kofoid. *' Ceratium carriense var. volans (Cleve) Sournia. ** A canthod in ium caryophyllum Kofoid. *" M icracan thod in ium quadrisp inum (Pavillard) Margalef. Confusion possible with Cladopyxis hrachiolata Stein. Heterod in ium de ton ii Rampi. Crypthecodin ium setense Biecheler. G oniodom a po lyedricum (Pouchet) Jorgensen, H eter­ aulacus po lyed ricum (Pouchet) Drugg et Loeblich, Tria­ d in ium po lyedricum (Pouchet) Dodge, G oniodom a polyedra Rampi. Heteraulacus sphaericum (M urray et Whitting) Loe­ blich III, Triad in ium sphaericum (M urray et W hittman) Dodge. Reported as P yrod in ium sch ille ri (M atzenauer) Schiller [= P yrod in ium bahamense Plate var. compressum (Bohm) Steidinger, Tester et Taylor]. A lexandrium lusitan icum Balech. R eported as G oniodom a ostenfe ld ii Paulsen by Lecal (1954). Reported as G onyaulax subulata Kofoid et Michener. This taxon resembles A m y la x triacantha (Jorgensen) Sournia (Dodge 1982, p. 217). Reported as G o n yau la x l triacantha Jorgensen by Lecal (1954). G onyaulax sp in ifera sensu Schiitt. G onyaulax dig ita le Kofoid, Pro toperid in ium digita le Pouchet. Resembles G onyaulax b irostris Stein. R eported by Narusevich and Tokarev (1989) in an un­ determ inated location of the M editerranean Sea. The comments by Schiller (1935-1937, p. 290) on the similarity betw een G onyaulax k o fo id ii and G. pacifica Kofoid could induce confusion between both taxa (Pavillard 1937, p. 16; Taylor 1976, p. 104). G onyaulax m in im a Matzenauer. Resembles G onyaulax ovata M atzenauer (Schiller 1935-1937, p. 289; Taylor 1976, p. 105). i()7 P avilla rd in ium b ria n ii (Rampi) Sournia (= M urm ye lla hrifl/îü Rampi). G onyaulax levanderi (Lemm erm ann) Paulsen, Cerato­ corys .spinifera Schroder. G onyaulax diacantha (M eunier) Schiller, G onyaulax longisp ina Lebour, A m y la x diacantha Meunier. G onyaulax m iln e ri (M urray et Whitting) Kofoid, G o­ n iodom a m iln e ri M urray er Whitting. * ‘ * G onyaulax po lyedra Stein. G onyaulax g rind ley i Reinecke, non G. reticulatum Ko­ foid et Michener. H eterod in ium la tic inctum Kofoid. H eterod in ium pu lch rum Bohm, H eterod in ium richa rd ii Pavillard. H eterod in ium mediocre f. sinistrurn (Kofoid) Kofoid et Adamson. 160 234 F. Gômez Ostreopsis m onotis (M eunier) Lindemann. Ceratium h iconicum Murray et Whitting, M urrayella bi- conica (M urray et Whitting) Pavillard and P av illa rd in i­ um b iconicum Rampi are considered synonyms, os P avilla rd in ium interm edium (Pavillard) de Toni ( - M urraye lla interm edia Pavillard). non Centrodin ium in term edium Pavillard. P avilla rd in ium splendidum (Rampi) Rampi (= M u r­ rayella splendida Rampi). Resembles C ory thod in ium reticulatum (Stein) Loeblich et Loeblich III. 121 Prorocentrum curvatum Kofoid. Non C orythod in ium globosum (Kofoid) Taylor. O xytoxum sceptrum (Stein) Schroder. O xytoxum challengeroidesKoioxé. O xytoxum mediterraneum Schiller. O xytoxum tenuistriatum Rampi. This taxon resembles O xytoxum ovale Schiller "* O xytoxum ligusticum Rampi. O xytoxum gracile Schiller. M urraye lla ovalis Pavillard. See also comments on the genus by Sournia (1986. p. 73). G onyaulax m itra (Schiitt) Kofoid, Oxytoxum gigas Ko­ foid. Based on the germination of recent cysts (D 'O nofrio etal. 1999). M eier et al. (2002) reported 14 species of calcareous di­ noflagellates from recent cysts (4 new species), only this taxon that germ inated from one cyst from the Levan­ tine Basin is included. D ip lopsa lis asymmetrica (Mangin) Lindeman, D ip lo p ­ salopsis bom ba (Stein) Dodge et Toriumi, Dissodium asymmetricum (Mangin) Loeblich III. Considered as a synonym of D ip lope lta bomba Stein ex Jorgensen by Dodge (1982 p. 157). Dissodium lenticu lum (Bergh) Loeblich III, G lenodin i­ um lenticula (Bergh) Schiller. D ip lopsa lis o rb icu la ris (Paulsen) Steidinger et Williams. Usually a brackish water species. G lenodin ium ro tundum (Lebour) Schiller. Originally described from the Tyrrhenian Sea as Peri­ d in ium tyrrhen icum Balech (Balech 1990). Nearly all of the marine species of Perid in ium Ehren­ berg have been transferred to P ro toperid in ium Bergh. P ro toperid in ium quinquecorne (Abé) Balech. This taxon presents synonyms such as D iplopsalis m in o r (Paulsen) Lindemann, Z ygab ikod in ium lenticulatum (Manguin) Loeblich et Loeblich III, Diplopeltopsis m i­ n o r (Paulsen) Pavillard, D ip lopsa lis lenticula f. m in o r Paulsen (see Dodge and Toriumi 1993, Elbrachter 1993). Non P ro toperid in ium b iconicum (Dangeard) Balech. .Minuscula bipes (Paulsen) Lebour. P ro toperid in ium b im ucronatum (Schiller) Balech. The synonymy between P erid in ium sourn ia i FJ.R. Taylor and P ro toperid in ium bisp inum (Schiller) Balech is de­ batable. According to Schiller (1935, p. 223) Perid in ium curtipes Jorgensen is a synonym of P erid in ium crassipes Kofoid, consequently a confusion could be expected. P ro toperi­ d in ium crassipes (Kofoid) Balech and Pro toperid in ium curtipes (Jorgensen) Balech are different species: 1) P ro toperid in ium crassipes (Kofoid) Balech (= P erid in i­ um crassipes Kofoid), 2) P ro toperid in ium curtipes (Jor­ gensen) Balech { - P erid in ium crassipes Paulsen 1907. non Paulsen 1930). See also Balech (1988. p. 110). 148 Peridin ium decipiens var. curvipes Ostenfeld, P ro tope ri­ d in ium subcunipes (Lebour) Balech. Protoperid in ium longipes (Karsten) Balech. According to Balech (1976) this taxon is related to the freshwater species Pro toperid in ium achrom aticum (Levander) Balech. P rotoperid in ium ovatum Pouchet [= P. g lobu lus var. ovatum (Pouchet) Schiller, Perid in ium ovatum (Pouchet) Schiitt] have been considered as synonyms. This taxon can be confused with P ro toperid in ium ovum (Schiller) Balech. Also reported from the Tyrrhenian Sea based on cysts by M ontresor et al. (1998). Protoperid in ium spin iferum (Schiller) Balech. The orthographic similarity between P. sphaeroides (Dangeard) Balech and P sphaeroideum (Mangin) Balech is confusing (Sournia 1978, p. 29). This taxon resembles P ro toperid in ium brachypus (Schiller) Balech. P rotoperid in ium angustum (Dangeard) Balech. Most of the recently described species of Scrippsiella Balech ex Loeblich are reported from the germination of cysts (M ontresor et al. 1994, D ’Onofrio et al. 1999). Scrippsiella faeroense D ickensheets et Cox, non Scripp­ siella faeroense (Paulsen) Balech et Soares. Reported by Rampi (1941) as Blepharocysta striata Schütt (see Carbonell-Moore 1994). Podolampas sp in ife r Pavillard. Tuberculodinium vancampoae (Rossignol) Wall (= Pterospermopsis vancampoae Rossignol). Taylor (1976 p. 183) reported the presence of this taxon in the M editerranean Sea based on Margalef (1948). One specimen that resembles C yeye Margalef from the Alboran Sea. one specimen of C yeye and other unde­ terminated species of this genus were observed from the Balearic coasts (unpublished obs.). C eratoperid in i­ um mediterraneum Abboud-Abi Saab requires a more detailed description. Iwataki et al. (2002) reported this taxon based on the material from the Aegean Sea by Pennik and Clarke (1977). Cachonina nie i Loeblich III. K atod in ium rotundatum (Lohmann) Loeblich III, M as­ sartia rotundata (Lohmann) Schiller, A m p h id in iu m ro ­ tundatum Lohmann, K atod in ium m inutum (Lebour) Sournia. Cladopyxis bac illi fera Schiller. Cladopyxis c layton ii Holmes. Cladopyxis setifera Lohmann, M icracan thod in ium bacillife rum (Schiller) Deflandre. The ^ h u s Exuviella was included in Prorocentrum by Dodge (1975). McLachlan et al. (1997) proposed the separation of both genera. Schiller (1931-1933, p. 26) reported this taxon as E x u ­ viella (?) aperta Schiller (described from the A driatic Sea in 1928). Inadequate description according to Dodge (1975). P. micans var. gibbosum Schiller, P. gibbosum (Schiller) Schiller, P. blatta Athanassopoulos. Resembles P ro ro ­ centrum micans Ehrenberg. According to Dodge (1975): P rorocentrum bidens Schiller, P lebourae Schiller, E xuvie lla oblonga Schiller [ - Prorocentrum oblongum (Schiller) Taylor], E. lentic- ulata M atzenauer, E. elongata Rampi. Prorocentrum p yrifo rm is (Schiller) Hasle. 161 unecKiisi OI Meaiierranean iree-iivmg ainoiiageuaies z j j Prorocentrum m in im um (Pavillard) Schiller and P ro ro ­ centrum cordatum (Ostenfeld) Dodge may be syn­ onyms (Velikova and Larsen 1999). 176 P rorocentrum ohtiLsidens Schiller, also P. monaceme Kufferath described in the Ligurian Sea (Kufferath 1957). P. hentschelii Schiller, P. sigmoides Bohm, P macrurus Athanassopoulos. Resembles P. micans Ehrenberg. "* According to Dodge (1975): Prorocentrum mexicanum Osorio-Tafall, P. obtusum Ostenfeld, P. b roch i Schiller, P. ovale Schiller, P. ovalis Rampi, P. ram p ii Sournia. Prorocentrum sch ille ri Bohm in Schiller. 180 P rorocentrum nanum Schiller and P pus illum (Schiller) Loeblich were considered as synonyms until Puigserver and Zingone (2002). Prorocentrum cornutum Schiller. 182 P rorocentrum sphaeroideum Schiller. P. robustum Oso­ rio Tafall. P rorocentrum adria ticum Schiller. This taxon resembles Prorocentrum mexicanum O so­ rio-Tafall that is here considered a synonym of P ro ro ­ centrum m axim um (G ourret) Schiller. Regarded as a doubtful dinoflagellate by Sournia (1986, p. 37). D issod in ium is a genus of parasitic dinoflagellates with a complicate life cycle including planktonic life cycle stages similar to those of the genus Pyrocystis. In con­ trast, Pyrocystis is a perm anently free-living pho- totrophic dinoflagellate with a predom inant coccoid stage and a flagellated dinospore stage (e.g., E lbrachter etal. 1987). 187 Pyrocystis lunu la (Schütt) Schütt, D issod inum lunu la (Schütt) Pascher. '** D issodin ium fus ifo rm is (Thompson ex Murray) Matzenauer. D issodin ium gerbau ltii (Pavillard) F.J.R. Taylor Léger (1973) reported the presence of this taxon in the Spanish M editerranean coast by Margalef et al. (1957). Drebes (1981) reported that Pyrocystis m arga le fii Léger is probably identical with the resting stages of D issod in ium pseudolunula Swift ex E lbrachter et Drebes. D issod in ium m in im um M atzenauer. 192 Pyrocystis pseudonoctiluca Wyville-Thomson ex M ur­ ray, D issod in ium pseudolunula Swift ex E lbrachter et Drebes. Regarded as a doubful dinoflagellate by Sournia (1986, p. 97). Commonly reported as A dinom onas Schiller. Regarded as a doubtful dinoflagellate by Sournia (1986, p. 97). 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Printed in the Netherlands. 43 An annotated checklist of dinoflagellates in the Black Sea Fernando Gomez ̂ & Laura Boicenco^ ̂D epartm en t o f A q u a tic B iosciences, The U n ivers ity o f Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan ^N a tio n a l Ins titu te f o r M a r in e Research and D eve lopm ent ‘G rigo re A n tip a ’, 300 M am a ia Bdv, R O -900581, Constantza, R om ania E -m a il: fem aru io .gom ez@ fitop lancton .com Received 14 May 2003; in revised form 7 September 2003; accepted 18 September 2003 Key w ords: Pyrrhophyta, D inophyta, phytoplankton, harm ful and toxic algal bloom s, biogeography, M editer­ ranean, Black Sea Abstract An annotated checklist o f free-living dinoflagellates (D inophyceae) of the Black Sea, based on literature records, is reported and com pared to the M editerranean Sea and world oceans. Toxic species and/or responsible o f harmful algal bloom s (HAB) are marked in the checklist. From the 267 species (54 genera) listed nearly all taxa can be considered as cosm opolitan and no species as endemic. Several typically A rctic-boreal species (non recorded from the M editerranean Sea) are reported from the Black Sea. The taxonom y and the biogeography o f the taxa are discussed. Introduction The Black Sea (~41-A 6° N) is a semi-enclosed basin whose only connection to the world’s oceans is through narrow straits (< 1 1 0 m depth), the D ard­ anelles and the Bosphorus, both opening to the M ar­ m ara Sea. The fresher waters o f the Black Sea (salinity ~ 17) flow to the M editerranean Sea by means o f an upper layer flow; saltier M editerranean waters (~ 38 .5) flow to the Black Sea in a lower current. A perm anent halocline is maintained by colder low-salinity surface water averaging 17.5-19 overlying deep waters with salinity about 22. Low near-surface salinity is main­ tained by the influx o f freshwater from rivers and decreases to <13 near the mouths of the Danube and D nieper rivers (see references in Sorokin, 2002). In the last decades the Black Sea basin has ex­ perienced huge changes in w ater quality caused by provide competitive advantage for mixo- or hetero- trophic dinoflagellates com pared to autotrophic diat­ oms, with high dinoflagellates to diatom s ratio (Hum- borg et al., 1997). A change in dom inant species was observed as well as an increase in red tide events (Bologa et al., 1995; M ihnea, 1997). The high de­ gree o f eutrophication in the B lack Sea could favour invasive species (i.e., v ia ballast waters; M oncheva & Kamburska, 2002) to com pete for niches. Among phytoplankton taxa, dinoflagellates w ith more than 200 potential toxic species (Sournia, 1995) require special attention. Krakhmalny (1994) reported a list o f 193 dino­ flagellates (including infraespecific taxa) in the Black Sea. O ther checklists are available from Georgian (Ko- makhidze & M azm anidi, 1998), U krainian (Zaitsev & Alexandrov, 1998), Turkish (Ozturk, 1999; Turkoglu & Koray, 2000, 2002; Koray et al., 2000), Bulgarian W human iMerventions both uir llwi the rivers and on the nutrient and pollutant discharge. Significant changes on phytoplankton, zooplankton, zoobenthos and fisheries have been reported (Bakan & Buyukgungor, 2000). The high nitrate and phos­ phate to silicate ratios as well as organic material R ^ ià iik B F coasts (Skolka, 1977; Bodeanu, 1987-1988; Petranu, 1997). L iterature sources are com piled here and an an­ notated checklist is discussed. This study attempts to assess the biodiversity o f dinoflagellates, here defined 170 mailto:femaruio.gomez@fitoplancton.com 44 as species richness, in the Black Sea and also to com pare this richness to adjacent seas in order to es­ tablish the biogeographical affinities o f the Black Sea dinoflagellates. resources from other geographical areas are cited in the text where appropriate. Results and discussion M aterial and m ethods This study is based on literature records o f dinofla­ gellates from the B lack Sea (108 references). The species are arranged alphabetically and taxa are named with their nom enclatural authorities (Table 1). The nom enclature is updated and the synonyms are repor­ ted. The numbers following a species name in the checklist refer to the list o f references. Exclusively freshwater taxa such as C eratium h iru n d in e lla (O F. M üller) Bergh, parasitic species such as Paulsenella chaetocera tis (Paulsen) Chatton or taxa insufficiently known or o f doubtful validity such as the genera C ystod in ium K lebs or H ypnod in ium Klebs have been excluded. However the prim arily freshwater species (see Popovsky & Pfiester, 1990) that apparently are able to tolerate the salinity o f the offshore waters of the Black Sea are listed, although not considered for biogeographical purposes. The species included in w hat are considered to be valid or reliable records are reported in bold type. The records o f insufficiently known or dubious species, requiring more precise taxonom ical investigation, are presented in norm al type. M ost o f these taxa mainly correspond to athecate dinoflagellates. It should be taken into account that the fixatives comm only used (Lugol, form aldehyde) do not sufficiently preserve them to allow species identification. Body shape and morphology often change during the process of fixa­ tion so that it is even difficult to determine the genus. In addition, som e o f the older descriptions are not sufficiently detailed or are inappropriate - as also oc­ curred for som e thecate species [i.e., P ro to pe rid in iu m s ina icum (M atzenauer) Balech, P. deficiens (M eunier) Balech]. The taxa considered as Harmful A lgal Bloom (HAB) species are based on the species listed by Faust & Gulledge (2002) and H allegraeff (2002) as well as A m p h id in iu m opercu la tum C laparède et Lachmann and H eterocapsa tr iq u e tra (Ehrenberg) Stein. The Black Sea taxa have been compared to those in checklists from the M editerranean and the adjacent seas. References concerning the presence o f the taxa in the M editerranean Sea are om itted due to space lim­ itation, but can be found in Gom ez (2003). Literary The Black Sea dinoflagellates flora is represented by 267 species from 54 genera (Table 1), being about one half monotypic genera (30 genera). The most nu­ merous genera were P ro to pe rid in iu m Bergh emend. Balech (41 species), C era tium Schrank (26 species) and D inophys is Ehrenberg (20 species) as well as the primarily freshwater genera G lenodin ium (Ehrenberg) Stein, P erid in ium Ehrenberg (also G lenodin iops is Wo­ loszynska, Perid in iops is Lem m erm ann) and species o f G ym nod in ium Stein (30 species) that are able to tolerate a wide range of salinity. Concerning the geographical distribution, nearly all the Black Sea species can be considered as cos­ mopolitan with some exceptions as discussed below. Species richness and b io d ive rs ity About 1400-1800 species (115-131 genera) consti­ tute marine living dinoflagellates in the world oceans (Sournia, 1995; Steidinger & Tangen, 1997). Accord­ ing to this non-updated value, the Black Sea comprises about 15% o f the world species and about 40% of the dinoflagellate genera (54 genera). This low species richness com pared to the M editer­ ranean Sea (673 species, 104 genera; Gomez, 2003) is primarily attributable to the general low diversity in brackish waters, usually more stressed than mar­ ine waters. The low transparency and the toxic deep layer (m ost o f the deeper w aters are isolated from any source of oxygen, and have a high content o f hydro­ gen sulphide) reduce the biotic layer. Consequently the oxygenic life is restricted to the upper waters, de­ creasing the num ber of niches available com pared to oceanic waters [for exam ple for the deep-living flora (Sournia, 1982)]. The contents o f organic m atter could favour a high species richness o f heterotrophic dinofla­ gellates as Noctilucales and partially Gymnodiniales, the latter usually difficult to identify at species level. Stoyanova (1999) reported high abundance (85-170 cells 1“ *) o f the aberrant heterotrophic dinoflagellates S pa tu lod in ium pseudonoctiluca (Pouchet) Cachon et Cachon ex Loeblich et Loeblich III, Scaphodin ium m ira b ile M argalef and P eta lod in ium p o rc e lio Cachon et Cachon. She suggested that the high abundance o f these new records in the B lack Sea is a consequence 171 45 Table 1. List of taxa. The species considered as valid records are reported in bold type. The records of insufficiently known, questionable or dubious species, requiring more precise taxonomical investigation, are presented in normal type. The numbers following a species name in the checklist refer to the list of references. HAB = Harmful Algal Bloom species; Cold = typical species from cold waters; Pacif. = apparently Indo-Pacific species. Achradina pulchra Lohmann HAB Akashiwo sanguinea (Hirasaka) G. Hansen et Moestrup [= Gymnodinium sanguineurn Hirasaka, G. splendens Lebour, G. nelsonii Martin] 15.17 -20.23,27.33,34.37,59.61,75.78.89,94,96,110,114,117,119,127,133-135,143 HAB Alexandrium monilatum (Howell) Balech [= Gonyaulax monilata Howell, Gessnerium mochimaensis Halim ex Halim, G. monilata (Howell) Loeblich, Pyrodinium monilatum (Howell) F.J.R. Taylor] 23.59.75,76.78,79.137,139 HAB, cold Alexandrium ostenfeldii (Paulsen) Balech ef Tangen [= Goniodoma ostenfeldii Paulsen, Gonyaulax ostenfeldii (Paulsen) Paulsen, Protogonyaulax ostenfeldii (Paulsen) Fraga et Sanchez, Heteraulacus ostenfeldii (Paulsen) Loeblich, Gessnerium ostenfeldii (Paulsen) Loeblich et Loeblich UI, Triadinium ostenfeldii (Paulsen) Dodge] Amphidinium acutissimum Schiller [= A. acutum Schiller, non A. acutum Lohmann] Amphidinium amphidinioides (Geitler) Schiller [= A. geitleri Huber-Pestalozzi, A. wigrense Woloszynska, A. bourrellyi Wawrik, Gymnodinium amphidinioides Geitler] "' '32 Amphidinium conradii Schiller [= Gymnodinium glaucum Conrad] Amphidinium crassum Lohmann [= A. phaeocysticola Lebour] 59,61,143 Pacif. Amphidinium cucurbita Kofoid et Swezy Amphidinium curvatum Schiller Amphidinium elenkinii Skvortsov [= A. larvale Lindemann, A. hyalinum Entz, A. tatrae Woloszynska, A. tenagodes Harris, A. luteum Skuja, A. gyrinum Harris, A. turicense Huber-Pestalozzi, A. lohamari Skuja, A. skujae Christen, Gymnodinium rarum Litvinenko] Cold Amphidinium extensum Wulff "0.114,119 Amphidinium flagellons Schiller Amphidinium globosum Schroder Amphidinium lacustre Stein [= A, lacustriforme Schiller, A. schroederi Schiller] Amphidinium lanceolatum Schroder Cold Amphidinium longum Lohmann [= A. acutum Lohmann, non A. acutum Schiller] HAB Amphidinium operculatum Claparède et Lachmann [= A. klebsii Kofoid et Swezy, A. massartii Biecheler, A. wislouchii Hulburt, A. hoefleri Schiller et Diskus] Amphidinium ovum Herdman Amphisolenia bidentata Schroder [non A. bidentata Pavillard, non A. bidentata Okamura] Cold Amylax triacantha (J0rgensen) Sournia [= Gonyaulax triacantha Jdrgensen, Amylax lata Meunier] Centrodinium intermedium Pavillard ' Ceratium belone Cleve [= C. pacificum Schroder] "",133,134 Ceratium buceros (Zacharias) Schiller Ceratium candelabrum (Ehrenberg) Stein * Ceratium carriense Gourret [= C. volans Pavillard, C. massiliense Pavillard] "0133,134 Ceratium compressum Gran [for synonymy with C. platycome, see Balech (1988: 141)] "".'33,134 Ceratium declinatum (Karsten) Jdrgensen [= C. tripos declinatum Karsten] ""-'33,134 Ceratium extensum (Gourret) Cleve [= C. strictum (Okamura et Nishikawa) Kofoid, C. biceps Kofoid] 8-9.18,60,61,94,%, 133,134 Ceratium fakatum (Kofoid) Jprgensen [= C. pettnatum f.falcata Kofoid, C. pennatum vw. falcatum J0rgensen] Ceratium furca (Ehrenberg) Claparède et Lachmann [= C. bipes Claparède et Lachmann] 8.9,14,15,18-20, 33.34.46.59-61,74-76,79,90,94,96,107,109-111,114,119,125,132-135,143 Ceratium fusus (Ehrenberg) Dujardin \yax. fusus, var, seta and var. schuettii] 2.8.9,18.27,33-35, 42.46.59-61,74,79,85,90,94.%,99,107,109,110-112,114,119,125,133-135,143,144 Ceratium hexacanthum Gourret [= C. reticulatum (Pouchet) Cleve] "" "'-94,133,134 Ceratium horridum (Cleve) Gran [= C, tripos var. horridum Cleve, C. intermedium (J0rgensen) J0rgensen, C, claviger Kofoid, C tenue {Ostenfeldet Schmidt) J0rgensen, C. inclinatum Kofoid, C, tenuissimum Kofoid, C. mollis Kofoid, G. batavum Paidsen, C. leptosomum J0rgensen, C. horridum var, denticulatum J0rgensen] ""-94,133-135 Ceratium incisum (Karsten) J0rgensen ""-'33.134 Ceratium inflatum (Kofoid) J0rgensen 8.60.61.94.114,133-135, Ceratium kofoidii J0rgensen ""-'33,134 Ceratium lineatum (Ehrenberg) Cleve ""-"'-'33,134 Continued on p. 46 172 46 Table I. Continued Cold Ceratium longipes (Bailey) Gran [= C. arcticum var. longipes (Bailey) Graham et Bronikovsky] Ceratium longirostrum Gourret "0-94.132-135 Ceratium macroceros (Ehrenberg) Cleve 8-61.94.114 Ceratium massiliense (Gourret) Karsten [also var. armatum (Karsten) Jdrgensen] "O-"'-133.134 Ceratium minutum Jorgensen Ceratium pentagonum Gourret 46.61.94,135, Ceratium pulchellum Schroder [= C, tripos \ar. pulchellum Peters] "0.94,133,134 Ceratium teres Kofoid Ceratium tripos (O.F. Müller) Nitzsch [= C. schroederi Nie, C. neglectum Ostenfeld, C. tripodioides (Jorgensen) Steemann Nielsen] 8.9,18,31,33,34,42,46.58,60,61,74,79,90,94,%,99,107,109,110,114,119,125,133-135 Ceratium volans Cleve [= C. carriense var. volans (Cleve) Sournia, non C. volans Pavillard] "". 133,134 Cladopyxis brachiolata Stein [= C. spinosa (Kofoid) ScM ïct] Cochlodinium adriaticum Schiller [= Gyrodinium adriaticum Schiller] "1-86.88 Cochloditiium brandtii Wulff Cochlodinium citron Kofoid et Swezy "1-128.144 Cochlodinium geminatum (Schütt) Schütt [= Gyrrmodinium geminatum Schütt] Cochlodinium helicoides Lebour [= C. helix Schütt pro parte, C. helix Kofoid et Swezy, reported as synonym C. helix (Pouchet) Lemmermann] " ' ■ ' 28 Cochlodinium lebourae Kofoid et Swezy Cochlodinium pirum (Schütt) Lemmermann [= Gymnodinium pirum Schütt] Corythodinium compressum (Kofoid) F.J.R. Taylor [= Oxytoxum compressum Kofoid] Corythodinium diploconus (Stein) F J.R. Taylor [= Oxytoxum diploconus Stein] HAB Dinophysis acuminata Claparède et Lachmann [— D. ovum var. baltica Paulsen, D. arctica sensu Woloszynska, D. baltica (Paulsen) Woloszynska, D. cassubica Woloszynska, D. levanderi Woloszynska, D. paulsenii Woloszynska, D. boehmii Paulsen, D. borealis Paulsen, D. lachmatmii Paulsen, D. skagii Paulsen] 9.18.59-61,94.96,114.133-135.143 HAB Dinophysis acuta Ehrenberg [= D. dens Pavillard, D. groenlandica (Schiller) Balech] 46.59-61,89,94,133.134 Cold Diftophysis apiculata Meunier "' Cold Diftophysis arctica Mereschkowsky [= D. laevis (Bergh) Pouchet, D. rotundata Levander, D. granulata Cleve, non D. laevis Bergh, non D. rotuttdata Claparède et Lachmann, non D. arctica sensu Woloszynska] HAB Dinophysis caudata Saville-Kent [= D . homunculus Stein, D. diegensis Kofoid] 9.18.34,46.59-61.90.94,96.108.114,119.133-135.143 Diftophysis detitata Schiller HAB Dinophysis fortii Pavillard [= D. laevis Pouchet, D. lapidistrigiliformis Abé, D. intermedia Pavillard] 33,46.61.94.110,114,125. 133-135.143 HAB Dinophysis hastata Stein [non Phalacrortta hastatum Pavillard, non Ph. Hensen] 9.18,34.59-61.94,96,110.114,133.134 Diftophysis meunieri Schiller [= D. cuiteiformis Meunier, non D. cuneiformis Mangin] Diftophysis mifiuta (Cleve) Balech [= Phalacroma mifiutum Cleve] HAB, cold Dinophysis ftorvegica Claparède et Lachmann [= D. debilior (Paulsen) Paulsen, resembles to D. acuta Ehrenberg] "1-143 Dinophysis ovum Schütt [= D. brevisulcus Tai et Skogsberg pro parte, non Phalacroma ovum Schütt] 1 •9.18,58.59.61.94. 96.110.114,135.143 Dinophysis parva Schiller [= D. ittfundibula Schiller] ""-"4.133.134 Dinophysis punctata Jorgensen [non D. punctata Balech] "0.94,133.134 HAB Dinophysis sacculus Stein [= D. acuminata f. reniformis Pavillard, D. rettiformis (Pavillard) Kofoid et Skogsberg, D. pavillardii Schroder, D. ventrecta Schiller, D. phaseolus Silva] 9.15.17-20.33.34,59-61,90.94,96.107-110,114,119.133-135,143 Dinophysis schilleri Sournia [= Phalacroma sphaeroideum SchiUer]^^'^^'^^ Diftophysis schuettii Murray et Whitting [= D. uracatttha Schütt, non D. uracantha Stein] Dinophysis similis Kofoid et Skogsberg [= D. sphaerica Schütt, D. simplex Balech, D. tai Balech, non D. simplex Bohm] _ Dinophysis sphaerica Stein [— D. vanhoffenii Ostenfeld] HAB Dinophysis tripos Gourret [= D. caudata var. tripos (Gourret) Gail] Diplopelta bomba Stein ex Jorgensen [= Diplosalis lenticula Stein, Peridiniopsis asymmetrica Mangin, Diplopelta asymmetrica (Mangin) Lebour, Diplopsalopsis asymmetricum (Mangin) Abé, Dissodium asymmetricum (Mangin) Loeblich HI] Continued on p. 47 173 47 Table 1. Continued Diplopsalis lenticula Bergh [= Glenodinium lenticula (Bergh) Schiller, Dissodium lenticulum (Bergh) Loeblich HI] 8.9.18.33.34.59-61.85.88.89.%.109-112,114,119,128,133,134,143 Diplopsalopsis orbicularis (Paulsen) Meunier [= Peridinium orbiculare Paulsen] 9 '8-6l-96,114,128,143 Glenodinium behningii (Lindemann) Kisselew [= Diplopsalis behningii Lindemann] "'114,143 Glenodinium caspicum (Ostenfeld) Schiller "1110.143 Glenodinium inflatum Meunier Glenodinium obliquum Pouchet " ' Glenodinium paululum Lindemann 9,15.18-20.27,34,42,59.61.88,89.96,107.109,110.114.117,119,143 Glenoitinium pilula (Ostenfeld) Schiller [= Diplopsalis pilula Ostenfeld, Peridinium pilula (Ostenfeld) Lemmermann] 9,14,15,18-20,34,58,59,61,96,114,143 Glenodinium pulvisculus (Ehrenberg) Stein [= Peridinium pulvisculus Ehrenberg] "* Goniodoma acuminatum (Ehrenberg) Stein [= Peridinium acuminatum Ehrenberg, non Peridinium polyedricum Pouchet] Goniodoma polyedricum (Pouchet) Jorgensen [= Peridinium polyedricum Pouchet, Triadinium polyedricum (Pouchet) Dodge, Goniodoma acuminata Stein pro parte, non Peridinium acuminatum Ehrenberg] 9.18,59,61,96,110,143 Gonyaulax africana Schiller "4,135 Gonyaulax apiculata (Pénard) Entz [= G. apiculata var. clevei Ostenfeld, Peridinium apiculatum Pénard, G. clevei Ostenfeld, G. polonica Woloszynska, G. limmetica Lindemann, G. austriaca Schiller] 8.33,34.59 Gonyaulax birostris Stein [= Gonyaulax glyptorhynchus Murray et Whitting, G. highleyi Murray et Whitting] "0. '33,134 Cold Gonyaulax cochlea Meunier [= G. polygramma Meunier] 9.18.22.25.58.59.61,94,96.114,117 Gonyaulax diegensis Kofoid [= G. spinifera sensu Schiitt] 9,18,34,46,59-61,94,96,114,119,133,134,143 Gonyaulax digitedis (Pouchet) Kofoid [ — G, spinifera Stein, Protoperidinium digitale Pouchet] 8,18,59,61,94,96,114,119 Gonyaulax elegans Rampi Gonyaulax fragilis (Schiitt) Kofoid [= Steiniella fragilis Schiitt] " ' Gonyaulax gracilis Schiller "' Gonyaulax minuta Kofoid et Michener [= G, minima Matzenauer] 58,59,61,89,131 Gonyaulax monacartiha Pavillard "0.94,133,134 Gonyaulax monospina Rampi Gonyaulax orientalis Lindemann [— Goniodoma orientale (Lindemann) Balech, Triadinium orientale (Lindemann) Dodge, Gonyaulax lebourae Balech pro parte, non G, orientalis sensu Lebour] HAB Gonyaulax polygramma Stein [=G . Jc/iMeHu Lemmermann] 8 - 15,17,18,25 -28,34,59-61,68,69,72,73,94,96,110,114,115,119,133,134, 137,143 Gonyaulax scrippsae Kofoid 58,59,61,143 Gonyaulax spinifera (Claparède et Lachmann) Diesing [=G. levanderi (Lemmermann) Paulsen, non G. spinifera Stein] 8.9.18.46.59-61,89,94,96,109,114,131,133,134 Gonyaulax verior Soumia [— G, diacantha (Meunier) Schiller, G. longispina Lebour, Amylax diacantha Meunier] ^ Gymnodinium agile Kofoid et Swezy [non G, agile sensu Herdmann] 9,18,59,61,96,110,114,117 Gymnodinium agiliforme Schiller 58,61,89,96 Gymnodinium aeruginosum Stein [= G, acidotum Nygaard, G, viride Pénard, G. campaniforme Popovsky] Gyrrmodinium auratum Kofoid et Swezy " " Gymnodinium biconicum Schiller ' "4 Gymnodinium conicum Kofoid et Swezy [= G, viridis Lebour] Gymnodinium flavum Kofoid et Swezy [non Gyrodinium flavum Kofoid] Gymnodinium fuscum (Ehrenberg) Stein [= G. caudatum Prescot, Cystodinium gessneri (Baumeister) Bourrelly] 9,18,96,119 Gymnodinium gracile Bergh [= G, spirale var. nobilis Pouchet, G. roseum Lohmann, G. abbreviatum Kofoid et Swezy, G. lohmannii Paulsen] Gymnodinium helveticum Pénard [= G. helveticum var. apiculata (Zacharias) Utermohl, Glenodinium apiculatum Zacharias in S c h i l l i n g ] '7-'5.17,19.20.27,59,61,96.119,143 Gymnodinium galeaeforme Matzenauer Gymnodinium gibbera Schiller " " Gymnodinium grammaticum (Pouchet) Kofoid et Swezy [= G. punctatum var. grarnmaticum Pouchet] Gymnodinium lachmannii Saville-Kent Continued on p. 48 174 48 Table L Continued. Gymnodinium marinum Saville-Kent Gymnodinium minus Lebour Gymnodinium najadeum Schiller 19-22,25.34,58,59.61,75.76.79.89.96,119,143 Gymnodinium neapolitanum Schiller "1 96.114.143 Gymnodinium paradoxum Schilling Gymnodinium pygmaeum Lebour [possibly identical with Gymnodinium aureolum (Hulburt) G. Hansen] Pacif. Gynvtodinium radiatum Kofoid et Swezy Gymnodinium rhomhoides Schiitt 12.14,15,17—20,33,34,58,59,61,90,96,110-112,114,119 Gyrmiodinium rotundatum Klebs 94 Gymnodinium semidivisum Schiller Gymnodinium simplex (Lohmann) Kofoid et Swezy [= Protodinium simplex Lohmann] ' 94 Gymnodinium sphaericum (Calkins) Kofoid et Swezy [= G. gracile \ar. sphaerica Calkins] Pacif. Gyrwiodinium sulcatum Kofoid et Swezy Gymnodinium uberrimum (Allman) Kofoid et Swezy [= G. mirabile Pénard, G. mirabile var. rufescens Pénard, G. rufescens Lemmermann, G. bogoriense Klebs, G. rotundatum Klebs, G. obesum Schiller, G. limneticum Woloszynska, G. poculiferum Skuja, G. limitatium Skuja, G. irregulare Christen, G. uberrimum var. rotundatum Popovsky, Gyrodinium traunsteineri Lindemann, Melodinium uberrimum Kent, Peridinium uberrima Allman] 23,75.76.132,139 Gymnodinium variabile Herdman Cold Gymnodinium wulffii Schiller [non Gyrodinium wulffii Schiller] 58.59,61 Cold Gyrodinium britannicum Kofoid et Swezy [= Spirodinium spirale var. acutum Lebour] Gyrodinium capsulatum Kofoid et Swezy Gyrodinium coniutum (Pouchet) Kofoid et Swezy [= Gymnodinium spirale var. cornutum Pouchet] 85.86.132 Gyrodinium dorsum Kofoid et Swezy Gyrodinium falcatum Kofoid et Swezy [= Gyrruiodinium fusus Schiitt pro parte, Pseliodinium vaubanii Soumia] 9.14.15.18-20.34,61.96.110,119,143 Gyrodinium fissum (Levander) Kofoid et Swezy [= IG.fissoides Elbrachter, IGymnodinium fissum Levander] 59,61,144 Gyrodinium fusus (Meunier) Akselman [= Spirodinium fusus Meunier, G.fusiforme Kofoid et Swezy] 9.18.26,27.29,33,34, 42.59.61.79.94.96.107.114.117.119.128.143 Gyrodinium glaebum Hulburt [= Gyrrmodinium mirabile Pénard] Gyrodinium lachryma (Meunier) Kofoid et Swezy [= Spirodinium lachryma Meunier] 9.18.27.33,34,59, 61.94.96.114.117.119.128.135.143 Gyrodinium nasutum (Wulff) Schiller [= Spirodinium nasutum Wulff) 59,61,96,117,128,143 Gyrodinium pavillardii Biecheler 9" Gyrodinium pellucidum (Wulff) Schiller [= Gyrrmodinium pellucidum Wulff] 94 Gyrodinium pingue (Schiitt) Kofoid et Swezy [= Gymnodinium spirale var. pinguis Schiitt, Spirodinium varians Wulff] 9.18.59.61.96.112.114.143 Gyrodinium prunus (Wulff) Lebour [— Spirodinium prunus Wulff) Gyrodinium pusillum (Schilling) Kofoid et Swezy [= Spirodinium pusillum (Schilling) Lemmermann, Gymnodinium pusillum Schilling] "4 Gyrodinium spirale (Bergh) Kofoid et Swezy [= Gymnodinium spirale Bergh] 59,61,128 Heterocapsa rotundata (Lohmann) G. Hansen [= Amphidittium rotundatum Lohmann, A. pellucidum Redeke, Gymnodinium minutum Lebour, Katodinium rotundatum (Lohmann) Pott, K. minutum (Lebour) Soumia, Massartia rotundata (Lohmann) Schiller] HAB Heterocapsa triquetra (Ehrenberg) Stein [= Glenodinium triquetrum Ehrenberg, Peridinium triquetrum (Ehrenberg) Lebour, Properidinium heterocapsa (Stein) Meunier] 9,18-23,25,27,28,34,41,58—61,70,75,76,78,85,86,88,89,94,96,97,110,132—135,137,139,143 Heterodinium murrayi Kofoid 94 Schiller, M. austriacum Schiller, Katodinium crassifilum (Schiller) Loeblich IB, K. austriacum (Schiller) Loeblich IB] Katodinium vorticella (Stein) Loeblich IB [= Gyrrmodinium vorticella Stein, Peridinium vorticella Stein, Massartia vorticella (Stein) Schiller, M. pratensis Baumeister, Katodinium viride Christen, K. vemale Christen, K. pratensis (Baumeister) Loebhch BI] 59.61 Continued on p. 49 175 49 Table 1. Continued KolkwitzieUa acuta (Apstein) Elbrachter [= Glenodinium acutum Apstein, Diplopsaiis acuta (Apstein) Entz, Entzia acuta (Ap- stein) Lebour, Peridinium latum Paulsen, KolkwitzieUa salebrosa Lindemann, K. gibbera (Lindemann) Lindemann, Apsteinia acuta Abe] 61,%. 119,143 HAB Kryptoperidinium foUaceum (Stein) Lindemann [= Glenodinium foliaceum Stein] '8 59.61 HAB Lingulodiniuinpolyedra (Stein) Dodge [= Gonyaulax polyedra Stein] 8.9,14.15,17—20.23.25.33,46,58—61,72,75,76,78.85.86.89,90, 94.96,110.111,114,118,119.132-135,139,143 Mesoporos perforatus (Gran) Lillick [= Exuviella perforata Gran, Porella adriatica Schiller, P. bisimpressa Schiller, P. globulus Schiller, P. asymmetrica Schiller, Porotheca perforata (Gran) Silva] 58,61,94 HAB Noctiluca scintillons (Macartney) Kofoid [= N. miliaris Suriray ex Lamarck] 7.8,12.18,31,35,36,46,47,51,59-61.75,76,81.94,97, 101.110,114.128.129.133-136.141,143 Ohlea rotunda (Balech) Balech ex Soumia [= Peridiniopsis rotunda Lebour, Glenodinium rotundum (Lebour) Schiller, D fpkpW » mmn&z (Lebour) Wood, D. rnmndntn Steidinger et Williams] 9,18.34.59.61.96.110.114 OriyAysM ojryfojroMks Kofoid 23.59.75.76.137.139 Oxyrrhis marina Dujardin [= 0. maritima Van Meel, O. tentaculifera Conrad] 58.59.61.143 Oxytoxum adriaticum Schiller Oxytoxum brunellii Rampi ^̂ 3 Oxytoxum milneri Murray et Whitting [= O. subulatum Kofoid] ^ Oxytoxum mitra Stein Oxytoxum parvum Schiller [= 0. tenuistriatum Rampi, reported as ‘O. parvulum' Schiller] Oxytoxum variabile Schiller [— Oxytoxum gracile Schiller] Palaeophalacroma unicinctum Schiller [= Heterodinium detonii Rampi, Epiperidinium michaelsarsi Gaarder] Cold Peridiniella danica (Paulsen) Okolodkov et Dogde [= Glenodinium danicum Paulsen ex Braarud pro parte] 15.18-20.27.34.59.61.88.96.110.114 Peridiniopsis oculatum (Stein) Bourrelly [= Glenodinium oculatum Stein] Peridiniopsis thompsonii (Thompson) Bourrelly [= Glenodinium quadridens (Stein) Schiller, Peridinium quadridens Stein] ^ Peridinium aciculiferum Lemmermann [= P. umbonatum var. aciculiferum Lemmemann, P. stagnale Meunier, Glenodinium aciculiferum (Lemmermann) Lindemann] 51.143 Peridinium bipes Stein [= P. tabulatum (Ehrenberg) Claparède et Lachmann, Glenodinium tabulatum Ehrenberg, G. apiculatum Ehrenberg] 34.58.61 Peridinium cinctum (O F. Müller) Ehrenberg [= Peridinium tabulatum Pénard, P. cinctum var. lemmermannii West, var. laesum Lindemann, var. regulatum Lindemann, var, irregulatum Lindemann, var. angulatum Lindemann, var. carinatum Steinecke et Lindemann, non var. gibbosum Lefèvre, non var. palustre Lindemann, Also P. cinctum f. regulatum (Lindemann) Lefèvre, f. angulatum (Lindemann) Lefèvre, f, ovoplanum Lindemann, f. meandricum Lefèvre, f. westii (Lemmermann) Lefèvre, f, tuberosum (Meunier) Lefèvre, P. germanicum Lindemann, P. eximium Lindemann, P. rhenanum Lindemann] 9,18,61,84.94.96.143 Peridinium elpatiewskyi (Ostenfeld) Lemmermann [= P. umbonatum var, elpatiewskyi Ostenfeld, P. pygmaeum Lindemann, Glenodinium elpatiewskyi (Ostenfeld) Schiller, Peridiniopsis elpatiewskyi (Ostenfeld) Bourrelly] 5* Peridinium umbonatum Stein [= Peridinium incorrspicuum Lemmermann, P. pusillum (Pénard) Lemmermann, P. orrei Huitfeld- Kaas, P. umborujtum var. papilliferum Lemmermann, P. javanicum Bernard, P. umbonatum var, inaequale Lemmermann, P. inconspicuum var. armatum Lemmermann, P. marchicum Lemmermann, P. tabulatum var, caudatum Playfair, P. minimum Wo- loszynska, P. tatricum Woloszynska, P. tatricum var, spinulosa Woloszynska, P. linzium Lindemann, P. munusculum Lindemann, P. munusculum f. spiniferum Lindemann, P. caudatum Playfair, P. geminum var, angulosum Playfair, P. geminum var, elegans Playfair, P. geminum var. excavatum Playfair, P. marchicum var, keyense Nygaard, P. steinmannii Woloszynska, P. parvulum Woloszynska, P. arrbiguum Lindemann, P. umbonatum f. spiniferum (Lindemann) Lefèvre, P. inconspicuum var. excavatum (Playfair) Lefèvre, P. inconspicuum f. armatum (Lemmerman) Lefèvre, P. inconspicuum f. spiniferum (Lindemann) Lefèvre, P. africarmm f. tatricum (Woloszynska) Lefèvre, P. africanum var. spinulosum (Woloszynska) Lefèvre, P. inconspicuum var. balatonicum Entz, Glenodinium guildfordense (Playfair) Lindemann, G, geminum (Playfair) Lindemann, G. pusillum Pénard, G. lefevrei Lindemann, Gymnodinium oligoplacatum Skuja. Also including Peridinium umbonatum war. lubieniense (Wolszynska) ' Popovsky f t Pfeister, flenWininm Wfemense Wolszynska, see also Elbrachter & Meyer (2001)] 59,61,143 - . ̂— mmmrn K##iiuiuumKm tabulatum Playfair, P. australe Playfair, P. hieroglyphicum Playfair, P. striolatum Wailes, P. vancouverense Wailes, non Peridinium tabulatum (Ehrenberg) Claparède et Lachmann] 5L96 Continued on p. 50 176 50 Table I. Continued Petalodinium porcelio Cachon et Cachon '^5 Phalacroma acutum (Schiitt) Pavillard [= P. vastum var. acutum Schiitt, Dinophysis acutoides Balech, non D. acutum Ehrenberg] Phalacroma favus Kofoid et Michener [= Dinophysis favus (Kofoid et Michener) Abe vel Balech] 5-50 Phalacroma ovatum (Claparède et Lachmann) Jprgensen [= Dinophysis ovata Claparède et Lachmann] 51.94,135 Phalacroma parvulum (Schiitt) Jprgensen [= P. porodictyum Stein var. par\’ula Schiitt, Dinophysis oviformis Schiller; possible small cell of D. rotundata Claparède et Lachmann according to Reguera & Gonzalez Gil (2001)] 50,94,133,134 Phalacromapulchellum Lebour [— Dinophysis pulchella (Lebour) Balech] •8-51,96,110 HAB Phalacroma rotundatum (Claparède et Lachmann) Kofoid et Michener [= Dinophysis rotundata Claparède et Lachmann, P. rudgei Murray er Whitting, D. whittingae Balech] 9,15,17-19,20,27,33,34,46,59-61,90,94,96.110,114.119,129,133-135,143,144 Plectodinium nucleovolvatum Biecheler [= P. miniatum (Kofoid et Swezy) F.J.R. Taylor, Cochlodinium miniatum Kofoid et Swezy]^^ Podolampas elegans Schiitt Podolampas spinifera Okamura Polykrikos kqfoidii Chatton [— P. schwarzii Kofoid pro parte] Polykrikos schwartzii BiitschU [= P. auricularia Bergh] 8,18,42,59,61.94,96,110,114,118,129 Preperidinium meunieri (Pavillard) Elbrachter [= Diplopsaiis lenticula Bergh f. minor Paulsen, Zygabikodinium lenliculatum Loeblich et Loeblich IB, Peridinium lenticulum Mangin, Glenodinium lenticula f. minor (Paulsen) Pavillard, Diplopeltopsis minor (Paulsen) Pavillard] ^^ 51 Pronoctiluca acuta (Lohmann) Schiller Pronoctiluca pelagica Fabre-Domergue [= Rhynchomonas marina Lohmann, Pelagorhynchus marinus Pavillard] 24.94,128,144 Pronoctiluca spinifera (Lohmann) Schiller [= P. tentaculata (Kofoid et Swezy) Fabre-Domergue] Prorocentrum aporum (Schiller) Dodge [= P. antarcticum (Hada) Balech, Exuviella granii Gaarder] 59,60,94.133-135 HAB Prorocentrum balticum (Lohmann) Loeblich IB [— P. pomoideum Bursa, Exuviella baltica Lohmann, E. aequatorialis Hasle] 18,46,60.61.75,76.94.96.110.114.133,134,143 Prorocentrum compressum (Bailey) Abe ex Dodge (= P. lebourae Schiller, Exuviella compressa Bailey, E. oblonga Schiller, E. lenticulata Matzenauer, E. elongata Rampi] 8,9.14.15.18—20.33.34.46.58—61.63,90.94.96.107.110.114.119,127.133—135.143,144 HAB Prorocentrum cordatum (Ostenfeld) Dodge [= Exuviella cordata Ostenfeld, E. pyriformis Schiller, ?P. minimum (Pavillard) Schiller] 9-33,42.49.56,58.60.61.63.67-69.72.73.81-87.89,90.94.96-99.105-107.109-112.114-115.118.119,125.129.132-134.137.143 Prorocentrum dentatum Stein [= P. obtusidens Schiller, P. veloi Osorio-Tafall, P. monacense Kufferath] 50.75.76.94.133.134 HAB Prorocentrum lima (Ehrenberg) Dodge [— Exuviella marina Cienkowski, E. caspica Kisselew, E. cincta Schiller, E. ostenfeldii Schiller] 18,32.58.59.61,89.94.96,107.110 Prorocentrum maximum (Gourret) Schiller [= P. brochii Schiller] 50.94.133.134.143 HAB Prorocentrum micans Ehrenberg [= P. schilleri Bohm in Schiller, P. levantoides Bursa] 9.14,15.17-20.25-27.30. 32.33,46.58-61.75.76.78.79.81.84-86.89,90.94.96.98.99.107.109-111.114.118.119.125.129.132-135,139.143 HAB Prorocentrum minimum (Pavillard) Schiller [= P. mariae-lebourae (Parke et Ballantine) Loeblich BI, P. triangulatum Martin, P. cordiformis Bursa, IP cordatum (Ostenfeld) Dodge] 2,46.59,60.75.76.78.79.94.133.134.138,139 Prorocentrum obtusum Ostenfeld 9,18,34.61,89.96 Prorocentrum ovum (Schiller) Dogde [— Exuviella ovum Schiller] Prorocentrum pusillum (Schiller) Loeblich [= Exuviella pussilla Schiller, non P. nanum Schiller] Prorocentrum rostratum Stein [= Prorocentrum styliferum Lohmann] ^^-^5 Prorocentrum rotundatum Schiller 50.94.133-135 Prorocentrum scutellum Schroder [= P. sphaeroideum Schiller, P. robustum Osorio-Tafall] •-•^-15,19,20-23,25.28.29.33, 34.46,58.60.61.94,96.109.114.119.133-135 Prorocentrum triestmum Schiller [ — P. redfieldii Bursa, P. pyrenoideum Bursa] 60,133.134 Prorocentrum vaginulum (Stein) Dodge [— Dinopyxis vaginula Stein, Exuviella vaginula (Stein) Schiitt] ^^ 51 Protoceratium areolatum Kofoid 59.60.94,133.134 HAB Protoceratium reticulatum (Claparède et Lachmann) BUtschli [= Gonyaulax grindleyi Reinecke] 9,18.33.34. 46.58,59.61.79.90,94,96.110.112.114.119.133.135 Protoperidinium abei (Paulsen) Balech [— Peridinium abei Paulsen, P. biconicum Abe, non P. biconicum Dangeard] Protoperidinium achromaticum (Levander) Balech [ = P. finitimum Balech, Peridinium achromaticum Levander] 58.59,61,128.143 Continued on p. 51 177 51 Table I. Continued Protoperidinium bipes (Paulsen) Balech [= Minuscula bipes (Paulsen) Lebour, Peridinium minusculum Pavillard Glenodinium bipes Paulsen, non Peridinium bipes Stein] 9.18,27,33,34,5^ 61,94,96.109,110,114,119,128,135.143,144 Protoperidinium brevipes (Paulsen) Balech [= Peridinium brevipes Paulsen, P. varicam Paulsen, P. incurvum Lindemann] 8.9.18.27.33.34.46.58.60.61.94.96.110.114.119.133-135 Protoperidinium brochii (Kofoid et Swezy) Balech [— P. adriaticum Broch, P. divergens var. adriaticum Schiller] 8.61.90.128 Protoperidinium claudicans (Paulsen) Balech [= Peridinium claudicans Paulsen] 8.60.128.133-135.143 Protoperidinium conicoides (Paulsen) Balech [= Peridinium conicoides Paulsen] 50,61.131.133.134 Protoperidinium conicum (Gran) Balech [= Peridinium divergens var, conica Gran] 8,42.59-61,94.128.133-135,143 HAB Protoperidinium crassipes (Kofoid) Balech [see Balech (1988: 110) for synonymy with P. curtipes] 8,9,18.33-35.59.61,94,96.99.110,119.114.135,143 Protoperidinium curtipes (Jprgensen) Balech [= Peridinium curtipes Jprgensen, P. crassipes Paulsen, non Paulsen nec Schiller] 94.128,135 Protoperidinium curvipes (Ostenfeld) Balech [ = Peridinium curvipes Ostenfeld] ‘̂ -94,135 Protoperidinium decipiens (j0rgensen) Parke et Dodge [= Peridinium decipiens J0rgensen] 9.18,58,61,96 Protoperidinium deficiens (Meunier) Balech [= Peridinium deficiens Meunier] 94 Protoperidinium depressum (Bailey) Balech [= Peridinium depressum Bailey] 8,9,18,33 -35,46.60,61,94,96,110,113,114.119,128, 133-135,143 Protoperidinium diabolus (Cleve) Balech [= Peridinium diabolus Cleve, including P. longipes (Karsten) Balech] 8,35,60. 61.94.128.133.134.143 Protoperidinium divergens (Ehrenberg) Balech [ = Peridinium divergens Ehrenberg] 8,9.18,34.35.46.59-61.94.96.107.114.119.128. 133.134.143 Protoperidinium elegans (Cleve) Balech [= P.fatulipes (Kofoid) Balech, Peridinium aimulatum Kofoid et Michener] 8,58,59.61 Protoperidinium excentricum (Paulsen) Balech [= Peridinium excentricum Paulsen, P. perrieri Fauré-Frémient] 58,59,61,94.143 Protoperidinium globulus (Stein) Balech [= Peridinium ovatum (Pouchet) Schiitt, P. globulus var. ovatum (Pouchet) Schiller, also P. globulus var. ovatum (Pouchet) Krachmalny, P. globulus var, quamerense (Schroder) Krachmalny] 8,9.18,37.59-61,94,96,114.117.119.128,133.134.143,144 Protoperidinium grande (Kofoid) Balech [= P. truncatum (Graham) Balech] 50.94.133,134 Protoperidinium granii (Ostenfeld) Balech [— Peridinium granii Ostenfeld ex Paulsen] 8,9,18.27.34.59-61. 79.90.94.96.110.114.119.128.133-135.143 Protoperidinium inflatum (Okamura) Balech [= Peridinium inflatum Okamura, P. crassum Dangeard] Cold Protoperidinium knipowitschii (Ussatschew) Balech [— Peridinium knipowitschii Ussatschew] 34.59,61.96.143 Protoperidinium leonis (Pavillard) Balech [= Peridinium leonis Pavillard P- conicum Meunier, P. saltans Pavillard, P. striatum Bohm, P. leonis var. concavilaterale Kisselew] 8,61.94.128.135 Protoperidinium longispinum (Kofoid) Balech [= Peridinium longispinum Kofoid P michaelis Ehrenberg pro parte] 9,46.61.89 Protoperidinium marielebourae (Paulsen) Balech [= Peridinium obtusum (Karsten) Lebour, non P. obtusum (Karsten) Faure- Fremiet] 94.133 Protoperidinium minutum (Kofoid) Loeblich IB [the synonymy with P. monospinum (Paulsen) Zonneveld et Dale is debatable] 18.61.96.143 Protoperidinium oblongum (Aurivillius) Parke et Dodge [= Peridinium oblongum Cleve, P. divergens var. oblongum Aurivillius, P. oceanicum var. oblongum Paulsen, P. venustum Matzenauer] ^ 94 Protoperidinium oceanicum (VanhofFen) Balech [= Peridinium divergens var, oceanicum Stein] 8,59,61,128,143 Protoperidinium pallidum (Ostenfeld) Balech {= Peridinium pallidum Osi&nîc\dî\ 8,9.18,34,46.59,61,94,96.114,128 Protoperidinium pedunculatum (Schiitt) Balech [= Peridinium pedunculatum Schiitt] 8,61,94.96.143 Protoperidinium peUucidum Bergh [= Peridinium pellucidum (Bergh) Schiitt] 8,46.58-61.94.96.109.110.119.133-135.144,143 Protoperidinium pentagonum (Gran) Balech [= Peridinium pentagonum Gran, P. sinuosum Lemmermann] 8,33,59-61. 94.114.119.128.131.133-135.143 a var, pyriformis Pat Pacif. Protoperidinium sinaicum (Matzenauer) Balech [= Peridinium sinaicum Matzenauer] Protoperidinium pyriforme (Paulsen) Balech [= Peridinium steinii var, pyriformis Paulsen, also Peridinium breve Paulsen] 59-61,94,96,119,133-135 Continued on p. 52 178 52 Table 1. Continued Protoperidinium solidicome (Mangin) Balech [= P. spiniferum (Schiller) Balech, P. spinosum Schiller] 8.9,18,34,35, 46,58,59,61,94,96,110,114,128,131,135,143 Protoperidinium steinii (Jprgensen) Balech [= P. steinii Jprgensen, P. michaelis Stein] 1-8,9,18,25,33,34,46,59-61, 90,94,96,107,110,111,113,114,119,128,133,134,143,144 Protoperidinium subinerme (Paulsen) Loeblich IB [= Peridinium subinerme Paulsen] 58-61,94,128.133-135 Protoperidinium thorianum (Paulsen) Balech [= Peridinium thorianum Meunier, Glenodinium thorianum Paulsen] ^9 Ptychodiscus noctiluca Stein [= P. inflatus Pavillard P carbiatus Kofoid] ^9 Pyrocystis elegans Pavillard 50,133,134 Pyrocystis lunula (Schiitt) Schiitt [= Gymnodinium lunula Schiitt] 8,61,81 Pyrophacus horologium Stein emend. Wall et Dale 9,18,59-61,94.96,110,114,119,133,134.143 Pyrophacus steinii (Schiller) Wall et Dale [= P. horologicum var. stei?iii Schiller] 94,135 Scaphodinium mirabile Margalef [= Leptospathium navicula Cachon et Cachon] HAB Scrippsiella trochoidea (Stein) Balech ex Loeblich BI [= Peridinium trochoideum (Stein) Lemmermann, P.Jaeroense Paulsen, Scrippsiella sweeneyae Balech ej: Loeblich IB] 8,9,18,21-23,27,28,34,41,46,58-61,75,76,86.89.94,96,114,133-137.139,143 Spatulodinium pseudonoctiluca (Pouchet) Cachon et Cachon ejc Loeblich et Loeblich BI [= Gymnodinium pseudonoctiluca Pouchet] 1̂ 5 Torodinium robustum Kofoid et Swezy [= Gymnodinium teredo Schiitt pro parte] 51 Woloszynskia neglecta (Schilling) R.H. Thompson [= Gymnodinium neglectum (Schilling) Lindemann, Glenodinium neglectum Schilling] 59 of the eutrophication. However it is likely that these species remained unnoticed in previous studies. C o ld w aters species: A rc tic -b o re a l a ffin ities? The low species richness could be associated with the low temperatures in the Black Sea (<4°C in winter) that only favour cryophilic or eurythermal species. The Arctic Seas with 95 and 189 species listed in the Canadian and Russian waters, respectively (Hsiao, 1983; Okolodkov, 1998) also present low species richness compared to temperate or warm oceans. Most of the freshwater taxa (from continental waters; Popovsky & Pfiester, 1990) can be con­ sidered as cryophilic/eurithermal species, being here discarded for marine biogeography. Athecate species such as A m ph id in ium longum Lohmann (= A. acu­ tum Lohmann), A. extensum Wulff, A. ovum Herd- man (sand-living), G yrod in ium b ritann icum Kofoid et Swezy and also G ym nod in ium w u lff ii Schiller are reported from the cold waters of the North Atlantic Ocean, but not or rarely reported in the Mediterranean waters (Gomez, 2003). Okolodkov & Dodge (1996) reported only four Arctic-boreal species, A lexand rium os ten fe ld ii (Paulsen) Balech et Tangen, A m ylax triaca n th a (Jorgensen) Soumia, C era tium a rc ticum (Ehrenberg) Cleve, D inophys is norvég ien Claparède et Lach­ mann and the bi-polar D inophys is a rc tica Meresch- kowsky, P ro to p e rid in iu m is la n d icu m (Paulsen) Ba­ lech, P. sa ltans (Meunier) Balech and P. thulesense Balech, All these species except C. a rc ticum and the last three are reported from the Black Sea. The re­ cords of Arctic-boreal species proposed by Okolodkov & Dodge (1996) are scarce and/or dubious in the Mediterranean Sea (Gomez, 2003). D inophys is a rc tica , D . no rveg ica and D . ap- icu la ta Meunier are not or rarely reported in the Mediterranean waters (Gomez, 2003). Similarities have been reported in the developmental stages of D. acum ina ta , D . acuta and D. norveg ica (e.g., Reguera & Gonzalez Gil, 2001). Genetic ana­ lyses showed that D . acum ina ta and D. norveg ica were nearly identical (>99%) (Rehnstam-Holm et al., 2002). D. a p icu la ta , reported only by Krakhmalny (1994) in the Black Sea, is according to Okolodkov (1998) related to D . acum ina ta . D ino p h ys is a p icu la ta presented only one record in the Mediterranean Sea (Gomez, 2003). A m ylax tr iaca n th a only presents one dubious re­ cord in the Mediterranean Sea and A lexa n d rin um o s t T n f m ^ s r e p o r t ^ r i ^ r W " B O T 3 r i i waters (Gomez, 2003). Other thecate species that can be con­ sidered as cryophilic are G o nyau lax cochlea Meunier, P ro to pe rid in iu m k n ip o w its c h ii (Ussatchev) Balech, P ro tope rid in ium defic iens and P e rid in ie lla dan ica (Paulsen) Okolodkov et Dodge. P. kn ip o w itsch ii is 179 53 rather similar in shape to the cosmopolitan spe­ cies P ro to pe rid in iu m g rande (Kofoid) Balech [Taylor, 1976: 150] or to the bi polar P. sa ltans (Meunier) Ba­ lech [Balech, 1974:64] as well as P erid in iu m fa tu lip e s Kofoid [Kisselew, 1950: 203]. P. deficiens, with one dubious record from the Mediterranean Sea (Gomez, 2003), could be considered a cold water species. P e rid in ie lla dan ica , typically known from the North Atlantic Ocean (Okolodkov & Dodge, 1995), is repor­ ted from the North Adriatic Sea (Vilicic et al., 2002) with additional, doubtful, records from the warm wa­ ters o f the southern Mediterranean basin (Dowidar, 1974; Skolkaetal., 1986). C eratium long ipes (B a ile y ) Gran (= C. a rc ticum var. long ipes (Bailey) Graham et Bronikovsky) seems to be more common in cold waters (Okolodkov & Dodge, 1996). Indo -P ac ific species? A reduced group of species not reported in the At­ lantic Ocean to the best o f our knowledge, but in the Indian and/or Pacific waters, includes dubious Indo-Pacific species such as A m p h id in im cu cu rb ita Kofoid et Swezy, G ym nod in ium rad ia tum Kofoid et Swezy (recently reported by Krakhmalny, 2001) and G. su lcatum Kofoid et Swezy (Mediterranean; Gomez 2003). Among thecate dinoflagellates the only reports are of P ro to pe rid in iu m s ina icum , which resembles to P ro tope rid in ium tuba (Schiller) Balech, both doubtful or insufficiently known taxa (Taylor, 1976: 160). N on-M ed ite rranean taxa a n d /o r in troduced species? Nearly all the species reported from the Black Sea (Table 1) are also reported from the Mediterranean Sea. Several exceptions were A m p h id in iu m c o n ra d ii Schiller, A. ovum Herdman [both from the North At­ lantic Ocean; Parke & Dodge (1976)], C och lod in ium c itron Kofoid et Swezy [doubtful record by Skolka et al. (1986) in the Mediterranean Sea] as well as the Atlantic species C och lod in ium p iru m (Schiitt) Lem­ mermann. Excluding these dubious records only A l­ exandrium m on ila tum (Howell) Balech remains as a non-Mediterranean taxon, together with several Artic- boreal species and A. cu cu rb ita and G. rad ia tu m as artificially Indo-Pacific taxa. L A lexandrium m on ila tu m , responsible for blooms in the Black Sea since 1991 (Moncheva et al., 2001a), is typically known from sub- and tropical regions of the Atlantic and Eastern Pacific Ocean, although it was also recorded in the cold waters of the Chesapeake Bay (Steidinger & Tangen, 1997: 499). Live cells of A. m on ila tum are easily identifiable compared to con­ generic species, but difficult from fixed samples. A dubious record, as Gessnerium m ochim aensis Halim ex Halim, is reported from the Suez Canal in the sum­ mer (El-Sherif & Ibrahim, 1993). It is unusual the proliferation of this taxon, an a p r io r i thermophilic species, in the cold waters of the Black Sea. The exchange of species, toxic or not, between the Mediterranean and Black Seas seems to be rare. Des­ pite A. m on ila tum is being reported from Bulgarian waters close to the Bosphorus/Dardanelles Straits, the introduction to the Mediterranean Sea, favoured by the westward surface current system, is not repor­ ted. For example K aren ia b revis (Davis) G. Hansen et Moestrup, a common toxic species in the Aegean Sea eutrophic waters (Gotsis-Skretas & Frigilos, 1990), is not reported in the Black Sea. Moncheva et al. (2001b) reported that despite the fact that the Aegean Sea, like the Black Sea, could be considered a eutrophic basin, the bloom-forming assemblages show a low taxonomic similarity. This has been attributed to both natural factors and dissimilarities and to the gradients in nutrient levels and their ratios (Moncheva et al., 2001b). As non-indigenous plankton species (introduced species) from the Black Sea, Moncheva & Kam- burska (2002) listed G ym nod in ium ube rrim um (All- man) Kofoid et Swezy, Oxyphysis oxytoxoides Kofoid, G ym nod in ium fuscum (Ehrenberg) Stein, G yrod in ium cf. aureo lum Hulburt, ‘Gyrodinium sim­ plex’, S pa tu lod in ium pseudonoctiluca , S caphodin ium m ira b ile , P e ta lod in ium p o rc e lio as well as A lexan ­ d riu m m onila tum . Red tides by the freshwater species G ym nod in ium ube rrim um were reported from the western Black Sea since 1990’s (Moncheva et al., 2001a). However this taxon presents a high number of related species or synonyms indicative of its difficult identification (Pop­ ovsky & Pfiester, 1990: 117). As reported in Wyatt & Carlton (2002) G. ube rrim um is a common bloom- forming species in European and North American lakes and its appearance in estuarine areas of the Black Sea is not unexpected. Moncheva & Kamburska (2002) reported a possible origin o f_ O xyphysis o xy to xo id ^ . f io m Alaska/California. However this species was reported from the Mediterranean (Gomez, 2003), recently from the Marmara Sea (Balkis, 2000) and all major oceans (Soumia, 1986: 44). G ym nod in ium fuscum is primar­ ily a freshwater taxon of difficult identification, with dubious records in the Mediterranean Sea (Gomez, 180 54 2003). More uncertainties appear with G ym nod in ium aureo lum (Hulburt) G. Hansen related to the Gym ­ nod in ium m ik im o to i complex (Hansen et al., 2000). G ym nod in ium s im plex (Lohmann) Kofoid et Swezy is also a species of complex identification frequently reported in the Mediterranean Sea (Gomez, 2003). Stoyanova (1999) reported for the first time the noctilucaceans S pa tu lod in ium pseudonoctiluca , Scaphodin ium m ira b ile and P eta lod in ium p o rce lio in the Black Sea. S. pseudonoctiluca is reported from all major oceans (Soumia, 1986; 52). These three taxa, and especially the leptodiscaceans, S. m ira b ile and P. p o rce lio , strongly differ from the typical appearance of the dinoflagellates (Peridiniales) and that, together with the scarcity of available literature, is responsible for the under estimation of these ubiquitous species, going unnoticed under routine microscopical analysis. For example S. m ira b ile is reported from the Mediter­ ranean Sea (Gomez, 2003), Atlantic Ocean (Margalef, 1973) also recently from the Marmara Sea (Balkis, 2000). S. m ira b ile and P. p o rce lio can be found in the we stem Pacific Ocean (F. Gomez, unpublished results). E xclus ive ly M ed ite rra n e a n -B la ck Sea species Several species seem to be restricted to the Mediterranean-Black Sea waters such as several inap­ propriately described unarmored taxa: G ym nod in ium najadeum Schiller, G. neapo litanum Schiller and G. sem idivisum Schiller. The aberrant dinoflagellate Peta lod in ium p o rc e lio Cachon et Cachon (Stoyanova, 1999) can be considered exclusively a Mediterranean- Black species, but probably this taxon remains un­ noticed in the world’s oceans. The citation of the thecate G onyau lax elegans Rampi constitutes the only worldwide record of this dubious species never repor­ ted after the initial description in the Mediterranean Sea (Gomez, 2003). Many of the species of the genus G onyau lax Diesing described by Rampi are considered as synonyms of other congeneric species (see Dodge & Saunders, 1985). Endem ic species? The geologic evolutioB.of the Ponto-Caspian basins involved a succession of separations/isolations and in more recent geologic time the reconnection to the ocean (Mediterranean Sea) (e.g., Mudie et al., 2002). These events resulted in the evolution of di­ verse modem organism assemblages of freshwater, brackish water, and marine taxa of mixed origins consisting of endemic (autochthonous) Ponto-Caspian species, Mediterranean-Atlantic immigrants, and Arc­ tic Pleistocene glacial relicts. For macroscopic organ­ isms, the autochthonous Ponto-Caspian species are characterized by wide adaptive capacities and con­ stitute a significant portion of the invasive species currently spreading to regions in northem Europe and to the Great Lakes (Reid & Orlova, 2002). In the semi-enclosed Black Sea, with special hydrological, chemical and trophic conditions, a high endemism by Ponto-Caspian relict algal species could be expected. A candidate could be P ro rocen trum caspicum (Kisselew) Krakhmalny described from the Caspian Sea and further from the Arctic Sea (Kisselew, 1950). However this taxon is considered a synonym of Prorocentrum lim a (Ehrenberg) Dodge (Dodge, 1975). P rorocentrum corda tum (Ostenfeld) Dodge originally described from the Caspian Sea is con­ sidered endemic and prominent in the Ponto-Caspian basins (Makarova, 1969), but the cosmopolitan Prorocentrum m in im um (Pavillard) Schiller is con­ sidered to be synonym (Marasovic et al., 1990; Velikova & Larsen, 1999). Several morphological varieties (infraespecific taxa) such as P rorocentrum cordatum var. ara lensis (Kisselew) Krakhmalny or A m ph id in ium k lebs ii f. po n ticum Rouchijajnen are reported (Kisselew, 1950; Krakhmalny, 1994). In conclusion, no taxa can be recognized as endemic species. F in a l remarks The extreme environmental conditions (high nutrient concentrations and modified nutrient ratios) are as­ sociated with low species richness and dominance of mono-specific blooms such as N o c tilu c a sc in til- lans, P rorocentrum cordatum , H eterocapsa triqu e tra , Scrippsie lla trochoidea (Stein) Balech ex Loeblich III, among others (Bologa et al., 1995; Mihnea, 1997; Ve­ likova et al., 1999). Compared to the Mediterranean waters, several cold-water species appeared, indicative of the Arctic Seas affinities or the presence of glacial period relicts. Despite the strong environmental modi­ fications that could favour invasive species in compet­ ition for niches, it is difficult to establish a tentative list of introduced species. The non-indigenous spe­ cies list proposed by Moncheva & Kamburska (2002) is composed of doubtful taxa and species unnoticed in previous studies and/or taxa recently recognized at species level. More in deep taxonomical studies, with the application of recent taxonomical approaches, are 181 55 necessary to establish the species richness in the Black Sea waters. Acknowledgem ents This checklist has been possible with the collabora­ tion of colleagues supplying less accessible literature. We thank Mrs. M. Ford for English corrections. E.G. acknowledges the financial support of the European Commission (ICB2-CT-2001-80002). References Aubert, M., P. Revillon, J. Aubert, G. Léger, C. Drai, A. Amoux & C. Diana, 1990. Mers d’Europe: Études hydrobiologiques, chimiques et biologiques. Transfert de polluants entre la Mer Noire, la Mer de Marmara et la Mer Egée. Revue Internationale d’Océanographie Médicale 100: 1-44. Aubrey, D., S. Moncheva, E. Dcmirov, V. Diaconu & A. Dimitrov, 1996. Environmental changes in the western Black Sea related to anthropogenic and natural conditions. Journal of Marine Systems 7:411^25. Bakan, G. & H. Buyukgungor, 2000. The Black Sea. 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E-mail: fernando.gomez@fitoplancton.com ABSTRACT Aim To investigate biogeographical patterns based on published dinoflagellate records from the Mediterranean and Black Seas, and to provide a tentative list of endemic and Indo-Pacific dinoflagellates in the Mediterranean Sea. Location Mediterranean Sea, Black Sea. M ethods Checklists of dinoflagellates of the Mediterranean and Black Seas were compared with worldwide literature records. Only species reported in the Indo- Pacific Ocean or exclusively known in the Mediterranean Sea were selected for biogeographical analysis. Results Dinoflagellates in the Mediterranean Sea comprised c. 43% of the world marine species and c. 88% of the dinoflagellate genera. Species richness among the Mediterranean sub-basins showed marked differences due to the less reliable records of unarmoured (athecate) and rare dinoflagellates. These differences disappeared when only the more easily identifiable taxa were considered. O f the 673 dinoflagellates cited in the Mediterranean, 87% were also reported in the Atlantic Ocean. Only 40 taxa (6% of the total) were considered to be potential Indo-Pacific species. Most were reported from the Ligurian Sea (21), and only two species from the Levantine basin. The other 48 taxa (7% of total) were known exclusively from the Mediterranean Sea, mainly from the Ligurian Sea. Half of these taxa were reported by a single author. M ain conclusions Substantial dinoflagellates species richness can be attributed, in part, to the historical tradition of taxonomic studies in the Mediterranean Sea. The list of species of both Indo-Pacific and exclusively Mediterranean species included taxa of dubious taxonomic validity or that were insufficiently known. The exclusion of these questionable taxa revealed the near absence of endemic dinoflagellates in the Mediterranean Sea compared with macroscopic organisms. This could be related to: (I) continuous replenishment o f the plankton populations by the inflow of Atlantic water through the Strait of Gibraltar, (2) the possibility that species introduced during the Pliocenic flooding after the Messinian salinity crisis have not had enough time to diverge from their Atlantic ancestors, and/or (3) the reliance on traditional taxonomy based on morphological characters, which precludes the detection of cryptic spéciation. Keywords Black Sea, dinoflagellate, endemic, Erythrean invader, Indo-Pacific, Lessepsian migrant, marine biogeography, Mediterranean Sea, phytoplankton. IN T R O D U C TIO N It has been estimated that c. 26% of the total Mediterranean marine fauna (4238 species, Fredj et a l, 1992) are endemic. This rich biodiversity represents 4-18% of the total number of species in the world’s oceans (Fredj et a l , 1992; Bianchi & Morri, 2000). The generally high biodiversity of the Mediterranean Sea may be explained by the synergy of: (i) a © 2005 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi doi:10.1111/j. 1365-2699.2005.01373.x 261 187 mailto:fernando.gomez@fitoplancton.com http://www.blackwellpublishing.com/jbi F. Gômez historical tradition of taxonomie studies, (ii) a wide variety of climatic and hydrographic conditions, and (iii) the fluctuating hydrography of the Mediterranean Sea on a geological scale as commimication with the Atlantic and Indian Oceans opened and closed due to changing sea levels and plate tectonics, serving as a type o f ‘diversity piunp’ (Fredj et a l, 1992; Bianchi & Morri, 2000). The biodiversity of the Mediterranean Sea is undergoing rapid alteration within the context of a globally changing climate (Jeftic et a l, 1992; Bianchi & Morri, 2000). The basin has been subject to introductions of non-indigenous species by ship traffic since the opening of maritime routes five centuries ago. Since 1869 a narrow, man-made channel has connected the Mediterranean and the Indian Ocean: the Suez Canal has been considered the major gateway for the entry of invading species, and over 300 Erythrean species have established populations (Galil, 2000). This northbound migration of Erythrean invaders, formerly Lessepsian migrants, appears to have been accelerated during the past few decades by a rise in the sea temperatures as well as by the activation of the Aswan High Dam, leading to more oligotrophic conditions on the Mediterranean side of the Canal (For, 1990). Exotic macro- phytes, invertebrates and fish are found in most coastal habitats in the Mediterranean Sea. In addition to the Erythrean invaders, species are intentionally or accidentally introduced into the Mediterranean via ship fouling, ballast waters, aquacultme, trade in living bait, wrapping of firesh seafood in living algae, aquariology, and scientific research (Bianchi & Morri, 2000). The Mediterranean Sea is a remnant of the extensive Tethys Ocean of the Triassic (c. 200 Ma bp). During the Cretaceous (c. 120 Ma bp), the Mediterranean was opened to communi­ cation with the Atlantic Ocean. Later in the Miocene (c. 10 Ma bp), the isthmus of Suez was formed, isolating the Mediterranean from the Indo-Pacific Ocean. Towards the end of the Miocene, the connection with the Atlantic Ocean closed again as the Messinian salinity crisis led to nearly complete evaporation of the sea. The Messinian salinity crisis occurred synchronously throughout the Mediterranean Basin c. 5.96 Ma BP, and caused a large fall in sea level (> 1000 m). The Messinian salinity crisis ended 5.33 Ma bp, during the Pliocene, with the reopening of the Strait of Gibraltar (Krijgsman et a l, 1999) which inundated the Mediterranean Basin in only 35 years (Blanc, 2O02}rDuri«g ffieiQuatemary, the alternating ice ages and warm interglacial periods resulted in repopulation of the Mediterranean with boreal or subtropi­ cal species, respectively, of Atlantic origin. Bianchi & Morri (2000) separated the present marine biota into several biogeographical categories: (I) temperate Atlantic-Mediterra­ nean, (2) cosmopolitan/panoceanic, (3) endemic, palaeoende- mic (Tethyan origin) and neoendemic (Pliocenic origin), (4) subtropical Atlantic (interglacial remnant), (5) boreal Atlantic (ice-age remnants), (6) Red Sea migrants, and (7) eastern Atlantic migrants (especially in the Alboran Sea). Exchange through the Strait of Gibraltar can be considered the main source of species to the Mediterranean Sea, excluding the Tethys relics that survived the extreme environmental changes associated with the Messinian sahnity crisis. Fredj et a l (1992) reported that 67% of the Mediterranean fauna (excluding protists) were also known fi-om the Atlantic Ocean. The introduction of exotic species modifies the ecosystem: endemic species imable to tolerate this perturbation will go extinct and exotic species will flourish. Studies of this dilemma require characterization of the marine biota. Studies on Mediterranean biogeography are numerous, but nearly all are focused on macroscopic organisms, whereas studies on the biogeographical affinities of marine phytoplankton are almost non-existent. Halim (1990) reported a list of Indo-Pacific dinoflagellates. Marino (1990) concluded that it is difficult at present to quantify the number of endemic phytoplankton species. Several authors link the changing nitrogen-silicon ratio in the Mediterranean Sea to a large increase in the number of blooms of phytoplankton species that do not require silica for their growth (a shift from diatoms to dinoflagellates) (Turley, 1999). More than 200 dinoflagellate species have a negative impact on human activity through the production of potent toxins which may accumulate in the food chain (red-tides or harmfiil algal blooms) (Soumia, 1995). In terms of species richness, the number of species of dinoflagellates is comparable only to that of diatoms. About 1500 diatoms (Soumia et a l, 1991) and 1555 dinoflagellate species comprise the marine phytoplankton in the world’s oceans (Gomez, 2005). The cdms of this study are to establish the biogeographical origin of the Mediterranean dinoflagellates, and to present a checklist of species candidates considered to be endemic or Indo-Pacific taxa. The validity of these species and the low endemism compared vrith macroscopic groups are discussed. M E TH O D S A matrix was constructed based on the checklist of dinoflag­ ellates reported by Gomez (2003a) for each Mediterranean sub-basin, and by Gômez & Boicenco (2004) for the Black Sea. The distribution of each taxon in the world’s seas was established from scmtiny of more than 1100 references. Only some references of interest are cited due to space limitations. The species cited in the Atlantic waters were eliminated as potential endemic or Indo-Pacific taxa. The remaining group of species was divided into: (1) exclusively- Mediterranean species, potential candidates as endemic species, and (2) Indo- Pacific species known exclusively from the Mediterranean and Indo-Pacific Basins. RESULTS A N D D ISCU SSIO N Dinoflagellates recorded from the Mediterranean Sea comprise 673 species (104 genera), a value close to the 660 species previously reported by Marino (1990) (this author did not report a species checklist). Soumia et a l (1991) reported that 1424-1772 species comprising c. 115-131 genera constitute the dinoflagellates in the world’s oceans. Gômez (2005) listed 1555 262 Journal o f Biogeography 33, 261-270, © 2005 Blackwell Publishing Ltd 188 Endem ic and Indo-Pacific p lank ton in th e M e d ite rran ean Sea species and 117 genera. Thus, although the Mediterranean represents only a small percentage of the world’s ocean (0.82% by surface area and 0.32% by volume), nearly 43% of the world’s marine dinoflagellate species occur there, including c. 88% of the dinoflagellate genera. This percentage is higher than the average value of 6.3% (4-18%) for marine macro­ scopic organisms in the Mediterranean Basin (Bianchi 8c Morri, 2000). The species richness of dinoflagellates in the Mediterranean Basin is highly variable among its sub-basins. In the Ligurian Sea, the smallest of the Mediterranean sub-basins, 74% of the total species have been reported. The number of species cited in the Ligurian and Ionian Seas compared with other sub­ basins (Alboran or Aegean Seas) substantially increases when the less reliable records of unarmoured (athecate) dinoflagel­ lates are included. Innamorati et al. (1986, 1989a,b) and Skolka et al. (1986) cited many freshwater species and synonyms considered as separate species for the Ligurian and Ionian Seas, respectively. Also suspect among the armoured (thecate) dinoflagellates are the large number of species of Histioneis Stein, Heterodinium Kofoid and, to a lesser extent, Oxytoxum Stein and Gonyaulax Diesing, cited in the Ligurian Sea. Many of the species described by Rampi (see references in Rampi 8c Bernhard, 1980) and Halim (1960) have not been reported after the initial descriptions (Gômez, 2003a). These rare taxa and unarmoured forms accounted for the variable distribution of species among the Mediterra­ nean sub-basins (Fig. I). These unreported taxa should be interpreted as having been overlooked by non-specialist authors and/or due to the scarcity of taxonomic studies in these sub-basins, rather than as being absent. More easily identifiable genera, such as Ceratium Schrank, have been the subject of several biogeographical studies (e.g. Dodge 8c Marshall, 1994). In the eastern Mediterranean basin, the Aegean Sea, with only half the total species richness reported in the Ionian or Adriatic Seas, had more records of Ceratium species than either of the aforementioned sub-basins (Gômez, 2003a). In the Alboran Sea, vrith about one-third of the total species cited in the Ligurian Sea, 46 species of Ceratium were reported, as opposed to the 52 species of the Ligurian Sea (Gômez, 2003a). If the more difficult-to- recognize unarmoured forms and dubious taxa are disregar­ ded, the species richness for each sub-basin is quite similar. For example, the Levantine Basin shows greater species richness than the Adriatic or Ionian Seas. High species richness in some Mediterranean sub-basins is probably due to the unequal number of studies, rather than true differences in species richness among the sub-basins. Indo-Pacific species Since the Miocene, communication between the eastern Mediterranean (Tethys Sea) and the Indian Sea has been closed (Maldonado, 1985). A narrow, man-made channel connecting the Mediterranean with the Red Sea was opened during the Egyptian Empire period (Sneh et a l, 1975). Since the completion of the Suez Canal in 1869, Erythrean species have colonized the Mediterranean marine biota (For, 1978). It has been calculated that these species (over 300) now constitute nearly 5% of the global Mediterranean fauna and 13% of the species found in the Levantine Basin (Fredj et a l, 1992; Galil, 2000). The 168 km of the Suez Canal are characterized by extreme physical and chemical conditions: high turbidity, high temperatures, and two salinity barriers represented by the hypersalinity of the Bitter Lakes in the south and the Nile freshwater dilution at the north. The residual current tends to flow from the Red Sea for 10 months, reversing in late summer. The completion of the Aswan High Dam in 1965, and the increase of the cross-sectional flow, have minimized the two salinity barriers. The progressive increase of the water fluxes (and reduction of the salinity gradients) could favour northbound migration directly through the Suez Canal (Halim, 1990). Ships navigating the Canal may likewise facilitate migration of species via transport in their ballast waters (Shefer et a l, 2004). From the 673 species of free-living dinoflagellates listed by Gômez (2003a), 40 species (6% of the total) were cited exclusively from the Mediterranean Sea and Indo-Facific Ocean (Table I). Most of the taxa were reported from the Facific Ocean, and only 11 species from the Indian Ocean. In this case the low munber of studies in the Indian Ocean Atlantic Ocean Balear-Prov Adriatic496-21-3845 N- 267 „ Black Sea 40 N- Strait of Gibraltar Tyrrtieniaroy ;182 -0-1 Aegean^^>^ Levantine Suez 268-2-3 Canal Ionian 283-11-8 AlgerianGulf of 35 N- A boran Total number of species-lndoPaclflc-Excluslvely Mediterranean 10°W Figure 1 Map of the Mediterranean sub-basins and the Black Sea. Number of dinoflagellate species cited in each Mediterranean sub-basin and the Black Sea based on Gomez (2003a); Gômez & Boicenco (2004); number of dinoflagellate species tentatively considered as Indo- Pacific taxa (see Table 1 for species list); number of exclusively Mediterranean dinoflagellates (see Table 3 for species list). Journal o f Biogeography 33, 261-270, © 2005 Blackwell Publishing Ltd 263 189 F. Gômez Table 1 Species reported only in Mediterranean and Indo-Pacific waters Alexandrium insuetum Balech (Tyr) * Amphidinium curvatum Schillert (Lig, Ion, Adr, BS) * Amphidinium inflatum Kofoidf (Alg) * Amphidinium lissae SchillerJ (Lig, Adr) * Amphidinium vasculum Kofoid & Swezyf (Ion) Amphidoma elongata Kofoid & Swezy (Alb, Alg) Amphisolenia complanata Kofoid & Skogsberg (Lig) Centrodinium elongatum Kofoid (Alb) *Ceratium egyptiacum Halim (Lev) Ceratoperidinium yeye Margalef (Alb, Bal, Lev) Cochlodinium turbineum Kofoid & Swezy (Adr) Craspedotella pileolus Kofoid (Lig) *Gonyaulax ligustica Rampi§ (Bal, Lig) Gonyaulax rugosum Wailes (Ion) Gymnodinium attenuatum Kofoid & Swezy (Lig, Ion) Gymnodinium canus Kofoid & Swezy (Ion) Gymnodinium lineatum Kofoid & Swezy (Ion) Gymnodinium lira Kofoid & Swezy (Lig) *Gymnodinium multilineatum Kofoid & Swezyf *Gymnodinium sulcatum Kofoid & Swezyf (also BS) Gymnodinium ovulum Kofoid & Swezy (Lig) Gymnodinium ravenescens Kofoid & Swezy (Lig) Gymnodinium sphaeroideum Kofoid (Lig, Ion) Gymnodinium translucens Kofoid & Swezy (Lig) Gyrodinium acutum (Schiitt) Kofoid & Swezy (Bal, Tyr, Ion) Gyrodinium biconicum Kofoid & Swezy (Ion) Gyrodinium rubricaudatum Kofoid & Swezy (Lig) *Heterodinium crassipes SchiUerf (Adr) Heterodinium dubium Rampi% (Lig) Histioneis detonii RampiH (Lig) *Histioneis elongata Kofoid & Michener (Lev) Leptodiscus medusoides Hertwig (Bal, Lig, Tyr) * Oxytoxum areolatum Rampi§ (Bal, Ion, Adr) Parahistioneis acutiformis Rampif (Lig) Petalodinium porcelio Cachon & Cachon (Lig) Protoceratium pepo Kofoid & Michener (Lig) Protoperidinium tregouboffii (Halim) Balech (Lig) Scrippsiella precaria Montresor & Zingone** (Tyr, Ion) Triposolenia longicornis Kofoid (Lig) Warnowia pulchra Schiller** (Tyr, Lig) *Taxa cited in the Indian Ocean. Alb, Alboran; Alg, Algerian; Bal, Balear-Provençal; Lig, Ligurian; Tyr, Tyrrhenian; Ion, Ionian; Adr, Adriatic; Aeg, Aegean; Lev, Levantine; BS, Black Sea. fFrom Australian waters (Wood, 1963a,b). fFrom the Red Sea (Halim, 1969). §From the Arabian Gulf (Dorgham & Moftah, 1986). liOnly reported in the south Pacific Ocean (Rampi, 1948, 1950). **Reported in the Pacific Ocean (Chihara & Murano, 1997). compared with other major oceans should be taken into account. Most of the Mediterranean Indo-Pacific dinoflagellates corresponded to taxa described by Kofoid and collaborators (Kofoid & Michener, I91I; Kofoid & Swezy, 1921; Kofoid & Skogsberg, 1928) from the eastern Pacific Ocean (Table 1). This literature is commonly referenced for the identification of Mediterranean species, and many authors working in the Mediterranean have assigned their observations to the Pacific taxa illustrated by Kofoid. For unarmoured dinoflagellates, despite the excellent and detailed descriptions by Kofoid & Swezy (1921) compared with other, older studies, poor fixation due to the commonly use4 preservatives formaldehyde and iodine hindered identification. With these preservatives, body shape and morphology often change dining the process of fixation so that even determination of the genus becomes difficult (Steidinger & Tangen, 1997). The list of Mediterranean Indo-Pacific taxa is full of dubious or poorly known species. Ceratium egyptiacum Halim was reported as an example of a recent Erythrean invader (Halim, 1990). The taxon shows variable morphology associated with the stress of environmental changes (sahnity > 47) in the Suez Canal (Dovridar, 1972). Ceratium egyptiacum, which resembles Ceratium pulchellum Schroder, was reported only from the proximity of the Suez Canal, with no records in the Indian or Pacific Oceans. Alexandrium insuetum Balech is recognizable only by a few specialists; Steidinger & Tangen (1997) reported differences in the sulcal plates between the Mediterranean and Pacific specimens. Conyaulax ovalis Schiller and Conyaulax ovata Matzenauer may be synonyms, and both taxa are dubious. The description of Conyaulax rugosum Wailes was insufficient. Protoperidinium tregouboffii Halim was reported only by Balech (1962) in the Pacific Ocean. This taxon shows similarity to the cosmopolitan Protoperidinium brachypus (Schiller) Balech. Ceratoperidinium yeye Margalef (= C. medi- terraneum Abbud Abi-Saab) has recently been reported fi-om the Pacific Ocean (Gomez et a l, 2004). This taxon may be overlooked in other oceans. Halim (1969) reported Pyrodinium bahamense var. compressum (Bohm) Steidinger, Tester et Taylor (formerly P. schilleri (Matzenauer) Schiller) fi-om Port Said, just on the Mediterranean side of the Suez Canal; however no other Mediterranean records exist ofethis distinc­ tive taxon, which has been investigated extensively due to its toxicity. The Noctilucales Haeckel Petalodinium porcelio Cachon & Cachon and Leptodiscus medusoides Hertwig have been found recently in Pacific waters (Gomez & Furuya, 2005). These taxa are barely recognizable as dinoflagellates, and are probably going unnoticed in the world's oceans (Gômez & Furuya, 2004, 2005). For Craspedotella Kofoid, the record by Cachon & Cachon (1969) in the Mediterranean Sea differed fi-om the description by Kofoid fi-om the Pacific Ocean. In the Black Sea, it is doubtful that Amphidinium cucurbita Kofoid et Swezy, Cymnodinium radiatum Kofoid & Swezy, Cymnodinium sulcatum Kofoid & Swezy and Protoperidinium 264 Journal o f Biogeography 33, 261-270, © 2005 Blackwell Publishing Ltd 190 Endem ic and Indo-Pacific p lank ton in th e M ed ite rran ean Sea sinaicum (Matzenauer) Balech belong to Indo-Pacific taxa (Gômez & Boicenco, 2004). The absence of information on dinoflagellates before the opening of the Suez Canal hinders attempts to determine the biogeographical origins of present Mediterranean species. According to Marino (1990), tropical invaders fi-om the Red Sea only partially compensate for the lack of Atlantic species in the eastern Mediterranean Sea. Since the highest number of Indo-Pacific macroscopic species occurred in the Levantine basin (Galil, 2000), it is expected that, likewise, a majority of Indo-Pacific dinoflagellates would occur here. In the Levantine basin only the doubtful taxon C. egyptiacum and Histioneis elongata (the latter illustrated by Polat & Koray, 2002) remain as Indo-Pacific dinoflagellates. Most of these tentative Indo- Pacific dinoflagellates, however, were reported from the Ligurian Sea (21 species) (Fig. 1). The present study did not find any clear candidate Indo-Pacific species. Curiously, the toxic and distinctive dinoflagellate Dinophysis miles Cleve, a solid example of an Indo-Pacific species, frequently occurring even in the Red Sea, has never been reported in the Mediterranean Sea. Halim (1990) reported a tentative Hst of 17 armoured Mediterranean-Indo-Pacific dinoflagellates. However the Indo-Pacific origin of these species is questionable due to the fact they were also reported in the Atlantic Ocean. Further­ more, several of the species are dubious or invalid taxa (Table 2). According to Por (1978), Red Sea species in the Levantine Basin will increase and decline according to future climatic fluctuations. The increase of temperature and salinity in the Mediterranean Sea, associated with climate change, could facilitate the adaptation of introduced Red Sea/Indian Ocean species. The Strait of Gibraltar is another route for the entrance of tropical species. For example, Gymnodinium catenatum Graham, a distinctive toxic dinoflagellate, has apparently entered the Mediterranean Sea through the Strait of Gibraltar (Gômez, 2003b). Global warming is expected to promote northward expansion of tropical species in the eastern Atlantic towards the Strait of Gibraltar. Studies on the phytoplankton composition along the coasts of Africa and the Alboran and Algerian Seas are nearly non-existent, precluding the detection of tropical phytoplankton species entering the Mediterranean Sea from the Atlantic. As most monitoring studies are carried out along the Italian coasts or in the north-west Mediterranean Sea, when tropical species are detected it is difficult to estabhsh the biogeographical origin of the invaders. Permanent studies in key areas, including the Strait of Gibraltar, the Bosphorus- Dardanelles Straits and the surrounding waters of the Suez Canal, will be useful for monitoring the expansion of tropical species. Exclusively Mediterranean species Endemism, the number of species living exclusively in the Mediterranean, is expected to be high in this semi-enclosed basin (Bianchi 8c Morri, 2000). The semi-enclosed Mediterra­ nean conditions are thought to have led to spéciation and neoendemism of Pliocenic invaders introduced during or after the Messinian salinity crisis (Fumestin, 1979). Relics of the Tethys Sea could survive the Messinian salinity crisis, as proposed for some benthic fauna (Wilke, 2003). Around 25% of the marine macroscopic species in the Mediterranean Sea are endemic (Bianchi 8c Morri, 2000), with > 50% endemism for some benthic fauna (Fredj et a l, 1992). In contrast to this general trend, Bouchet 8c Tariani (1992) reported that the deep fauna of the Mediterranean is characterized by a very low degree of endemism compared with the other areas of the world’s oceans. Table 2 Mediterranean-Indo-Pacific species according to Halim (1990, p. 16) and citations of these taxa from the Adantic Ocean Species Records in Atlantic Ocean/comments Ceratium egyptiacum Halim Dinophysis giganteum Kofoid et Michener Dinophysis umbosa Schiller Heterodinium dubium Rampi Heterodinium minutum Rampi (?) Histioneis inclinata Kofoid et Michener mmmm^cms kofoid ... Histioneis subcarinata Rampi Gonyaulax ovalis Schiller Oxytoxum caudatum Schiller Oxytoxum laticeps Schiller Oxytoxum variabile Schiller Prorocentrum maximum Matzenauer Protoperidinium hirobis Abé Protoperidinium nipponicum Abé Protoperidinium tregouboffii Halim Pyrodinium schilleri (Matzenauer) Schiller = ? Ceratium pulchellum Schroder, see text Closely related to Dinophysis cuneus (Schiitt) Abé Wood (1968) Reported only by the authority in the Pacific Ocean (Rampi, 1950) Non-existent, Heterodinium minutum Kofoid & Michener? Wood (1968), Balech (1988) I'"" '" Balech (1971), only by Rampi (1950) in the Pacific Doubtful taxa, insufficient description Wood (1968), Marshall (1976), Moita & Vilarinho (1999), etc. Wood (1968), Marshall (1976), Parke & Dodge (1976), Moita & Vilarinho (1999) Establier & Margalef (1964), Wood (1968), Margalef (1973), Marshall (1976), Parke 8c Dodge (1976), etc. Doubtful taxon, Prorocentrum maximum (Gourret) Schiller? Wood (1968), Balech (1971), Marshall (1976), Okolodkov (1998) Steidinger et al (1967), Lessard 8c Swift (1986), similar to Protoperidinium ovum Schiller See text Only by Halim (1969) in the Mediterranean Sea Journal o f Biogeography 33, 261-270, © 2005 Blackwell Publishing Ltd 265 191 F. Gômez In the present study 48 dinoflagellate species were described and reported exclusively from the Mediterranean Sea, mainly by Rampi and Schiller in the Ligurian and Adriatic Seas, respectively (Table 3). Half these species were reported by a single author. Among the Dinophysiales Lindemann, species of the genera Amphisolenia Stein and Histioneis were poorly described and strongly resembled cosmopolitan species. In the original descriptions, based on single or few specimens, the authors failed to take into account the high morphological variability in the life cycle of Dinophysiales (Reguera & Gonzalez Gil, 2001). As an example, Halim (1960) described several new species of Histioneis that strongly resemble immature (or damaged) specimens of a population of the cosmopolitan Histioneis longicollis Kofoid existing in the type locality (Fig. 2). Ceratium brunellii Rampi strongly resembles the cosmopolitan Ceratium incisum (Karsten) Jorgensen. Dodge & Saunders (1985) considered many of the species of Oxytoxum Stein, described by Rampi, as synonyms of common species. As occurred with other Noctilucales (Gomez & Furuya, 2004, 2005), Cachonodinium Kofoid goes uimoticed in the world’s oceans and probably Creuetodinium (Greuet) Loeblich 111 is not a dinoflagellate. Records of the remaining half of the exclusively Mediter­ ranean species were reported by multiple authors, and thus are somewhat more credible. The identifications, however, were frequently based on older texts, which are imperfect. For example, Schiller (1933) described numerous unarmoured dinoflagellates of the genera Amphidinium Claparède 8c Lachmann and Cymnodinium Stein. These early descriptions were insufficiently detailed, often based on specimens deformed by the fixation used, and should be interpreted with caution (Fig. 3). More recently, Sournia (1986) questioned the validity of taxa such as Archaeosphaerodiniopsis Rampi, Adin i- monas Schiller or Pachydinium Pavillard. While the contribu­ tions of Schiller and other earlier workers in the field are important references for dinoflagellate identification, research­ ers who rely solely on the older literature, without considering more recent work in the field of phytoplankton taxonomy, risk inaccuracies in their species accounts. In the case of two genera, Protoperidinium Bergh and Scrippsiella Balech, identification at species level is limited to a few experts, which may explain the scarcity of records outside the Mediterranean Basin. The complex life cycle of the genus Pyrocystis Murray ex Haeckel precludes the consideration of Pyrocystis margalefii Léger for biogeographical purposes. The poor description of Asterodinium libanum Abboud-Abi Saab, the high morphological variability and the unknown life cycle of the order Brachidiniales Soumia, probably morphotypes of some species of Karenia G. Hansen & Moestrup, also prevent consideration of this taxon as an exclusively Mediterranean species (Gomez, 2003c; Gomez et a l, 2005). These questionable dinoflagellate records reported as exclu­ sively Mediterranean represented less than 7% of the total species. These taxa should be considered as ‘false endemics’ due to dubious taxonomic identification or the sparse geographical information. Based on the present study. Adinimonas oviforme Schiller Alexandrium foedum Balech (Tyr) * Amphisolenia sigma Halim (Lev) Amphidinium conus Schiller (Adr,Lig) Amphidinium stigmatum Schiller (Lig,Ion Adr) * Archaeosphaerodiniopsis verrucosa Rampi (Lig) Asterodinium libanum Abboud-Abi Saab (Lig,Lev) Cladopyxis quadrispina Pavillard Dinophysis alata Jorgensen * Cachonodinium caudatum (Cachon et Cachon) Loeblich III (Lig) * Ceratium brunellii Rmnpi (Lig) * Gonyaulax trottii Rampi (Lig) *Greuetodinium cylindricum (Greuet) Loeblich III (Lig) Gonyaulax elegans Rampi (Lig, also in BS) Gymnodinium caput Schiller Gymnodinium najadeum Schiller (also in BS) Gymnodinium neapolitanum Schiller (also in BS) Gymnodinium pulchrum Schiller (LigAdr) Gymnodinium tridentatum Schiller (Adr) Gymnodinium voukii Schiller *Heterodinium balechii Rampi (Lig) *Heterodinium debeauxii Rampi (Lig) *Heterodinium grahamii Rampi (Lig) Heterodinium kofoidii Pavillard *Heterodinium laticeps Léger (Lig) *Histioneis alata Rampi (Lig) *Histioneis bernhardii Rampi (Lig) *Histioneis elegans Halim (Lig) Histioneis expansa Rampi (LigTev) *Histioneis imbricata Halim (Lig) Histioneis faouzii Halim (Lig) Histioneis kofoidii Forti & Issel (TyrAdr) *Histioneis ligustica Rampi (Lig) Histioneis marchesonii Rampi (Bal,Lig,Lev) *Histioneis rampii Halim (Lig) *Histioneis speciosa Rampi (Lig) *Histioneis sublongicollis Halim (Lig) *Histioneis villaffanca Halim (Lig) *Oxytoxum obesum Rampi (Lig) Oxytoxum depressum Schiller *Oxytoxum radiosum Rampi (Lig) Pachydinium mediterraneum Pavillard * Parahistioneis sphaeroidea Rampi (Lig) *Prorocentrum venetum Tolomio & Cavolo (Adr) Protoperidinium maranense Tolomio (Adr) P. parthenopes Zingone & Montresor (Tyr) *P)Toq'stis margalefii Léger (Lig) Scrippsiella ramonii Montresor (Tyr,lon) Table 3 Dinoflagellate species known exclusively from the Mediterranean Sea :-r *Taxa reported only by the authority. 266 Journal o f Biogeography 33, 261-270, © 2005 Blackwell Publishing Ltd 192 Endem ic an d Indo-Pacific p lan k to n in th e M e d ite rran ean Sea Figure 2 Illustrations of (a) Histioneis vil- lafranca Halim; (b) Histioneis elegans Halim; (c) Histioneis longicollis Kofoid; (d) Histioneis sublongicollis Halim; (e) Histioneis faouzii Halim, adapted from Halim (1960). The new species described by Halim (1960) from single or few specimens strongly resemble the cosmopolitan H. longicollis. Scale bar = 20 pm. Figure 3 Illustrations of (a) Gymnodinium caput Schiller; (b) Gymnodinium najadeum Schiller; (c) Gymnodinium neapolitanum Schiller; (d) Gymnodinium pulchrum Schiller, adapted from Schiller (1933). The descrip­ tions by Schiller (1933) are insufficiently detailed for precise identification of unarmoured taxa. Scale bar = 20 pm. dinoflagellates show a lower percentage of endemic species compared with macroscopic or benthic species (Fredj et a l, 1992; Bianchi & Morri, 2000). In fact, no taxon considered in this study can be confirmed as being of exclusively Mediterra­ nean origin. The Black Sea is an extreme case of a quasi-enclosed basin, which first came into contact with the world’s oceans through the Bosphorus-Dardanelles Strait c. 12,000 yr b p (Çagatay et a l, 2000). Gomez & Boicenco (2004) compiled the dinoflagellate taxa cited in the Black Sea. They, likewise, concluded that no taxon could be recognized as endemic. Neoendemism According to van der Spoel (1994), the continuity of the marine pelagic environment provides very limited scope for isolation creating different habitats. Endemicity is difficult to prove in microscopic organisms because they are not easily recognizable: distinctive morphological features are rare compared with higher plants and animals; and the field has been distinctly understudied. Based on new molecular tools, the genetic distances in several ribosomal genes (18S rRNA for deep evolutionary divergences) are used to delimit the species. When physical barriers separate populations, as in the semi-enclosed Mediterranean Sea, the geographical isolation is expected to develop the endemism associated with genetic divergence. If it is assumed that no species survived the extreme environmental changes that occurred during the Messinian salinity crisis and the rapid re-inundation that followed, the neoendemic taxa that entered through the Strait of Gibraltar from the Atlantic Ocean had a maximum of 5.33 Ma to diverge in gene sequence from their Atlantic ancestors. The molecular clock approach has been applied recently to marine a c dinoflagellates for the first time. John et a l (2003) estimated 23 Ma as the average time of origin of the Alexandrium tamarense species complex. Estimations based on the molecu­ lar clock approach should be considered very cautiously due to the difficulties in obtaining exact and comparable molecular clock rates for the non-protein-coding I6S gene, and other factors (Ayala, 1997). Nonetheless, according to the value reported by John et a l (2003), the 5.33 Ma after the re-inundation of Mediterranean Basin was insufficient for the spéciation of dinoflagellates such as Alexandrium Halim. Hydrographic circulation through the Strait of Gibraltar, with a strong surface inflow of Atlantic water, favours the introduc­ tion of Atlantic species (Gomez et a l, 2000). The Atlantic waters with a residence time of 80-100 years in the Mediterranean Basin could facilitate continuous exchange of plankton of Atlantic origin. This mechanism is more limited for non-free- swimming macroscopic or benthic species. This could explain the near absence of endemic dinoflagellate species in the Mediterranean compared with macroscopic organisms. The classic taxonomy based on morphological characters is insuffr^ cient for detecting morphologically similar, but distinct, forms in the Mediterranean Sea. Consequently, the occurrence of cryptic species cannot be discounted. 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(1991) Marine phytoplankton: how many species in the world oceans? Journal o f Plankton Research, 13, 1093-1099. van der Spoel, S. (1994) The basis for boundaries in pelagic biogeography. Progress in Oceanography, 34, 121-133. Steidinger, K.A. 8c Tangen, K. (1997) Dinoflagellates. Identi­ fying marine phytoplankton (ed. by C.R. Tomas), pp. 387- 584. Academic Press, San Diego, CA, USA. Journal o f Biogeography 33, 261-270, © 2005 Blackwell Publishing Ltd 269 195 h. üomez Steidinger, K A , Davis, J.T. & Williams, J. (1967) A key to the marine dinofl^dlate genera of the west coast of Florida. State of Florida, Board of Ckmservation Tedmical Series, 52, 1- 45. / . • Turley, C.M, (1999) Tte changing Mediterranean Sea - a sensitive ecosystem? Progress in Oceanography, 44, 387-400. Wilke, T. (2003) Salentkydrobia gen, nov. (Rissooidea; Hyd- robiidae): a potential relict of die Messmiad salinity crisis, Zoolopcal Journal of the Linnean Society, 137, 319-336. Wood, E.J.F. (1963a) Dinofl^llates in the Australian region. II. Recent Collections. ÇSJRQ Australian LHvision of Fisheries Oceanography Report, 14, 1-55. Wood, E.J.F. (1963b) Dinoflagellates in the Australian region; lU. Further Collections. CSIRO Australian Division of Fish­ eries Oceanography Report, 17, 1-20. Wood, E.J.F. (1968) Dinoflagellates of the Caribbean Sea and adjacent areas. University of Miami Press, Coral Gables, FL, USA. Fernando Gômez has dedicated his research career to ùni^dling phytophinkttm ditersity and community structure in the Mediterranean Sea, particularly the Straits of Gibraltar and Ligurian Sea, the Eastern Atlantic, and the Northem, Equatorid ̂ d Southern Padfic His favourite research topic is the taxonomy, ecology and biogeography of marine dinoflag­ ellates. He is currendy with the Protista & Mathematics Division of the Department of Zoology, Natural History Museum, London, UK, where he is inVestijgating the morphological and molecular diversity of marine microplank­ ton in European waters, with financial support firom the European Commission’s Marie Curie Intra-European Fellow­ ship Scheme. Editor John Lambshead 270 Journal o f Biogeography 33, 261-270, © 2005 Blackwell Publishing Ltd 196 3.2. Taxonomîa y distribuciôn de dinoflagelados poco conocidos: 3.2.1. B ra c h id in iu m , A s te ro d in iu m , M ic ro c e ra tiu m . Gomez, F. 2003. New records of Asterodinium Sournia (Brachidiniales, Dinophyceae). Nova Hedwigia 77, 331-340. Gômez, F. & Claustre, H. 2003. The genus Asterodinium (Dinophyceae) as a possible biological indicator of warming in the Western Mediterranean Sea. Journai o f the Marine Biotogicai Association o f United Kingdom 83, 173-174. Gômez, F., Yoshimatsu, S. & Furuya, K. 2005. Morphology of Brachidinium capitatum F.J.R. Taylor (Brachidiniales, Dinophyceae) collected from the western Pacific Ocean. Cryptogamie Algologie 26, 165-175. Gômez, F., Nagahama, Y., Takayama, H. & Furuya, K. 2005. Is Karenia a synonym of Asterodinium-Brachidinium? (Gymnodiniales, Dinophyceae). Acta Botanica Croatica 64, 263-274. Gômez, F. 2006. The Dinoflagellate Genera Brachidinium, Asterodinium, Microceratium and Karenia in the Open SE Pacific Ocean. Aigae 21, 445-452. Gômez, F. 2007. Observations on a distinctive H-shaped dinoflagellate. An example of the projection of body extensions in gymnodiniold ceils. Acta Botanica Croatica 66, aceptado. 197 N ova H edw igia 77 3— 4 331— 340 Stuttgart, N ovem ber 2003 New records of Asterodinium Soumia (Brachidiniales, Dinophyceae) by Fernando G om ez Department of Aquatic Biosciences, The University of Tokyo 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan. E-mail; fernando.gomez@fitoplaicton.com Phone +81 3 5841 5291 FAX +81 3 5841 5308 With 22 figures and 1 table Gômez, F. (2003): New records of Asterodinium Soumia (Brachidiniales, Dinophyceae). Nova Hedwigia 77: 331-340. A bstract: New records of species of the rare planktonic dinoflagellate genus Asterodinium Soumia are reported. From the Mediterranean Sea and NE Atlantic Ocean: ( 1 ) three specimens of Asterodinium sp. sensu Sournia from the G ulf of Cadiz and Strait of Gibraltar (NE Atlantic Ocean), (2) one specimen o f Asterodinium sp. 1 from the Strait of Gibraltar, (3) three specimens of Asterodinium cf. libanum A hhoud-A h i Saab from the Bay of Villefranche-sur-Mer(Ligurian Sea, NW Mediterranean Sea), (4) three specimens of Asterodinium g rac ile from the Tyrrhenian Sea and Strait of Sicily (Mediterranean Sea). Most taxa were recorded from 70 to 100 m depth, with exceptions in the Strait of Gibraltar and the Corsica Channel. From a longitudinal transect (138°E) in the Philippine Sea (NW Pacific Ocean) are reported: (5) four specimens of Asterodinium gracile, (6) Asterodinium cf. gracile, (7) one specimen of Asterodinium sp.l and (8) Asterodinium sp.2. These records were collected between 50 to 175 m depths. Asterodinium gracile shows high morphological variation. The ecology of the genus is reviewed and discussed. Key w ords: Asterodinium, dinoflagellate,Dinophyceae, Dinophyta, phytoplankton,Gulf of Cadiz, Strait o f Gibraltar, Mediterranean Sea, Atlantic Ocean, Pacific Ocean, Kuroshio Current Introduction Asterodinium Sourma. is a genus o f photosynthetic scarcely reported in the literature. These unarm ored species are m em bers o f the fam ily B rachidiniaceae* of the order Brachidiniales* A .R . Loeblich III ex Soum ia (L oeb lich III 1982, S ourn ia 1984) or P tychod isca les F ensom e, Taylor, N orris, Sarjeant, W harton et W illiam s (Fensom e et al. 1993). DOI: 10.1127/0029-5035/2003/0077-0331 0029-5035/03/0077-0331 $2.50 © 2003 J. C ram er in der Gebriider Borntraeger V erlagsbuchhand lung , D -14129 B erlin • D -70176 S tu ttgart 331 198 mailto:fernando.gomez@fitoplaicton.com Species o f the genus A sterodinium have dorsoventrally fla ttened cells w ith tw o elongate extensions radiating from the hyposom a and three from the episom a; a w ell-developed nucleus and ch loroplasts are present. The genus w as orig inally described from the M ozam bique Channel (SW Indian O cean) based on Asterodinium gracile Soum ia (type species), Asterodinium spinosum Soum ia and an undescribed species, Asterodinium sp. (Sournia 1972a,b). According to Sournia (1986, p. 50) no further records of these species exist. However, Estrada (1979) reported an unidentified species o f Asterodinium in coastal w aters o f the NW M editerranean Sea and Abboud- Abi Saab (1985) found Asterodinium gracile in L ebanese coastal w aters (Eastem M editerranean Sea). A bboud-A bi Saab (1989) fu rther reported the new species, Asterodinium libanum A bboud-A bi Saab, but w ith an insufficient description. To the best of my knowledge, no other docum ented records o f species belonging to the genus Asterodinium have been published. This study reports the findings of several species o f Asterodinium co llected from 1997 to 2002 in the M editerranean Sea, E astem A tlantic and W estem Pacific O ceans and provides inform ation on the ecology and distribution o f these species. M ateria l and methods New records of Asterodinium from Mediterranean-Atlantic waters were obtained from samples collected during the following research cruises or coastal monitoring (Fig. 1 ): ( 1 ) Cruise carried out 18-25 June 1997 aboard R/V “Cornide” in the Gulf of Cadiz, Strait of Gibraltar and Alboran Sea (see Garcia et al. 2002 for sampling details); (2) cruise carried out 2-9 September 1997 aboard R/V “Thalassa” in the Strait of Gibraltar (see Gomez et al. 2000 for sampling details); (3) coastalmonitoring performed at the permanent station “Point B” (80 m depth) in the Bay of Villefranche-sur-Mer (Ligurian Sea) from January 1998 to January 2000 (see Gômez & Gorsky 2003 for sampling details) and (4) PROSOPE-cruise carried out 11-30 September 1999 aboard R/V “'I’halassa” in the Eastern Atlantic Ocean and Mediterranean Sea (see Dolan et al. 2002 for sampling details). Seawater samples were collected with oceanographicbottles, preserved with acidified Lugol’s solution (e.g., Hasle & Syvertsen 1997, p. 334) and stored in the dark. Only during the cruise in the Strait of Gibraltar, seawater samples were concentrated using a 5-|um pore mesh. Sub-samples (10-100 ml) were allowed to settle for 24-48 h in Utermohl chambers (Utermohl 195 8). Cells were observed with an inverted light microscope using bright field optics. New records of Asterodinium from the Pacific Ocean were obtained from samples collected during a cruise aboard R/V “Soyo-Maru” in the Philippine Sea (Fig. 2). Seawater samples were collected with Niskin bottles from 5, 10,20, 30 ,40 ,50 , 60, 70, 80,90, 100, 125, 150, 175 and 200 m depth (*)The family Brachidiniaceaeand the order Brachidinialesare based on BrachidiniumF.J.R. Taylor. In the original publication of Taylor ( 1963) this genus was spelt Brachydinium , but in 1967 Taylor introduced the orthographicallycorrected spelling B rachid in ium [see also Articles 60 and 61 of the current version of the International Code of Botanical Nomenclature (ICBN; Greuter et al. 2000) dealing with the correction of orthographical errors]. Contrary to Soumia’s (1973) conclusion, Taylor’s (1967) correction of his own orthographicalerroris in no way contrary to these articles and should be followed. The spelling Brac/i/Jm/Hm is indicated as the correct one in the ING (Farr et al. 1979) and in NCU-3 (Greuter et al. 1993); both entries are authored by Paul C. Silva, one of the most reliable specialists in the application of the ICBN to phycologicalnomenclature. 332 199 45“ N France igunan strait of Gibraltar Tyrrhenian Sardinia t Alborân Sea TunisiaGulf of Càdiz Ionian Sea35“ Morocco -5“ E 10“ E 15“ E Fig. 1. Map of the Western Mediterranean Sea and Gulf of Cadiz. 45“ N Japan Sea Yellow Sea V L ! PACIFIC OCEAN Philippine S e a 130“E 140“ E120“ E Fig. 2. Map of the NW Pacific Ocean. along the meridian 138° from 28° ON to 34° 20N. Nine stations were sampled from 3-20 May 2002 and nine from 3-9 July 2002. Samples were preserved with acidified Lugol's solution and stored at about 5°C. Samples were pre-concentratedby settling in glass cylinders, and concentrates were left to settle in standard sedimentation chambers. Concentratesequivalentto 400 ml were examined in a Nikon inverted microscope using bright field optics. Cells were photographed on an inverted light microscopeconnectedto a Nikon digital camera. 333 2 0 0 Results A ste ro d in iu m g rac ile Soum ia The identification is based on the draw ing o f A. gracile provided by Soum ia (1972a). It is rep roduced in S ourn ia (1986, p. 155) and in F ensom e et al. (1993, p. 56) although erroneously nam ed Asterodinium spinosum . To my best know ledge this is the only illustration available. In this study, it is assum ed that A. gracile presents a high m orphological variability in size and in the relative proportion o f the extensions. As the extensions are flexible (especially the tw o lateral apical ones) the angle of the extensions w ith respect to the cell body is not considered as a taxonom ic character. The distribution or num ber o f chloroplasts did not seem to be usable for species d ifferen tia tion . In the M edite rranean Sea, four ind iv iduals w ere reco rd ed in sam ples from the Tyrrhenian S ea and the S tra it o f S icily co llec ted during the P R O S O P E -cru ise (Fig. 1). T h e ir m ax im al leng th w as 49-52 pm and the w id th at the c ingu lum level w as 21-23 pm (F igs 12, 22). A ll the specim ens resem b led A. g racile in shape. T he la tera l an terio r ex tensions had rounded ends in all these specim ens, w hereas those illu stra ted by S ourn ia (1972a) had m ore po in ted tips. S o u rn ia ’s specim en o f A. gracile had a m axim um size of -SO pm (as m easured from the scale in his figure 8), thus being som ew hat larger than the specim ens collected in the M editerranean Sea. In the Pacific O cean, 4 specim ens m ore sim ilar to the type m aterial w ere collected from two stations located in the K uroshio Current. A t one station tw o specim ens were collected at different depths (80 and 175 m ). T he specim en from 175 m depth (m axim al length 90 pm , cingulum 28 pm. Figs 4, 14) was m ore intensely p igm ented than the other one (m axim al length 85 pm , cingulum 22 pm ) (Figs 5, 15). A t a nearby station, two sim ilar specim ens w ere observed in the sam e sample. They show ed m ore e lo n g ate ap p e n d ic es than all the o th er sp ec im en s (F igs 3, 13). O nly one cell w as m easured , show ing a m ax im al leng th o f 160 pm , w hile the w idth o f ce ll a t the c ingulum w as 21 pm . T he ra tio betw een the length o f the cen tra l ap ica l ex ten sio n and the ce ll w id th a t the cingu lum is approx . 1.3 in S o u rn ia ’s (1972a) illu s tra tio n . T he sp ec im en in m y F ig u re 3 had a ra tio >4, w hile the o ther specim ens from the P acific O cean had a variab le ra tio rang ing from 1.6-2.3. T he sp ec im en s from the M editerranean Sea also show ed a ratio low er than the type m ateria l. F or the presen t, all the cells are considered to be m em bers o f the Asterodinium gracile com plex. A nother specim en is included in this group but here nam ed A. cf. gracile (Figs 10, 20). It w as found in o ffshore sub trop ical w aters o f the P hilipp ine Sea. It d iffe red from the sp ec im en s o f the A. gracile com plex by its sh o rte r ex ten sio n s. T he w idth o f the cell a t the level o f the c ingulum w as 27 pm . T he d istance betw een the tips o f the tw o la te ra l ap ical arm s w as 52 pm and the leng th o f the longer antap ical ex tension w as 30 pm . N o p rec ise m easu rem en t o f the to ta l leng th w as taken due to the bending o f the central apical extension, but it seem s to be around -5 5 pm (Figs 10, 20). 334 2 0 1 i % # T • Figs 3-12. Photom icrographs o f A s te ro d in ium spp. Figs 3-5. A s te ro d in ium g ra c ile from the Pacific Ocean. Fig. 6. A s te ro d in ium sp. sensu Sournia (1972a) from the G ulf o f Cadiz. Fig. 7. A ste ro d in ium sp .l from the Strait o f Gibraltar. Fig. 8. A sterod in ium sp. 1 from the Pacific Ocean. Fig. 9. A ste rod in ium sp.2 from the Pacific Ocean. Fig. 10. A ste ro d in ium cf. g ra c ile from the Pacific Ocean. Fig. 11. A s te ro d in iu m c f. lib a n u m from the M editerranean Sea. Fig. 12. A ste ro d in iu m g ra c ile from the M editerranean Sea. Scale bars 20 mm. A s te ro d in iu m cf. l ib a n u m A b b o u d -A b i S aab In sa m p le s co llec te d in th e B a y o f V ille fra n ch e -su r-M er (L ig u rian S ea), th ree in d i­ v idua ls w ere o bserved . T h e le n g th w as 42 pm and th e c in g u lu m w as 27 pm long. T h is tax o n is m o rp h o lo g ic a lly d iffe ren t w ith a le ss d e lica te ap p e aran c e co m p ared to o th e r sp e c ie s o f A ste ro d in iu m w ith short ex ten s io n s (F ig s 11, 21). I t is h e re c a lle d A. 335 202 Figs 13-22. Line drawings of Asterodinium spp. Figs 13-15. Asterodinium g rac ile from the Pacific Ocean. Fig. 16. As terodiniumsp. sensu Sournia (1972a) from the Gulf of Cadiz. Fig. 11 .Asterodinium sp.l from the Strait of Gibraltar. Fig. 18. Asterodinium sp .l from the Pacific Ocean. Fig. 19. Asterodinium sp.2 from the Pacific Ocean. Fig. 20. Asterodinium cf. gracile from the Pacific Ocean. Fig. 21. Asterodinium cf. libanum from the Mediterranean Sea. Fig. 22. Asterodinium g rac ile from the Mediterranean Sea. Scale bars 20 mm. libanum , although A bboud-A bi Saab (1989) did not provide a Latin diagnosis and neither line draw ings nor good quality illustrations; therefore it is d ifficult to com pare w ith the original description. A ste ro d in iu m sp. sensu Soum ia (1972a) Soum ia (1972a) reported a single cell from the Indian O cean, but he did not describe it as a new species because it was considered that the specim en w as dam aged. T hree specim ens that strongly resem ble A sterodinium sp. as reported by S oum ia (1972a) in m orphology and size w ere collected from the Eastern A tlantic O cean. The first specim en was found in the G ulf o f C adiz (Figs 6 ,1 6 ). Two sim ilar specim ens 336 203 Table 1. New r&coxA^oi Asterodinium . Taxa # Location Lat N Long depth Date Figure Asterodinium gracile Soumia 1 Sardinia Channel 37° 59 8° 32 E 90 17/09/1999 A. gracile Soumia 1 Strait of Sicily 36° 28 13° 19 E 80 18/09/1999 A. gracile Soumia 1 South Tyrrhenian Sea 39° 12 14° 08 E 70 27/09/1999 12 A. gracile Soumia 1 Corsica Channel 41° 54 10° 26 E 30 28/09/1999 A. c f gracile Soumia 1 Offshore Philippine Sea 32° 00 138° E 90 13/05/2002 10 A. gracile Soumia 1 Kuroshio area 33° 00 138° E 80 07/07/2002 5 A. gracile Soumia 1 Kuroshio area 33° 00 138° E 175 07/07/2002 4 A. gracile Soumia 2 Kuroshio area 33° 30 138° E 100 07/07/2002 3 Asterodinium cf. libanum 1 Villefranche Bay 43° 41 7° 19 E 50 Sept98 Abboud-Abi Saab A. cf. libanum Abboud-Abi Saab 2 Villefranche Bay 43° 41 7° 19 E 50 Sept-Oct99 11 Asterodinium sp. sensu 1 Gulf of Cadiz 36° 34 6° 47 W 75 23/06/1997 6 Soumia 1972 A. sp. sensu Sournia 1972 2 Strait of Gibraltar 35° 54 5° 38 W 20 5/09/1997 Asterodinium sp.l 1 Strait of Gibraltar 35° 58 5° 55 W 100 3/09/1997 7 Asterodinium sp.l 1 Kuroshio area 33° 00 138° E 50 11/05/2002 8 Asterodinium sp.2 1 Kuroshio area 31° 00 138° E 125 06/07/2002 9 w ere subsequently collected in the Strait o f G ibraltar (Fig. 1, Table 1). T he m axim al length w as 32-34 pm and the cell w idth at the cingulum w as 14 pm . A lso, the specim ens co llec ted from the G u lf o f C adiz and S tra it o f G ib ra lta r p resen ted a ‘dam aged aspect’, w hereas other cells in the plankton appeared undam aged. Asterodinium sp .l This taxon differs from previous records by the presence o f shorter extensions with rounded tips and w ith a cell body slightly m ore elongated than in A. cf. libanum. One specim en w as collected at the A tlantic side o f the S trait o f G ibraltar (Figs 7, 17) (U n fo rtu n a te ly no size m e asu rem en ts w ere p erfo rm ed ). A seco n d sp ec im en , apparently sim ilar to the A tlantic one, was colleeted from the offshore subtropical waters o f the Philippine Sea (Figs 8 , 18). The m axim al length w as 51 pm and the width at the cingulum was 27 pm. Asterodinium sp.2 From the w aters o f the K uroshio C urrent w as co llected a specim en that d iffered from other records. Cells possessed tw o parallel antapical extensions, short lateral apical extensions, and a longer central apical extension (Figs 9, 19). The nucleus occupied a h igher proportion o f the cell body than in the other species and extended into the episom a. D ue to the bending o f the central apical extension, the m axim um length is estim ated to be around - 6 0 pm. T he w idth o f the cell at the cingulum was 18 pm. 337 204 Discussion Ecological characteristics Due to the small num ber of observations, it is difficult to establish the ecological characteristics o f Asterodinium . However some trends w ere noticed in the vertical distribution of the taxa (Table 1). In the Indian Ocean, Soum ia (I972a,b) recorded individuals o f Asterodinium at 100 m depth. Estrada (1979) reported an unidentified species o f Asterodinium from surface w aters o f the N W M editerranean Sea. In the Bay o f V illefranche (Ligurian Sea), three specim ens o f Asterodinium libanum w ere collected at 50 m (at a station w ith a m axim al depth of 80 m, see G om ez & Gorsky 2003). In the Tyrrhenian basin and the Sicily Strait, three specim ens o f Asterodinium gracile w ere collected in deep waters (70-90 m depth), and one individual at 30 m depth. On the A tlantic side o f the Strait o f Gibraltar, a specim en o f Asterodinium sp .l was found at 100 m depth, w hile in the G ulf o f Cadiz, one specim en o f Asterodinium sp. sensu Soum ia (1972a) was found at 75 m depth. Concerning the records o f Asterodinium sp. sensu Sournia (1972a) found near the sill o f the S trait o f Gibraltar, it should be taken into account that m ixing events can alter the vertical distribution o f the species (G om ez et al. 2000). Asterodinium species have w ell-defined chloroplasts and this m ay be an adaptation to the low irradiance levels in deep waters, since other photosynthetic deep w ate rs sp ec ie s (e .g ., C era tium p la ty c o rn e D aday ) a lso c o n ta in h ig h e r concentrations of chlorophyll com pared to taxa found in shallow w ater (Falkow ski 1980). The m ost recent records clearly confirm this trend, one specim en collected at 175 m depth ju st below the K uroshio axis (Fig. 4) presented a healthy aspect w ith m ore intense p igm entation com pared to the shallow er one (Fig. 5). It should be taken into account that the w arm Kuroshio Current is characterized by highly trans­ parent waters. Thus, the genus Asterodinium m ay be considered as a m em ber o f the shade flora (Sournia 1982). Concerning the tem poral distribution of Asterodinium , som e trends are apparent: Estrada (1979) reported an unidentified species o f Asterodinium in Septem ber 1975 along the M editerranean Spanish coasts. Abboud-Abi Saab (1985) from 3 years o f m onitoring in L ebanese coastal w aters exclusively reported A sterodin ium gracile in the autum n and A sterodin ium sp. in the spring. D uring our b iannual study o f the phytoplankton com position o f the B ay o f V illefranche-sur-M er, A sterod in ium w as observed only in S eptem ber and O ctober (Table 1). S ince the research cru ises w ere perfo rm ed in June and S eptem ber, the offshore records on ly appeared during .. 4 these m onths. L ate sum m er is the m ost oligotrophic p eriod in the M edite rranean Sea and it seem s to be the m ost favourab le period for the deve lopm en t o f these sp e c ie s . G o m ez & C la u s tre (2 0 0 3 ) m e n tio n th a t th e re c e n t o c c u r re n c e o f Asterodinium in the areas o f the w estern M editerranean Sea in tensively investigated in the pas t (e.g ., the L igurian Sea; see G om ez 2003) could be associa ted w ith the p rogressive w arm ing o f the M editerranean waters and unusual high tem peratures in Septem ber 1999. 338 205 D ue to the sm all size and delicate features such as pelliculate cells w ith flexible radiating arm s, plankton net sam pling probably dam ages specim ens o f Asterodinium . Their detection in oligotrophic w aters requires sedim entation of large volum es o f seaw ater w ith very low phytoplankton abundance. Asterodinium in not included in the m o st com m only used lite ra tu re for p h y to p lan k to n id en tifica tio n , w ith the exception o f Sournia (1986) and Fensom e et al. (1993), and it is likely this it often escapes notice during routine analyses. F urther research should address the Asterodinium gracile complex', does it constitute one sp ec ie s w ith h igh m orpho log ica l variab ility , d epend ing on env ironm en ta l conditions, or are different species involved? Acknowledgements M editerranean and Atlantic samples were collected from cruises within the context of projects: CANIGO (EU MAS3-CT96-0060), JGOFS-France PROSOPE, and ICTIO-Alboran 97 cruise by the Spanish Institute of Oceanography. Financial support by Spanish Ministry of Science and Technology is acknowledged. Pacific Ocean samples were collected from cruises o f the SOYO program by the National Research Institute of Fisheries Science, Japan. I thank the comments and suggestions by the Editor and reviewers. I acknowledge the financial support by the European Commission (ICB2-CT-2001-80002). References ABBOUD-ABI SAAB, M. (1985): Étude quantitative et qualitative du phytoplancton des eaux côtières libanaises. - Lebanese Sci. Bull. 1: 197-222. 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NORRIS, W.A.S., SARJEANT, D.I. WHARTON & G.L. ‘ WILLIAMS ( 1993): A classificationof living and fossil dinoflagellatès.-Mi cropaleontoIogy,Specia la# fe Publication Number 7: 1 -351. American Museum of Natural History, Sheridan Press, Hanover, PA. GARCIA, C M., L. PRIETO, M. VARGAS, F. ECHEVARRIA, J. GARCIA-LAFUENTE, J. RUIZ & J.P. RUBIN (2002): Hydrodynamics and the spatial distribution of plankton and TEP in the Gulf of Cadiz (SW Iberian Peninsula) - J. Plankt. Res. 24: 817-833. GÔMEZ, F., F. ECHEVARRIA, C M. GARCIA, L. PRIETO, J. RUIZ, A. REUL, F. JIMÉNEZ- GÔMEZ & M. VARELA (2000): Microplankton distribution in the Strait of Gibraltar: coupling between organisms and hydrodynamic structures. - J. Plankt. Res. 22: 603-617. 339 206 GÔMEZ, F. (2003): Checklistof Mediterraneanfree-livingdinoflagellates.-Bot. Mar. 46: 215-242. GÔMEZ F. & H. CLAUSTRE (2003): The gsnus Asterodinium (Dinophyceae)as a possible biological indicator of warming in the Western Mediterranean Sea. - J. Mar. Biol. Ass. U.K. 83: 173-174. GÔMEZ, F. & G. GORSKY (2003): Microplankton annual cycles in the Bay of Villefranche, Ligurian Sea, NW Mediterranean Sea. - J. Plankt. Res. 25: 323-339. GREUTER, W., J. McNEILL, F.R. BARRIE, H.M. BURDET, V. DEMOULIN, T.S. FILGUEIRAS, D.H. N ICOLSON , P C . SILVA, I.E . SKOG, P. T R EH A N E, N .J. TU R LA N D & D .L . HAWKS WORTH (2000): International Code of Botanical Nomenclature (Saint Louis Code). - Regnum Vegetabile 138: 1-474. Koeltz Scientific Books, Konigstein, Germany. GREUTER, W., R.K. BRUMMITT, E. FARR, N. KILIAN, P.M. KIRK & PC. SILVA (1993): NCU-3. Names in Current Use for Extant Plant Genera. - Regnum Vegetabile 129: 1-1464. Koeltz Scientific Books, Konigstein, Germany. HASLE, G.R. & E.E. SYVERTSEN (1997): Marine Diatoms. - In: TOMAS, C.R. (ed.): Identifying marine phytoplankton:5-385. Academic Press, San Diego. LOEBLICH, A.R. Ill (1982): Dinophyceae. - In: PARKER, S.P. (ed.): Synopsis and classification of living organisms: Vol. 1, pp. 101-115. McGraw-Hill, New York. SOURNIA, A. (1972a): Quatre nouveaux dinoflagellés du plancton marin. - P hyco log ia ll: 71-74. SOURNIA, A. ( 1972b): Une période de poussées phytoplanctoniquesprés de Nosy-Bé (Madagascar) en 1971. Espèces rares ou nouvelles du phytoplancton. - Cah. O.R.S.T.O.M., Sér. Océanogr. 10: 151-159. SOURNIA, A. (1973): Catalogue des espèces et taxons infraspécifiques de Dinoflagellés marins actuels publiés depuis la révision de J. Schiller. I. Dinoflagellés libres. -Nova Hedwigia Beih. 48: 1-92. SOURNIA, A. (1982): Is there a shade flora in the marine plankton? - J. Plankt. Res. 4: 391-399. SOURNIA, A. (1984): Classification et nomenclature de divers dinoflagellés marins (classe des Dinophyceae). - Phycologia 23: 345-355. SOURNIA, A. (1986): Atlas du phytoplancton marin. Vol. I: Introduction, Cyanophycées, Dictyochophycées, Dinophycées et Raphidophycées. - Editions du Centre National de la Recherche Scientifique, Paris. TAYLOR, F.J.R. (1963): Brachydinium, a new genus of the Dinococcales from the Indian Ocean. - J. South Afr. Bot. 29: 75-78. TAYLOR, F.J.R. (1967): Phytoplankton of the South Western Indian Ocean. - Nova Hedwigia 12: 433-476. UTERMÔHL, H. ( 1958): Zur Vervollkommung der quantitativenPhytoplankton-M ehodik. - Mitt. Int. VereinigungTheor. Angew. Limnol. 9: 1-38. Received 3 June 2002, accepted in revised form 8 May 2003. 340 207 rrmted in the United Kingdom The genus Asterodinium (Dinophyceae) as a possible biological indicator of warming in the western Mediterranean Sea Fernando Gomez* and Hervé Claustre^ * Department of Aquatic Biosciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan. ^Laboratoire d’Océanographie de Villefranche-sur-Mer, CNRS-INSU and University P. & M. Curie, BP 08, 06238 Villefranche-sur-Mer Cedex, France. * Corresponding author, e-mail: fernando.gomez@fitoplancton.com The presence of two dinoflagellate species of the genus Asterodinium, which are a priori representative of warm waters, is reported for the first time in the western Mediterranean Sea. Asterodinium libanum was identified in the Bay of Villefranche-sur- Mer (Ligurian Sea), while Asterodinium gracile is reported in the Tyrrhenian Sea. These findings are discussed in the context of the progressive warming of Mediterranean waters. Since 1960, a monotonie increase of the temperature has been recorded in the Mediterranean waters, apparently as a result of the combined global warming and local anthropogenic effects (Béthoux et al., 1990; Turley, 1999). Several studies have shown that the marine biodiversity of the Ligurian and Tyrrhenian basins is sensitive to climate change, with tropical species appearing since 1985 (Francour et ah, 1994; Astraldi et ah, 1995). However most of the studies on changing biodiversity in the Mediterranean Sea, deal with macroscopic species such as fish, invertebrates or macroalgae (Bianchi & Morri, 2000). During the last century, at least 16 exotic phytoplankton species have become common in European Atlantic waters (Elbrachter, 1999) with the establishment of thermophilic phytoplankton species in the North Sea (Nehring, 1998). However little is known about changes affecting the phytoplankton community of the Mediterranean Sea. Asterodinium is a distinctive genus of unarmoured dinoflagellates; cells are dorsoventrally flattened, with two characteristic radiating elongate extensions from the hypotheca and three other arms from the epitheca; they present a well-developed nucleus and chloro­ plasts. The genus was initially reported from the tropical Indian ocean with the description of two species Asterodinium gracile and A. spinosum (Sournia, 1986). Later, Asterodinium gracile the new species A. libanum were reported in Lebanese coastal waters (eastern Mediterranean Sea) (Abboud-Abi Saab, 1989). The present study reports recent records of Asterodinium species in the western Mediterranean Sea and is suggested as possible biological indicator of warming. Phytoplankton identification was performed as part of two studies. The first study was conducted over two years (1998 2000) at a permanent station (Station B) in the Bay of Villefranche-sur- Mer (Ligurian Sea, north-west Mediterranean Sea). The second study was performed as part of the PROSOPE cruise carried out in September 1999 aboard the RV ‘Thalassa’ from the Moroccan Atlantic coast to the eastern Mediterranean Sea (Figure 1). Unconcentrated seawater samples were preserved with Lugol’s solution and kept in cold and dark conditions until analysis in the laboratory. Subsamples (50-100 ml) were allowed to settle for 24 48 h in Utermohl chambers and observed by inverted light microscopy. Journal of the Marine Biological Association of the United Kingdom (2003) Three specimens of Asterodinium libanum Abboud-Abi Saab have been observed in the Bay of Villefranche-sur-Mer in September 1998 and September-October 1999 at 50 m depth. In September 1999, four individuals of Asterodinium gracile Sournia were recorded at four stations in the Tyrrhenian Basin and the Sicilian Strait, mostly in the 70-90 m layer (Rgure 2). The phytoplankton composition of the Ligurian Sea has been extensively investigated in the past. Halim (1960) reported the composition of dinoflagellates from a 3-y study (1952-1954) at the same Station B where we report the presence of A. libanum for the first time. The Asterodinium genus was described for the first time in 1972 but this genus is distinctive and easily identifi­ able, thus removing the possibility that Halim (1960) might have misidentified it. For example, Halim (1960) described six new species of Histioneis, a genus in the same size range as Asterodinium which is also preferentially found in the deep waters of the Bay of Villefranche. The Tyrrhenian basin has also been intensively investigated, but most of the studies were performed in the Bay of Naples or coastal lagoons. These shallow and eutrophic environments seem to be unfavourable for the development of Asterodinium species. Coinciding with the records of A. gracile in September 1999, a climatically-driven ecosystem disturbance was reported in the - . . . ■ - ... J 5'EO' Longitude Figure 1. Location of the records o î Asterodinium Sournia in the western Mediterranean Sea. I , A. libanum; # , A. gracile. 208 mailto:fernando.gomez@fitoplancton.com A . F ig u re 2. Light microscopy photographs: (A) Asterodinium gracile (x400) from the Tyrrhenian Sea; (B) Asterodinium libanum (x630) from the Bay of Villefranche-sur-Mcr (Ligurian Sea). Scale bar; 20fim . north-western M editerranean, w ith a deepening of the therm o- ciine and an anomalous increase of summer sea surface tem pera­ tures (of 2“ 3°C); these changes resulted in marked m ortality of sessile invertebrates (e.g. sponges and gorgonians) (Romano et ah, 2000; C errano et ah, 2000). Seawater w arm ing can affect the m arine biota by a direct influence of tem perature, causing changes in survival, repro­ ductive success and dispersal pattern and an indirect influence due to the change of the ocean circulation patterns (Bianchi & M orri, 2000). Since the completion of the Suez Canal in 1869 and more recently with the reduction of salinity of Bitter Lakes, the introduction of tropical species directly through the Suez Canal or via ballast waters seems to be favoured (Halim, 1990). T he progressive warm ing of the M editerranean Sea, and possibly the 1999 thermal anomaly might have favoured the increase in abundance of warm-water species such as those of the Asterodinium genus. This study was funded by the JGOFS-France PROSOPE programme. F.G. acknowledges financial support by the Spanish M inistry of Science and Technology and by the European Commission (ICB2-CT-2001-80002). R E F E R E N C E S Abboud-Abi Saab, M ., 1989. Les dinoflagellés des eaux côtières libanaises— Espèces rares ou nouvelles du phytoplancton marin. Lebanese Science Bulletin, 5, 5-16. Astraldi, M., Bianchi, C.N., Gasparini, G.P. & M orri, G., 1995. Climatic fluctuations, current variability and m arine species distribution: a case study in the Ligurian Sea (north-west M editerranean). Oceanologica Acta, 18, 139-149. Béthoux, J .P , Gentili, B., Raunet, J. & Tailliez, D., 1990. Warming trend in the western M editerranean deep water. Nature, London, 347, 660-662. Bianchi, C.N. & M orri, C., 2000. M arine biodiversity of the M editerranean Sea: situation, problems and prospects for future research. Marine Pollution Bulletin, 40, 367-376. Cerrano, C. et ah, 2000. A catastropliic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (NW Mediterranean), summer 1999. Ecology Letters, 3, 284—293. Elbrachter, M., 1999. Exotic flagellates of coastal N orth Sea waters. Helgolander Meeresuntersuchungen, 5, 235-242. Francour, P., Boudouresque, C.F., Hamelin, J.G ., Hamelin- Vivien, M L. & Q uignard, J .P , 1994. Are the M editerranean waters becoming warmer? Information from biological indica­ tors. Marine Pollution Bulletin, 28, 523-526. Halim, Y , 1960. Etude quantitative et qualitative du cycle écolo­ gique des dinoflagellés dans les eaux de Villefranche-sur-Mer. Annales de ILnstitut Océanographique, Paris, 38, 123 232. Halim, Y , 1990. O n the potential m igration of the Indo-Pacific plankton through the Suez Canal. Annales de l ’Institut Océanographique, Monaco, 7(n. sp), 11-27. Nehring, S., 1998. Establishment of thermophilic phytoplankton species in the North Sea: biological indicators of climatic changes? ICES Journal o f Marine Science, 55, 818-823. Romano, J.C ., Bensoussan, N., Walid, A N Y & Arlhac, D., 2000. Anomalie thermique dans les eaux du Golfe de Marseille durant l’été 1999. Une explication partielle de la m ortalité d’invertébrés fixés? Comptes-Rendues de l ’Académie des Science de Paris, Sciences de la Vie, 323,4:15^4:27. _ Sournia, A., \9 8 6 .^ A t Id n iu pf^tdpldhcim rrïânh. Introduction, cyanophycées, dictyochophycées, dinophycées et raphidophycées. Vol. I. Paris: Editions CNRS. Turley, C M., 1999. The changing M editerranean Sea— a sensitive ecosystem? Progress in Oceanography, 44, 387-400. Submitted 25 July 2002. Accepted 13 November 2002. Journal o f the .Marine Biological Association of the United Kingdom (2003) 209 Cryptogam ie, A lg o l, 2005, 26 (2): 165-175 © 2005 A dac. Tous droits réservés Morphology of Brachidinium capitatum FJ.R. Taylor (Brachidiniales, Dinophyceae) collected from the western Pacific Ocean Fernando G Ô M EZ"*, Sadaaki Y O S H IM A T S U ^ & K en F U R U Y A " " Station M arine de W im ereux, Université des Sciences et Technologies de Lille 28 avenue Foch, B P 80, F-62930 W im ereux, France ^ A kash iw o Research Institute o f K agaw a Prefecture 75-5, Yashimahigashi Takamatsu, Kagaw a 761-0111, Japan ̂ D epartm ent o f A qua tic Biosciences, The University o f T o kyo 1-1-1 Yayoi, B unkyo , B u n ky o 113-8657, Japan (Received 16 M ay 2003, accepted 15 A p r il 2004) Abstract — This is a first report of the genus B ra ch id in iu m FJ.R . Taylor from th e Pacific Ocean. O f the 17 specimens of B. cap ita tum reported here, 12 were collected from th e vicin­ ity of the Kuroshio in May (2 specim ens) and July (10 specimens), 3 from the w estern equa­ torial Pacific Ocean, one from the Sulu Sea, and one from T anabe Bay, Japan. The last-m entioned specimen was observed live. For the first time, the flagella and the sulcus of a m em ber of the o rder Brachidiniales A .R. Loeblich III ex Sournia are depicted in pho ­ tom icrographs. The ventral view corresponds to that seen when the position of the nucleus is in the left side of the cell. In several specimens, D API-staining show ed a secondary nucleus located in the opposite side o f the dinokaryon nucleus. In the live specim en, the sulcus was visible and the lateral extensions were observed to be moveable. Brachidinium I Brachydinium ! binucleate dinoflagellate / Pacific Ocean / phytoplankton / taxonomy Résumé — Morphologie de Brachidinium capitatum FJ.R. Taylor (Brachidiniales, D ino­ phyceae) récolté à l’ouest de l’Océan Pacifique. C 'est la prem ière signalisation du genre B ra ch id in iu m F.J.R. Taylor dans l’O céan Pacifique. Parm i les 17 spécim ens de B. cap ita tum rapportés ici, 12 ont été trouvés à proximité du Kuroshio en mal (2 spécim ens) e t juillet (10 spécim ens), 3 dans l’O céan Pacifique équatorial occidental et enfin, un seul spécim en dans la m er de Sulu ainsi que dans la Baie de Tanabe, Japon. Le dern ier spécim en a été observé vivant. Pour la prem ière fois, les flagelles et le sulcus d ’un m em bre de l’o rd re des B rachidiniales A .R. Loeblich III ex Sournia sont illustrés par des photom icrographies. La vue ventrale correspond à ce que l’on voit quand le noyau est du côté gauche de la cellule. D ans plusieurs spécimens, l’utilisation de la coloration au DABI a m ontré un noyau secon­ daire situé du le côté opposé au noyau dinokaryon. L’observation du spécim en vivant a m ontré nettem ent le sulcus ainsi que la m otilité des prolongem ents latéraux. Brachidinium ! Brachydinium / dinoflagellé binuclcé / Océan Pacifique / phytoplancton / taxonomie * Correspondence and reprints: fernando.somez@ifiloplanclon.com. Phone +33 3 2199 2926. Fax +33 3 2199 2901. 2 1 0 mailto:fernando.somez@ifiloplanclon.com 166 G om ez R , Yoshimatsu S. & Furuya K . INTRODUCTION B rachid in ium F.J.R. Taylor is a genus o f ph o to sy n th e tic p lank ton ic m arine u n arm o red d inoflagella tes [usually m isspelled as B rachyd in ium , see G om ez (2003a)]. B rach id in ium and A sterod in ium S ourn ia constitu te th e fam ily B rachid in iaceae, p laced in the o rd e r B rachid in iales A .R . L oeblich I II ex S ourn ia (L oeb lich III, 1982; S ou rn ia , 1984), o r P tychodiscales Fensom e, Taylor, N orris, S arjean t, W h a rto n et W illiam s (Fensom e et a i , 1993). A ccord ing to S te id inger & T angen (1997, p. 468) B rachid in ium has flattened cells w ith fou r e longate ex te n ­ sions rad ia ting from the h y posom a and an apical process on th e ep isom a. T h e su l­ cus has n o t been observed , b u t an incom plete cingulum and ch lo rop lasts are p resen t. A large, ovoid nucleus occupies m ost o f th e cell body. The type species B rach id in ium capitatum F.J.R. Taylor (Taylor, 1963) and one o th e r species, B rach id in ium catenatum F.J.R. Taylor, have b ee n d escribed from the sou thw est Ind ian O cean (Taylor, 1967; see Figs 2-4). T he au th o r m e n tio n ed th a t th e la tte r species m ight be a sm all neritic o r sum m er fo rm o f B. capitatum (Taylor, 1967) (Fig. 4). S ourn ia (1972) also rep o rted B. capitatum (see Figs 5-6) and described tw o new taxa, B rachid in ium taylorii S ournia (see Fig. 7) and B rach id in ium brevipes S ou rn ia (see Fig. 8 ), also from the sou thw est In d ian O cean . A ccord ing to S ou rn ia (1972, p. 153) B. taylorii show s a ro b u st aspec t w ith th icker arm s th an th e type species an d a sh o rte r apical p ro tuberance . T he su rface o f the cell is covered w ith fine peaks “ fines côtes ou c rê tes” . B rachid in ium brevipes show s sh o rte r arm s, a very reduced cen tral body and is also covered w ith fine p eaks (S ourn ia, 1972, p. 153-4). S ubsequently , B. capitatum and B rachidinium sp. w ere rep o rte d from the so u th e rn w aters o f th e In d ian O cean and the A rab ian Sea, respectively (S ou rn ia et a i , 1979; T arran et a l, 1999). T he type species was also re p o rted from th e n o r th ­ east A tlan tic O cean (M argalef, 1973) and the M e d ite rran e an S ea (L éger, 1971; A b b o u d -A b i Saab, 1985; Vilicic, 1998). In the northw est M e d ite rran e an Sea, E strad a & S ala t (1989) rep o rte d B rachidinium as a com ponen t o f the d eep p h y ­ to p lan k to n assem blages and P a lau et a l (1991) re p o rted B rachid in ium sp. from a cave. B rach id in ium taylorii S ourn ia was rep o rted from the so u th e as t A tlan tic O cean (K ruger, 1979) and the M ed ite rran ean Sea (M argalef, 1995). T he la tte r au th o r also listed B rach id in ium “ transversum ” b u t w ith no illu strations o r ad d i­ tiona l in fo rm atio n (M argalef, 1995). T he m orpho logy o f the species o f B achid in ium is poorly know n due to a lack o f records, d e ta iled illu strations and in fo rm ation on the u ltra s tru c tu re (i.e., flagellum /flagella; sulcus; nuclei; etc). Taylor (1963) d id no t observe the flagel- lum /flagella o r cingulum an d p laced B rachidinium in the o rd e r D inococcales . Pascher. H e p ro p o sed a te n ta tiv e o rien ta tion fo r th e genus (Figs 2 -3 ).T aylor (1980, p. 67)..shoyyed.a species o f B rach id in ium , whiph lia§^j)OQi:ly.dggjm d W c q s ^ _ “Ipn- g itud inal flagellum ” an d th e d in o k ary o n nucleus in the left side'ôT th e œ ï r ( R g . 9) F ensom e et a l (1993, p. 3) inc luded a line draw ing o f B. capitatum w ith tw o fla­ gella (Fig. 10). T hey did n o t m en tio n flagella o r sulcus in th e fam ily B rac h i­ d in iaceae (p. 56), b u t illu s tra te d d o rsa l and ven tra l views o f B. capitatum , in w hich the ven tra l view co rresp o n d s to the position o f the d inokaryo tic nucleus in the righ t side o f the cell (Figs 5-6). F ensom e et a l (1993, p. 56) re p o rte d th a t the o ri­ e n ta tio n w as b ased on S ourn ia (1972, 1986). H ow ever, S ou rn ia (1972, 1986) inc luded no illu stra tion o f flagellum /flagella o r sulcus o f B rachidinium . S ourn ia (1972) in tro d u ced a te rm ino logy describ ing the o rien ta tio n o f the o rd e r B rach i­ d in ia les an d considered th a t the d inokaryo tic nucleus is d isplaced to one side and 2 1 1 B ra ch id in iu m cap ita tum from Pacific Ocean 167 1(TN- 10 Km 120"E 160"E 160*W180' Fi g. 1. Location of the sampling stations in the western Pacific Ocean. The inset shows the Tanabe Bay where a live specimen was collected. the ex tensions o r arm s c loser to the nucleus w ere th e “ le ft” extensions. U n ce rta in ties rem ained , how ever, and S ourn ia (1986, p. 49) d o u b te d w h e th e r the cells w ere dorso -ven trally o r la terally fla ttened . S ourn ia (1986, p. 50), based on th e reco rd s by L ég e r (1971), re p o rted th a t B rach id in ium possesses a t least one flagellum , b u t th a t th e p o in t o f in se r­ tio n rem a in ed unknow n. L ég e r (1971) co llec ted 30 specim ens n am ed as B. capi­ tatum . H o w ev er his figure, rep ro d u ce d h e re (Fig. 11) d o es n o t seem to rep re se n t the type species. H is specim en draw ing has tw o ex ten sio n s rad ia tin g from the hyposom a, and tw o ex tensions and a c e n tra l p rocess from th e ep isom a. I t is in te rm ed ia te A stero d in iu m dixxd B rdch idm ium . S o m n \2L (1972) co m ­ m en ted on the possib ility o f an ‘op tical illu sion ' in th e p o s itio n o f th e cingulum . H is specim en has th e d in o k a ry o tic nucleus in the le ft side and a hypo the tical ‘su lcal’ flagellum arising fro m the re a r an d th e nucleus in th e rig h t side o f the cell (Fig. 11). L éger (1971) re p o rte d th a t h e w as unab le to loca te th e in se rtion o f the flagellum . This study rep o r ts fo r th e first tim e the flagella and th e sulcus in B rach id in ium , includ ing p h o to m icro g rap h s on the m o v eab le ex ten sio n s o f a live specim en, an d th e o ccu rrence o f a seco n d a ry nucleus (confirm ed by D A PI sta in ing). 2 1 2 168 Gom ez F.. Yoshimatsu S. & Furuva K. 3 1 Figs 2-11. Line drawings of several species of Brachid in ium reported in the literature. Fig. 2. B. capitatum adapted from Taylor (1963). Fig. 3. Ventral view of B. capitatum according to Taylor (1963). Fig. 4. Brachid in ium catenatum F.J.R. Taylor adapted from Taylor (1967). Figs 5-6. B. capi­ tatum adapted from Soumia (1972). These figures were also reproduced by Fensome et al. (1993), who proposed that they represented ventral and dorsal views, respectively. Fig. 7. Brachid in ium tay lo rii Sournia adapted from Soumia (1972). Fig. 8. B rachid in ium brevipes Sournia adapted from Soumia (1972). Fig. 9. A ventral view of a member of the genus Brachid in ium showing the longitudinal flagellum adapted from Taylor (1980. p. 67). Fig. 10. A ventral view of B. capitatum with two flagella adapted from Fensome et al. (1993, p. 3) apparently based on Soumia (1972, 1986). Fig. 11. “Brachidinium capitatum” adapted from Léger (1971). Scale bars 20 pm. MATERIAL AND METHODS S am ples w ere co llected during several cruises in the w estern Pacific O cean ; 1) Two cruises on b o ard R /V Soyo M a m (13-20 M ay and 3-10 July 2002) a long the m erid ian 138° in the vicinity of the K uroshio C urren t. N ine sta tions w ere sam pled fro m 30° 30’ N to 34° 15’ N in May, and 10 s ta tions w ere sam pled from 30° 0 ’ N to 34° 20’ N du ring the July cruise. A t each s ta tion , 15 d ep th s fro m 5-200 m w ere sam pled w ith N iskin bo ttles; 2) on board R /V H a ku h o M a m (7 N o- vem ber-18 D ec em b e r 2002) in th e Celebes, Sulu and S ou th C h ina Seas. Sam ples w ere co llected using N iskin bo ttles a t 10 sta tions a t six d ep th s from 0 to 150 m dep th ; 3) ab o a rd R /V M irai (15-28 January 2003) along th e e q u a to r from 160°E to 160°W (Fig. 1). Sam ples w ere collected w ith N iskin bo ttles from 9 s ta tions a t 14 d ep th s be tw een 0 to 200 m dep th . D uring all the cruises, sam ples w ere p re ­ served w ith acidified L ugo l’s so lu tion (H asle and Syvertsen 1997, p. 334) and s to red a t 5° C. Sam ples w ere p re-co n cen tra ted by settling in glass cylinders, and c o n cen tra tes se ttled in stan d ard sed im en tation cham bers. C o n cen tra tes equ ivalen t 213 B ra ch id in iu m cap ita tum from Pacific Ocean 169 to 400 m L w ere observed w ith a N ikon in v erted m icroscope eq u ip p ed w ith a N ikon digital cam era. Several o f th e Lugol fixed specim ens w ere iso la ted w ith a cap illary from the cham bers, transfe rred to a glass slide, and observed w ith an O lym pus m ic ro ­ scope equ ipped w ith N om arsk i D iffe ren tia l In te rfe ren ce C o n tra s t (D .I .C ) system . H igh m agnification m icropho tographs (x 6 0 0 ;x l0 0 0 ) w ere o b ta in ed w ith an O lym ­ pus digital cam era . Several specim ens w ere s ta in ed by add ing D A P I (4,6- d iam id ino-2-phenylindole). D A P I specifically b inds to d o u b le s tran d e d D N A , and w hen excited w ith U.V. light the D A P I-D N A com plex fluoresces a b rig h t b lue (P o rte r & Feig, 1980). E pifluorescence m icroscopy was do n e w ith O lym pus and Z eiss m icroscopes equ ipped w ith U V excita tion facility. In add ition , one specim en collected from the coasta l w ate rs o f Ja p an was observed live. S eaw ater sam ples w ere m onth ly co llec ted fro m a sta tion in T anabe B ay (see inset in the Fig. 1) at 0 ,5 ,10,15 m d ep th s and one m e tre above th e b o t­ tom (19.5 m dep th ). Sam ples (1 1) w ere filtered th ro u g h an 8 m m p o re size M illipore cellulose aceta te filter a t low p ressu re (<100 m m H g) to a final vo lum e o f 50 ml. This concen tra te w as left to se ttle in a com posite cham ber. F ro m th e b o t­ tom of the cham ber, 1 m l was exam ined on a S edgew ick-R after coun ting ch a m ­ ber. T he specim en was isolated w ith a capillary, tran sfe rred to a glass slide and cover w ith a glass slide. T he specim en was o bserved an d p h o to g rap h e d w ith an O lym pus light m icroscope and O lym pus cam era by using b rig h t field. RESULTS AND DISCUSSION A to ta l o f 17 specim ens of the genus B rach id in ium w ere o bserved in the u p p e r 90 m d ep th during the four cruises in the w estern Pacific O cean (Fig. 1). Ten specim ens w ere observed in the vicinity o f the K urosh io in July and only tw o in May. T he m axim um occurrence was in July (30° 0 ’ N, 138° E a t 60 m d e p th ) w ith 3 specim ens p e r sam ple (7.5 cells 1~̂ ) (Tab. 1). A ll the records a re considered to be o f th e type species, B. capitatum , which, a lthough from the sam e sam ple, show ed som e v aria tio n in size as well as the relative angle o f the extensions w ith resp ec t the cell body. T he m axim um length of the cells ranged from 50 to 140 m m and the w id th o f th e cell a t th e cin­ gulum was 25-55 pm. Cell orientation B rachidinium is a f la ttened a th eca te d inoflagellate . T h e p resence o f long appendices, resu lting in d iffe ren t inclinations o f th e cell, p lu s th e cell transparency , m ake it d ifficult to observe u ltra s tru c tu ra l details (such as th e in se rtio n o f th e f l a ? ^ - gella) by light m icroscopy. The transverse flagellum (TF h ere a fte r) was observed in several speci­ m ens by using D .I.C . optics. In one specim en, th e T F w as also o bserved u n d e r inverted m icroscopy w hen it was sep ara ted from th e cingulum (Figs 12-14). The nucleus o f this specim en was located in the righ t side o f th e cell. T he T F w as free m oving, d isp laced from the cingulum groove in the re a r (rev erse) focus o f th e cell (Fig. 12) and tu rn ed to the fro n t o f th e cell in the left ex trem ity of the cingulum groove (Fig. 13). In the fron t o f the cell the T F ran all along th e cingulum an d no in se rtion was observed (Fig. 14). Subsequently , the in se rtion o f th e flagellum was 214 170 Gom ez F.. Yoshimatsu S. & Furuva K. Table 1. Number of specimens recorded, date, stations, depth (m) in meters, geographic coordinates (latitude, longitude) and figures of the records of B rachid in ium in the western Pacific Ocean. # Date Sta. (m) Lat N Long Figure 1 24/1/1995 20 - 19.5 33° 42' 135° 21’ E Figs 27-28 1 10/5/2002 C3 - 5 33" 30’ 138" E 1 13/5/2002 Cl 3 - 5 30" 30’ 138" E 7/7/2002 C8 - 2 0 33° 30' 138° E Figs 16-21 1 7/7/2002 C7 - 5 0 33° 138" E 1 7/7/2002 C6 - 5 32" 30- 138° E 1 6/7/2002 C5 - 4 0 32° 138° E 1 6/7/2002 C2 - 6 0 31" 30’ 138" E Fig. 26 1 4/7/2002 B1 - 1 0 30° 138" E Figs 22-25 3 4/7/2002 B1 -6 0 30° 138" E 1 3/12/2002 10 - 3 0 8" 50’ 121"48’E 1 15/1/2003 6 - 1 0" 160" E 1 17/1/2003 7 -9 0 0" 165° E Figs 12-15 1 25/1/2003 13 -8 0 0" 165° W located in the rea r focus of th e cell. Thus, th e aspect of the specim en in figures 12- 14 co rresponds to the dorsal view (nucleus in the righ t side o f the cell). This spec­ im en was la te r successfully tran sfe rred to a glass slide and observed u n d e r a m icroscope w ith D .I.C . The specim en ap p eared m the sam e view, also w ith th e nucleus in th e righ t side o f the cell, b u t the T F was now d isplaced from the groove and a h igher p ro p o rtio n of th e T F was seen m oving freely (Fig. 15). D .I.C p h o tom icrog raphs o f a second specim en w ith the nucleus in th e le ft side of the cell w ere taken (Figs 16-21). F igures 16-17 show a sim ilar focus (b o th righ t an tap ical and the left la te ra l an tap ical ex tension in focus), w ith the T F located along the groove. T he T F d id no t arise from the re a r focus o f the cell. F igure 18 shows, in a d iffe ren t focal p lane, the left an tap ica l and the righ t la te ra l an tap ical extensions, w ith the T F visible in the righ t side of the cell a long th e groove. T he end of the T F w as located in th e cen tra l p a r t o f the cell (see also fig. 21). W e w ere unab le to focus on the area o f the T F origin. The flagellum did n o t arise from the back o f th e cell (Figs 16-17). This position , w ith the nucleus in the left side o f the cell, is the v en tra l view. A fte r these observa tions the specim en w as sh ak en un til th e T F was partia lly sep ara ted from the cingulum . T he T F tu rn ed aro u n d th e left side o f the cingulum (Figs 19-20) ( re a r o f th e cell,'as in Fig. 16). A t a d iffe ren t focal p lane m o st o f the T F was visible (Fig. 21). T he aspect o f this specim en, w ith th e nucleus in th e left side, co rresponds to the ven tra l view (Figs 16-21). A th ird specim en w ith the nucleus in the righ t side was also observed w ith D .I.C . optics (Figs 2 2 ,2 4 ) and inverted m icroscopy (Fig. 23). A p a rt o f a fla­ gellum th a t could co rrespond to the longitud inal flagellum was observed betw een th e two an tap ical ex tensions (Fig. 22). T he T F ran along the cingulum in a fron ta l focus (Fig. 24). This position , w ith the nucleus in the righ t side, co rresponds to the do rsa l view. 215 B ra c h id in iu m c a p ita tu m fro m Pacific O cean 171 ________ L'ôiT^r^ Figs 12-21. Photom icrographs of B ra c h id in iu m showing the transverse flagellum (TF). Figs 12-15. D orsal view of a specim en u nder inverted m icroscopy (Figs 12-14), and direct microscopy (Fig. 15). See the end of the T F displaced from the cingulum and free moving in the rear focus of the cell (Fig. 12). See the cingulum groove where the T F ran (Fig. 13). P lease note that T F along the cingulum does not arise from the frontal focus (Fig. 14). The specim ens was transferred to a glass slide and observed with D.I.C. optic w hen T F appeared partially separated from the cingu­ lum (Fig. 15). Figs 16-21. D.I.C. photom icrographs of the ventral view of o th e r specim en. Figs 16- 17 the T F ran all along the cingulum in the rear focus of the cell. Fig. 18. the end of the T F was ob­ served in the central pa rt of the cingulum in the frontal focus of the cell. Figs 19-21. T he specim en was shaken until the T F was partially displaced from the cingulum in the rea r focus (Figs 19-20) and the fron ta l focus (Fig. 21). A G = A pical groove; N= dinokaryon nucleus; T F = transversal flagellum. Scale bars 20 pm. A n a l te rn a t iv e m e th o d to e lu c id a te th e ce ll o r ie n ta t io n is b a s e d o n th e lo c a tio n o f th e su lc u s (v e n tra l s id e ). T h e su lcu s w as n o t v is ib le in th e L u g o l-fix ed sp e c im en s , b u t w as v is ib le in th e live s p e c im e n o b se rv e d w ith a d ire c t m ic ro sco p e . T lie n u c le u s o f th is s p e c im e n w as lo c a te d in th e r ig h t s id e o f th e ce ll (F igs 27-28). F ig u re 27 fo cu sse s o n o n ly o n e o f th e fo u r ex ten s io n s , c o r re s p o n d in g to th e f ro n t o f th e sp e c im e n . F ig u re 28, sh o w in g th re e e x te n s io n s in fo cu s (c lo se r to th e glass s lid e ) , c o r re s p o n d s to th e r e a r o f th e cell, w ith th e su lcus b e in g v isib le . F ig u re s 27- 28, w ith th e n u c le u s in th e r ig h t s id e o f th e ce ll, c o r re s p o n d to th e d o rsa l view . In th e s e fo u r sp e c im en s , b a s e d o n th e tra n sv e rse f lag e llu m o r th e su lcus, th e v e n tra l v iew _ c o rre sp o n d s to th e n u c le u s b e in g o n th e le f t s id e o f th e ce ll (F igs 29-30). T lie o c c u r re n c e o f a su lc u s (Fig. 28) p ro v id e s e v id e n c e o f th e e x is te n c e o f th e lo n g itu d in a l f lag e llu m in th e g e n u s B ra c h id in iu m ( p a r tia lly o b s e rv e d in Fig. 22). T h is o r ie n ta t io n is c o n tra ry to F e n so m e et al. (1993, p. 3 ,5 6 ) . T a y lo r (1980, p. 67) r e p o r te d a n illu s tra tio n o f B ra c h id in iu m w ith a w e a k ly d e f in e d su lcu s in th e le ft s id e o f th e ce ll (Fig. 9). F ro m o u r o b se rv a tio n s , h o w e v e r, th e su lc u s is c e n tra lly lo c a te d in B r a c h id in iu m (F ig . 28). B in u c le a te sp e c im e n s T h e n u c le u s o f B ra c h id in iu m w as re la tiv e ly la rg e , o v o id , a n d o c c u p ie d a s ig n ific an t p r o p o r t io n o f th e b o d y cell. I t w as c lea rly v is ib le in L u g o l-fix ed spec i- 216 172 G o m ez F.. Yoshim atsu S. & F u ru va K . T Z# Figs 22-28. Figs 22-25. D orsal view of a specimen. Figs 22, 24. D.I.C. photom icrographs. Fig. 22. See a part of a flagellum, possibly the longitudinal flagellum. Fig. 23. Inverted m icroscopy photom icrograph of the specimen. Tlie arrow indicates the m icronucleus (pN) or secondary nucleus. Fig. 24. F rontal focus showing the T F along the cingulum. Fig 25. Epifluorescence pho ­ tom icrograph of the sam e specim en stained with D A PI and illum inated with U.V. light. The arrow indicates the secondary nucleus. Fig. 26. Inverted microscopy photom icrograph of o ther specimen in dorsal view. The arrow shows the secondary nucleus. Figs. 27-28. Photom icrographs of the dorsal view of a specimen observed live. Fig. 27. Frontal focus. Fig. 28. R ear focus. See the sulcus. A n inset betw een the figures 27-28 shows a low magnification photom icrograph taken prior to the m ovem ent of the lateral extensions of the specimen; AG = A pical groove; N = dinokaryon nucleus; pN = secondary nucleus; T F = transversal flagellum; LF = longitudinal flagellum; S = sulcus. Scale bars 20 pm. m e n s a n d a p p e a rs d a rk e r th a n th e re s t o f th e ce ll su rfa c e (e.g ., F igs 14, 23, 26), w h e re a s it w as le ss v is ib le in th e cell o b se rv e d live (F igs 27-28). T h e d in o k a ry o n n u c leu s w as c o n firm e d by D A P I-s ta in in g (Fig. 25). In a d d itio n , se v e ra l o f th e L u g o l-fix ed sp e c im e n s sh o w e d a s e c o n d a ry sm all n u c le u s in s ide o f th e cell o p p o ­ site th e d in o k a ry o n n u cleu s, w ith b o th n u c le i s ta in in g th e sa m e d a rk b ro w n c o lo u r (Fig. 26). In a D A P I-s ta in e d s p e c im e n (F igs 22-24), th e m ic ro n u c le u s f lu o re sc e d 217 B ra ch id in iu m cap ita tum from Pacific Ocean 173 VENTRAL DORSAL Figs 29-30. Line drawings of the ventral (Fig. 29) and dorsal (Fig. 30) views in Brachid in ium . w hen excited w ith U.V. light and the d in o k a ry o n nucleus ap p e a red b rig h te r than the m icronucleus (Fig. 25). S ourn ia (1972) d id n o t find ch lo rop lasts in B. brevipes. S ourn ia (1972) and L éger (1972) re p o r te d one c ircu lar 'p la s t ' in the opposite side of the nucleus in th e ir line draw ings (Fig. 8 and L éger (1972, p. 29)). This could b e in te rp re ted as the first ev idence o f th e occu rrence o f a secondary nucleus in Brachidinium . The occurrence o f b inuc lea te d inoflagellates is very rare. T he freshw ate r dinoflagellate K ryp toperid in ium fo liaceum (S te in) L in d em an n p re se n te d rhdhonu- cleate and b inuclea te stra in s, K ty p toperid m m m foUaceum^ con ta ined - a fu c o x a n t^ iïs^ s th in-contain ing d ia tom as a cytoplasm ic endo-sym bion t (K em p to n et al., 2002). The origin o f the secondary nucleus in B rachid in ium w as n o t clarified in the p re s ­ en t study. Live cell and moveable extensions The ex tensions in Brachid in ium a re m oveable , as re p o r te d by L éger (1971), based on observa tions by C achon on a live specim en co llec ted from V illefranche-sur-M er (L igurian Sea). W e include, for th e first tim e, p h o to m icro ­ graphs o f a live specim en o f B rachid in ium . D uring o u r m icroscopical observations, 218 174 G om ez F., Yoshimatsu S. & Furuva K . th e specim en m oved th e la te ra l an tap ical extensions from the initial position p a r ­ allel to th e cingulum (see inset betw een the figure 27 and 28), to a final position w ith th e tw o la te ra l ex tensions aligned w ith th e tw o cen tra l an tap ical extensions (Figs 27-28). This last ap p earan ce was no t found in o u r o b se r\'a tio n o f the Lugol- fixed specim ens. S ourn ia (1972) has rep o rted d iffe ren t angles o f th e la tera l ex ten ­ sions fro m fixed specim ens (Figs 5-6). T he m ovem en t occu rred w hen the specim en w as o b serv ed a t a h igh m agnification w ith high light intensity, and took ab o u t 10 seconds. T he changes in th e shape o f this live specim en o f Brachidinium , and the com m on changes o f m orpho logy during the life cycle o f u n arm o u red d inoflagel­ la tes w ith e longate ex tensions (e.g., K onovalova, 2003) cast som e doub ts o n the validity of all species o f B rachid in ium o th e r than the type. The type species o f the closely re la ted genus A ste ro d in iu m is also supposed to show a high m orphological variab ility (G om ez, 2003a). M ost records o f B rachidinium are from the 1970s, and species such as B. catenatum (Fig. 4) and B. brevipes (Fig. 8) have n o t b een re p o rted a fte r the in itia l descrip tions. The descrip tion o f B rachidinium brevipes, w ith a ro ugh surface, is based on m orphological fea tu res th a t can be considered as intraspecific variables in o th e r dinoflagellates. H ie m orphology o f B rachid in ium taylorii (Fig. 7) is the sam e as som e form s o f B. capitatum . B rachidinium catena­ tum (Fig. 4) is a doub tfu l taxon according to Taylor (1967). Brachidinium capita­ tum req u ires fu rth e r stud ies on the m orphological variab ility as well as for un ique characteristics such as secondary nuclei and m oveable extensions. A cknow ledgem ents. This study was supported by G rant-in-aid for Creative Basic R esearch (12NP0201, D O B IS) from the MEXT, Japan. We are grateful to Dr. K. N akata, the scientists and crew of Soyo M a m (N ational R esearch Institu te of Fisheries Science), R /V H a ku h o M a ru (O cean R esearch Institute, the University of Tokyo) and R /V M ira i (JA M STEC ) for their kind help in collection of samples during the cruises to the Kuroshio; Sulu Sea (KH02-4) and the w estern equatorial Pacific O cean (M R02-K06). We thank collaboration of Prof. Y. Fukuyo and Y. Nagahama. Thanks to Dr. N eelam R am aiah for correction of the English. 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TA Y LO R F.J.R., 1967 — Phytoplankton of the South W estern Indian Ocean. N ova H edw ig ia 12: 433-476. TA Y LO R F.J.Rl, 1980 — O n dinoflagellate evolution. BioSystem &13: 65=408..,.==.-=^ VILICIC D., 1998 — Phytoplankton taxonom y and distribution in the offshore southern A driatic. N atu ra C roatica 7:127-141. 2 2 0 Acta Bot. Croat. 64 (2). 263-274,2005 CODEN: ABCRA 25 ISSN 0365-0588 Is Karenia a synonym of Asterodinium-Brachidinium (Gy mnodiniales, Dinophyceae)? F e r n a n d o G o m e z '* , Y u k io N a g a h a m a ,̂ H a r u y o sh i T a k a y a m a ,̂ K en F u r u y a ^ ' Station Marine de Wimereux, Université des Sciences et Technologies de Lille, CNRS UMR 8013 ELICO, 28 avenue Foch. BP 80, F-62930 Wimereux, France. - Department of Aquatic Biosciences, University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657,Japan. ̂Hiroshima Prefectural Fisheries and Marine Technology Center, Hatami 6-1-21. Ondo-cho, Kure Hiroshima 737-1205, Japan From material collected in open waters of the NW and Equatorial Pacific Ocean the de­ tailed morphology of brachidini aceans based on two specimens o f Asterodinium g racile is reported for the first time. SEM observations showed that the straight apical groove, the morphological characters and orientation of the cell body were similar to those described for species of Karenia. Brachid in ium 2cnà Asterodinium showed high morphological vari­ ability in the length of the extensions and intermediate specimens with Kam iia . Karenia-\\\ie. cells that strongly resemble Brachid in ium and Asterodinium but lacking the extensions co-occurred with the typical specimens. The life cycle and morphology of Karenia papilionacea should be investigated under natural conditions because of the strong simi­ larity with the brachidiniaceans. Key words: Phytoplankton, Asterodinium, Brachidin ium , Brachydinium, Gymnodinium, Karenia, Dinophyta. apical groove, SEM, Pacific Ocean. Introduction Fixatives, such as formaline or Lugol. do not sufficiently preserve unarmoured dino­ flagellates to allow species identification. Body shape and morphology often change dur­ ing the process o f fixation so that even differentiating between the genera Gymnodinium Stein and Gyrodinium Kofoid et Swezy is difficult (E l b r a c h t e r 1979). Most of the origi­ nal descriptions, often based on fixed specimens, were insufficiently detailed and the mor- phological characters for the differentiation of the species were sparse. T a k a y a m a (1985) developed a scanning electron microscopy (SEM) technique that allowed the observation of the apical grooves (acrobase) in some gymnodinioid cells. A revision by D a u g b je r g et al. (2000) combined large subunit (LSU) rDNA sequences, ultrastructure and chloroplast * Corresponding address: femando.gomez@titoplancton.com, fax +44 20 79425054 Present address: Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom ACTA BOT. CROAT. 64 (2), 2005 263 2 2 1 mailto:femando.gomez@titoplancton.com GÔMEZ F.. N a g a h a m a Y.. T a k a y a m a H ., F u ruy a K. pigment composition, which allowed for the division of the large heterogeneous genus G ym no d in iu m into four genera: G ym no d in iu m sensu stricto, with a horseshoe-shaped api­ cal groove and peridinin as the main carotenoid; A k a s h iw o G. Hansen et Moesüiip, with a clockwise spiral apical groove and peridinin; K a re n ia G. Hansen e t Moestrup, with a straight apical groove and fucoxanthin; and K a r lo d in iu m J. Larsen, with a short straight apical groove, a ventral pore, and fucoxanthin. Later the genus Takayam a de Salas, Bolch, Botes e t Hallegraefif, with sigmoid apical grooves, was also erected (De S a l a s et al. 2003). Since then, the description o f new species of the genus K a re n ia has proliferated (e.g.. B o t e s et al. 2003; H a y w o o d et al. 2004). Unialgal cultures have been established by isola­ tion of vegetative cells from coastal waters and maintained under laboratory conditions. The abundant material available allows detailed studies on the ultrastructure, pigment and toxin composition and molecular phylogeny. Little is known on the morphology and the life cycle o f these species under natural conditions. There are few records of gymnodinioid cells identified at the species level in open wa­ ters. Morphological characters such as the occurrence of body extensions facilitate identifi­ cation under routine analysis in taxa such as G y ro d in iu m fa lc a tu m Kofoid e t Swezy (= G ym n o d in iu m fu s u s Schiitt pro parte). Observations of live specimens o f G. fa lc a tu m from natural samples (E l b r Ac h t e r 1979; Y o sh im a t s u 1990) or temporal cultures (K o ­ n o v a l o v a 2003) showed high morphological variability and fast changes of cell shape and length of extensions. Stages of the life cycle o f G. fa lc a tu m were described as separate spe­ cies, such as P s e lio d in iu m v a u b a n ii Soumia (K o n o v a l o v a 2003). The occurrence of extensions is the main character of the unarmoured genera B ra ­ c h id in iu m F.J.R Taylor and A s te ro d in ium Soumia. which species were described from single or a few preserved specimens. The only known morphological characters o f the bra­ chidiniaceans were the pronounced compressed cell body, yellow-green chloroplasts and the prominent nucleus. Despite the lack of morphological data, the order Brachidiniales A.R. Loeblich III ex Soumia was established exclusively for these genera. No photomicro­ graphs o f A s te ro d in iu m were available in the literature. From Mediterranean, Atlantic and Pacific waters, G ô m e z (2003) reported a high variability in the length of the extensions among the specimens of A s te ro d in iu m . Within this context, G ô m e z (2003, p. 339) con­ cluded: »Further research should address the A s te ro d in iu m g ra c ile complex; does it consti­ tute one species with high morphological variability, depending on environmental condi­ tions, or are different species involved?« B ra c h id in iu m is more com monly recorded than A s te ro d in iu m and one section plot o f its distribution is even available (M argalef 1975). B ra c h id in iu m also showed a high vari­ ability in thé length and relative position of the extensions, being often reported as B ra c h id in iu m sp. because the specimens cannot be ascribed to any known species. No de­ tailed study on the m orphological characters o f B ra c h id in iu m was available. Front Lugol-fixed specimens and one live specimen, G ô m e z et al. (2005) reported details of the m orphology of B ra c h id in iu m . So u r nia described 4 o f the 5 species of brachidiniaceans. From the same samples o f his records, So u r n ia illustrated gym nodinioid cells that he considered close to B ra c h id in iu m (So u r nia 1972, p. 157). Later So u r n ia (1986) hypoth­ esized that the Brachidiniales constitute a part o f the life cycle of more common dinoflagellates. Despite the scarcity of specimens of brachidiniaceans available and the delicacy of them, by using the T a k a y a m a ’S method, we have successfully obtained the first SEM pic­ 264 ACTA BOT. CROAT. 64 (2), 2005 222 IS KARENIA A S Y N O N Y M OF A S TE R O D IN IU M -B R A C H ID IN IU M l tures of a member of the order Brachidiniales based on two specimens o f A s te ro d in iu m g ra c ile Soumia. The morphological chai acters o f A s te ro d in iu m were similar- to those of some species o f the genus K a re n ia . Gymnodinioid cells which appearance strongly resem­ bled specimens of B ra c h id in iu m and A s te ro d in iu m but lacking the extensions co-occurred with the typical B ra c h id in iu m and A s te ro d in ium . The life cycle and the morphology of some species of K a re n ia should be investigated under natural conditions because they may correspond to forms of B ra c h id in iu m A s te ro d in iu m . Material and methods Sample collection and light microscopical observations were as in G ô m e z et al. (2004, 2005). For SEM, specimens were isolated with a capillar-y from sedimentation chambers and adhered to poly-L-lysine-coated cover-slip. Fixed cells attached to the cover-slip were rinsed twice in distilled water for 5 min each. Cells were then dehydrated through an etha­ nol series, transferred into isoamyl acetate (T a kayam a 1998), dried in a critical point drier (HCP-2, Hitachi, Japan), and coated with Au-Pd. Observations were made using SEM (S-430 and S-800, Hitachi, Japan). Results and discussion A sterodinium The new records of A s te ro d in iu m from the w estem Pacific Ocean (Tab. 1) showed a high variability in the length of the extensions as previously reported by G ô m e z (2003). Observations w ith Nomarski differential interference contrast (DIG) optics showed the transverse flagellum; however the insertion point was not clearly revealed (Figs. 1, 2). With SEM, the insertion point was observed in two specim ens o f A s te ro d in iu m g ra c ile (Figs. 8-15). The ventral view corresponded to the nucleus in the left hyposom e. The me- Tab. 1. Records of Asterodinium from the Pacific Ocean. Date, depth (m), geographic coordinates (latitude, longitude), and dimensions: width at the level of the cingulum (pm); total length (pm) of each record. Records from the vicinity of the Kuroshio Cunent can be found in Gô m ez (2003). Karenia-\ike cells are omitted. Taxon Date Depth Latitude Longitude Wide Length Asterodinium gracile 16 Nov 2002 50 5°11’N 124=05'E 25 65 Asterodinium g racile (Figs 8-15) 16 Nov 2002 50 5 °H ’N 124=05'E 23 55 Asterodinium g racile (Fig. 3) 17 Nov 2002 30 ” Asterodinium gracile 17 Nov 2002 75 5°N 121=E 23 60 Asterodinium gracile 19 Nov 2002 75 7°25'N 121=12’E 20 100 Asterodinium gracile 19 Nov 2002 50 7°25'N 121=12’E 24 105 Asterodinium gracile 03 Dec 2002 30 8°50'N 121=48'E 20 - Asterodinium gracile 18 Jan 2003 120 0° 170°E 21 110 Asterodinium gracile 17 Jan 2003 100 0° 165=E 22 60 Asterodinium sp. (Figs 4-7) 23 Jan 2003 120 0° 170=W 32 - ACTA BOT. CROAT. 64 (2), 2005 265 223 g ô m e z F .. N a g a h a m a Y., T a k a y am a H ., F u ruy a K. dian cingulum was descending and displaced by the cingulum width (Figs. 10, 14). The longitudinal flagellum was not observed with SEM, having probably been lost during sample preparation. The cavity that appeared below the term inal part o f the transverse flagellum might correspond to the place of the insertion o f the longitudinal flagellum (Figs. 11, 15). A vertically oriented cingular ridge runs between the two points o f flagellar insertion (Fig. 15). The ventral ridges are present in species o f Karenia and have an intercingular tubular structure that traverses the proxim al and distal ends o f the cingulum (H a y w o o d et al. 2004). The sulcal intrusion on the epitheca o f A. gracile is open and extends to left o f the apex (Fig. 14). A straight groove with rolled margins was visible in the central apical extension of both specimens (Figs. 9 ,13 ). The sulcus was not well defined under SEM (Figs. 11, 15). These m oiphological characters were sim ilar to those described for Karenia papilionacea Haywood el Steidinger or K. bicuneiformis Botes, Sym et Pitcher {=K. bidigitata Haywood et Steidinger) ( B o t e s et al. 2003; H a y w o o d et al. 2004). In Asterodinium gracile the carina or apical protm sion is ex­ tremely elongated and is named the central apical extension (Fig. 23). With DIC and SEM, trichocysts were observed in Asterodinium gracile, sometim es form ing clusters. SEM observations showed that the basal part o f the trichocysts was thicker that the term i­ nal hair (Fig. 13). The species Asterodmium spinosum Soum ia was described from a sin­ gle fixed specimen based on the occurrence o f two small spines in the central apical ex ­ tension ( S o u r n ia 1972). However, the present study reveals that these »spines« may be the thick basal part o f the fragile trichocysts. Asterodinium spinosum should not he con­ sidered a species separate from the type species. One of the specimens o f Asterodinium showed short extensions, being an intermediate between the typical Asterodinium and the Asterodinium that lacks any extensions (Fig. 3). Strongly dorso-ventrally compressed gymnodinioid cells with short lobulate extensions were observed showing the distinctive chloroplasts, the straight apical groove and the prominent nucleus of Asterodinium (Figs. 4-7). B rachidinium Light microscopy obseiwations of Lugol-fixed specimens and one live specimen of Brachidinium capitatum showed morphological characters such as a short straight apical groove (Fig. 20). The orientation and moiphology o f the cell body were similar to those in Asterodinium (Figs. 16, 18, 20), although the details o f the intercingular region were not clearly visible. Several of the specimens o f B. capitatum showed a darker area in the right hyposome (Figs. 16, 18, 26). This region appeared with a variable size and colour, often similar to the brown colour of the nucleus o f the Lugol-fixed specimens. After DAPI-stain­ ing this region fluoresced when excited with UV light hut less bright than the dinokaryon. G ô m e z et al. (2005) interpreted this darker'area ls a secondary nucleus in B.~cdpitdtuih as occuiTed in some freshwater dinoflagellates. However this region varied in size, shape and colour among the Lugol-fixed specimens (Figs. 16, 18) more than would be expected for a secondary nucleus. The occurrence of an accumulation body in the right hyposome of B. capitatum appeared a more probable explanation. The role of the accumulation bodies in dinoflagellates is poorly understood. It is believed to be in an endocytic pathway function­ ing as a lysosome (Z h o u and F r it z 1994). Among the species o f Karenia, K. papilionacea was also chaiacterised by an accumulation body that was visible in the right hyposome in 10% of cells under culture (H a y w o o d et al. 2004). 266 a c t a b o t . CROAT. 64 (2). 2005 224 IS A SYNONYM I 4̂; -ù t -TF Figs. 1-7. DIC photomicrographs of the ventral view of Asterodinium gracile in different focuses (30°N; 138°E, 80 m depth). See the nucleus in the left hyposome and the transverse flagellum. Figs. 3-7. LM micrographs o f Asterodinium. Fig. 3. Specimen o f Asterodinium in ventral view with short extensions from the Celebes Sea. Figs. 4-7. Specimen of Aste­ rodinium with lobulate extensions from the Central Equatorial Pacific. Figs. 4, 6. Dorsal views. Figs. 5, 7. Ventral and lateral views respectively. The arrows point to the nucleus, transverse flagellum and the apical groove (acrobase). AG=apical groove; TF= transverse flagellum; N=nucleus. Scale bars = 20 pm. Large ex tensions are one o f the m ain characteristics o f the B rach id in ia les. S pecim ens lacking the extensions are hai'd to assign to B rach id in ium or A sterod in ium and are co n se ­ quently poo led as un identified gym nodin io id cells un d er rou tine m icroscop ical ana lysis o f fixed phytoplankton . In the present study gym nodin io id cells that strong ly resem bled ACTA BOT. C R O A T. 64 (2), 2005 267 225 G ômez F„ N a gaham a y ., Ta kayam a H ., Fu r ü y a K. W ; ® ^ . / - Y f e s ^ 1 M jî rbr:... » - * 6 . . > .. . r V S " 4' " y . • \ * * .. Figs. 8-15 . SEM pictures o f two specimens o f A s te ro d in ium g ra c ile in the ventral view. Figs 8-11. Specim en with long extensions collected from the Kuroshio C urrent region (33° 30’N; 138°E, 100 m depth). Fig. 9. Detail o f the central apical extension. See the straight apical groove or acrobase and the trichocyst pores. Figs. 10-11. Detail o f the central body and the location o f the insertion o f the transverse flagellum. Fig. 11. The arrow points to a cavity where the longitudinal flagellum might arise. Figs. 12-15. Specim en w ith shorter extensions collected from the Celebes Sea (5°1F N ; 124°05'E , 50 m depth). Fig. 13. Detail o f the cen­ tral apical extension. See the apical groove and trichocysts. Figs. 14-15. D etail o f the central body. Fig. 15. A ventral ridge nins betw een the two points o f flagellar insertion. The arrow below the ventral ridge points to a cavity where the longitudinal flagellum might arise. A G=Apical groove; TF=transverse flagellum ; TC=tiichocyst; V R=ventral ridge; ICTS= Intercingular tubular structure. Scale bars = 20 pm. 268 A CTA BOX. C R O A T. 64 (2), 2005 226 IS KARENIA A S Y N O N Y M OF A S T E R O D IN IU M -B M C H ID IN IU M I B. c a p ita tu m cells lacking the extensions co-occurred with the typical B. c a p ita tu m (Figs. 17, 19, 26). Several o f the typical B. c a p ita tu m showed accum ulation body o f variable size and colour in the right hyposome (Figs. 16,18), which was also visible in the speci­ mens lacking the extensions (Fig. 19). These gym nodinioid cells were also reported in previous studies including records o f B. ca p ita tu m . In the SW Indian Ocean, So u r nia (1972) described two new species o f B ra c h id in iu m and also found the type species with variable morphology. From the same samples, So u r n ia illustrated gym nodinioid cells that he considered close to B ra c h id in iu m (Fig. 25). O bservations o f live specim ens of B ra c h id in iu m (L éger 1971 ; G ô m ez et al. 2005) have even showed the extensions to be moveable. In cultures, the carina o f K a re n ia p a p U io n a ce a contracts forw ard when the cells are stressed (H ayw ood et al. 2004, p. 170). So u r n ia ( 1972, p. 157) also illustrated the gymnodinioid cell folded with the carina contracted forw ard (Fig. 25). B ra c h id in iu m c a p ita tu m (Fig. 26) and K. p a p U io n ace a co-occur in the coastal waters o f the south of Ja­ pan (misidentified as K a re n ia b re v is (Davis) G. Hansen e t M oestrup) and in other warm to temperate waters ( I iz u k a 1976; H ayw ood et al. 2004). From the eastern M editerranean Sea, A bbo ud -A bi Saab (1989) found B. c a p ita tu m and also illustrated several unidenti­ fied gym nodinioid cells with sim ilar m orphology to the K a re n ia - l ik e cells reported in Sour nia (1972) and in the present study (Figs 17, 19). K a re n ia p a p U io n a c e a and B. ca p ita tu m are both cosmopolitan taxa that appear in surface waters in low abundance (M argalef 1975; H ayw oo d et al. 2004). In the table 2 the m orphological and ecological characters o f B. c a p ita tu m and K. p a p U io n ace a have been compared. The distinctive m orphological characters o f K . p a p i- lio n a ce a coincided with B. c a p ita tu m (Tab. 2, Figs 16-20). The K aren ia -M ke, cells that co-occurred with B. c a p ita tu m showed morphology sim ilar to that o f the Lugol-fixed cells o f the culture o f K. p a p U io n ace a at the Cawthron Institute, New Zealand (Fig. 21 ). According to H ayw ood et al. (2004), K a re n ia b ic u n e ifo rm is {= K . b id ig ita ta ) often co-occurs witli K. papU ionacea . In the present study several specimens were tentatively identified as K. b icu n e ifo rm is , also co-occurring with B. c a p ita tu m and the K aren ia -V ikc cells (Fig. 22). K a re n ia papU ionacea and K. b ic u n e ifo rm is are very close from morpholog­ ical and phylogenical points o f view (H ayw ood et al. 2004). No studies are available on the projection o f the cell body extensions in unarmoured dinoflagellates. Z irbel et al. (2000) reported that the length o f the extensions o f the ar­ moured dinoflagellate C era to co rys h o rr id a Stein varied as an adaptive strategy according to water motion. Specimens lacking the extensions appeared as early as 1 h after an in­ crease in turbulence. Cells with long extensions were transforming into cells with short or no extensions. This phenomenon was reversible and the extensions reappeared after a re­ duction in turbulence (Z irbel et al. 2000). The expansion of the cell body with the projection of extensions is expected to be easier for unarmoured dinoflagellates. Beyond the high shape plasticity with fast contractions of the carina of K. papU ionacea , a high variability in cell size in cultures is also obseiwable. H ayw ood et al. (2004, p. 175) reported, »Cellular size measurem ents are given as ranges, reflecting small to large cells present in cultures that were not separated into size classes be­ cause o f the intergradations between sizes and because the significance o f the size classes cannot be addressed until the life cycle of these species is known«. ACTA BOT. CROAT. 64 (2), 2005 269 227 g ô m ez F., N a g a h a m a Y .. Ta k a y a m a H ., Fu r u y a K. Figs. 16 -22 . L M m icrographs o f B ra c h id in iu m c a p ita tu m w ith and lacking the extensions, K a - ̂ 're n ia p a pU ionacea and K. cf. b ic u n e ifo rm is (= K . b id ig ita ta ) . Ail L ugol-fixed specim ens except Fig. 20, Fig. 16. Ventral view o f a specim en o f B ra c h id in iu m w ith a prom inent ac­ cum ulation body from the Philippine Sea (32°N ; I38°E , 30 m depth). Fig. 17. K a - ren ia -likQ cell that strongly resem bles B ra c h id in iu m but lacking the extensions (32°N ; 138°E, 80 m depth). Fig. 18. D orsal view o f a specim en o f B ra c h id in iu m w ith a less m arked accum ulation body (0°; 160°E, 0 m depth). Fig. 19. Karenia-W ke cell from the sam e sam ple as figure 16 w ith an accum ulation body (32°N; 138°E, 30 m depth). Fig. 20. Back focus o f the cell body o f a live specim en o f B. cap ita tu m in the dorsal view (see G ô m e z et al. 2005). Fig. 21. L ugol-fixed specim en o f K. papU ionacea from the culture o f the C aw thron Institu te, N ew Z ealand. Fig. 22. Tentatively K a re n ia b ic u n e ifo rm is (=K . b id ig ita ta ) (0°; 175°E, 15 m depth). A B =accum ulation body; A G=A pical groove; N -n u - cleus. Scale bars = 20 pm. 270 ACTA BOT. CROAT. 64 (2). 2005 2 2 8 IS KARENIA A S Y N O N Y M OF A S TE R 0D IN IU M -B R A C H ID IN IU M 7 Tab. 2. Comparative moiphological and ecological chaiacteristics of Brachid in ium capitatum (Lugol-fixed specimens from open waters and one live specimen from the coastal waters of Japan). Data from Karenia papUionacea (from cultures) based on HAYWOOD et al. (2004). Character Brachidin ium capitatum Karenia papUionacea Apical groove Straight, very short and bisects Straight, very short and bisects the carina.......................... ... the carina............. Carina (apical protrusion) Pointed Pointed Dorsoventral compression Moderate Moderate Nucleus shape Spherical to slightly oval Spherical to slightly oval Nucleus location Left hyposome Left hyposome Hyposome shape Bilobed, centrally excavated Bilobed, centrally excavated Hyposome excavation Pronounced Pronounced Cell width at the cingulum level 25-55 pm 1 8 ^ 8 pm Cingulum Median, descending and dis­ Median, descending and dis­ placed by the cingulum width placed by the cingulum width Sulcal intmsion on the epitheca No visible from Lugol-fixed Open sulcus extends to left of specimens apex Chloroplast number Many Typically 2-20 chloroplasts per cell Chloroplast shape Round to reniform in cell body, elongate plastids in the exten­ sions Round to reniform Chloroplast colour Yellow-green Yellow-green Fucoxanthin No tested yes Accumulation body occurrence -25% of the specimens in nature 10% of the specimens in culture Accumulation body number 1 1 Accumulation body location Right hyposome Right hyposome Accumulation body shape Spherical to oval Spherical to oval Accumulation body size Variable Variable Cell movements Carina and extensions change Carina contracts forward to of shape and length overlap the epitheca Geographical distribution Cosmopolitan (temperate to Cosmopolitan (temperate to warm) warm) Ecological distribution Surface, coastal to open waters (M a r g a l e f 1975) Surface, coastal to open waters Abundance in natural waters Low (M a r g a l e f 1975) Low (<1000 cells L“ )̂ Period of max. abundance Summer Sum m er' -------------- - - ' - Life cycle Unknown Unknown The life cycle and morphology of species such as K. papUionacea should be investi­ gated under natural conditions because they may correspond to a life stage of brachidinia- ceans. There are no reasons to retain the order Brachidiniales because the morphological characters of Brachidinium-Asterodinium do not differ from those in Karenia. ACTA BOT. CROAT. 64 (2), 2005 27! 229 g ô m e z F., N a g a h a m a Y., T a k a y a m a H ., F u r u y a K. rA Figs. 23-26. Line drawings of Asterodinium, Brachidinium and the related Karenia cell. Fig. 23. Typ­ ical Asterodinium gracile. Fig. 24. Karenia-Vikc cell related to the brachidiniaceans. Fig. 25. Two views of the Karenia-Wke cell related to Brachid in ium according to S o u rn ia (1972, p. 157). Fig. 26. Typical Brachidinium capitatum. Acknowledgements This study was supported by Grant-in-aid for Creative Basic Research (12NP0201, DOBIS) from the M E X t, Japan. We thank to the scientists and crew o f R N Soyo (National Research Institute o f Fisheries Science), R/V Hakuho M a m (Ocean Research In­ stitute, University of Tokyo) and R/V Mirai (JAMSTEC) for their kind help in the collection o f samples during cruises to the Kuroshio region, Sulu and the Celebes Seas (KH02-4) and the Equatorial Pacific Ocean (MR02-K06). We thank to J. Adamson for the micrograph of K. papUionacea from the culture of the Cawthron Institute, Nelson, New Zealand and thank S. Fraga for his suggestions. EG. acknowledges the support of the European Com­ mission (ICB2-CT-2001-80002). This is a contribution to the French IFB ’Biodiversité et Changem ent Global’ program. 272 ACTA BOT. CROAT. 64 (2), 2005 230 IS KARENIA A SYNONYM OF A S TE R O D IN IU M -B R A C H ID IN IU M I References A b b o u d -A bi S a a b , M., 1989: Les dinoflagellés des eaux côtières libanaises - espèces rares ou nouvelles du phytoplancton marin. Lebanese Sci. Bull. 5, 5-16. B o t e s , L., S y m , S.D., P it c h e r , G.C., 2003: K a re n ia c r is ta ta sp. nov. and K a re n ia h ic ii- n e ifo rn iis sp. nov. (Gymnodiniales, Dinophyceae): two new K a re n ia species from the South African coast. Phycologia 42, 563-571. D a u g b je r g , N.. H a n s e n , G., L a r s e n . J., M o e st r u p , 0 ., 2000: Phylogeny of some o f the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera o f unarmoured dinoflagellates. Phy­ cologia 39, 302-317. D e S a l a s . M.F., B o l c h , C.J.S., B o t e s , L., N a s h , G ., W r ig h t , S.W., H a l l e g r a e f f , G.M., 2003: Takayam a (Gymnodiniales, Dinophyceae) gen. nov., a new genus o f unarmoured dinoflagellates with sigmoid apical grooves, including the description of two new spe­ cies. J. Phycol. 39, 1233-1246. E l b r a c h t e r , M,, 1979: On the taxonomy of unarmoured dinoflagellates (Dinophyta) from the northwest African upwelling region. M eteor Forschungs-Ergebnisse D. 30, 1-22. G ô m e z , R, 2003: New records o i A s te ro d in iu m Soum ia (Brachidiniales, Dinophyceae). N ova H e d w ig ia 77. 331-340. G ô m e z , F , N a g a h a m a , Y., F u k u y o , Y , F u r u y a , K., 2004: Observations on C e ra to - p e r id in iu m (Dinophyceae). Phycologia 43, 416-421. G ô m e z , R, Y o sh im a t s u , S., F u r u y a , K., 2005: M oiphology of B ra c h id in iu m c a p ita tu m RJ.R. Taylor (Brachidiniales, Dinophyceae) collected from the western Pacific Ocean. Cryptogamie Algol. 26, 165-175. H a y w o o d , A.J., S t e id in g e r , K.A., T r u b y , E.W., B e r g q u is t , P R ., B e r g q u is t , P.L., A d a m ­ s o n , J., M a c k e n z ie L., 2004; Comparative morphology and molecular phylogenetic analysis o f three new species of the genus K a re n ia (Dinophyceae) from New Zealand. J. Phycol. 40, 165-179. I iz u k a , S., 1975: On occurrence of similar organisms to G ym n o d in iu m hreve Davis in Omura Bay. Bull. Plankton Soc. Japan 21, 109-112. K o n o v a l o v a , G.V., 2003: The life history o f G y ro d in iu m fa lc a tu m and validity o f Pse- lio d in iu m v a u b a n ii (Dinophyceae). Russian J. Mar. Biol. 29, 167-170. L é g e r , G., 1971: Les populations phytoplanctoniques au point 42°47'N , 7°29’E Green­ wich (Bouée laboratoire du COMEXO/CNEXO). Généralités et premier séjour. Bull. Inst. Océanogr. Monaco 69 (1412), 1-42. M a r g a l e f , R., 1975: Composiciôn y distribuciôn del fitoplancton marino en la region de afloramiento del NW de Africa, en m aizo de 1973 (Cam pana »Atlor II» del »Com ide de Saavedra»). Result. Exped. Cient. B /0 Com ide 4, 145-170. S o u r n ia , A., 1972: Une période de poussées phytoplanctoniques prés de Nosy-Bé (M ada­ gascar) en 1971. Espèces rares ou nouvelles du phytoplancton. Cah. O.R.S.T.O.M., sér. océanogr. 10, 151-159. S o u r n ia , A., 1986: Atlas du phytoplancton marin. Vol. I: Introduction, Cyanophycées, Dictyochophycées, Dinophycées et Raphidophycéei’. Editions du CNRS, Paris. ACTA b o t . CROAT. 64 (2), 2005 273 231 g ô m ez F., N agaham a Y.. Ta k a y a m a H ., F uruya K. T a k a y a m a , H., 1985: Apical grooves of unarmoured dinoflagellates. Bull. Plankton Soc. Japan 32, 129-140. T a k a y a m a , H., 1998: Morphological and taxonomical studies on the free-living un­ armored dinoflagellates occurring in the Seto Inland Sea and adjacent waters. Ph.D. Thesis, The University of Tokyo. Y o s h im a ts u , S., 1990: G y ro d in iu m fa lc a tu m Kofoid et Swezy. In: Fukuyo, Y., Takano, H., Chihara, M., Matsuoka, K. (eds.). Red tide organisms in Japan, an illustrated taxonomic guide, 60-61. Uchida Rokakuho Publ. Co. Ltd., Tokyo. Z h o u , J., F r i t z L., 1994: The PAS/accumulation bodies in P ro ro c e n tru m lim a and P ro - ro ce n tru m m acu losum (Dinophyceae) are dinoflagellate lysosomes. J. Phycol. 30, 3 9 ^ . Z ir b e l , M.J., V e r o n , R. L a t z , M L, 2000: The reversible effect of flow on the morphology of C era to co rys h o rr id a (Peridiniales, Dinophyta). J. Phycol. 36, 46-58. 274 a c t a BOT. CROAT. 64 (2), 2005 232 A lgae Volume 21(4): 445-452, 2006 The Dinoflagellate Genera Brachidinium, Asterodinium, Microceratium and Karenia in the Open SE Pacific Ocean Fernando Gômez Station Marine de Wimereux, Université des Sciences et Technologies de Lille, FRE 2816 ELICO CNRS, 28 aivnne Foch, BP 80, F-62930 Wimereux, France The morphometry and distribution of the unarmoured dinoflagellates Brachidinium capitatum FJ.R. Taylor, Asterodinium gracile Sournia, Microceratium orstomii Sournia and the toxic species Karenia papUionacea 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 Peru-Chile Current). Brachidinium capitatum and K. papUionacea often co-occurred, predominat­ ing B. capitatum in offshore surface waters. Asterodinium gracile was recorded at the bottom of the eu photic 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, hanuful algae bloom, Karenia papUionacea, Microceratium, phytoplankton, SE Pacific Ocean INTRODUCTION Most of the species of the genus Gymnodinium Stein were described during the late 1800's and early 1900's. Very little progress has been made since then and the taxonomic system has therefore remained almost unchanged since the 19*̂ ' century. Biecheler (1934) using a silver-impregnation method observed for the first time the apical groove in Gymnodinium. Takayama (1985) based on scanning electron microscopy (SEM) showed several types of apical grooves in unarmoured dinofla­ gellates. Daugbjerg et al. (2000) based on light microscopy, SEM, pigment composition and LSU rDNA sequences split Gymnodinium into four genera: Gymnodinium sensu stricto, Akashiwo G. Hansen et Moestrup, Karlodinium J. Larsen and Karenia G. Hansen et Moestrup. Since then, the description of new species of Karenia characterized by a short straight apical groove, with fucoxanthin and lacking peridinin, has proliferated. In some cases, a single species has been described under different names such as K. bicuneiformis Botes, Sym et ■̂ Corresponding author (fernando.gomez@fitoplancton.com) Pitcher and K. bidigitata Haywood et Steidinger and other taxa may be conspecific such as K. longicanalis Yang, Hodgkiss et G. Hansen and K. umbella de Salas, Bolch et Hallegraeff (Yang et al. 2001; Botes et al. 2003; de Salas et al. 2004; Haywood et al. 2004). Among the recently described species, Karenia papil- ionacea Haywmod et Steidinger showed several peculiar characteristics in cultures with an unusual plasticity and high size variability. In culture, K. papUionacea is also able to move forward the prominent apical process (Haywood et al. 2004, p. 170). Other close species,. K. bicuneiformis, showed pointed or bulbaceous antapical tips in natural waters that were rounded when the species is cultured (Haywmod et al. 2004, p. 173). The species of Karenia were described based on abundant materials cultured under optimal conditions for growth that does not reproduce the low turbulence and olig- otrophic conditions of the open ocean. Consequently lit­ tle is known on the morphology and the life cycle of species such as K. papUionacea under natural conditions. The dinoflagellate Brachidinium capitatum F.J.R. Taylor is a flattened unarmoured taxon easily identifiable by the four radiating elongate antapical extensions, apical process, numerous yellow-green chloroplasts and promi­ 233 mailto:fernando.gomez@fitoplancton.com 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. hre- vipes Sournia. From the same location, Sournia (1972a, b) described two closely related genera: Asterodinium Sournia with the species A. gracile Sournia and A. spin- osum Sournia and Microceratium Sournia with the species M. orstomii Sournia. Asterodinium differs from Brachidinium on having two elongate extensions radiat­ ing from the hyposome and three extensions from the episome. In comparison with Asterodinium, Microceratium Sournia has only one extension in the episome and two extensions in the hyposome. Co-occurring with these records, Soumia found gymnodinioid cells that he con­ sidered close to Brachidinium, illustrating the species recently described as Karenia papUionacea (Soumia 1972b, p. 157; Haywood et al. 2004, p. 171). Later Sournia (1986, p. 49) with the sentence "il pourrait s'agir ici de stades de développement d'autres dinoflagellés plus notoires" was hypothesizing that the brachidiniaceans, members of the genera Brachidinium, Asterodinium and Microceratium, constitute life stages of more common dinoflagellates. The brachidiniaceans have remained under-investigat­ ed during decades. Gômez et al. (2005a, b) based on light and scanning electron microscopy revealed the morpho­ logical similarities among Brachidinium capitatum, Asterodinium gracile and Karenia papUionacea. These three taxa coincided in distinctive morphological characters such as the straight apical groove, cingulum-sulcus junc­ ture, prominent nucleus in the left hyposome, numerous yellow-green chloroplasts, among otner cMTacters (Gômez et al. 2005b). Consequently the Sournia's (1986) hypothesis reappeared and the brachidiniaceans may be life stages of common coastal species that are able to pro­ ject body extensions. In coastal waters, brachidiniaceans with no extensions may be polled as unidentified gymnodinioid cells under routine microscopical analysis or refereed as Karenia brevis-like cells before the descrip­ tion of K. papUionacea (Iizuka 1975; Fraga and Sanchez 1985; Nézan 1998). Within this context, a cruise along a transect of 7500 Km from the Marquesas Archipelago to the Chilean 5”S- T'̂ .HNL 15'S- EGY Longitude Fig. 1. Map of the sampling stations during the BIOSOPE cruise in the SE Pacific Ocean. coasts through the severe oligotrophic waters of the South Pacific Gyre (Claustre and Maritorena 2003) pro­ vides the opportunity to investigate the distribution of the brachidinianceans and K. papUionacea under different trophic regimes. The present study also investigates the morphometry of Brachidinium capitatum, Karenia papil- ionacea and Asterodinium gracile. Microceratium orstomii has been recorded for the first time since the initial description. Intermediate specimens among these gen­ era, with variable disposition and size of the body exten­ sions are illustrated. The hypothesis of the conspecifity of these taxa is reported. MATERIALS AND METHODS Samples were collected at 12 stations from 5 to 270 m depth during the BIOSOPE (Biogeochemistry and Optics South Pacific Experiment) cruise on board R/V L'Atalante from 26 October to 12 December 2004 (Fig. 1). Eighty three samples collected by Niskin bottles were preserved with acidified Lugol's solution and stored at 5°C. Samples of 500 mL were concentrated via sedimentation in glass cylinders. Along 6 days, the top 450 mL of sam­ ple was progressively slowly siphoned off with small- Sofe tubing. Fift^mî? of conce®ale“ whole water was settled in composite settling chambers. The entire chamber was scanned at 200x with an 1X71 inverted Olympus microscope equipped with a DP70 Olympus digital camera and each specimen was pho­ tographed and measured at 400x with the DP70-BSW software (Olympus, Tokyo, Japan). The percentage of surface irradiance at each depth was calculated from underwater PAR (Photosynthetic Active Radiation, 400-700 nm) profile performed by a PNF-300 Profiling Natural Fluorometer sensor (Biospherical Instruments, San Diego, U.S.A.). The limit of the euphot- 234 Gômez: Bmcindimum, Asterodinium, Microceratium and Karenia 447 Karenia papUionacea Brachidinium capitatum Asterodinium graale 30 35 40 45 50 W idth a t th e cingulum level (pm ) Fig. 2. Histograms of the width at the cingulum level of the records of A. Knrnia papUionacea, B. Brachidinium capitatum and C. Asterodinium gracile. ic zone corresponds to the depth where PAR is reduced to 1% of its surface value. The variables represented in the section plots were produced by interpolation between casts using the kriging as the gridding method in the Surfer software (Golden Software, Golden, U.S.A.). RESULTS Karenia papUionacea A total of 41 specimens have been ascribed to the "standard" K. papUionacea. The width at the cingulum level ranged from 18 to 56 pm with an average width of 33.7 ± 10 pm (Fig. 2A). Karenia papUionacea and B. capita­ tum often co-occurred and the former predominated in the surface waters of productive regions (MAR and St. 20) whereas B. capitatum prevailed in oligotrophic off­ shore stations (Figs 3A, B). The highest abundance of K. papUionacea, 12 cells was recorded at 15 m depth in open waters of the Peru-Chile Current near the Juan Fernandez Archipelago and 8 cells L“’ near the Marquesas Archipelago (Fig. 3A). However, in these regions the abundance was higher if the specimens that cannot be strictly ascribed to K. papUionacea are included (Figs 41, J) Brachidinium and Asterodinium are easily identifiable due to the distinctive body extensions. The cell body of K. papUionacea corresponded to that of Brachidinium lack­ ing the extensions, maintaining the distinctive apical process, the prominent round to oval nucleus located in the left hyposome and the yellow-green pigmentation. The cell outline of the "standard" K. papUionacea showed a butterfly (Figs 4A-C) or Mexican-hat shape (Figs 4D-F). As reported in the cultures, in the present study large specimens (>40 pm wide) of K. papUionacea co-occurred with the smaller ones (Figs 4G, H). Other specimens with an elongate ellipsoidal shape and an apex that varied greatly from a pointed process to a prominent overhang­ ing apical process could not be strictly assigned to K. papUionacea (Figs 41, J). One of these specimens showed a nucleus that occupied most of the hyposome (Fig. 41). Brachidinium capitatum A total of 29 specimens of B. capitatum were observed. The width at the cingulum level ranged from 20 to 62 pm with an average value of 39.1 ±11.5 pm (Fig. 2B). The largest dimension of Brachidinium ranged from 65 to 130 pm with an average value of 98.4 ± 27.1 pm. All the specimens of Brachidinium appeared in the MAR HNL 2 4 0 rp Stations 8 GYR 12 Stations 8 GYR 1218 2 0 m a r HNL : 20% Brachidinium capitatumKarenia ̂papilionacea ■ 0. 1% 0.1%Asterodinium gracile lo c m 90“W 80°W 14C°W Ulcroceiatium orstomii I ggm 140°W 120°W 110“W 130°W 120°W130”W Longitude 110”W lOO'W Longitude Fig. 3. Section plots of the distribution of A. Karenia papilionacea, B. Brachidinium capitatum, C. Asterodinium gracile and D. Microceratium orstomii. Abundance expressed as cells L ’. The dashed lines represent the percentage of the surface irradiance. 235 448 A lgae Vol. 21(4), 2006 Q ' / , ,.,v if SÎJV'fe-. Fig. 4. Photomicrographs of hrachidiniacean-Karenia, bright field optics. A-C. Butterfly-shaped Karenia papilionacea, D-F. Mexican hat­ shaped K. papilionacea, G-H. Large cells of K. papilionacea, I-J. Unidentified ellipsoidal Karenia (note the large nucleus in Fig. 41), K. Unidentified Karenia with the conical episome, L. Unidentified Brachidinium with the conical episome, M. Brachidinium capitatum, N. Unidentified small Brachidinium with a round episome, O. B. capitatum with extensions of different size, P-T. Specimens of Asterodinium with variable degree of development of the extensions, U. W-Y, Microceratium orstomii, V. Unidentified Karenia-like cell occurring with Fig. 4W. Location (see Fig. 1) and depth of the records: A. HNL 40 m, B. St. 20 15 m, C. GYR 120 m, D. MAR 40 n, E. St. 14 5m, F. MAR 40 m, G. St. 14 5 m, H. MAR 15 m, I. EGY 150 m, J. St. 18 30 m, K. St. 20 60 m, L. EGY 75 m, M. GYR 5 m, N. MAR 20 m, O. St. 14 5 m, P. MAR 100 m, Q. HNL 60 m, R. EGY 150 m, S. St. 8 210 m, T. St. 20 60 m, U. EGY 150 m, V-W. St. 6 170 m, X. St. 2 170 m, Y. St. 12 180 m. All the photomicrographs at the same magnification, except the figures U-Y that are reduced by a factor of 1.6. Scale bars: 20 pm. 236 Gômez: Brachidinium, Asterodinium, Microceratium and Karenia 449 euphotic zone. Its vertical distribution was wider in open waters and shallower near the Marquesas Archipelago and the Peru-Chile Current. The deepest record occurred at 170 m depth in the clearest waters associated with the South Pacific Gyre. The highest abundance, 6 cells was recorded at 30 m depth in the surrounding waters of the Marquesas Archipelago (Fig. 3B). The length of the extensions showed a high variability. Nearly all the spec­ imens had four extensions of similar length that can be interpreted as a synchronic growth of the body exten­ sions (Fig. 4M). Exceptionally one of the specimens showed two alternate extensions longer than the other ones (Fig. 40). If a non-synchronic growth of the exten­ sions is discarded, it can be speculated that Brachidinium transforms into Asterodinium by the retraction of two of the four antapical extensions and the projection of the apical process. Nearly all the specimens of Brachidinium showed the distinctive apical process with variable degree of development (Figs 4L-0). One large specimen showed a conical episome, lacking the apical process (Fig. 4L). The contour of its episome resembled that of unidentified Karenia specimens that often co-occurred (Fig. 4K). One of the specimens of Brachidinium showed the smallest dimensions observed with only 16 pm wide and one of the lateral extensions was incompletely devel­ oped. Tlie shape of the episome, round and lacking the apical process (Fig. 4N), resembled that in Karenia bicuneiformis. Both species of Karenia, K. papilionacea and K. bicuneiformis are very close genetically and coincided in the main morphological characters (Haywood et al. 2004). Despite the shape and position of the nucleus is not usually conservative in some species of Karenia, the nucleus in K. papilionacea, K. bicuneiformis, Asterodinium, Brachidinium and Microceratium was invariably located in the left hyposome. Asterodinium gracile A total of 33 specimens of Asterodinium gracile were observed. The width at the cingulum level ranged from 17 to 28 pm with an average value of 22.2 ± 4 pm, show­ ing less size variability than in B. capitatum and K. papil­ ionacea (Fig. 2C). The largest dimension of Asterodinium ranged from 35 to 200 pm (85.3 ± 57.1 pm). Nearly all the specimens were collected below the euphotic zone with the deepest record at 210 m depth (St. 8, Fig. 4S), coincid­ ing with clearest waters (Fig. 3C). None specimen appeared in surface waters and the vertical distribution of the records of Asterodinium was shallower in more eutrophic stations (Fig. 3C). Some of the shallower records of A. gracile coincided with the deeper records of B. capitatum. Karenia papilionacea and A. gracile did not usually co-occur in open waters, except a few records of elongated cells of K. papilionacea below the euphotic zone (Fig. 3A). The highest abundance of A. gracile was record­ ed at St. 18 with 10 cells L'̂ at 100 m depth (Fig. 3C). The variable degree of development of the body extensions in A. gracile is shown in Figs 4P-T. In well-developed speci­ mens, the right hyposome was reduced and the cell body contents were expanded into the adjacent body exten­ sions. However, the left hyposome cannot be reduced due to containing the prominent nucleus (Fig. 4T). M icroceratium orstom ii Four Asterodinium-like specimens with only 3 exten­ sions, intermediate between Asterodinium and Brachidinium in terms of body extensions, corresponded to the description of M. orstomii (Sournia 1972a). From the episome only arose the elongate apical process or central apical extension and from the hyposome arose 2 antapical extensions (Figs 4U, W-Y). The extensions of Microceratium tended to be longer than in the common 5- extensions Asterodinium. The width at the cingulum level of Microceratium with values between 20-25 pm was simi­ lar to that of A. gracile. Exceptionally one of the speci­ mens reached 310 pm of total length and 40 pm wide at the cingulum level, being the largest brachidiniacean observed (Fig. 4W). This specimen co-occurred with one specimen of a large elongated unidentified Karenia (Fig. 4V). The specimens of Microceratium appeared at 150 m (Fig. 4U), 170 m (Figs 4W, X) and 180 m depth (Fig. 4Y; Fig. 3D). DISCUSSION Trends in the distribution of the brachidiniaceans- Karenia papilionacea ~ ^ The type species of Brachidinium and the other species, B. taylorii and B. brevipes, were described from surface samples. The two species of Asterodinium and Microceratium orstomii were collected at 100 m and 75 m depth, respectively (Taylor 1963; Sournia 1972a, b). From the same location, Sournia (1972b) also illustrated K. papilionacea collected from surface waters. In the offshore waters of the NE Africa upwelling, Margalef (1975) found exceptionally high abundances (up 4000 cells L"̂ ) of B. capitatum in the upper 30 m depth. In the same region, Estrada (1976,1978) reported up 10000 cells of B. capitatum coinciding with 20000 cells of flattened 237 450 Algae Vol. 21(4), 2006 Karenia brevis-like cells in offshore surface waters. Gômez (2003) and Gômez et al. (2005a, b) found Brachidinium and Asterodinium at an average depth of 35 and 85 m, respectively, in several regions of the NW and Equatorial Pacific Ocean. The same pattern was observed in the pre­ sent study in the SE Pacific Ocean (Figs 3B, C). Haywood et al. (2004) reported that the abundance of K. papilionacea was lower than 1000 cells in the late austral summer in the coasts of New Zealand. In the European Atlantic coasts Karenia brevis-like cells also appear in summer with abundances that never exceeded 1500 cells (Nézan 1998). Yeung et al. (2005) found K. papilionacea-like cells with an abundance of 10 cells in the pier of the Hong Kong University. In the present study in open waters, the higher abundances of K. papil­ ionacea, 10 cells L“\ were found in the more productive regions. Adaptation to light availability The brachidiniaceans and Karenia are characterized by an unusual yellow-green bright pigmentation. Brachidinium and Karenia were encountered in the surface and Asterodinium and Microceratium below the euphotic zone. The records below the euphotic zone and surface waters of tropical seas required highly versatile pigment composition to adapt to different light regimes. Most of dinoflagellates have chloroplasts that contain chloro­ phyll C2 and peridinin as the major carotenoid. However, the chloroplasts of Karenia have chlorophylls ĉ + C; and fucoxanthin-derived carotenoid but lacks peridinin (Tangen and Bjornland 1981), originated from a hapto- phyte tertiary endosymbiosis in an ancestral peridinin- containing dinoflagellate (Yoon et al. 2002). Karenia brevis (Davis) G Hansen et Moestrup, responsible of massive toxic blooms in the Gulf of México, is the best known species of the genus. This species has a robust photosyn­ thetic capability and accumulation of diadinoxanthin and diatoxanthin depending of the irradiance with minor adjustments in chlorophyll a and fucoxanthin con­ tents that facilitate acclimation to variable irradiance regimes (Evens et al. 2001). This pigment plasticity could explain that Asterodinium can survive near the nutricline below 200 m depth with less than 0.1% of the surface irradiance The availability of nitrate near the nutricline also favoied the pigment accumulation as observed in Asterodinhm (Gômez 2003; Gômez et al. 2005b). In addi­ tion, the cell shape of A. gracile with a strongly flattened cell body ind elongate extensions seems to be an adapta­ tion to increase the cross-section in light limiting condi­ tions. Other shade flora members such as Ceratium platy- corne Daday have highly pigmented wide flattened extensions (Sournia 1982). Size and shape changes The high variability of the size of the extensions of the brachidiniaceans has been remarked since the early works. In the description of Brachidinium, Taylor (1963) reported "the species is interesting in that the cells appear to exhibit a structural adaptation to their environ­ ment, namely, the production of elongate processes ... in this connection it might also be noted the specimen ... in less dense water exhibited a greater elongation of processes". The number of extensions of Microceratium (3-extensions) was lower, but the length of each exten­ sion was longer than in the typical 5-extensions Asterodinium (Figs 4P-Y). In addition to the increase of the cross-section for the photosynthesis, the elongated extensions are supposed to be associated with a reduc­ tion of the sinking speed and consequently a reduction of the energy required maintaining the cell in the euphotic zone. The projection of body extensions has been consid­ ered as an adaptive strategy for warm water dinoflagel­ lates under low turbulence conditions (Zirbel et al. 2000). Although the cell size is often an important taxonomic character in dinoflagellates, it can be variable. This vari­ ability was especially notorious in cultures of K. papil­ ionacea with a usual range of width of 18-32 ^m, but also co-occurring with cells 65-90 pm wide (Haywood et al. 2004) that has been also observed in natural waters in the present study (Figs 4G, H). Haywood et al. (2004, p. 175) reported "small to large cells present in cultures that were not separated into size classes because of the intergradations between sizes and because the signifi­ cance of the size classes cannot be addressed until the life cycle of these species is known." Karenia papilionacea is also characterized by fast changes of shapa ând in cul­ tures the apical process contracts forward when the cells are stressed (Haywood et al. 2004, p. 170) as already illus­ trated Sournia (1972b, p. 157). The live cells of Brachidinium were able to move the body extensions (Léger 1971; Gômez et al. 2005a). Karenia bicuneiformis was also able to change its morphology and the pointed or bulbaceous antapical tips observed in natural waters disappeared and the cells are rounder in cultures (Haywood etal. 2004, p. 173). According to Raven (1986) the reduced size of the "small" subpopulations of microalgae allows an opti­ mization of photon capture and nutrient uptake, such 238 Gômez: Brachidinium, Asterodinium, Microceratium and Karenia 451 Eutrophy H in h tiirh iilA nrA ■ offshore ' Oligotrophy Low turbulence Fig. 5. Scheme of the distribution of the tentative life stages of Brachidinium capitatum. that they may take optimal advantage of the conditions generally prevailing during the blooms (i.e., availability of nutrients, turbulence). In contrast, the "large" forms appeared to be more adapted for survival under non­ bloom conditions (Raven, 1986). Consequently under the optimal conditions for growth such as cultures and eutrophic coastal waters, the smaller forms of K. papil­ ionacea will predominate, whereas in open waters the projection of body extensions would constitute a compet­ itive advantage (Fig. 5). Toxic species such as Karenia have been intensively investigated in high turbulence conditions such as cultures and coastal waters. Little is known on the adaptation of these species to the stratified open ocean. ACKNOWLEDGEMENTS This is a contribution of the BIOSOPE of the LEFE- CYBER and the French IFB 'Biodiversité et Changement Global' programs. I thank to H. Claustre for the seawater samples and light data and J. Ras for her collection assis­ tance. REFERENCES Biecheler B. 1934. Sur le réseau argentophile et la morphologie de quelques Péridiniens. Comptes Rendus des Séances de la Société de Biologie 115:1039-1042. Botes L., Sym S.D. and Pitcher G.C. 2003. Karenia cristata sp. nov. and Karenia bicuneiformis sp. nov. (Gymnodiniales, Dinophyceae); two new Karenia species from the South African coast. Phycologia 42:563-571. Claustre H. and Maritorena S. 2003. The many shades of ocean blue. Science 302:1514-1515. Daugbjerg N., Hansen G., Larsen J. and Moestrup 0. 2000. Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unar­ moured dinoflagellates. Phycologia 39: 302-317. de Salas M.F., Bolch C.J.S. and Hallegraeff G.M. 2004. Karenia umbella sp. nov. (Gymnodiniales, Dinophyceae), a new potentially ichthyotoxic dinoflagellate species from Tasmania, Australia. Phycologia 43:166-175. Estrada M. 1976. Estudios sobre las poblaciones de organismos acuaticos en medio no uniforme. Ph. D. thesis, Univ. Barcelona, Spain. Estrada M. 1978. Mesoscale heterogeneities of the phytoplank­ ton distribution in the upwelling region of NW Africa. In: Boje R. and Tomczak M. (eds), Upwelling Ecosystems. Springer, Berlin, pp. 16-23. Evens T.J., Kirkpatrick G.J., Millie D.F., Chapman D.J. and Schofield O.M.E. 2001. Photophysiological responses of the toxic red-tide dinoflagellate Gymnodinium breve (Dinophyceae) under natural sunlight. /. Plankton Res. 23: 1177-1194. Fraga S. and Sanchez F.J. 1985. Toxic and potentially toxic dinoflagellates found in Galician Rias (NW Spain). In: Anderson D.M., White A.W. and Baden D.G. (eds). Toxic dinoflagellates. Elsevier, New York. pp. 51-54. Gômez F. 2003. New records of Asterodinium Sournia (Brachidiniales, Dinophyceae). Nova Hedwigia 77: 331-340. Gômez F., Yoshimatsu S. and Furuya K. 2005a. Morphology of Brachidinium capitatum F.J.R. Taylor (Brachidiniales, Dinophyceae) collected from the western Pacific Ocean. Cryptog. Algol. 26:165-175. Gômez F., Nagahama Y., Takayama H. and Furuya K. 2005b. Is Karenia a synonym of Asterodinium-Brachidinium? (Gymnodiniales, Dinophyceae). Acta Bot. Croat. 64: 263-274. Haywood A.J., Steidinger K.A., Truby E.W., Bergquist P R., Bergquist P.L., Adamson J. and Mackenzie L. 2004. Comparative morphology and molecular phylogenetic analysis of three new species of the genus Karenia (Dinophyceae) from New Zealand. /. Phycol. 40:165-179. Iizuka S. 1975. On occurrence of similar organisms to Gymnodinium breve Davis in Omura Bay. Bull. Plankton Soc. Japan 21:109-112. Margalef R. 1975. Composiciôn y distribuciôn del fitoplancton marino en la regiôn de afloramiento del NW de Africa, en marzo de 1973 (Campana "Atlor II" del Cornide de Saavedra). Resultados de Expediciones Cientificas BjO Cornide 4:145-170. Nézan E. 1998. Recurrent observations of a Gymnodinium breve­ like species. Harmful Algae News, IOC, UNESCO 17:7. ' " _ Raven J.A. 1986. Plasticity in algae. In; Jennings D.H. and Trewavas A.J. (eds). Plasticity in Plants. The Company of Biologist Ltd, Cambridge, pp. 347-372. Sournia A. 1972a. Quatre nouveaux dinoflagellés du plancton marin. Phycologia 11: 71-74. Sournia A. 1972b. Une période de poussées phytoplanctoniques prés de Nosy-Bé (Madagascar) en 1971. Espèces rares ou nouvelles du phytoplancton. Cahiers O.R.S.T.O.M., série océanographique 10:151-159. Sournia A. 1982. Is there a shade flora in the marine plankton? J. Plankton Res. 4:391-399. Sournia A. 1986. Atlas du phytoplancton marin. Vol. I: Introduction, Cyanophycées, Dictyochophycées, Dinophycées et 239 452 Algae Vol. 21(4), 2006 Raphidophycées. Editions du CNRS, Paris. Takayama H. 1985. Apical grooves of unarmoured dinoflagel­ lates. Bull. Plankton Soc. Japan 32:129-140. Tangen K. and Bjornland T. 1981. Observations on pigments and morphology of Gyrodinium aureolum Hulburt, a marine dinoflagellate containing 19-hexanoyloxyfucoxanthin as the main carotenoid. J. Plankton Res. 3:389-401. Taylor F.J.R. 1963. Brachydinium, a new genus of the Dinococcales from the Indian Ocean. J. South Africa Bot. 29: 75-78. Yang Z.B., Hodgkiss I.J. and Hansen G. 2001. Karenia longi­ canalis sp. nov. (Dinophyceae): a new bloom-forming species isolated from Hong Kong, May 1998. Bot. Mar. 44: 67-74. Yeung P.K.K., Hung V.K.L., Chan F.K.C. and Wong J.T.Y. 2(X)5. Characterization of a Karenia papilionacea-like dinoflagellate from the South China Sea. J. Mar. Biol. Assoc. U.K. 85: 779- 781. Yoon H.S., Hackett J. and Bhattacharya D. 2002. A single origin of the peridinin-, and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc. Nat. Acad. Sci. USA 99:11724-11729. Zirbel M.J., Veron F. and Latz M.I. 2000. The reversible effect of flow on the morphology of Ceratocorys horrida (Peridiniales, Dinophyta). J. Phycol. 36:46-58. Received 18 August 2006 Accepted 17 November 2006 240 Short communication ACT A BOT ANIC A CRO ATIC A 66 ( 1 ) Observations on an H-shaped dinoflagellate. An example of the projection of body extensions in gymnodiniacean cells F e r n a n d o G ô m e z Station Marine de Wimereux, Université des Sciences et Technologies de Lille-Lillel, FRE 2816 ELICO CNRS, 28 avenue Foch, BP 80, F-62930 Wimereux, France. *Corresponding address: femando.gomez@fitoplancton.com, fax+33 321992901 Running title: H-shaped dinoflagellate Little is known about the morphological versatility of the unarmoured dinoflagellates. The morphology of the unarmoured dinoflagellate with a distinctive H-shaped contour is described fiom sub-surface waters of the Strait of Gibraltar (NE Atlantic) and the northern Phihppine Sea (NW Pacific). The cell body was slightly hexagonal with two rounded-tip apical arms and two antapical sharp-pointed homs. A carina with a straight groove was located between the two apical arms. The cingulum was excavated, with a descending displacement of more than one-half body length and had an overhang. A round nucleus was located in the left hyposome. These forms may correspond to a gymnodiniacean cell that is able to project body extensions under unfavourable environmental conditions. Key words: Gyrodinium, Karenia, dinoflagellate, Dinophyceae, phytoplankton, microalgae, Atlantic, Pacific 241 mailto:femando.gomez@fitoplancton.com Introduction During the routine microscopical analysis of several thousands of phytoplankton sangles fiom the Atlantic, Mediterranean and Pacific waters, two similar specimens of an unknown distinctive dinoflagellate were observed. The present study describes the morphology of this interesting dinoflagellate fiom two distant geogr^hical areas. Materials and methods Samples fiom the Atlantic Ocean were collected during a cruise aboard RW Thalassa (2-9 September 1997) in the Strait of Gibraltar (Mediterranean Sea-Atlantic Ocean) (Fig. 1). Eight stations were visited and samples were collected at 9-11 depths at each station and 2.5 L seawater fi*om Niskin bottles was filtered through 5-p.m pore size mesh and the retained particles were carefully washed out, placed in glass bottles and preserved with acidified Lugol’s solution. Sub­ samples (10-100 ml) were allowed to settle for 24-48 h in Utermohl chambers (Gomez et al. 2000, Gomez 2003). The specimen was photographed on an inverted microscope connected to a Leica Wild camera. The specimen showed the aitire cell contents during the first microscopical observation. However, the cell body appeared empty after a re-examination several months later. Samples fi"om the Pacific Ocean were collected during a cruise aboard R/V Soyo-Maru (13-20 May 2002) in the Kuroshio Current and the northern Philippine Sea (Fig. 1). Seawater samples were collected using Niskin bottles at nine stations along the meridian 138‘’E fiom 28°0’N to 34°20’N, at 15 depths ranging between 5 to 200 m Sample treatment and microscopical observations as in Gomez et al. (2005). « Results Two specimens of this highly distinctive dinoflagellate were observed from samples collected from Atlantic and Pacific waters (Gomez 2003, 2006; Gomez et al. 2005). The first specimen was collected in the Atlantic side of the Strait of Gibraltar at 65 m depth (2 September 1997; 35°58’N, 5°55’W; bottom depth 160 m). The phytoplankton assemblage was dominated by the diatom Pseudo-nitzschia spp. with a marked sub-siq)erficial maximum at 40 m depth. The second specimen 242 was collected in the northern Philippine Sea at 150 m depth (16 May 2002; 30°N, 138®E; bottom depth 4050 m). The plankton assemblage at that depth was dominated by naked ciliates (<100 cells L ’). The maximal length of the H-shaped specimens was 52 and 55 pm and the width at the level of the cingulum was 25 and 27 pm for the Atlantic and Pacific specimens, respectively. The contour of the cell body in ventro-dorsal view was slightly hexagonal (Figs 2, 4, 6-8). The apex showed a carina or crest with a straight apical groove (Figs 7, 8). The excavated cingulum was descending and displaced by one-half of the body length and had an overhang (Fig. 6). The sulcus swung to the left before meeting the returning end of the cingulum. The intercingular region the cingulum and sulcus was Z shaped (Figs 6, 7). A pore was observed near the beginning of the cingulum. This may correspond to a perifiagellar pore where one or both flagella emerged (Fig. 6). The specimen was shaken until the transverse flagellum was separated fiom the cingulum (Fig. 9). The flagellum arose probably from the perifiagellar pore showed in the figure 6. The nucleus was round and located in the left side of the hyposome (Figs 7, 8, 10). The specimens showed four extensions of ~20 pm long radiating fiom the cell body. This resulted in the distinctive H-shaped contour (Fig. 4). Two curved flattened apical extensions with rounded-tips were projected from the episome (Fig. 14). The apical arms were in a different focal plane (Figs 6-8, 12-13). The right apical arm was more dorsally located than the left one (Figs 7, 8). The angle of the apical arms with respect to the episome was variable because the junctions were flexible (Figs 2, 4, 6-7). The two antapical extensions were straight and with acute ends. The left horn formed a right angle with the basis of the hyposome, whereas the right horn slightly diverged (Fig. 7). In left lateral view, the cells showed an elongate bk conical contour with the episome smaller than hyposome (Figs 3, 5, 10). The round nucleus was visible in lateral view as a pale region (Figs 10, 11). The Pacific specimen, observed in a better stage of conservation, showed a green pigmentation Although, it was not discernible the presence of chloroplasts (Figs 6-8). 243 Discussion No tabulation neitho* apical pore was observed. The forms of this study correspond to an unarmoured dinoflagellate (Figs 15-17). The groove along the carina reminds the straight apical groove that can be found in species belonging to the genera Brachidinium F.J.R. Taylor, Asterodinium Soumia, Microceratium Soumia and Karenia G. Hansen et Moestrup (GOMEZ et al. 2005, Go m e z 2006). Flexible arms with rounded tips can be found in gymnodiniaceans such as Brachidinium or Asterodinium (GÔMEZ et al. 2005). However, the brachidiniaceans are strongly dorso-ventral flattened cells with a fucoxanthine-derived pigmentation. The forms of the present study were slightly dorso-ventrally compressed and the pigmentation seems to be closer to a typical peridinine-containing dinoflagellate. The shape of the intercingular region, descending and with an overhand, is similar to numerous species described under the genus Gyrodinium Kofoid et Swezy. The two apical arms and the two antapical homs are most distinctive characters of the specimens. The projection of body extensions has been described as a strategy for the reduction of sinking speed in thecate species such as Ceratocorys horrida Stein (ZiRBEL et al. 2 0 0 0 ). Little is known about the morphological versatility of the unarmoured dinoflagellates. The two specimens of the present study were found near the bottom of the euphotic zone at each location and predominating phytoplankton post-bloom conditions. It is hypothesized that the H-shaped forms corresponded to a stage of a versatile dinoflagellate that is able to project body extensions under unfavourable environmental conditions. — - Acknowledgements The study in the Atlantic Ocean was supported by EU project CANIGO (MAS3-CT96-0060) and in the Pacific Ocean by a Grant-in-aid for Creative Basic Research (12NP0201, DOBIS) fi'om the MEXT, Japan. I was supported by a fellowship of the European Commission (ICB2-CT-2001- 80002) held at the University of Tokyo with Prof. K. Fumya as host. 244 References Gô m e z , F., 2003: New records of Asterodinium Sournia (Brachidiniales, Dinophyceae). Nova Hedwigia 77, 331-340. Gô m e z , F., 2006: The dinoflagellate genera Brachidinium, Asterodinium, Microceratium and Karenia in the open SE Pacific Ocean. Algae 21,1-10. Gô m e z , F., Ec h e v a r r ia , F., G a r c ia , C.M., Prieto , L., Ru iz , J., REUL, A., Jïm é n e z -G ô m e z , F., V a r e l a , M., 2000: Microplankton distribution in the Strait of Gibraltar coupling between organisms and hydrodynamic structures. J. Plankton Res. 22, 603-617. Gô m e z , F., N a g a h a m a , Y., T a k a y a m a , H ., F u r u y a K., 2005: Is Karenia a synonym of Asterodinium-Brachidiniuml (Gymnodiniales, Dinophyceae). Acta Bot. Croat. 64,263-274. Z irbel, M.J., V ero n , F., L a t z , M.I., 2000: The reversible effect of flow on the morphology of Ceratocorys horrida (Peridiniales, Dinophyta). J. Phycol. 36,46-58. 245 Figure captions Fig. 1. Map of the stations occupied in the Atlantic and Pacific Oceans ^ circles). Largo" circles indicate the locations of the two records of the H-shaped dinoflagellate. Figs 2-14. Photomicrographs of the H-shaped dinoflagellate, non-reversed images in bright field optics. Figs 2-3. Specimen from the Atlantic Ocean Dorsal and left lateral views, respectively. Figs. 4-14. Specimen fiom the Pacific Ocean. Figs 4-5. Dorsal and left lateral views, respectively. Fig. 6. Ventral view. See the Z-shaped intercingular region. The inset illustrates a tentative perifiagellar pore. Fig. 7. Ventral view. The arrow in the inset indicates the straight groove in the carina. Fig. 8. Dorsal view. The arrow indicates the contour of the apical groove. Fig. 9. Ventral view. The specimen was shaken until the transverse flagellum was separated fiom the cingulum Figs 10-11. Left latero-ventral view. See the round nucleus. Figs 12-13. Apical views. Fig. 14. Detail of the tips of ftie qjical extensions. N=nucleus; TF=transverse flagellum. The black spot in the photographs is not related to the cell. Scale bars = 20 jxm Figs 15-17. Line drawings of the H-shaped dinoflagellate. Ventral, dorsal and left lateral view, respectively. Scale bar = 20 pm 246 Cadiz 1 / o / l i f c z C . N ^ rb a te Gulf of C adiz # T a r i ^ \ Ceuta 45°N 7°W 6°W North Atlantic • Ocean ISÔ E5°W 1 2 0 “E 130°E 140°E 247 L * 1 2i .MPT: • ' L 12 rt-’ 14 * r f , \ 248 249 3.2. Tœconomia y distribuciôn de dinoflagelados poco çonocidos: 3 .2 .2 , C e ra to p e rld in lu m . ■ r Gomez, F. & Abboud-Abî Saab, M., 2003. Records of Çeratoperidinium Margalef (Dinophyceae) from the Mediterranean Sea. Vie et Milieu 53, '4 3 -4 6 . . Gômez, P., Nagahama, Y., Fukuyo, Y. & Furuya, K., 2004. Observations on Ceratoperidinium (Dinophyceae). Phycologia 43 , 416-421. 250 v m MILIEU, ZUU3, 53 : 43-40 RECORDS OF CERATOPERIDINIUM MARGALEF (DINOPHYCEAE) FROM THE MEDITERRANEAN SEA F. G Ô m r , M. ABBOUD-ABI SAAB" ^Department o f Aquatic Biosciences, Graduate School o f Agriculture and L ife Sciences, The University o f Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan **National Center fo r M arine Sciences, P.O. Box 534, Batroun, Lebanon femando.gomez@fitoplancton. com mabisaah@cnrs. edu. lb CESATOPEKIDINIVM DINOFLAGELLATE DWOPHYCEAE PinrfOPLANKTON MEDITERRANEAN SEA CEBATOrElUDlNWM DINOFLAGELLÉ DINOPHYCEAE PHYTOPLANCTON MER MÉDITERRANÉE ABSTRACT. - Records of dinoflagellates of the rare genus Ceratoperidinium Mar- galef ex Loeblich III are reported from the Mediterranean Sea. C. yeye Margalef was collected from frie Bay ofPaltna de Mallorca (Balearic Is.) and C cf. yeye from the Alborân Sea. From the Lebanese coastal waters, C. yeye was also reported and C. mediterraneum Abboud-Abi Saab. Ofrier taxon, Ceratoperidinium sp., characte­ rised by a distinct elongate apical process* is reported from the Bay of Palma de Mallorca. These species were collected from neritic and ep^lagic waters and usually associated with phytoplankton post-bloom conditions. RÉSUMÉ. - Des données sur un genre rare de Dinoflagellé Ceratoperidinium Mar­ galef ex Loeblich 111 de Méditerranée sont exposées. C. yeye Margalef a été trouvé dans la Mer d’Alborân et la Baie de Palma de Mallorca (lies B^éares). Dans les eaux côtières libanaises, C. yeye et C. mediterraneum Abboud-Abi Saab ont aussi été recoltéà. Ceratoperidinium sp., caractérisé par un prolongement apical distinct, a été signalé dans la Baie de Palma de Majorque. Ces espèces ont ét^ collectées dans des eaux néritiques, épipélagiques et souvent associées aux conditions d’un post-bloom de phytoplancton. Dinoflagellates are well represented in the oligotrophic waters of the Mediterranean Sea. De­ spite the relative high number of studies performed in the Mediterranean Sea, some taxa are rarely re­ ported and information on their ecology and distri­ bution is scarce. This is the case for the species of the genus Ceratoperidinium, The ^tem adc position of this genus, which shape is reminiscent of peridinialeans and brachydiniaceans, remains uncertain. Ceratoperidinium has been consid­ ered as a thecate dimflagellate of the order Peridiniales (Loeblich m 1982, Soumia 1986), but thecal pl£des have not beat observed. According to Fensome et al. (1993), the rigid wall may be evidence of a pellicle. These authors placed this genus in the Ptychodiscales as an athecate dinoflagellate. Ceratoperidinium yeye Margalef ex Loeblich III The type species of the genus Ceratoperidinium was described from one individual in the Spanish Mediterranean coastal waters (Margalef 1969). The species presented a total length of 184 pm (63 pm excluding the antapical appendices) and a transversal diameter of 50 pm (Fig. 1 A). This taxon was re-described as Ceratoperidinium margalefii by Loeblich III (1980) due to the lack of Latin di­ agnosis. Later, Abboud-Abi Saab (1989) reported one specimen of C. yeye found in November 1988 at 5 m depth in the Lebanese coastal waters (33° 57’ 34” N, 35° 35’ 47” E). The Lugol fixed specimen was collected from waters with a temperature of 22°C, salinity 39.53, nitrate 0.26 pM and phosphate 0.04 pM. Mainly diatoms composed the surround­ ing phytoplankton assemblage, reaching an abun­ dance of 6.1 cells ml"' and dinoflagellates (mainly athecate forms) reaching an abundance of 3 cells ml''. The total length of the specimen was 236 pm, 67 pm excluding the appendices and the transdiameter was 59 pm. The cell size excluding the antapical q>pendices represented 25% of the to­ tal l e n ^ . This specimen presented differences with the type species such as bigger size and protu­ berances that started at the 1/3 from the proximal 251 44 GOMEZ F., ABBOUD-ABI SAAB M. part, distributed regularly towards the tips of the antapical appendices (Fig. IB). Velasquez (1997) reported two records of C. yeye in the Gulf of Lions (NW Mediterranean Sea) in February 1988. During a survey carried out in September 1999, one specimen that resembles C. yeye was observed at 20 m depth in the NW Alborân Sea (36"05’N, 05̂ !̂ 2’W) from Lugol fixed water samples (Fig. ID ). Temperature was 17.3°C, salinity 36.77, nitrate 0.15 pM and phosphate 0.03 pM. The microphytoplankton assemblage was dominated by diatoms that reached an abundance of 7.7 cells ml"', mainly Dactyliosolen fragilissiinus, Leptocylindrns danicus, L. minimus and Pseudo-nitzschia spp, whereas dinoflagellates reached an abundance of 2.6 cells ml"' dominated by Gymnodinium catenatum. The observed phytoplankton assem­ blage corresponded to post-bloom conditions, in contrast with an assemblage dominated by Chaetoceros curvisetus more typical under the eutrophic conditions in this area (Gomez et al. 2000). No size measurements of this specimen were performed. Cell size excluding the antapical appen­ dices represented 29% of the total size whereas in the Margalef s figure this ratio was 34%. The antapical appendices were thicker than those Fig. 1. - Line drawings of the records of Ceratoperidinium spp in the Mediterranean Sea. A, The type species, Cerato­ peridinium yeye Margalef, adapted from Margalef (1969). B, C. yeye from the Lebanese coastal waters. C, C. yeye col­ lected from the Bay of Palma de Mallorca (Balearic Is.). D, Ceratoperidinium cf. yeye recorded from the NW Alborân Sea. E, Ceratoperidinium mediterraneum Abboud-Abi Saab from the Lebanese coastal waters. F, Ceratoperidinium sp. collected from the Bay of Palma de Mallorca. Scale bar: 50 pm. 252 CERATOPERIDINIUM (DINOFLAGELLATE) FROM THE MEDITERRANEAN 45 shown in Margalef (1969) and protuberances were not observed along the appendices. In October 2001, a specimen of C. yeye was ob­ served at 10 m depth in the Bay of Palma de Mallorca (Balearic Is.) (39°32'N, 2“36.3’E) from Lugol fixed water samples. The cell was 131 |im long (51 J im excluding the appendices) and the transdiameter was 42 pm (Fig. 1C). The antapical appendices were also thicker than those in Margalef s drawing and both of them presented clear protuberances in the middle of the appendices. Ceratoperidinium mediterraneum Abboud-Abi Saab Abboud-Abi Saab (1989) described this species from the Lebanese coastal waters from one speci­ men. The main characteristic of this taxon in com­ parison to C. yeye is the presence of a tip-rounded tubular apical (capitate) process (Fig. IE). The to­ tal length was 134 pm, 46 pm excluding the appen­ dices and the cingulum was 42 pm width (cell size excluding the antapical appendices represented 34% of the total size). The type species was found in July 1982 at 5 m depth in a coastal station (34°00’50'’N, 35'̂ '30’40” E). The temperature was 27.2°C, salinity 39.2, nitrate 0.11 pM and phos­ phate 0.03 pM. The phytoplankton assemblage cor­ responded to spring post-bloom conditions domi­ nated by diatoms (mainly Dactyliosolen frag i- lissimus) reaching an abundance of 23.6 cells mT̂ whereas the abundance of dinofageliates was low (0.32 cells m f ) . In October 1988, at the same sta­ tion and the same depth, another specimen was col­ lected with a total length of 137 pm (55 pm exclud­ ing the appendices) and the cingulum was 47 pm width. Cell size excluding the antapical appendices represented 40% of the total size. This specimen was collected from waters with a temperature of 26.6'^C and a salinity of 39.3. Ceratoperidinium sp In November 2001, one specimen of the genus Ceratoperidinium was collected in the Bay ol Palma de Mallorca (Balearic Is.) at 10 m depth. The cingulum diameter was 39 pm width and 112 pm of total length (including antapical and api­ cal appendices) (Fig. IF). This taxon presented a distinctive curved apical process more elongate than that of C. mediterraneum. In Cerato­ peridinium sp. the antapical appendices were thicker than those in C. yeye and C. mediterraneum and protuberances along the antapical appendices were not observed. These characteristics resemble the antiapical appendices of the specimen C. cf. yeye, collected from the .Alborân Sea. Based on the Table I. - Records of Ceratoperidinium spp, including historical records. I.ncatiitn (depth) C. ̂ e Castelloncoasi (10 m) Lebanese coasi (5 m ) Gulf o f Lions M allorca üay (10 m) C c f yeye NW Alborân Sea (20 ni) C, mediterraneum I.ebanese coast (5 m) Ceratoperidinium sp M allorca Bay (10 ni) 1 Aug., 1%7 1 Nov., 1988 2 Feb., 1988 1 Oct.. 2001 1 Sept.. 1999 2 .lul., 1982, Oct.. 1988 1 Nov.. 2001 Reference M argalef. 1969 .Abboud-.Abi Saab, 1989 Velasquez. 1997 This study This study .Abboud-.Abi Saab, 1989 This studv O Historical records of C. yeye □ C. mediterraneum 0 New record of C, yeye € ) Ceratoperidinium cf, yeye J l. Ceratoperidinium sp Fig, 2. - L ocation o f the records o f C eratoperid in ium spp. 253 46 GOMEZ P., ABBOUD-ABI SAAB M. length of the apical process, C. mediterraneum ap­ pears as an intergraded taxon between C yeye and Ceratoperidinium sp. Final remarks As general trend, C yeye, C mediterraneum and Ceratoperidinium sp. seem to appear in coastal wa­ ters, being preferentially recorded from surface wa­ ters and usually associated with phytoplankton post-bloom conditions. Most of the specimens were collected under thermophilic conditions (summer- autumn), however the records by Velasquez (1997) in the Gulf of Lions in winter prevent us to consid­ ering Ceratoperidinium as a strictly warm-waters genus. According to the available knowledge on the geographical distribution of Ceratoperidinium, these species can be considered as an exclusively Mediterranean taxa (Table 1, Fig. 2). Despite the distinctive morphology, relative large size and be­ ing preferentially found in the surface coastal wa­ ters (more intensely studied), the records of these taxa are extremely low. A c k n o w l e d g e m e n t s . - The sample from the Alborân Sea was provided by Dr H Claustre within the context of JGOFS-France PROSOPE programme. F.G. acknowled­ ges the financial support by Spanish Ministry of Science and Technology and by the European Commission (ICB2-CT-2001-80002). R E F E R E N C E S Abboud-Abi Saab M 1989. Les Dinofiagellés des eaux côtières libanaises- Espèces rares ou nouvelles du phytoplancton marin. Leb Sci Bull 5(2); 5-16. Fensome RA, Taylor FJR, Norris G, Sarjeant WAS, Wharton DE Williams GL 1993. A classification of living and fossil dinoflagellates. J Micropaleontology Spec PubI 7: 1-351. Amer Mus Nat Hist, Sheridan Press, Hanover, PA. Gomez F. Echevarria F, Garcia CM, Prieto L, Ruiz J, Reul A, Jinrènez-Gômez F, Varela M 2000. Micro­ plankton distribution in the Strait of Gibraltar: cou­ pling between organisms and hydrodynamic structures. J Plank Res 22: 603-617. Loeblich AR 111 1980. Dinoflagellate nomenclature. Taxon 29: 321-324. Loeblich AR 111 1982. Dinophyceae. In Parker SP ed. Synopsis and classification of living organisms, McGraw-Hill, New York. I: 101-115. Margalef R 1969. Composicion especifica del fitoplanc- ton de la costa catalano-levantina (Mediterraneo occi­ dental) en 1962-1967. Inv Pesq 33: 345-380. Soumia A 1986. Atlas du phytoplancton marin. Vol. I: Introduction, Cyanophycées, Dictyochophycées, Di- nophycées et Raphidophycées. Editions du C.N.R.S., Paris 219 p. Velasquez ZR 1997. Fitoplancton en el Mediterraneo Noroccidental. Ph.D. Univ Politècn Catalunya, 272 +55 p. Reçu le 16 avril 2002; received April 16, 2002 Accepté le 24 septembre 2002; accepted September 24, 2002 254 P hycologia (2004) Volume 43 (4), 416-421 Published 30 Julv 2004 Research Note Observations on Ceratoperidinium (Dinophyceae) F er n ando G o m e z '*, Y uk io N a g a h a m a '. Y a su w o F u k u y o ̂ a n d K e n F u r u y a ' Department of Aquatic Biosciences, The University of Tokyo. l - l - I Yayoi. Bunkyo. Tokyo 113-8657, Japan 'Asian Natural Science Environmental Center. The Univcrsit}’ of Tokyo. 1-1-1 Yayoi. Bunkyo. Tokyo 113-8657, Japan F. G o m l z , Y. N a g a h a m a , Y. F o k o v o a n d K. F u r u y a . 2004. Observations on Ceratoperidvnnm (Dinophyceae). Phycologia 43:416-421. Until now, the rare dinoflagellate genus Ceratoperidinium Margalef has been recorded only from the Mediterranean Sea. For the first time, photomicrographs (bright field, Nomarski and cpifluorcsccnce) are reported from Lugol-fixcd samples collected from the Sulu and Celebes Seas and the western Equatorial Pacific Ocean. The specimens showed high variability in the relative size o f the flexible extensions. Several speeimens corresponded to the type species. Ceratoperidinium yeye, and lacked the apical extension. Other specimens showed an apical extension o f variable size that corresponded to the description of C. mediteiraneaum. This taxon is considered to be a morphological variety o f C. yeye on the basis o f the high interspecimen variability in the length o f the extensions; specimens intermediate between C. yeye and C. mediterra- neaum occur where both fomis coexist. The ventral view is proposed (confirmed by 4,6-diamidino-2-phenylindole staining) to be that with the nucleus located in the left side o f the cell. Thecal plates were not observed in specimens stained with Fluorescent Brightener 28. Consequently, the placement o f this genus in the order Peridiniales on the basis o f the initial description from a single cell should be reeonsidcrcd. Ceratoperidinium Margalef is a genus of planktonic marine dinoflagellate rarely reported in tlie literature. Margalef (1969) described the type species Ceratoperidinium yeye Margalef from a single individual collected in coastal waters of the Spanish Mediterranean Sea. Margalef reported a cell body that was pentagonal in outline and compressed dorsoventrally. The cingulum was weakly impressed and a sulcus was not ob­ served. The cell surface was rigid and lacked sculpture or relief. No thecal plates were observed. The hypotheca (hy- posoma) was drawn out into two long, slightly curved, rigid, cylindrical appendices with a row of three swellings at their extremities. The tips of the antapical extensions presented a tentacle-like shape. One large pusule, plastids and small drops of lipid occur in the cytoplasm and the nucleus is centrally located. Later, Loeblich (1982, p. 108) and Soumia (1986, p. 96) translated the description by Margalef (1969) to English and French, respectively. The type species was redescribed as C. margalefii by Loe­ blich (1980) because of the absence of a Latin diagnosis. As reported by Sournia (1982, p. 153), Loeblich only added the Latin diagnosis, but instead of retaining the name with a new authority, C. yeye Margalef ex Loeblich III, he proposed the new name C. margalefii Loeblich III. The case of C. yeye is comparable to that of taxa such as Petalodinium porcelio J. Cachon & M. Cachon, in which the original publication of the type species lacked the Latin diagnosis; under the Inter­ national Code of Botanical Nomenclature (Greuter et a l 2000; article 45.5 ex. 5), the name should retain its original author­ ship and date. * Corresponding author (fem ando.gom ez0filoplancton.com ). After the initial record by Margalef (1969), Abboud-Abi Saab (1989) reported one specimen of C. yeye from Lebanese coastal waters. She fiirther reported a new species, C. medi­ terraneum Abboud-Abi Saab (Abboud-Abi Saab 1989), that differs from the type species by the presence of a rounded tubular apical (capitate) process. The description of C medi­ terraneum lacked a Latin diagnosis, line drawings and good- quality illustrations. This almost inaccessible publication goes unnoticed in or omitted from later literature. Velasquez (1997) reported C yeye in the Gulf of Lions (NW Mediterranean Sea) and more recently Gomez & Ab­ boud-Abi Saab (2003) reported new records of C. yeye from the Alborân and Balearic Seas. These authors also reported a Ceratoperidinium sp. with a distinctive curved apical process more elongate than that in C mediterraneum (Gomez & Ab­ boud-Abi Saab 2003). There are no other records, either for the Mediterranean Sea (Gomez 2003) or for the rest of the world, to the best of our knowledge. Ceratoperidinium has been placed in the family Ceratoper- idiniaceae Margalef (Loeblich 1982) or incertae sedis (Sour­ nia 1986), both in the order Peridiniales Haeckel, and later tentatively as an unarmoured taxon of the order Ptychodis­ cales Fensome, Taylor, Norris, Sarjeant, Wharton & Williams (Fensome a/. 1993). This study presents photographic records of the genus for the first time. We tried to elucidate the presence of cellulose thecal plates by using the Fluorescent Brightener staining technique. The position and the shape of the nucleus were studied by using a DNA fluorochrome. The orientation of the cell is proposed for the first time. The morphological vari­ ability in the relative size of the extensions is emphasized. 255 16“ Ni 12“ N- 8“ N- Philippines is. Philippine ' Sea Soum China Sea a ^ Celebes ^ V Sea e 3 2 Western Pacific Ocean D Hawaii -20 N 10 N # # # # # # # # # 6 7 8 9 10 11 12 13 14 EQ 120“ E 124“ E 120"E 140“ E 160“ E 180 Fig. 1. Locations o f the sampling stations in the tropical and western Equatorial Pacific Ocean ’ ïëfw" 10 s Specimens were collected during two cruises: (1) aboard R/ V Hakuho-maru (7 November-18 December 2002) in the Cel­ ebes, Sulu and South China Seas (Fig. 1 ). Sea water samples were collected by using Niskin bottles in 10 stations at six discrete depths from 0 to 150 m; and (2) aboard R/V Mirai (15—28 January 2003) along the equator from 160°E to 160°W. Sea water samples were collected by using Niskin bottles in nine stations at 14 discrete depths from 5 to 200 m. Samples were preserved with acidified Lugol's solution (Hasle & Sy- vertsen 1997) and stored at about 5°C. Samples of 400 ml were concenfrated by settling in glass cylinders: concentrates were left to settle in standard sedimentation chambers and examined in a Diaphot inverted microscope (Nikon, Tokyo, Japan) using bright field optics. Cells were photographed on an inverted light microscope connected to a Nikon digital camera (Coolpix 4500). Several specimens were isolated using a capillary tube from the chambers, transferred to a glass slide and observed with ein Olympus microscope (BX51; Tokyo, Japan) equipped with Nomarski differential interference contrast (DlC) optics. High-magnification microphotographs (X600 or XI000) were obtained with an Olympus digital camera (C3040ZOOM). One specimen was stained by adding Fluorescent Brightener 28 (Sigma, St Louis, MO, USA) following the protocol of Fritz & Triemer (1985). Three specimens (one under division) were stained by adding a mix containing 4,6-diamidino-2- phenylindole (DAM; Sigma) and Fluorescent Brightener. The DAPI specifically binds to double-stranded DNA, and when excited with ultraviolet (UV) light the DAPI—DNA complex fluoresces a bright blue (Porter & Feig 1980). Epifluorescence microscopy was done with Olympus (BX60) and Zeiss Ax- iophot2 microscopes (Zeiss, Jena, Germany) to excite with UV light for DAPI and Fluorescent Brightener stains. Eight specimens were observed from the Sulu and Celebes Seas and five from the western Equatorial Pacific Ocean. The maximum occurrence was in the Sulu Sea (station 4; 7°25'N. 121°12.5'E), with four specimens (10 cells 1“') at 30 m depth (Fig. 1: Table 1). Nine specimens had an apical protuberance that differed from the type species; they were closer to C. mediterraneum. here considered to be a morphological variety of the type species (Figs 2-4, 8, 9, 12-14). Three specimens corresponded to the type species, lacking the apical process (Figs 5, 10, 11). One specimen was intermediate between these two taxa (Fig. 6), with a wider section at the base of Table 1. Stations, depth, geographic coordinates (latitude, longitudej and dimensions: W, width at the level o f tlie cingulum; L, total length o f each record o f Ceratoperidinium yeye. Station Deptli (m) Latitude Longitude W (pm) L (pm) Figs 4 - 3 0 7^25.3'N I2 F I2 .5 E 43 205 2-3 4 .^30 7'25.3'N 12L 12.5E 37 165 4 - 3 0 7”25.3'N 12U12.5’E 48 180 8-9‘f l8 - 2 0 4 - 3 0 7°25.3'N 1 2 r i2 .5 ’E 38 150 15 4 - 5 0 7"25.3'N 1 2 F 1 2 5 E 38 180 2 - 3 0 5"10.8'N 124'04.9'E 39 105 12-13 6' - 3 0 6”54.1'N 119"11.1’E 37 100 14, 16-17, 21-24 6- - 2 0 6“54.1'N 119^11.1’E 52 200 11 6: - 6 0 0' 160'E 68 225 10 6 -1 0 0 0" lôO'-E 45 172 8 - 7 0 0° 170"E 48 185 4 9= -1 2 0 0° 175^E 52 145 5 IF -1 2 0 0̂ 175"W 65 230 6-7 ' Specimen undergoing division. ̂No apical process. ’ -A.picaJ process scarcely developed. 256 P h yco lo g ia , V ol. 43 (4), 2004 •■ f-r .'•% '< m Figs 2 -1 4 . Ceratoperidinium yeye, bright field optics. See Table 1 for location o f the records and the size o f the specimens. Scale bars = 20 pm. Figs 2, 3. Ventral view s o f one specimen. The arrow in Fig. 3 indicates a knob on one o f the antapical extensions, and the arrow in the inset Ihc extremity o f the apical process. Fig. 4. Dorsal view o f a specimen showing a hole (arrow). Fig. 5. Ventral view o f another specimen lacking the apical process. Figs 6, 7. A specimen intermediate between C. yeye and the morphological variety C. mediterraneum. Fig. 7 shows a lateral view o f the cell body with a wider section at the base o f the short apical extension. 257 Gomez et al.: O bservations on the dinoflagellate Ceratoperidinium the apical tip seen in lateral view (Fig. 7). One of the speci­ mens was observed under division, with two contours of groove observed in one side of the cells (Figs 14, 16, 17, 21- 24). The size of the extensions relative to the cell body varied between the specimens (Figs 2-14). The antapical appendices were highly flexible. One of the specimens had a protuberance in one of the antapical appendices that we named ‘the knob’ (Fig. 3). As general trend, the antapical extension was slightly shorter in the side where the cingular groove was more apical (near the nucleus). From Lugol-fixed specimens, the maxi­ mum length ranged from 100 to 230 pm and the width at the cingulum level was 37-68 pm; specimens lacking the apical extension were larger than the others (Table 1). The cingulum was weakly impressed, and inclined relative to the base of the cell body. Neither flagellum nor sulcal groove was observed (Figs 18, 19). A slight irregularity, perhaps pores, appeared near the basis of the hyposoma (Fig. 20). The DAPI staining reveals the nucleus to be kidney-shaped and located laterally, glowing brightly under UV excitation (Fig. 17); under light microscopy, it appears as a pale area (Fig. 22) and microfilaraents (chromosomes) can sometimes be seen (Fig. 15). Cellulose thecal plates were not observed in specimens stained with Fluorescent Brightener and a mixture of DAPI Fluorescent Brightener illuminated with UV light. However, cellulose thecal plates were observed in cells of Prorocentrnm added to the samples as a positive control. The same protocol has been successfully used previously with other thecate di­ noflagellates. Dinoflagellates have been divided into naked (or un­ armoured) and thecate (or armoured). However, the distinction is not clear-cut (Dodge & Crawford 1970). The scarce infor­ mation on our genus is based on the single record by Margalef (1969). The systematic position of this genus remains uncer­ tain; the pentagonal shape of the cell body is reminiscent of peridinialeans, but the presence of extensions suggests the brachydiniaceans. Loeblich (1982, p. 108), based on Margalef (1969), reported ‘the thecal tabulation is unknown; however, the presence of a large apical pore indicates that a thecal layer is present’. We have not observed any apical pore. Loeblich (1982) placed this genus in the family Ceratoperidiniaceae Margalef of the order Peridiniales. Soumia (1986, p. 96) placed Ceratoperidinium in an undetermined position — in­ certae sedis - in the order Peridiniales. Fensome et al. (1993) interpreted that the rigid wall that might be evidence of a pellicle and tentatively placed the genus as an athecate dino­ flagellate of the order Ptychodiscales. According to Fensome et al. (1993, p. 54) the ptychodiscacean cell wall tends to be very flexible, due to the presence of a well-developed pellicle with cellulose as principal component (Morrill & Loeblich 1981). Fluorescent Brightener specifically stains cellulose, the main component of the dinoflagellate theca (Fritz & Triemer 1985). According to our results, Ceratoperidinium lacks the thecal plates that are characteristic of members of the order Peridiniales. The orientation of the genus is unresolved. Neither flagel­ lum nor sulcal groove was observed. The description by Mar­ galef reported one large pusule and that the nucleus was lo­ cated centrally (see also Loeblich 1982, p. 108). However, the use of DAPI staining in this study reveals that the nucleus is located laterally (Fig. 17) with microfilaments (chromosomes) visible under DlC microscopy (Fig. 15). The cingulum is left-handed and weakly impressed (Figs 18-20). Observation at different focus levels reveals that a discontinuity in the cingulum occurs in the side opposite the nucleus (Fig. 19). We consider that this view, with the nucleus in the left side of the cell, is the ventral position (Figs 25, 26). The specimens collected in the Pacific Ocean were very variable in the relative size of the antapical extensions (Figs 2-14). At the same stations were found specimens with and without an apical extension (Table 1). In the Mediterranean waters, Gomez & Abboud-Abi Saab (2003) reported the pres­ ence of C. yeye and Ceratoperidinium sp. (with an elongate and curved apical extension) at the same location. Conse­ quently, C. mediterraneum was reported as intermediate be­ tween C. yeye and Ceratoperidinium sp. Athecate dinoflagel­ lates such as P.seliodinium vauhanii Soumia are very variable with respect to the size of their flexible extensions (Soumia 1972). Recently, Konovalova (2003) reported that P. vauhanii constitutes one stage in the life history of Gyrodinium falca- tum Kofoid & Swezy. Within this context, the relative size of the apical extension of Ceratoperidinium should not be con­ sidered as a criterion for the differentiation of species. Until further research, taxa such as C. mediterraneum or Cerato­ peridinium sp. (Gomez & Abboud-Abi Saab 2003) should be considered as a morphological variety of the type species. Cell division occurs in specimens with short apical extensions. Specimens lacking the apical extension showed a larger size than those with the apical extension. Despite the distinctive morphology and the relatively large size (> 200 |xm), records of Ceratoperidinium are extremely rare. Even distinctive taxa remain insufficiently known, es­ pecially in open waters of the subtropical and tropical oceans. ACKNOWLEDGEMENTS This study was supported by Grant-in-aid for Creative Basic Research (12NP0201, DOBIS) from the MEXT, Japan. Sam­ ples in the Sulu and Celebes Seas were collected during the KH-02-4 cruise by the Ocean Research Institute of the Uni­ versity of Tokyo. We are thankful to the Philippine Govern­ ment for permission for investigation in the Sulu Sea. Samples from the western Equatorial Pacific Ocean were collected dur­ ing the MR02-K06 cruise by the Japan Marine Science and Technology Center (JAMSTEC). F.G. acknowledges the finan- Figs 8, 9. Ventral and lateral views, respectively, o f another specimen. Figs 10, II . Two different specimens lacking an apical extension; dorsal view. The arrow in Fig. 10 (inset) indicates the extremity' o f the antapical extension. Figs 12, 13. Dorsal and ventral views, respectively, o f the same specimen. Fig. 14. Specimen undergoing division. The arrows indicate the cingular grooves. 258 Phycologia, Vol. 43 (4), 2004 y -'i '- \ !k 4 4 >" è y . M l . w. tkfU j;0 A T ^' : . k‘: ‘•' u ■• # . F igs 15 -2 4 . Ceratoperidinium yeye. D lC (except Fig. 17, epifluorescence). Scale bars = 20 p,m. Fig. 15. Specimen in dorsal view showing microfilaments within the kidney-shaped nucleus. Fig. 16. Specimen in dorsal view undergoing division. Fig. 17. The DAPI-Fluorescent Brightener-stained specimen showing the nucleus glowing brightly in a lateral location under UV excitation. No Fluorescent Brightener-stained cellulose (blue) was observed that would indicate the presence o f thecal plates. Figs 18-20. Detail o f the cingulum. Fig. 18. Ventral view. The arrow indicates the cingulum. Fig. 19. Ventral view. The arrows indicate the discontinuitv' in the cingular groove (the fibres are not related to the specimen). Fig. 20. The arrow points to pores in the surface o f the base o f the hyposoma. Figs 21 -2 4 . Specimen undergoing division. Note the shape o f the nucleus in Fig. 22 (also Fig. 17). 259 Gômez et al.: Observations oa Ae dinoflagellate Ceratoperidinium ventral dorsal Figs 25, 26. Schematic Une drawings of the Orientation (ventral and dorsal, respectively) of a Ceratoperidinium cell. cial siqjport by Ae European Commission (ICB2-CT-2001- 80002). REFERENCES A bboud-A bi Saab M . 1989. Les d inofiagellés des eaux côtières li­ banaises - espèces ra res o u nouvelles du ^ y ttq ila n c to n m arin. Leb­ anese Science Bulletin 5: 5-16. D odoe J.D. & C raw ford R.M. 1970. A survey of thecal fine structure in the Dinophyceae. Botanical Journal o f the Linnaean Society 63: 53-67. F ensome R.A., Taylor F.J.R., N orris G., Sarjeant WA S., W harton D.I. & W illiams G.L. 1993. A classification o f living and fossil dinoflagellates. American Museum of Natural History, Sheridan Press, Hanover, Pennsylvania. 351 M*. [Journal o f Micropaleontol­ ogy, qjecial publication 7.] Fkrrz L. & Tbjemer R.E. 1985. A rapid, stnqile technique utilûâng caloofiuor vridte M2R for the visualization of dinoflagellate Aecal plates. Journal o f Phycology 21: 662-664. Gômez F. 2003. Checklist of Mediterranean fiee-Uving dinoflagellates. Botanica Marina 46: 215-242. Gômez F. & Abboud-A bi Saab M. 2003. Records of Ceratoperidinium Margalef (Dinophyceae) from the Nfeditenanean Sea. Vie et Milieu 53: 4^-46. CHieuter W, M cN eill J ., B arrie F.R., B urdet H.M., D emoulin V., F ilgueiras T.S., N icolson D .H ., S dlva P.O., Skog J .E ., T rehane P., T urland j. & H awksworth D.L. 2000. International Code o f Bo­ tanical Nomenclature (Saint Louis Code). Koeltz Scientific Books, Konigstein, Germany. 474 pp. [Regpum Vegetabile 138.] H asle G.R. & Syvertsen E.E. 1997. Marine diatrans. In: Identijying marine phytoplankton (Ed. by C.R. Tomas), pp. 5-385. Academic Press, &m Diego. Konovalova G.V. 2003. The life histray of Gyrodinium fcdcatum and vaUdity of Pseliodirdum vaubanii (Dmq;>hyceae). Russian Journal o f MaNpe Biplogy 29: 167-170. ; Loeblich À.R. ill. 1980. Dinofla^Ilate nonrénclàture. Taxon 29:321- 324. L o e b lich A R. IlL 1982. Dinophyceae. In: Synopsis and classification o f living organisms (Ed. by S.P. Parker), pp. 101-115. McGraw- Hill;NearYdrk M argalef R. 1969. Conqiosicion eqjecifica del fitoplancton de la costa catalano-levantina (Mediterraneo occidental) en 1962-1967. Investigaciones Pesqueras 33: 345-380. M orrill L.C. & Loeblich AiL HI. 1981. The dinoflagellate pellicular wall layer and its occurrence in die division Pyrrbofdiyta. Journal o f Phycology 17: 315-323. Porter K.G. & Feig Y.S. 1980. The use of DAPI for identifying and counting aquatic microflraa. Limnology and Oceanograpl^ 25: 943-948. Sournia A. 1972. Une période de poussées phytoplanctoniques prés de Nosy-Bé (Madagascar) en 1971. Eqièces rares ou nouvelles du phytoplancton. Office de la recherche scientifique et technique d'Outre-mer. Cahiers, série océanographique 10: 151-159. SouRNiA A. 1982. Catalogue of the species and infiaspecific taxa of the recent marine dinoflagellates (IHnopfayceae) publidied since the revision by J. SchiUer FV. ArchtvJSr I^tistenîainde 126: 151-168. Sournia A. 1986. Atlas du phytoplancton marin: introduction. Cy­ anophycées, Dictyochophycées, Dinophycées et Raphidophycées, vol. 1. Editicms du Centre Natitmal de la Recherche Scientifique, Paris. 219 HJ. V elasquez Z.R. 1997. Fitoplancton en el Mediterràneo Norocciden­ tal. MiD thesis. Universitat Politècnica de Catahmya, Barceltma. 272 + 55 pp. Received 30 June 2003; accepted 6 January 2004 Communicating editor: T. Horiguchi 260 3.2. Taxonomia y distribucién de dinoflagelados poco conocidos: 3.2.3. Gynogonadinium gen. prov. Gômez, F. Gynogonadinium aequatoriale, gen. e t sp. nov. a new dinoflagellate from the open western Equatorial Pacific. Algae, enviado. 261 Gynogonadinium aequatoriale gen. et sp. nov., a new Dinoflagellate from the Open Western Equatorial Pacific Fernando Gômez Station Marine de Wimereux, Universirte de FRE 2816 ELICO CNRS, Université des Sciences et Technologies de Lille-Lillel, 28 avenue Foch, BP 80, F-62930 Wimereux, France Corresponding author (femando.gomez@fitoplancton.com) Phone +33 321992926 FAX +33 321992901 Short running title: Gynogonadinium aequatoriale gen. et sp. nov. A new genus and species of marine dinoflagellate fiom the open western equatorial Pacific Ocean, Gynogonadinium aequatoriale gen. et nov. sp., is described from light and scanning electron micrographs. This laterally compressed unarmoured taxon had a triangular cell body in lateral view with two different elongate extensions. The end of the apical extension was spherical with a groove that arises from the epicone in the ventral side of the cell. The antapical extension was longer. The dorsal part of the cingulum showed undulated lists in each margin. The nucleus was ellipsoidal and perpendicularly crossed the cingulum. Dimensions of cells were 90-110 //m long and 43-50 //m wide in lateral view at the level of the cingulum Gynogonadinium is placed in the order Gymnodiniales, family uncertain. Key Words: Dinophyceae, equatorial Pacific Ocean, Gynogonadinium aequatoriale, phytoplankton, taxonomy 262 mailto:femando.gomez@fitoplancton.com INTRODUCTION Taxonomic studies of unarmoured dinoflagellates from open waters of tropical oceans are few in number. The Western Pacific Warm Pool (western equatorial Pacific Ocean) is a poorly studied region of the world’s oceans for phytoplankton taxonomy. From samples collected in that region under influence of the phenomenon of El Nino in 2003, several specimens of a distinctive unarmoured dinoflagellate, which could not be ascribed to any known genus, were found. Despite the scarce specimens available and its delicacy, by using the Takayama’s method (Takayama 1985) was successfully obtained SEM pictures. This dinoflagellate with a distinctive shape and unique morphological characters is here described. MATERIALS AND METHODS A cruise was carried out on board R/V Mirai (15-28 January 2003) along the Equator from 160°E to 160°W. Samples were collected from 9 stations at 14 depths between 0 and 200 m depth. Samples were collected using Niskin bottles, preserved with acidified Lugol’s solution and stored at 5°C. Subsamples (400 mL) were allowed to settle in glass sedimentation cylinders. The top 350 mL of each sample was siphoned off progressively over 5 days using a length of small-bore tubing. The remaining 50 mL was settled in composite sedimentation chambers. Light microscopy observations were made as described in Gomez et al. (2004). For scanning electron microscopy (SEM), specimens were isolated with a cq)illary from sedimentation chambers and adhered to poly-L-tysine-coated cover-slip. Fixed cells attached to the cover-slip were rinsed twice in distilled water for 5 min each. Cells were then dehydrated through an ethanol series, dried in a critical point drier (HCP-2, Hitachi, Tokyo, Japan), and coated with Au-Pd (Takayama 1985). Observations were made using a SEM (S- 800, Hitachi, Tokyo, Japan). 263 RESULTS AND DISCUSSION Gynogonadinium aequatoriale gen. et sp. nov. Figs. 1-14 Diagnosis: Cellula latérale compressae, 90-110 pm longae et 43-55 pm latae. Media pars aequa portione a cingulo divisa. Hypoconus et epiconus triangulatus. Duo longa curvaque brachia tumescentihus extremitatibus, aliquid dissimilar. Cellula apertae femina gonada. Nucleus dinokaryoticus elongatus, in parte centralis cellulae situs. Cells of Gynogonadinium aequatoriale are laterally compressed, with size 90-110 pm in length 43-55 pm in width. The cingulum divides the cell in two similar parts. Hypocone and epicone are triangular in shape. Two curve extensions of different size arise from the extremes. The cell resembles the female gonad. The dinokarion is located in the part central of the cell. Holotype: Figure 8 collected by F. Gômez. Isotype: Figures 3-7. Type locality: Western equatorial Pacific Ocean (0°, 160°E), 15 m depth. Etymology: Gyn-, Gyno- (from Greek: female, woman); Gonad-, Gonado- (fiom Latin: ovary or testis based on Greek: gonos: “seed”): referring the contour of the cell that resembles the female gonad. Aequator (fiom Latin: equator): referring to the type locality. Morphology: Based on light microscopy, the outline of the cell body in lateral view was triangular with two elongate extensions. The median cingulum was slightly deflected antapically on the dorsal side. The outline of the cell resembled a female gonad (Figs. 1, 3). One flexible, elongated apical extension arose fiom the ventral side of the cell body. The end of the apical extension was spherical with ~5 pm in diameter (Figs. 1-4). The antapical extension, also arising fiom the ventral side of the cell body, was longer than the apical extension. The ending of the ant^ical extension was roughly spatulate in shape (Fig. 5). The 264 nucleus was visible undo* differential interference contrast optics (Fig. 6) and, when stained with DAPI (4,6-diamidino-2-phenylindole), glowed brightly under UV excitation. In lateral view, the nucleus had an elongate ellipsoidal shape, perpendicularly crossing the median cingulum. The part of the nucleus located in the epicone was curved towards the ventral side (Figs. 5-7). The brownish pigmentation suggested the presence of peridinine. No chloroplasts were observed. Unfortunately from Lugofpreserved specimens cannot be tested the presence of the chlorophyll-a by epifluorescence microscopy. One of the specimens was successfully prepared for SEM (Figs. 8-13). SEM allowed observing the sulcus, two flagellar pores (Fig. 12) and an apical groove from the epicone to the extreme of the apical extension (Figs. 10, 11). The groove surrounded the spherical-shaped end of the apical extension (Fig. 11). The margins of the cingulum in the dorsal side showed undulated hsts, anterior and posterior (Fig. 13). The specimens ranged from 90-110 pm long and 43-55 pm wide at the cingulum level (Table 1). Habitat: Seven specimens were collected from five consecutive sanqiling stations along 2200 km in the equator from 160”E to 180° between 15 and 110 m depth. This study was a part of twelve cruises carried out in the open Pacific between 41 °N and 34°S (Gômez 2005). The records of Gynogonadinium aequatoriale were restricted to the westernmost edge of the Equatorial Pacific Ocean (Table 1). Species comparison: Gynogonadinium is laterally compressed taxon and consequently the ventral side is difi&ult to observe under light microscopy. If the ventral position is forced (Figs. 2, 4), the outline of this taxon could resemble Gyrodinium falcatum Kofoid et Swezy (=Pseliodinium vaubanii Soumia) (Kofoid 1931; Konovalova 2003). However, Gynogonadinium (Figs. 14-15) has a cell body of triangular contour in lateral view whereas Gyrodinium falcatum has an ellipsoidal shape in both lateral and dorso-ventral views. Other distinctive morphological characters such as the undulated cingular lists and the extensions are unique in Gynogonadinium. The cingular lists have been described in armoured 265 dinoflagellates (Almazan Becerril and Hemandez-Becerril 2002; Vershinin and Morton 2005), but rarely in unarmoured dinoflagellates. Balech (1975, p. 11) illustrated cingular list in Gymnodinium cf. diploconus Schütt The qjical groove as found in Gynogonadinium is a morphological character of some gymnodiniaceans (Takayama 1985). I hesitate to assign this species to any currently known family, and until further research, Gynogonadinium is placed in the order Gymnodiniales, family uncertain ACKNOWLEDGEMENTS This study was supported by a fellowship of the European Commission (ICB2-CT-2001- 80002) held at the University of Tokyo with K. Fumya as host. I thank H. Takayama and Y. Nagahama for assistance on SEM preparations. I am gratefiil to the scientists and crew of R/V Mirai (JAMSTEC). This is a contribution to a Grant-in-aid for Creative Basic Research (12NP0201, DOBIS) fiom the MEXT and the French IFB ‘Biodiversité et Changement Global’ program. REFERENCES Almazan Becerril A. and Hernandez-Becerril D.U. 2002. A new species of the dinoflagellate (Dinophyceae) genus Dinophysis fiom the Mexican Caribbean Sea, Dinophysis siankanensis sp. now. Phycologia 41: 314-3M. WâlmiNN Publicacion 11, Buenos Aires. Gomez F., Nagahama Y., Fukuyo Y. and Furuya K. 2004. Observations on Ceratoperidinium (Dinophyceae). Phycologia 43: 416-421. Gomez F. 2005. Histioneis (Dinophysiales, Dinophyceae) fiom the western Pacific Ocean. Botanica Marina 48: 421-425. 266 Kofoid C.A. 1931. Report on the biological survey of Mutsu Bay. 18. Protozoan fauna of Mutsu Bay. Subclass Dinoflagellata; Tribe Gymnodinoidae. Fac. ScL Rep. Tohoku Imperial Univ. 4^ ser., Biol. 6: 1-43. Konovalova G.V. 2003. The hfe history of Gyrodinium falcatum and validity of Pseliodinium vaubanii (Dinophyceae). Russian J. Mar. Biol. 29: 167-170. Takayama H. 1985. Apical grooves of unarmored dinoflagellates. Bull. Plankton Soc. Japan 32: 129-40. Vershinin A. and Morton S.L. 2005. Protoperidinium ponticum sp. nov. (Dinophyceae) from the northeastern Black Sea coast of Russia. Bot. Mar. 48: 244-247. 267 Table 1. Gynogonadinium aequatoriale: stations, depth, geographic coordinates (latitude, longitude), date and dimensions: W, width at the level of the cingulum in lateral view; L, total length of each record. Station Depth (m) Latitude Longitude Date W (um) L(//m) Figures 6 -15 0° 160°E 15 Jan 2003 48 110 1-2, 8-13 6 -30 0° 160°E 15 Jan 2003 45 95 5-7 7 -30 0° 165°E 17 Jan 2003 52 105 - 8 -110 0° 170°E 18 Jan 2003 43 90 - 9 -15 0° 175°E 20 Jan 2003 55 110 - 9 -40 0° 175°E 20 Jan 2003 53 110 3-4 10 -40 0° 180° 21 Jan 2003 50 105 - 268 FIGURE LEGENDS Figs. 1-7. Photomicrographs of Gynogonadinium aequatoriale, bright field optics. 1-2. Right lateral and ventral view of one specimen (also Figs. 8-13). 3-4. Another specimen in lefl: lateral and ventral view. 5-6. Nomarski differential interference contrast (DlC) micrographs of another specimen See nucleus in Fig. 6. 7. Epifluorescence photomicrographs of the same specimen stained with DAPI (4,6-diamidino-2- phenylindole) showing the nucleus glowing brightly under UV excitation N= nucleus. Scale bars: 20 pm. Figs. 9-13. Gynogonadinium aequatoriale, scanning electron micrographs (also Figures 1-2). 9-10. Left lateral and ventro-left lateral view, respectively. 10-11. Detail of the ^ical extension. The arrows indicates the apical groove. 12. Detail of die cingulum-sulcus area. See the flagellar pores. 13. Detail of the cingulum in the dorsal part of the cell. AG= qiical groove C= cingulum; CL= cingular list; LFP = longitudinal flagellum pore; S= sulcus; TFP = transverse flagellum pore. Figs. 9-10, Scale bars: 20 pm. Figs. 11-13, Scale bars: 5 pm Figs 14-15, Gynogonadinium aequatoriale, line drawings. 14. Left lateral and 15. ventral view, respectively. Scale bars: 20 p m 269 3 r» r ' f t'- # \ . B&KNI ■f V S t i ' 270 i È m 3# 271 112 3.2. Taxonomia y distribucién de dinoflagelados poco conocidos: 3.2.4. Noctiiucales: Scaphodinium, Petalodinium, Leptodiscus, Spatulodinlum, Kofoidinium, Pomatodinium. Gômez, F. & Furuya, K., 2004. New records of Scaphodinium mirabile (Dinophyceae), an unnoticed dinoflagellate In the Pacific Ocean. Phycological Research 52, 13-16. Gômez, F. & Furuya, K., 2005. Leptodiscaceans (Noctllucales, Dinophyceae) from the Pacific Ocean: First records of Petalodinium and Leptodiscus beyond the Mediterranean Sea. European Journal of Protistology 41 , 231-239. Gômez, F. & Furuya, K., 2006. Kofoidinium, Spatulodinlum and other kofoldlnlaceans (Noctllucales, Dinophyceae) In the Pacific Ocean. European Journal of Protistology 43, aceptado. Gômez, F. & SoulssI, S. 2006. On the ecology and unusual life cycle of the dinoflagellate Spatulodinlum pseudonoctiluca In the NE English Channel. Comptes Rendus Biologies, enviado. 273 Phycological Research 2004; 52; 13-16 Research note New records of Scaphodinium mirabile (Dinophyceae), an unnoticed dinoflagellate in the Pacific Ocean Fernando Gômez* and Ken Furuya Department of Aquatic Biosciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan SUMMARY Previous records of dinoflagellate Scaphodinium mira­ bile Margalef (Leptodiscaceae, Noctllucales) were restricted to the Mediterranean-Black Sea and Eastern Atlantic Ocean. Nine and 34 specimens were observed in the upper 100 m layer in May and July, respectively, in a cross-section in the vicinity of the Kuroshio Current (NW Pacific Ocean). Nearly all the Lugol-fixed speci­ mens appeared folded over themselves, an appearance that differs from the view reported in the scarce literature available. Key words: aberrant dinoflagellate, Dinophyceae, Dino- phyta, Kuroshio Current, Noctllucales, Pacific Ocean, phytoplankton, Scaphodinium, taxonomy. The role of heterotrophic and mixotrophic phytoplank­ ton, in particular dinoflagellates, on pelagic food webs has recently received significant attention (Gaines and Elbrachter 1987; Hansen 1991). However, among heterotrophic dinoflagellates, taxa belonging to the order Noctiiucales Haeckel (see Gômez 2003 for a species list) have received less attention, with the exception of the red tide species Noctiluca scintillans (Macartney) Kofoid. The morphology of the Noctllucales differs markedly from the Peridiniales, notably by the presence of contractile muscle-like fibrils involved in movements and cell shape changes (Cachon and Cachon-Enjumet 1964, 1966; Cachon and Cachon 1967a,b, 1969). Members of die family Leptodiscaceae F.J.R. Taylor are shaped, encapsulated nucleus. No chloroplasts are present and the cytoplasm contains a uniform network of myo-fibrils (Cachon and Cachon 1969; Sournia 1986). The type species of this monotypic genus, Scaphod­ inium mirabile Margalef, was originally described from the Spanish Mediterranean coastal waters (Margalef 1963). From the NW Mediterranean Sea, Cachon and Cachon-Enjumet (1964) reported the taxonomic Junior synonym Leptospathium navicula. The species has been further reported in the Mediterranean Sea (Margalef 1969a,b; Léger 1971; Abboud-Abi Saab 1989; Gômez and Gorsky 2003), the Eastern Atlantic Ocean Margalef (1973, 1975) and recently from the Marmara and Black Seas (Balkis 2000; Stoyanova 1999). This study reports for the first time Scaphodinium mirabile in the Pacific Ocean. Notes on the distribu­ tion, morphology, and on the reasons for the apparent underestimation of this species are given below. The material was collected from two cruises (13 -20 May and 3 -1 0 July, 2002) aboard RA/ Soyo-maru carried out along the meridian 138° in the vicinity of the Kuroshio Current. During the cruise in May, nine stations were sampled from 30°30'N to 34°15'N . In July 10 stations were sampled from 30°0'N to 34°20'N. At each station, 15 discrete depths from 5 -2 0 0 m were sampled with Niskin bottles (Table 1). Seawater samples were preserved with acidified Lugol's solution (Hasle and Syvertsen 1997; p. 334) and stored at about 5°C. Samples were preconcentrated via settling in glass cylinders, and concentrates settled in standard sedi­ mentation chambers. Concentrates equivalent to 400 mL were observed with a Nikon inverted microscope equipped like extension (the velum) not associated with either the cingulum or the sulcus (Taylor 1976; p. 184; Fensome eta l. 1993; p. 182; regarding the authorship of the family Leptodiscaceae see Fensome e ta l. 1993; p. 183). Scaphodinium is an extremely flattened biflagellate cell, usually folded over one of its faces. The flattened portion is projected in both ends, with the extension closest to the nucleus being bilobulate, shorter and wider than the other. No sulcus or cingulum have been reported; the proximal parts of both flagella are sheathed in tube-like channels located next to the large, egg­ The number of samples analyzed was 131 in May and 144 in July, representing a total volume of 106 L of seawater examined in both cruises. In May nine specimens of Scaphodinium were found in eight samples (6% of the total samples), whereas in July, 34 specimens *To whom correspondence should be addressed. Email: fernando.gomez@fitoplancton. com Communicating editor: G. Hansen. Received 2 5 April 2003; accepted 12 August 2003. 274 14 F. Gômez and K. Furuya l i l m £> 8 â 8 Z S î, es CM Ü e t û (O t) 8 k O O O I t - O O ^ - O O O O l l O O O O O t- O O ' - O O O O O O O 0 0 0 0 t - 0 C \ J 0 » - 0 v - 0 0 I o O t - ^ O O O O O O O O O O I o OOO I o o o > - o o o o o o o O poO O t- O O O t- O O O O O O O O O O O t- O O t- t- O O O O 0 0 0 0 0 c s j 0 » - 0 r - 0 0 0 0 O ' - OOO Ov J OOOOOOOO 0 r - 0 0 0 0 0 » - 0 0 0 0 t - 0 OO l O O O O O O O O O O O I O O O O O O O O r - T - T - O O O O o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o OO l O O O O O i - O O O O O O O O r - O r - O O O O O O O O O O o o o o o o o o o o o o o o o OO l OOOOCS J OOOOOOO o o o o o o o o o o o o o o o 5 o O O O O O O O O O ^ O J £ ) 0 O-r- c \ j o o ' ^ L O c o p ' C O O > o c M i n r ^ o â ............................. T T T T 7 were found in 29 samples (20% of the total samples). The maximum number of specimens found in a single sample (0.4 L) was three (Table 1). Nearly all the specimens were recorded in the upper 100 m layer. The number of records was higher in the summer than in the spring (Table 1). The morphology of leptodiscaceans results in a difficult interpretation of cell orientation. According to the interpretation by Cachon and Cachon (1969) the part of the cell containing the flagella is considered the hyposoma. During routine microscopical observation, the specimens appeared in several views with different appearances (Figs 1 -4 ,6 -12 ). The non-folded view found in the literature (Sournia 1986; fig. 143) was only found in two of 43 specimens observed (Figs 1,2). The flagella were not visible in most specimens, probably because they were lost as a result of the fixation. The transverse flagellum (TF), as defined by Cachon and Cachon (1969), is usually coil-shaped and larger than the longitudinal flagellum (Figs 2 ,3 ,8 -10 ). The inser­ tion of the TF is located between the nucleus and the bi-lobuled extremity (Figs 3,7). Fensome e ta l. (1993; p. 182) apparently followed the interpretation of the orientation by Cachon and Cachon (1969). However the orientation of the cell and the labeling of the flagella by Fensome e ta l. (1993; their fig. 186D) is the reverse of Cachon and Cachon (1969) interpreta­ tion and even the path of each flagellum is different. Nearly all the Lugol-fixed specimens appeared folded, extremity against extremity (Figs 3 ,4 ,6 -10 ). In lateral views, considered here as the view showing the extreme low thickness in relation to the cell body, the flagella appeared to the exterior side (Figs 3 ,6 -10). One of the specimens observed was undergoing binary fission (Figs 11,12). Scaphodinium can be considered homogeneously distributed in the euphotic zone, with no clear latitudi­ nal trends, despite the studied area covering a wide range of hydrographical and trophic conditions. It can only be inferred that this taxon tends to be more abundant in the summer (Table 1). In the Black Sea, this species was also more common during the summer (Stoyanova 1999). The salinity does not seem to influence on the distribution of Scaphodinium, if it is species as een recor e , rom t e sa me waters o the eastern Mediterranean basin (salinity of 38 -39 ) to the brackish waters of the Black Sea with salinity values of 1 5 -18 (Stoyanova 1999). Concerning the trophic conditions, the eutrophic Black Sea waters strongly differ from the oligotrophy that prevails in the adjacent waters of the Kuroshio Current. Despite its relatively large size, which renders the organisms easily collectable by net or bottle sampling, records of Scaphodinium are scarce. Other reasons for the underestimation of Scaphodinium, during routine analyses are: 275 An unnoticed dinoflagellate in the Pacific Ocean 15 LF \ TF 8 10 f Figs 1-12. Photomicrographs of Scaphodinium mirabile Margalef and (Fig. 5) of an appendicularian. 1,2. A non-folded specimen with a coil-shape transverse flagellum (TF). Scale bar = 100 pm (May St. 9, 80 m depth). 3,4. Two views of the same specimen. The arrow points at the insertion of the TF (July B02, 60 m depth). 5. An appendicularian here presented for a comparison to the lateral views of Scaphodinium. 6,7. Lateral views of a specimen showing the longitudinal (LF) and transverse flagella (July St. 3, 40 m depth). 8-10. Several views of the same specimen showing the TF (May St. 6, 20 m depth). 11,12. Two views of a specimen under division (July St. 6, 5 m depth). 276 16 F. Gômez and K. Furuya 1 Scaphodinium is usually missing in the literature used for phytoplankton identification, with the excep­ tion of Sournia (1986) and Fensome et ai. (1993). The original description of the species (Margalef 1963) and further records (Cachon and Cachon- Enjumet 1964; Margalef 1969a,b, 1973, 1975; Léger 1971; Abboud-Abi Saab 1989; Stoyanova 1999; Balkis 2000) appeared in journals that are not easily accessible. 2 The morphology of leptodiscaceans is highly modi­ fied compared to typical dinoflagellates (Peridini- ales). The lack of a cingulum, sulcus and the possible loss of the flagella by fixation, contribute to the difficulties in identification. In the microscope, Lugol-fixed cells of Scaphodinium appear In views with different appearances that only with difficulty can be considered as a dinoflagellate (Figs 1-4 ,6-10). 3 The photomicrographs or drawings reported in the literature show views of non-folded cells. However, in this study nearly all Lugol-fixed specimens were folded with no visible flagella, and may look like the damaged tail of an appendicularian to a non­ experienced observer (Fig. 5). In conclusion, correct identification of species of this group of heterotrophic dinoflagellates is a critical step in the evaluation of its role in pelagic food webs. ACKNOWLEDGMENTS This study was supported by Grant-in-aid for Creative Basic Research (12NP0201, DOBIS) from the MEXT, Japan. F.G. acknowledges the financial support by the European Commission (ICB2-CT-2001-8(X)02). Dr K Nakata provided samples from cruises of the SOYO program by the Japanese National Research Institute of Fisheries Science. REFERENCES Abboud-Abi Saab, M. 1989. Les dinoflagellés des eaux côtières libanaises- Espèces rares ou nouvelles du phyto- plancton marin. Leban. Soi. Bull. 5: 5-16. Balkis, N. 2000. Five dinoflagellate species new to Turkish : seas. Oebalia 26; 97-108. n . J,; and C c on M. 196 a. Ç mbodiniu e/e nov. gen. nov. sp. péridinien Noctiluci ae Savil e- en . Protistologica 3: 313-8. Cachon, J. and Cachon, M. 1967b. Contribution à l'étude des Noctilucidae Saville-Kent, I. Les Kofoidininae Cachon J. et M. Évolution, morphologique et systématique. Protistolog­ ica 3: 427-44. Cachon, J. and Cachon, M. 1969. Contribution à l'étude des Noctilucidae Saville-Kent. Évolution, morphologique, cytologie, systématique. II. Les Leptodiscinae Cachon J. et M. Protistologica 5: 11-33. Cachon, J. and Cachon-Enjumet, M. 1964. Leptospathium navicula nov. gen., nov. sp. et Leptophyllus dasypus nov, gen. sp., péridiniens Noctilucidae (Hertwig) du plancton néritique de Villefranche-sur-Mer. Bull. Inst Océanogr. Monaco 62: 1-12. Cachon, J. and Cachon-Enjumet, M. 1966. Pomatodinium impatiens nov. gen. nov. sp. péridiniens Noctilucidae Kent. Protistologica 2: 23-30. Fensome, R. A., Taylor, F. J. R, Norris, G., Sarjeant, W, A. S., Wharton, D. I. and Williams, G. L. 1993. A classification of living and fossil dinoflagellates. J. Micropaleontology 1: (special publication) 1-351. Gaines, G. and Elbrachter, M. 1987. Heterotrophic nutrition. In Taylor, F, J. R. (Ed.) The Biology of Dinoflagellates. Botanical Monographs, Vol. 21. Blackwell Science, Oxford, pp. 224-68. Gômez, F. 2003. Checklist of Mediterranean free-living dino­ flagellates. Bot. Mar. 46: 215-242. Gômez, F. and Gorsky, G. 2003. Microplankton annual cycles in the Bay of Villefranche, Ligurian Sea, NW Mediterra­ nean. J. Plank. Res. 25: 323-39. Hansen, P. J. 1991. Quantitative importance and trophic role of heterotrophic dinoflagellate in a coastal pelagic web. Mar. Ecol. Prog. Ser. 73: 253-61. Hasle, G. R. and Syvertsen, E. E. 1997. Marine Diatoms. In Tomas, C. R.w (Ed.) Identifying Marine Phytoplankton. Academic Press, San Diego, pp. 5-385. Léger, G. 1971. Les populations phytoplanctoniques au point 42°47'N, 7°29'E. Bouée laboratoire du C.O.M.E.X.O./ C.N.E.X.O. Généralités et premier séjour (21-27 février 1964). Bull. Inst Océanogr. Monaco S9: 1-42. Margalef, R. 1963. Scaphodinium mirabile noy. gen. nov. sp., un nuevo dinoflagelado aberrante del plancton mari no. Miscelânea Zool. Barcelona ̂: 1-2. Margalef, R. 1969a. Composiciôn especffica del fitoplancton de la costa catalane-levantina (Mediterrâneo occidental) en 1962-67. Inv. Pesq. 33: 345-80. Margalef, R. 1969b. Small scale distribution of phytoplank­ ton in western Mediterranean at the end of July. Pubbl. Staz. Zool. Napoli 37 (Suppl ): 40-61. Margalef, R. 1973. Fitoplancton marino de la regiôn de afloramiento del NW de Africa. Res. Exped. dent. B/0 Cornide 2: 65-94. Margalef, R. 1975. Composiciôn y distribuciôn del fitoplanc­ ton marino de la regiôn de afloramiento del NW de Africa. Res. Exped. dent. B/0 Cornide 4: 145-70. n ro uc ion, yanop yc es, ic oc op yc es, mop y- cées et Raphidophycées. Editions du Centre National de la Recherche Scientifique, Paris, 219 pp. Stoyanova, A. P. 1999. New representatives of noctilucales in the Bulgarian Black Sea coastal water. Comptes Rend. Acad. Bulgare Sci. 52: 119-22. Taylor, F. J. R. 1976. Dinoflagellates from the International Indian Ocean Expedition. A report on material collected by R/V 'Anton Bruun' 1963-64. Biblioteca Bot. 132: 1-234. 277 ELSEVIER Available online at www.sciencedirect.com S CIENCE DIR EOT* European Journal o f Protistology 41 (2005) 231-239 European Journal of PROTISTOLOGY www.elsevier.de/ejop Leptodiscaceans (Noctilucales, Dinophyceae) from the Pacific Ocean: First records of P e t a l o d i n i u m and L e p t o d i s c u s beyond the Mediterranean Sea Fernando Gomez^’*, Ken Furuya^ ^Station Marine de Wimereux, Université des Sciences et Technologies de Lille, CNRS UMR 8013 ELICO, 28 avenue Foch, BP 80, F-62930 Wimereux, France ^Department o f Aquatic Biosciences, The University o f Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan Received 31 March 2005; received in revised form 11 May 2005; accepted 14 May 2005 Abstract Records of dinoflagellates of the family Leptodiscaceae (Noctilucales) from the Kuroshio Current, Philippine, Celebes, Sulu, South China Seas and the western and central Equatorial Pacific Ocean are described. Scaphodinium mirabile was the most common leptodiscacean. Two specimens that differed from the type species of Scaphodinium were found; one specimen showed a highly bifurcate proximal extremity and another showed two dissimilar proboscides from the distal extremity. Another unidentified leptodiscacean showed an arrowhead-shaped contour with the margins folded. Six specimens of Petalodinium porcelio were found, being the first record beyond the Mediterranean-Black Seas. Six specimens were tentatively assigned to the genus Leptodiscus, being the first record beyond the western Mediterranean Sea. The folded specimens that ranged from 90 to 120 pm in diameter and with a prominent flagellum were tentatively considered to be young specimens of Leptodiscus. The abundance of the leptodiscaceans is underestimated in the world’s oceans. © 2005 Elsevier GmbH. All rights reserved. Keywords: Scaphodinium', Petalodinium', Leptodiscus', Noctilucales; Dinophyta; Pacific Ocean Introduction The Noctilucales Haeckel differ markedly from the rest of the dinoflagellates, notably by the presence of contractile muscle-like fibrils involved in cell shape changes and movements. The noctilucaceans have been placed as an order in the class Dinophyceae (Sournia 1986) or as the class Noctiluciphyceae Fensome et al. The family Leptodiscaceae Kofoid is the least known "Corresponding author. Tel.: + 33 321992926; fax: +33 321992901. E-mail address: femando.gomez@fitoplancton.com (F. Gômez). 0932-4739/$ - see front matter i doi: 10.1016/j.ejop.2005.05.003 among the Noctilucales, Their cell bodie^^ e strongly anterb-postëriDfI5l*fettèhèdSvith â: biiafëraf^mmetry'of with equatorial wing-like expansions lacking the dome, being able to contract suddenly when the surrounding water is disturbed (Cachon and Cachon 1967, 1969, 1984, 1986). No chloroplasts have been reported. Neither sulcus nor cingulum has been reported. The leptodiscaceans comprise the monotypic genera Cacho- nodinium Loeblich I I I ( = Leptodinium J. Cachon et M. Cachon), Craspedotella Kofoid, Leptodiscus Hertwig ( = IFratjetella Lohmann), Leptophyllus J. Cachon et Cachon-Enjumet ( = Abedinium Loeblich Jr et Loeblich 2005 Elsevier GmbH. All rights reserved. 278 http://www.sciencedirect.com http://www.elsevier.de/ejop mailto:femando.gomez@fitoplancton.com 232 F. Gômez, K. Furuya / European Journal of Protistology 41 (2005) 231-239 III), Petalodinium J. Cachon et M. Cachon and Scaphodinium Margalef ( = Leptospathium J. Cachon et Cachon-Enjumet). Cachon and Cachon-Enjumet (1964) and Cachon and Cachon (1967, 1969, 1984, 1986) carried out most of the studies on these taxa from the coastal waters of the Ligurian Sea (NW Mediterra­ nean Sea). Since their observations, the records of leptodiscaceans have been scarce and several genera have never been reported after the initial descriptions. The deformation due to preservation and the bizarre appearance of the leptodiscaceans compared to other dinoflagellates makes the detection of these species difficult. The leptodiscaceans are extremely delicate and easily deteriorate during sample treatment. The study of live specimens of dinoflagellates during oceanic research cruises is difficult and examples are scarce (Elbrachter 1979). Unfortunately the analysis of fixed samples is not comparable to the detailed studies on the morphology and the life cycle carried out by Cachon and Cachon (1967) and Cachon and Cachon (1969) from thousands of live specimens collected from coastal waters. Little is known about the occurrence of the lepto­ discaceans in oceanic waters. Recently Gomez and Furuya (2004) reported the presence of Scaphodinium mirabile in the Pacific Ocean for the first time from two cruises in the vicinity of the Kuroshio Current. This study deals with the leptodiscaceans recorded in further cruises in the western Pacific Ocean. Material and methods Samples were collected in the western Pacific Ocean: (1) Two cruises on board R/V Soyo Maru (13-20 May and 3-10 July 2002) along the 138°E meridiin in the vicinity of the Kuroshio and adjacent wattrs. Nine stations were sampled from 30°30'N to 34°15'N in May, and 10 stations were sampled from 30°0'N to 34°20'N during the July cruise. At each station, 15 depths between 5 and 200 m were sampled; (2) cruise jn board R/V Hakuho Maru (7 November-18 December 2002) to the Celebes, Sulu and South China Seas. Samples were collected from 10 stations at six depths betveen the surface to 150 m depth; (3) on board R/V M ini (15-28 January 2003) along the equator from 160°E tD 160°W. Samples were collected from nine stations at 14 depths between 0 and 200 m depth; (4) Six cruises weie carried out at Stn. H on board R/V Oshoro Maru and Stn. A7 on board R/V Wakataka Maru in the Oyaîhio area during the spring and summer of 2003; (5) In addition, nine samples were collected from 5 to 100 m cfepth in a coastal station off Oshima Island, Sagani Bay (34°39.2'N, 139°31.3'E) on 7 June 2003 (Fig. 1). All samples were collected with Niskin bottles, preserved with acidified Lugol’s solution and stored at 5°C. Sub-samples (400 mL) were allowed to settle in glass sedimentation cylinders. The top 350 ml of each sample was siphoned off progressively over 5 days using a length of small-bore tubing. The remaining 50mL was settled in composite sedimentation chamfers and observed using a Nikon inverted microscope. Several of the Lugol-fixed specimens were isolated from the chambers with a capillary, transfeired to a glass slide, and observed with an Olympus mcroscope equipped with Nomarski Differential Interfereice Con­ trast (DIC) system and photographed at < 600 or X 1000. To show the location of the nucleus one of the specimens was stained with DAPI (4,6-dianidino-2- 40°N Philippine Sea 30“ NJapan L SeaSouth China Sea12°N 20“N Philippine -I Sea SagamI Bay35®N-Sulu Sea 10“NOshima Island 130-E 30' ^ Celebes _ Sea a 10“S4°N 160“W124“E 160°E120°E 140'E 180“ Fig. 1. Map of the station locations in the western Pacific Ocean. The insets show the Kuroshio Current and the Sagami Jay in the south Japan, and the Celebes, Sulu and South China Seas. 279 F. Gômez, K. Furuya / European Journal of Protistology 41 (2005) 231-239 233 phenylindole) and examined with an Olympus epifluor- escence microscope. Results and discussion Scaphodinium Margalef Scaphodinium is an extremely flattened cell that contains a uniform network of myo-fibrils. The flattened portion projects at both ends, with the extremity closer to the nucleus (here considered as the proximal part) bilobulate, shorter and wider than the other spatula­ shaped extremity (here considered as the distal part). Two flagella were located next to the large, egg-shaped, encapsulated nucleus. According to the orientation proposed by Cachon and Cachon (1969) the transverse flagellum was undulate, larger and sheathed in a tube­ like channel in the proximal part; the longitudinal flagellum was shorter and rarely observed from fixed specimens. Nearly every one of the Lugol-fixed speci­ mens appeared folded over one of its faces with the flagella on the convex surface (Gômez and Furuya 2004). In the vicinity of the Kuroshio Current 9 and 34 specimens of 5“. mirabile were found in May and July, respectively (Gômez and Furuya 2004). In the marginal seas of the western Pacific Ocean seven specimens were found, mainly in the more productive waters of the Celebes Sea. In the equatorial Pacific Ocean, only six specimens were found, nearly all in the frontal zone between the western Pacific warm pool and the Equatorial Upwelling Regimen (Table 1, Fig. 2). In the coastal waters of Sagami Bay, off Oshima Island, three specimens were collected. No leptodiscaceans were observed in the subarctic waters of the Oyashio Current. Nearly all the specimens corresponded to S. mirabile, characterized by a slightly bifurcate proximal extremity and the spatula-shaped distal extremity. Two specimens that did not agree with the general characteristics of the type species were observed; One specimen, Scaphodi­ nium spl, showed a high degree of bifurcation of the proximal extremity (Figs. 3-5, Table 1). The distal extremity was lobulate, lacking the spatula-shaped contour of the type species (Fig. 4). Another specimen, Scaphodinium sp2, showed larger differences compared to the type species (Figs. 6-11). From the distal extremity arose two different proboscides: a small rounded proboscis and a large acute proboscis of about 1/4 of the cell length (Figs. 6 and 7). The proximal extremity was slightly bifurcated (Fig. 8). Assuming a bilateral symmetry, the nucleus was slightly marginally located (Figs. 9 and 10). A step-like discontinuity was observed in the margin of the specimen more distal from the nucleus (Fig. 11). A specimen of comparable shape, that cannot be ascribed to any of the known genera of leptodiscaceans, was also found. The outline of this cell was arrowhead- shaped and the proximal extremity bifurcated. The margins of the cell appeared folded as far as the region of the nucleus (Figs. 12 and 13, Table 1). Petalodinium Cachon et Cachon Petalodinium is an also an extremely flattened taxon. The proximal extremity is slightly more acute than the Table 1. Records of leptodicaceans (excluding Scaphodinium mirabile) in the western Pacific Ocean Taxon Date Depth Latitude Longitude Length Figure Scaphodinium spl (highly bifurcated) 9/05/2002 70 33°N 138°E 170 Figs. 3-5 Scaphodinium sp2 (with proboscides) 10/05/2002 150 33°30'N 138°E 150 Figs. 6-11 Arrowhead-shaped leptodiscacean 11/12/2002 100 14°30'N 118°E 120 Figs. 12 and 13 Petalodinium porcelio ̂ Petalodinium porcelio 4/07/2002 11/12/2002 40 75 30°N 14°30'N 138°E 118°E 380 Fi^V 14, and 15 Figs. 16^nd 17 Petalodinium porcelio 8/07/2002 40 33°45'N 138°E 370 Fig. 18 Petalodinium porcelio 17/11/2002 30 5°N 121°E 360 — Petalodinium porcelio 18/11/2002 50 5°N 121°E 350 Figs. 19-21 Petalodinium porcelio 15/01/2003 110 0° 160°E — Leptodiscus sp. 19/11/2002 75 7°25.3'N 121°12.5'E 110 Figs. 22-24 Leptodiscus sp. 17/01/2003 0 0° 165°E 120 Figs. 25-28 Leptodiscus sp. 07/06/2003 50 34°39.2'N 139°31.3'E 100 Figs. 29 and 30 Leptodiscus sp. 06/07/2002 70 32°N 138°E 90 Fig. 31 Leptodiscus sp. 04/07/2002 40 30°N 138°E 115 Fig. 32 Leptodiscus sp. 07/07/2002 70 34°15'N 138°E 110 Fig. 33 Date; depth (in meters); geographic coordinates (latitude, longitude); and total length (units as micrometers) o f each record (diameter o f folded specimens of Leptodiscus). ^Folded specimens of Petalodinium porcelio. 280 234 Kuroshio F. Gômez, K. Furuya / European Journal of Protistology 41 (2005) 231-239 Philippine Sea Kuroshio Philippine Ses C1 B1 C3 C6 C9 C10 C11 C12 C13 £ 100 Q 150 . May 2002 3 4 'N South China Sulu Sea 3 3 'N 32" N 3 f N Latitude along 138"E 0 f 100 £ -150 O July 2002 33"N 32"N 31"N Latitude along 138'E 200 30" N30" N 34"N Celebes Sea Philippine Sea Western Pacific warm pool Equatorial Upwelling Region 0: 50: £ lOOi & Q 1504 17 10 6 4 F': O z Z - <5 • • Z • ï T i ® i 1 % ) 200^ (S ) November 2002 100 £28°C'Î 150 O January 2003 160"E 170"E 180" 170"W Longitude along the Equator 1-200 160"W Fig. 2. Section plot of the records (marked by circles) of Scaphodinium mirabile in the western Pacific Ocean. Isotherms are shown. distal one. As in Scaphodinium, the transverse flage­ llum is partially in a tube-like channel close to a big egg-shaped, encapsulate nucleus. The longitudinal fla­ gellum is shorter and it is difficult to observe from the fixed material. The most distinctive characteristic is the network of myo-fibrils with rectangular contours that uniformly covers the cell (Cachon and Cachon 1969; Sournia 1986). The type species was described from surface hauls from the Ligurian Sea (Cachon and Cachon 1969) with no further records in the Mediterra­ nean Sea. Later Stoyanova (1999) reported a high abundance of Petalodinium porcelio in the coastal waters of the western Black Sea, also with no further records. During the present study six specimens of Petalodi­ nium were found (Table 1). Two of the specimens appeared folded over themselves with an appearance that closely resembled 5. w/rflMe (Figs. 14 and 15). However, the network of fibrils with prominent rectan­ gular contour differed from the less marked and more irregular reticulation of Scaphodinium. Another speci­ men had a more elongate appearance and the margins partially folded (Figs. 16 and 17). The reticulation of the specimens was visible under bright field optics (Fig. 18) and even clearer under DIC optics (Fig. 19). The transverse flagellum was partially sheathed in a tube­ like channel (Fig. 20). After DAPI-staining the nucleus glowed brightly under UV excitation (Fig. 21). The nucleus was large as in Noctiluca scintillans (Macartney) Kofoid, which ultrastructure has been investigated (Soyer 1969, 1972). Assuming the similarity with Noctiluca, the nucleoli could occupy 1/3 of the nuclear mass and the black round spots in the surface of the nucleus and its periphery were considered as the nuclear ampullae (Soyer 1969) (Figs. 20 and 21). Leptodiscus tnedusoides Hertwig ^^TIre“tÿpé*^ims^bL the family Leptodiscaceae has the ̂ form of a medusa with a contractile margin. A single flagellum arose from a blind tube on the convex surface. The nucleus and the cytostome were centrally located on the top of the cell (Cachon and Cachon 1969). According to Cachon (1964) the parasitic dinoflagellate Figs. 3-13. Photomicrographs of leptodiscaceans, bright field optics. 3-5, Scaphodinium spl (highly bifurcated). 3, Detail of the distal extremity. 5, Details of the bifurcate proximal extremity. 6-11, Scaphodinium sp2 (with proboscides). 6, See the short and the large acute proboscides in the distal extremity. 7, Details of the short proboscis. 8, Details of the bifurcate proximal extremity. 9, See the nucleus marginally located. 10, See the nucleus and the cytostome region. 11, Details of the step-like discontinuity in the cell margin more distal from the nucleus. 12-13, Arrowhead-shaped leptodiscacean with the margins folded. See Table 1 for the location of the records. N = nucleus; CYT = cytostome; LF = large proboscis; SP = short proboscis. Scale bars: 50 pm. 281 F. Gômez, K. Furuya / European Journal of Protistology 41 (2005) 231-239 235 11 12 282 236 F. Gômez, K. Furuya / European Journal of Protistology 41 (2005) 231-239 g # # # B ^ a w i # 283 F. Gômez, K. Furuya / European Journal of Protistology 41 (2005) 231-239 237 Amoebophrya leptodisci Cachon infests the region of the nucleus. The circular contour of Leptodiscus and the lack of a prominent reticulation prevent this taxon being confused with folded specimens of other leptodicaceans such as Petalodinium. Hertwig (1877) described L. medusoides from the port of Messina (Sicily), being further exclusively reported in other areas of the western Mediterranean Sea (Cachon and Cachon 1969; Margalef 1969; Vila et al. 2001). According to Cachon and Cachon (1969) this taxon was common in surface waters under calm conditions. These authors remarked ihsA Leptodiscus was . very easily destroyed during sample collection. Despite the prob­ able underestimation of its abundance, Cachon and Cachon (1969) reported abundances of 80 cells L""'. Taking into account that this taxon can reach 2 mm in diameter, this constitutes a high biomass. Vila et al. (2001) considered L. medusoides as a potentially harmful species because it was associated with dense mucilage able to cause the breakage of fishermen’s nets. Until now the distribution of Leptodiscus seems to be restricted to the western Mediterranean Sea. If the doubtful genus Pratjetella is accepted as a synonym (see discussion in Sournia, 1986, p. 112), Leptodiscus could also occur in the Atlantic Ocean. Six-folded leptodiscaceans with a medusoid shape were tentatively assigned to the genus Leptodiscus (Figs. 22-33, Table 1). Several specimens, after sample treatment, maintained a well-developed flagellum aris­ ing from the convex side. The length of the flagellum was close to the diameter of the folded cell (~ 100 pm). According to Hertwig (1877) the cell diameter was 600-1500 pm and Cachon and Cachon (1969) found specimens of 2000 pm. In the present study, the diameter of the specimens observed was smaller than 120 pm, being closer to the other medusoid leptodiscacean, Craspedotella pileous, described from the tropical Pacific Ocean (Kofoid 1905). The shape of Craspedotella, close to a hydromedusa, is even more medusiform than that of Leptodiscus. Cachon and Cachon (1969) found C. pileous in very deep waters (>300m depth), but their observations did not agree with Kofoid’s original from the eastern Atlantic Ocean. No information is available on the occurrence of flagella in Craspedotella. Due to the occurrence of flagella, the specimens of the present study were not assigned to Craspedotella. The well-developed flagellum, considered as the transverse flagellum following Cachon and Cachon (1969), was preserved in three of the six specimens observed. The percentage of individuals that maintained the flagellum after fixation in Leptodiscus was higher than for the Lugol-fixed cells of S. mirabile. Even folded, the diameter of the individuals observed in the present study (90-120 pm) was not in accordance with the 600-2000 pm of diameter reported for Lepto­ discus in the literature (Sournia 1986, p. 53). Cachon and Cachon (1969, p. 27) reported the occurrence of small individuals of Leptodiscus of about 100 pm in diameter. They suggested that these specimens result directly from sporogenetic reproduction, whereas the larger specimens (>700 pm) resulted from reproduction by bipartition. Cachon and Cachon-Enjumet (1964) only found six specimens in sporogenesis after examining 10,000 individuals. These authors also found differences in the chemical composition between the small and large forms. It cannot be disputed that this feature could favour the preservation of the smaller specimens. According to Cachon and Cachon (1969) the adults of Leptodiscus were extremely fragile and disintegrated very easily. No large specimens were observed in the present study. It can be hypothesised that the few small specimens observed during the present study constitute a fraction of a more numerous population of Leptodiscus. According to Cachon and Cachon (1969, p. 25) the transverse flagellum is well developed, especially in the young trophonts. They reported that the transverse flagellum did not grow proportionally, keeping the same length in both young trophonts and adults of 2000 pm in diameter. They also reported that the flagellum provided efficient propulsion in the young specimens whereas in the large specimens it only produced a current towards the cytostome. The longitudinal flagellum of Leptodiscus ( < 5 pm long), which is not easily visible, is regarded as vestigial (Cachon and Cachon 1969, p. 25). There may be considerable diversity of leptodisca­ ceans yet to be described. The fragility, transparency and polymorphism of the leptodiscaceans are respon­ sible for the scarce records, going unnoticed in the leptodiscaceans are important for the evolution of the dinoflagellates, but molecular phylogenetical studies have not yet been applied. More work, including the development of appropriate fixation techniques for these organisms, is necessary. Figs. 14-21. Photomicrographs of Petalodinium porcelio. 14-18, Bright field optics. 14-15, Two views of a folded specimen. 16-17, Another specimen. See the flagellum. 18, Non-folded specimen. 19-21, Specimen observed under DIC and epifluorescence microscopy. 20, See the flagellum partially encapsulated. 21, The specimen stained with DAPI showing the nucleus glowing brightly under UV excitation. The arrows point the black round spots considered as nuclear ampullae. See Table 1 for the location of the records. CYT = cytostome; N = nucleus; NA = nuclear ampulla; TF = transverse flagellum. Scale bars, Figs. 14-19: 100 pm and Figs. 20 and 21: 50 pm. 284 238 F. Gômez, K. Furuya / European Journal of Prolisloiogy 41 (2005) 231-239 m23 r Figs. 22-33. Photomicrographs of Leptodiscus sp., bright field optics. 22-24, Damaged specimen with the transverse flagelum. 25-28, Another specimen; see the prominent flagellum. 29-30, Two views of a further specimen. 31-33, Three different specimens. See Table 1 for location of the records. N = nucleus; TF = transverse flagellum. Scale bars: 100 pm. Acknowledgements This study was supported by Grant-in-aid for Creative Basic Research (12NP0201, DOBIS) from the MEXT, Japan. We are grateful to the scientists and crew of R/V Soyo Maru (Nat. Res. Inst. Fish. Sci.), R/V Hakuho Maru (ORI, Univ. Tokyo), R /V Mirai (JaM- STEC), R/V Seiyo Maru (Tokyo Univ. Fish.), R/V 285 F. Gômez, K. Furuya / European Journal of Protistology 41 (2005) 231-239 239 Oshoro Maru (Hokkaido Univ.) and R/V Wakataka Maru (Tohoku Nat. Fish. Res. Inst.) for their kind help in collection of samples. Thanks to Dr. H. Yamazaki (Tokyo Univ. Fish.) for the invitation to participate in the cruise in Sagami Bay. F.G. acknowledges the support of the European Commission (ICB2-CT-2001- 80002). This is a contribution to the French IFB ‘Biodiversité et Changement Global’ programme. References Cachon, J., 1964. Contribution à l’étude des Péridiniens parasites. Cytologie, Cycles évolutifs. Ann. Sci. Nat. Zool. Sér. 12, 1-158. Cachon, J , Cachon, M., 1967. Contribution à l'étude des Noctilucidae Saville-Kent, 1. des Kofoidininae Cachon J. et M. Évolution, morphologique et systématique. Protisto­ logica 3, 427-444. Cachon, J., Cachon, M., 1969. Contribution à l'étude des Noctilucidae Saville-Kent. Évolution, morphologique, cy­ tologie, systématique. II. Les Leptodiscinae Cachon J. et M. Protistologica 5, 11-33. Cachon, J., Cachon, M., 1984. An unusual mechanism of cell contraction: Leptodiscinae Dinoflagellates. Cell Motil. Cytoskel. 4, 41-55. Cachon, J., Cachon, M., 1986. Adaptation des dinoflagellés à la vie planctonique. Boll. Zool. 53, 239-245. Cachon, J., Cachon-Enjumet, M., 1964. Leptospathium navi­ cula nov. gen., nov. sp. et Leptophyllus dasypus nov. gen. sp., Péridiniens Noctilucidae (Hertwig) du plancton néri­ tique de Villefranche-sur-Mer. Bull. Inst. Océanogr. Mon­ aco 62 (1292), 1-12. Elbrachter, M., 1979. On the taxonomy of unarmored dinophytes (Dinophyta) from the Northwest African upwelling region. Meteor Forsch.-Ergebnisse 30, 1- 22 . Gômez, F., Furuya, K., 2004. New records of Scaphodinium mirabile (Dinophyceae), an unnoticed dinoflagellate in the Pacific Ocean. Phycol. Res. 52, 13-16. Hertwig, R., 1877. Über Leptodiscus medusoides, eine neue den Noctiluciden verwandte Flagellate. Jenaische Z. Naturwiss. NF 11, 307-323. Kofoid, C.A., 1905. Craspedotella pileolus, a new genus of the Cystoflagellata, an example of convergence. Bull. Mus. Comp. Zool. Harvard Coll. Cambridge 1904/1906 46, 163. Margalef, R., 1969. Composiciôn especifica del fitoplancton de la costa catalano-levantina (Mediterrâneo occidental) en 1962-1967. Inv. Pesq. 33, 345-380. Margalef, R., 1975. Composiciôn y distribuciôn del fito­ plancton marino en la regiôn de afloramiento del NW de Africa, en marzo de 1973. Res. Exp. Cient. B/O Comide 4, 145-170. Sournia, A., 1986. Atlas du phytoplancton marin. Vol. 1: Introduction, Cyanophycées, Dictyochophycées, Dinophy- cées et Raphidophycées. Editions CNRS, Paris. Soyer, M.O., 1969. L’enveloppe nucléaire chez Noctiluca miliaris Suriray (Dinoflagellata). IL Rôle des ampoules nucléaires et de certains constituants cytoplasmiques dans la mécanique mitotique. J. Microsc. 8, 709-720. Soyer, M.O., 1972. Les ultrastructures nucléaires de la Noctiluque (Dinoflagelé libre) au cours de la sporogenèse. Chromosoma (Berlin) 39, 419-441. Stoyanova, A.P., 1999. New representatives of noctilucales in the Bulgarian Black Sea coastal water. Comptes Rend. Acad. Bulgare Sci. 52, 119-122. Vila, M., Camp, J., Garcés, E , Masô, M., Delgado, M., 2001. High resolution spatio-temporal detection of potentially harmful dinoflagellates in confined waters of the NW Mediterranean. J. Plankton Res. 23, 497-514. 286 p p . I I w \ v , v i . i i y . 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 45 47 49 51 53 55 Available online at www.sciencedirect.com - ScienceDirect ELSEVIER European Journal o f Protistology I (HH) European Journal of PROTISTOLOGY www.elsevier.de ejop Kofoidinium, Spatulodinium and other kofoidiniaceans (Noctilucales, Di­ nophyceae) in the Pacific Ocean Fernando Gômez*, Ken Furuya Department o f Aquatic Bioscience, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan Received 7 July 2006; received in revised form 24 November 2006; accepted 7 December 2006 Abstract Examples of rarely reported dinoflagellates of the family Kofoidiniaceae F.J.R. Taylor (Noctilucales) from the northwest, equatorial and southeast Pacific Ocean are described and illustrated. Kofoidinium was the most ubiqui'.ous genus with a maximum abundance of 10 cells L \ Specimens of this genus were identified to four species: Kofoidir.ium sp. that showed a pointed extension that emerges from the antero-ventral region and K. velelloides, both of which had diameters that ranged from 40 to 200 pm; Kofoidinium pavillardii which showed a rounded epitheca and a larger size (~300-700pm in diameter); and another species, tentatively identified as K. splendens, that contained red circular inclusions. Further research is needed to clarify the characteristics that separate K. splendens from the other species. This study is the first to record the genus Spatulodinium in tropical waters and in the southern hemisphere. S cf. pseudonoctiluca was found in the southeast Pacific Ocean, as well as other smaller specimens with a different shape or disposition of the tentacle that may belong to two other species. In the northwest and equatorial Pacific, specimens of Spatulodinium showed a green pigmentation that suggested the existence of the first species known in the order Noctilucales to contain its own chloroplasts. Immature stages of kofoidiniaceans, some containing symbiotic microalgae, are illustrated, as well as mature stages related to Pomatodinium and to unknown genera of kofoidiniaceans. Kofoidiniaceans are shown to be common and widely distributed in the Pacific, and are probably also frequent in other oceans, but are rarely recognised. © 2007 Published by Elsevier GmbH. Keywords: Kofoidinium', Spatulodinium', Pomatodinium', Noctilucales; Dinophyta; Pacific Ocean Inifrodiicfib The noctilucaceans, whose morphology differs strongly from that of typical Peridiniales, are of particular interest in the evolution of the dinoflagellates. After Noctiluca scintillans (Macartney) Kofoid, mem­ bers of the family Kofoidiniaceae are the most common noctilucaceans. However information on this group has ^Corresponding author. E-mail address: femando.gomczr«:fitoplancton.com (F. Gomez). 0932-4739/$-see front matter © 2007 Published by Elsevier GmbH, doi: 10.1016,/j.ejop.2006.12.002 and Cachon (1967b). They demonstrated that the kofoidiniaceans undergo an exceptional morphological transformation during their life cycle, e.g., they de­ scribed 6 stages, a to f in Kofoidinium pavillardii, and they showed that several life stages had been described as separate species (Cachon and Cachon 1967b). Pouchet (1885) described the first kofoidiniacean, Gymnodinium pseudonoctiluca. He already noted the strong morphological changes of this taxon and illustrated this single species with different morpholo- 61 63 65 67 69 71 Please cite this article as; Gômez, F., Furuya, K., Kofoidinium, Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. European Journal of Protistology (2007), doi: 10.1016/j.ejop.2006.12.002 ______ 287 http://www.sciencedirect.com http://www.elsevier.de F. Gomez, K. Furuya / European Journal of Protistology I (I gies. One of the forms corresponded to a large AmphidiniumAikQ cell, and the mature stage was a round or oval, laterally compressed cell with a tentacle. However, further authors considered the immature stages as separate species such as Gymnodinium pyr- ocystis Jorgensen, G. fulgens Kofoid et Swezy, G. lebouriae Pavillard and G. viridis Lebour (= G. conicum Kofoid et Swezy) (Cachon and Cachon 1967b; Kono­ valova and Selina 2002). Specimens from the NW Mediterranean Sea, illustrated by Pavillard (1921) under the name Gymnodinium pseudonoctiluca, were probably immature stages of Kofoidinium. Later, Pavillard found the mature stage, which he described as a member of a new genus and named it Kofoidinium velelloides (Pavil­ lard, 1928). Another doubtful species, described from Canadian arctic waters, is Kofoidinium arcticum, known only from the first description (Bursa 1964). Cachon and Cachon (1967b) erected the genus Spatulodinium from Gymnodinium pseudonoctiluca and described the species Kofoidinium pavillardii Cachon et Cachon, 1967 and K. splendens Cachon et Cachon, 1967. They regarded G. pseudonoctiluca Pouchet, 1885 as the basionym for both Spatulodinium and Kofoidinium because the immature stages of these genera were similar in morphology. Two other genera, Pomatodinium Cachon et Cachon- Enjumet, 1966 and Cymbodinium J. Cachon et M. Cachon, 1967, have been included in the family Kofoidiniaceae (Sournia 1986). Pomatodinium has the shape of a gastropod larva and may contain zoox- anthellae (Cachon and Cachon-Enjumet 1966). The genus Cymbodinium has the shape of a veliger larva and only one flagellum has been observed (Cachon and Cachon 1967a). Cymbodinium, the least known of these genera, was first placed in the family Leptodiscaceae Kofoid and later in the family Kofoidiniaceae F.J.R. Taylor (Sournia 1986). Information on the life cycle and detailed morphology of kofodinianceans is nearly restricted to the study based on live specimens collected by Cachon and Cachon in the coastal Ligurian Sea (NW Mediterra­ nean). Little is known about the distribution and morphology of kofoidiniaceans in oceanic waters. However, they are probably often present in oceanic plankton samples, but are rarely recognised in the fixed condition. The present study investigates the distribu­ tion of kofoidiniaceans in several regions of the Pacific Ocean and illustrates the appearance of these dino­ flagellates in fixed samples in the hope that they will be more commonly recognised and reported. The occur­ rence of body inclusions and tentative symbiotic microalgae is illustrated. Several life stages such as Gymnodinium lebouriae or G. pseudonoctiluca and other unidentified immature stages are illustrated. This study illustrates unknown species thought to belong to the genus Spatulodinium and other unknown genera of kofoidinaceans, including the first species in the order Noctilucales thought to contain its own chloroplasts. 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 45 47 49 51 53 Fig. 1. Map of the station locations in the Pacific Ocean (marked by circles). 1. Oyashio Current. 2, 3. Kuroshio Current and 55 Philippine Sea in May and July, respectively. 4. Celebes, Sulu and South China seas. 5. Western and central equatorial Pacific. 6. Southeast Pacific Ocean. Material and methods Sample collection and light microscopical methods used in the northwest and Equatorial Pacific Ocean were described in Gômez and Furuya (2005) and are not repeated here. In the southeast Pacific Ocean, samples were collected during the BIOSOPE (Biogeochemistry and Optics South Pacific Experiment) cruise on board R/V L ’Atalante from the Marquesas Is. to the coast of Chile (26 October-12 December 2004) (Fig. 1). Samples 57 59 61 63 65 67 69 71 73 75 77 79 81 83 85 87 89 91 93 95 97 90® 105® 120® 135® 150® 165® 180® 165® 150® 135® 120® 105® 90® Longitude Please cite this article as: Gômez, F., Furuya, K., Kofoidinium. Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. European Journal of Protistology (2007), doi: 10.1016/j.ejop.2006.12.002 288 F. Gômez, K. Furuya / European Journal of Protistology I (IIH) 11 13 15 17 from 12 stations comprised 83 samples collected by Niskin bottles from 5 to 270 m depth. These were preserved with acidified Lugol’s solution and stored at 5°C. Samples of 500 mL were concentrated via sedi­ mentation in glass cylinders. The top 450 mL of sample was slowly siphoned off with small-bore tubing during 6 days. The remaining 50 mL of concentrate, representing 500 mL whole water, was then settled in composite settling chambers. The entire chamber was scanned at 200 X with an 1X71 Olympus inverted microscope equipped with an Olympus digital camera. Each speci­ men was photographed and measured at 400 x with Olympus DP70-BSW software. Results Distribution of Kofoidinium Kofoidinium was the most ubiquitous genus of noctilucaceans in the open waters of the Pacific Ocean. A latitudinal transect in the vicinity of the Kuroshio Current to the south of Japan (138°E) was investigated in May and July 2002. In May, 15 individuals of Kofoidinium were found from 131 samples analysed (Fig. 2), and in July, 32 specimens were found in 144 samples analysed (Fig. 3). During the cruise in the marginal seas of the western Pacific Ocean 10 specimens were observed from 81 samples (Fig. 4). In the western and central equatorial Pacific 30 specimens were found from 124 samples (Fig. 5). In the southeast Pacific 57 59 61 63 65 67 69 71 73 19 21 23 25 27 29 31 33 35 37 39 41 45 47 49 51 53 55 Kuroshio Current 01 Bi Philippine Sea Kuroshio Current CIO C11 012 C13 f 22°C^ l i ...; :. i i ; 1 5 0 -# ^ 34”N 33“N 32°N Latitude 31'N 30'N South China Sulu Sea ,15“C'Nov-Dee 2002 200-1 Philippine Sea 82 C8 July 2002 34®N 33®N 32“N Latitude 3 fN 30TN Celebes Sea Philppine Sea Western Pacific Warm Pool Equatorial Upwelling Region 7 8 9 10 11 12 13 14 0 i t I • - 100 •- 150 January 2003 f * Marquesas Is. 160"E South Pacific Gyre 170*5 180* Longitude 170*W 160*W Peru-Chile Current & 100 .2 T p ^ 25*CT 9- 150 Oct-Dec 2004 140‘W 130*W 120'W 110*W Longitude 100*W Figs 2-6. Section plots of the records of Kofoidinium (mature stage) in the Pacific Ocean indicated by filled rhombuses (see also Fig. 1). 2, Records along the meridian 138°E in May. 3, Records from the same location in July. 4, Records from Celebes, Sulu and South China seas. 5, Records from the western and central equatorial Pacific. 6, Records from the southeast Pacific. Isotherms are shown. Please cite this article as; Gômez, F., Furuya, K., Kofoidinium, Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. European Journal of Protistology (2007), doi: 10.1016/j.ejop.2006.12.002 75 77 79 81 83 85 87 89 91 93 95 • I 101 103 105 107 109 111 289 F. Gômez, K. Furuya / European Journal of Protistology I (nil) 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 45 47 49 51 53 55 Ocean, 42 specimens of Kofoidinium were found in the 83 samples analysed (Fig. 6). No kofoidiniaceans were found in the sub-arctic waters of the Oyashio Current off Hokkaido. It is difficult to discern a pattern in the distribution of Kofoidinium. The highest abundance was only 4 speci­ mens per sample (10cellsL“ *). In the Kuroshio Current and adjacent waters, the abundance was higher in summer than in spring (Figs 2, 3). Specimens of Kofoidinium were only found near the surface in the SE Asia marginal seas (Fig. 4), but in other waters they were found at depths down to 200 m. Overall, no clear longitudinal or vertical pattern in the distribution was observed, suggesting ubiquitous distribution of the organism in warm waters (Figs 2-6). The trophic conditions in these regions were described in Gômez et al. (2005). In the equatorial and southeast Pacific Ocean, the records of Kofoidinium tended to be more abundant in the most eutrophic regions, such as the vicinity of the Marquesas Islands and Peru-Chile Current (Fig. 6). In the Pacific Ocean the specimens were recorded in a wide range of temperature from 14 °C near the Chilean upwelling to 30 °C in equatorial surface waters (Figs 2- 6). Morphology of Kofoidinium It is not easy to identify kofoidiniaceans to species due to the high morphological variability during their life cycle and the difficulties to delimit the species from preserved specimens. In the present study, the records of Kofoidinium have been tentatively grouped into four species: Kofoidinium sp., K. velelloides and K. pavillardii that are identifiable with more certainty and the more dubious K. splendens. The limits of this last taxon are unclear due to common morphological characters with the other species. In no case did preserved specimens of Kofoidinium retain the shell which is carried above the episome in life (see Cachon and Cachon 1967b). The smaller specimens encountered ranged from 40 to 200 pm in diameter. The most extended morphology was a- round to sli htl eili so' m l , fi te d yposome or ve um| ran ridges and bordered by a narrow differentiated band (Figs 7-10). The reduced episome formed a crest at the anterior margin of the cell. The nucleus was small and located in the episome. In the antero-dorsal margin appeared a short finger-like structure. The marginal differentiated band was thicker at the ends and in the antero-ventral region bifurcated forming a right angle. One extreme of this bifurcation of the marginal band was thick and formed a square-ended protrusion. The other branch was slightly curved and projected towards the episome (Fig. 7). One of the main characteristics of the Pacific specimens was the pointed extension that arises from the episome towards the ventral side of the cell. This pointed extension was flexible and tended to be in a different plane from the flattened hyposome (Figs 7 and 8). These small Pacific specimens that differed from the description of K. velelloides in Cachon and Cachon (1967b) are here named Kofoidinium sp. Specimens lacking the pointed extension, the square-ended protru­ sion and with a large nucleus located anteriorly in the hyposome (Fig. 10) were closer to K. velelloides as illustrated by Cachon and Cachon (1967b). Due to their transparency and small size, Kofoidinium sp. and K. velelloides could be more easily overlooked during sample analysis than the highly visible K. pavillardii (Figs 8, 9, 11-15). Kofoidinium pavillardii is the largest species of the genus. The diameter was longer than 300 pm and reached 700 pm (Figs 8 and 11). The round hyposome occupied nearly all the cell body. The marginal hyaline band is interrupted at about 2/3 of the cell height with thicker end regions, especially the ventral one. More anteriorly than the ends of the marginal band are located two hook-shaped structures, the anchorage mechanisms that held the hemispherical transparent dome or shell (Figs 11 and 14). These delicate hyaline domes are easily detached from the cell and had presumably been lost. The ventral anchorage mechan­ ism (Fig. 14) is bigger than the dorsal one (Fig. 11). The shape of the episome varied between the specimens, sometimes forming, a prominent crest (Fig. 12), and in others more reduced (Fig. 11). The specimen in Fig. 12 has the shape of K pavillardii as illustrated by Cachon Figs 7-23. Photomicrographs of kofoidiniaceans, bright field optics. 7, Kofoidinium sp. (0°, 165°W, 150 m depth) with anterior episome at the left, the hyposome at the right and the ventral projections at the top. 8-9, Kofoidinium pavillardii (large cell) and Kofoidinium sp. (small cell) (0°, 170°E, Cm depth); the inset in Fig. 8 shows the Kofoidinium sp. cell at a different focal plane. 10, K velelloides, note the prominent nucleus (0°, 160°E, 110 m depth). 11, Kofoidinium pavillardii. See the ventral anchorage mechanism in the inset (34°15'N, 138° E, 150 m depth). 12-15, Kofoidinium pavillardii (30°N, 138°E, 125 m depth). 13, Detail of the dorsal margin of the hyposome. 14, Detail of the antero-ventral region and the anchorage mechanism. 15, Detail of the inclusions in the margin of the hyposome. 16, Kofoidinium splendens (7°25'N, 121°12'E, 10 m depth). 17-21, K splendens with red inclusions (0°, 170°W, 80 m depth). 19, Detail of the inclusions in the cell body. 20, The arrows indicate the concentric ridges with red inclusions. 21, Detail of red inclusions in the periphery of the hyposome. 22-23, Unidentified pairs of kofoidiniaceans, probably stage “c” after binary fission (0°, 175°W, 30 m depth). 23, Detail of the presumed symbiotic microalgae. AM = anchorage mechanism for shell; CR = concentric ridges; F = fibrils; PE = pointed extension; SQ = square-ended projection; TF = transverse flagellum. Scale bars = 50 pm. 57 59 61 63 65 67 69 71 73 75 77 79 81 83 85 87 89 91 93 95 97 101 103 105 107 109 111 Please cite this article as: Gômez, F., Furuya, K., Kofoidinium, Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. European Journal of Protistology (2007), doi:10.1016/Tejop.2006.12.002 _______ 290 F. Gômez, K. Furuya / European Journal of Protistology I ( llll) I l l- I l l W hile the identification o f K. velelloides and K. pavillardii is relatively easy, the determ ination o f d iagnostic characters o f K. splendens and its validity as a species require fu rther research (Fig. 13). Specimens > 200 pm (usually 300-400 pm) w ith a sm oothly rounded left cingular crest have been considered as K.. splendens (Figs 16-21). C achon and C achon (1967b) considered th a t body inclusions are characteristic of K. splendens. However, the specim en o f Fig. 12, whose shape resem bled K. pavillardii, had a differentiated band 10 I k AM 1 4 l i ' ' 9 A M 1 7 ^ - - A r - 22 am Please cite this article as; Gômez, F., Furuya, K., Kofoidinium, Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. European Journal of Protistology (2007), doi:10.1016/j.ejop.2006.12.002 291 m m F. Gômez, K. Furuya / European Journal of Protistology I (im) 1 3 5 7 9 1 1 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 t ; 45 47 49 51 53 55 filled with brownish granules (Figs 13 and 15). The specimens that harbour body inclusions in the margin of the hyposom e, and also in the concentric ridges or dispersed over the cell body are here assigned to K. splendens (Figs 16-21). According to Cachon and Cachon (1967b) these red body inclusions in the Lugol-fixed specimens are o f polypeptide nature rather than lipid bodies; thus, the possibility o f that these red inclusions are symbiotic microalgae m ay be discarded. In the present study no symbiotic microalgae were observed in m ature stages o f Kofoidinium. N o noctilucacean species has been reported to have chloroplasts (excluding chloroplasts o f the ingested prey or symbiotic microalgae). Tentative symbiotic micro­ algae were observed in an unidentified kofoidiniacean (Figs 22 and 23). This observation was m ade in a pair of recently divided cells. According to Cachon and Cachon ( 1967b) such reproduction by bipartition is restricted to the im m ature cells. The presumed symbiotic microalgae were distributed along tracts and showed an ellipsoidal to ro tund shape and were 5-7 pm in diam eter (Fig. 23). A t the same sampling station, structures that appeared to be symbiotic m icroalgae were found in an unidenti­ fied im m ature stage (Figs 24 and 25). Distribution and morphology of Spatulodinium Spatulodinium pseudonoctiluca has the shape o f a disc, abou t 100-120 pm in diameter, which has been de­ form ed into a shallow cone by pushing in the left side so tha t the right side has become somewhat convex. A net o f fibrils (Fig. 33) is thought to facilitate the ingestion o f the prey o f these heterotrophs. The main characteristic o f the genus is the occurrence o f a long unstriated movable tentacle projecting from the ventral side in the anterior part o f the cell (Figs 26, 28-32). It is true that Kofoidinium velelloides (Fig. 7) and other unidentified kofoidiniaceans (Fig. 39) also have tentaculoid projec­ tions, but these differ in size or origin. Only one specimen with the m orphology reported for the type species was encountered (Fig. 29). Spatulodinium was previously regarde^ ; as a m oûot ic genus onl kn wn from boreal-arctic waters from Europe to the Japan Sea. The specimen identified as Spatulodinium pseudonoctilu­ ca from the Peru-Chile C urrent constitutes the first record of this genus in the southern hemisphere (Fig. 29). Beyond the type species, other specimens that differed from the type o f Spatulodinium were observed. Three specimens corresponded to a large cell (~ 150 pm diameter) with a long tentacle and showing a green pigm entation (Figs 26-28). In SE Asia marginal seas, only one m ature specimen was recorded in the open waters o f the Sulu Sea (Figs 26 and 27). Two other specimens o f “ green” Spatulodinium sp. 1 were observed in the western and central equatorial Pacific Ocean (Fig. 28). The tentacle was very long in one o f the specimens (two times the cell body. Fig. 26) and shorter and with a pointed-ending in the other specimen (Fig. 28). In these “green” Spatulodinium sp. 1 the typical system of fibrils was not visible or was m asked by the green pigm enta­ tion (Figs 27 and 28). O ther unidentified species o f the genus were observed with two different morphologies. The tentacle o f the type species projected from the antero-ventral region. In these other specimens the tentacle appeared to project from the posterior part o f the cell. Several specimens of Spatulodinium sp. 2 were about one half (~50 pm) o f the diameter o f the type species and showed a thick tentacle with a triangular transparent halo (Fig. 30). Specimens of Spatulodinium sp. 3, also o f smaller size than the type species, showed a Daphnia-WkQ shape, with a clearly visible flagellum (Figs 31 and 32). The highest abundance o f Spatulodinium spp. with 7 specimens was encountered in a eutrophic region near the Juan Fernandez Archipelago, associated with a surface proliferation o f Gonyaulax polygramma Stein. Also im m ature life stages which have been described as Gymnodinium pseudonoctiluca (Fig. 33) and Gymnodi­ nium lebouriae (Fig. 34), precursors o f m ature stages o f both Spatulodinium and Kofoidinium, were found at the same station. Consequently these imm ature stages cannot be strictly ascribed to Spatulodinium because specimens o f Kofoidinium pavillardii were also observed Figs 24-41. Photomicrographs of kofoidiniaceans, bright field optics. 24-25, Tentatively identified as the immature stage of a kofoidiniacean with a green pigmentation (0°, 175°W, 60m depth). 26-27, “Green” Spatulodinium sp. 1 (7°25'N, 121°12'E, 75m depth); inset shows the same cell in a different orientation. 27, Detail of the green pigmentation of the same cell as in Fig. 26. 28, “Green” Spatulodinium sp. 1 (0°, 160°E, 40 m depth). 29, Spatulodinium cf. pseudonoctiluca (31°54'S, 91°27'W, 5 m depth). 30, Spatulodinium sp. 2 with a tentacle that is thicker in the proximal part (33°22'S, 78°6'W, 40 m depth). 31-32, “DapA/na-like” Spatulodinium sp. 3 with a tentacle that projects from the posterior episome region. 31, Specimen from 31°54'S, 91°27'W, 40m depth. 32, Specimen from 33°22'S, 78°6'W, 5 m depth. 33, Stage “c” of a kofoidiniacean described as Gymnodinium pseudonoctiluca (33°22'S, 78°6'W, 15 m depth). 34, Stage “d” described as Gymnodinium lebouriae (33°22'S, 78°6'W, 5 m depth). 35, Tentatively identified as Pomatodinium sp. (33°N, 138°E, 60 m). 36-38, Unidentified kofoidiniacean (32°N, 138°E, 100 m). Figs 36 and 37 resemble illustrations of Pomatodinium impatiens in the description by Cachon and Cachon-Enjumet (1966); note the prominent fibrils. 39-41, Unidentified kofoidiniacean with two long tentacles emerging from the margin of the hyposome, one smaller tentacle and a prominent anterior crest (0°, 180°, 200 m depth); note the concentric areolation in Fig. 40. C = cingulum; F = fibrils; L = left side; R = right side; S = sulcus; T = tentacle; TF = transverse flagellum. Scale bars = 50 pm. 57 59 61 63 65 67 69 71 73 75 77 79 81 83 85 87 89 91 93 95 97 101 103 105 107 109 1 1 1 Please cite this article as: Gômez, P., Furuya, K., Kofoidinium, Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. European Journal of Protistology (2007), doi: 10.1016/j.ejop.2006.12.002 292 in the same location. F. Gômez, K. Furuya / European Journal of Protistology I ( lll lj I l l - I l l Morphology of other kofoidiniaceans 5 C achon and C achon-E njum et (1966) described the 7 shape o f Pomatodinium as resem bling a gastropod larva, bu t w ith changes o f shape due to the contraction of fibrils (like those found in Kofoidinium, see Fig. 9); they also reported th a t it m ay con tain sym biotic m icroalgae. They illustrated Pomatodinium from a few live speci­ mens, bu t found the m orphology varied am ong fixed specimens. O ne specim en found by us in the K uroshio 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 45 47 49 51 53 55 W . A*. ^ T F 32 TF 33 nwr J Please cite this article as; Gômez, F., Furuya, K., Kofoidinium, Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. European Journal of Protistology (2007), doi: 10.1016/j.ejop.2006.12.002 293 F. Gômez, K. Furuya / European Journal of Protistology I (■■■) m m 1 region is assumed to belong to the genus P om atod in ium (Fig. 35). 3 A nother specimen was com posed o f two hemisphe­ rical transparent domes, one inside the other, and joined 5 a t their rims. An inner net o f fibrils joined the two hemispherical domes. One o f the views o f the specimen 7 (Fig. 37) was similar to the figure “ d ” o f P om atod in ium im pa tiens in P late I by C achon and Cachon-Enjumet 9 (1966). However in other views the m orphology o f the specimen differed from th e description o f P o m a tod i- 11 n iu m . In one view the specimen had the shape of a R om an Centurion^s helmet with the nucleus located in 13 one side o f the crest (Fig. 36). In one view the specimen could be m istaken for K o fo id in iu m (Fig. 38) and 15 provides a clear example o f the need to view kofoidi­ niaceans from different orientations to understand their 17 true shape. A nother unidentified kofoidiniacean (~ 110 pm long) 19 showed a very distinctive shape and extensions (Figs 39-41). The nucleus was located a t the base o f the 21 episome (Fig. 40). A semicircular crest w ith a concentric inner areolation was observed in the episome (Fig. 40). 23 The cingulum extended along the m arginal part o f the crest and the sulcus along the base o f the crest (Fig. 40). 25 The margin o f the hyposom e did not show the differentiated band that characterises K o fo id in iu m . The 27 specimens showed three tentaculoid extensions from the hyposome, each with rounded-tips (Figs 39 and 41). The 29 longer extension projected from the postero-ventral part o f the m argin o f the hyposome. A t the opposite side, 31 slightly anteriorly, emerged another long extension (Fig. 39). These extensions originated from a different 33 position com pared with the single tentacle o f S pa tu lo ­ d in ium . A third short finger-like extension was visible 35 emerging from the anterior-dorsal margin o f the hyposome (Fig. 39). 37 39 41 Discussion How many species o£ Kéfoidinium’! The existing literature on the life cycle o f kofoidinia- 45 ceans is restricted to Cachon and Cachon (1967b) and Konovalova and Selina (2002), and has been largely 47 overlooked. W hen Pavillard (1921) reported G ym nod i­ n ium pseudonoctiluca in the N W M editerranean Sea, he 49 was probably illustrating stage “c” o f K o fo id in iu m . Later, Pavillard (1928) found the m ature stage and 51 described K o fo id in iu m velelloides', he misspelled the epithet ‘velleloides’ tha t refers the jellyfish Vele lla ve le lla 53 Linnaeus, but subsequently corrected it (Pavillard 1937). Pavillard (1928) reported th a t the size o f K. vele llo ides 55 was 350 pm long. However as reported by Cachon and Cachon (1967b) and the present study, the size o f K. velello ides was usually less than 200 pm. This confusion 57 may be responsible for the fact tha t no new species was described until 1967 and all the previous records o f large 59 specimens o f K o fo id in iu m were ascribed to K. ve le llo ides (Balech 1962; Fenaux 1958; Halim 1967; Ram pi 1952). 61 The description of K. splendens by Cachon and Cachon (1967b) did not provide sufficient definitive criteria to 63 differentiate it from K. velello ides. The system o f anchorage o f the dome is different, but this m orpholo- 65 gical character is difficult to observe (Fig. 14). A high confusion exists in the literature. F or example in the 67 British Isles, Parke and Dodge (1976) listed X. and no K. ve lello ides and later Dodge (1982) reported 69 only K. velello ides. F or K o fo id in iu m splendens Taylor (1976, p. 185) reported "'P recise d is tin c tio n s between th is 71 species a n d K - velle lo ides - P a v il la rd are d if f ic u lt to m ake because o f the incompleteness o f the o r ig in a l 73 descrip tion a n d the d is to rte d cond ition o f the type specimens o f the la t te r " . Cachon and Cachon (1967b) 75 reported tha t K. splendens may harbour several symbio­ tic zooxanthellae that are lost under eutrophic condi- 77 tions as well as the red polypeptide bodies. This variability does not help in differentiating K. splendens 79 from K. velelloides. Cachon and Cachon (1967b) already reported speci- 81 mens o f K. velello ides of about 100 pm in length. Nearly all the previous studies that reported kofoidiniaceans 83 were based on net sampling and subsequently these small specimens could be lost. In addition, some 85 specimens may be overlooked during routine m icro­ scopical analysis due to their small size and transpar- 87 ency. In the present study specimens o f K o fo id in iu m sp. 40 pm in diameter were commonly observed. The 89 pointed extension and the square-ended protrusion (Fig. 7) are distinctive characters that were clearly 91 lacking in K . ve lello ides (Fig. 10). Bursa (1964) described K o fo id in iu m a rc ticu m in the 93 Canadian arctic waters. Cachon and Cachon (1967b, p. 437) and Taylor (1976, p. 184) reported that K . a rc tic u m 95 is a doubtful taxon, which was described from a single formaldehyde-fixed specimen evidently deformed due to 97 preservation. Beyond the initial description no records K o fo id in iu m splendens can be also confused with K. p a v illa rd ii . Both species have similar system o f ancho- 101 rage o f the dome (Cachon and Cachon 1967b). According to Taylor (1976) K o fo id in iu m lebouriae , 103 usually misspelled as ‘lebourae’, is the correct nam e for K. p a v il la rd ii because G ym nod in ium lebouriae is 105 considered as the basionym. Cachon and Cachon (1967b) stated that G ym nod in ium lebouriae is stage “d ” 107 of a kofoidiniacean and consequently it is not a valid species, which added more confusion. F or example 109 Yamaji (1980, p. 107) reported the non-existent species names " 'K o fo id in iu m lebourae (Pavillard) Cachon et 111 Please cite this article as: Gômez, F., Furuya, IL., Kofoidinium, Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. European Journal of Protistology (2007), doi: 10.1016/j.ejop.2006.12.002 294 F. Gômez, K. Furuya / European Journal of Protistology I (llll) 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 45 47 49 51 53 55 C achon” or considered K o fo id in iu m splendens as a synonym o f K o fo id in iu m lebouriae. The observations of the present study suggest the existence o f a small species with a pointed extension, here called K o fo id in iu m sp. (Fig. 7), K velello ides (Fig. 10), a large species, K. p a v il la rd ii { = K . lebouriae) (Fig. 11) and a fourth species, K. splendens (Fig. 17), o f more uncertain delimitation. How many species of Spatulodinium! S p a tu lo d in iu m is a monotypic genus, only known from northern hemisphere Euro-Asian boreal and arctic waters. This study is the first to describe the genus S p a tu lo d in iu m in tropical waters and in the southern hemisphere. In addition to the specimens with a green pigm entation th a t suggests the occurrence of chloro­ plasts (Figs 32-35), other specimens that differed from the type species were found (Figs 37-41). The monotypic character o f the genus needs to be reconsidered. In European Atlantic waters, im m ature stages pre­ sumed to belong to the genus S pa tu lod in ium have been described as G ym nod in ium lebouriae, G. fu lg e n s and G. con icum ( = G. v ir id is ), as well as probably G. p y ro c y s tis tha t was described with no illustration (Kofoid and Swezy 1921). In the tropical and southern Pacific Ocean, these im m ature stages were observed as well as other unidentified kofoidiniaceans. Kofoid and Swezy (1921) described A m p h id in iu m vasculum and A. p a c ificu m in tropical waters o f the Eastern Pacific Ocean. These forms strongly resemble the stage “d” o f a kofoidinia­ cean (Fig. 34). The suggestion that these large A m p h i­ d in iu m species, described from single specimens, could correspond to im m ature stages of S p a tu lod in ium in tropical waters, cannot be discarded. Other species of kofoidiniaceans As well as K o fo id in iu m and S pa tu lod in ium , the genera P o m a tod in iu m 3ind C ym bod in ium hâve been included in the family Kofoidiniaceae: : One of the specimens d in iu m (Fig. 35) and another specimen resembles that genus in one or two views (Fig. 37). Beyond the type locality, the Ligurian Sea, P. im patiens was reported from Spanish M editerranean coasts (M argalef 1969) and the N E A tlantic Ocean (Travers and Travers 1975; M argalef 1975). In the Pacific Ocean, Sakka et al. (2002) reported P o m a tod in iu m as a dom inant species in an atoll lagoon in French Polynesia, but this record is question­ able. The genus C ym bod in ium J. Cachon et M. Cachon is the least known kofoidiniacean. C ym bod in ium was described from the coastal Ligurian Sea (Cachon and Cachon 1967b); it was further reported with no illustration from N E A tlantic waters (Parke and Dodge 1976) and an estuary in Brazil (Bergesch and Odebrecht 1997). N o inform ation on the appearance of fixed specimens o f C ym bod in ium exists. These specimens may be too distorted by fixation to be identified. The noctilucaceans are o f great interest in the phylogenyn o f dinoflagellates. However, the existing phylogenetic inform ation is restricted to N o c tilu c a (Taylor 2004). M ost o f the species o f kofoidiniaceans were previously described from the N W M editerranean Sea. The present study reveals that there is an extensive bu t alm ost unknown diversity o f noctilucaceans in the oceans o f the world. Acknowledgements F.G . acknowledges the support o f the European Commission (ICB2-CT-2001-80002). Studies from the N E and Equatorial Pacific Ocean were supported by a G rant-in-aid for Creative Basic Research (12NP0201, DOBIS) from the M EX T, Japan. H. Claustre provided samples, collected by J. Ras, from the SE Pacific Ocean within the context o f the project BIOSOPE of the LEFE-CY BER. We are grateful to the scientists and crew of R/V Soyo M a ru (N at. Res. Inst. Fish. Sci.), R/V H a ku h o M a ru (Ocean Res. Inst., University Tokyo), R / V M ir a i (JAM STEC), R/V O shoro M a ru (H okkaido Univ.), R/V W a ka ta ka M a ru (Tohoku N at. Fish. Res. Inst.) and R/V L ’A ta la n te (IFR E M E R ). References 57 59 61 63 65 67: 69 71 73 75 77 79 81 83 85 87 89 91 Balech, E., 1962. Tintinnoidea y Dinoflagellata del Pacifico segun material de las expediciones Norpac y Downwind del Instituto Scripps de Oceanografia. Rev. Mus. Argent. Cienc. Nat. “ B. Rivadavia” . Cienc. Zool. 7, 1-253. Bergesch, M., Odebrecht, € ., 1997. Anâlise do fitoplancton, protozooplâncton e de alguns fatores abibticos no estuario da Lagoa Dos Patos. Atlântica Rio Grande 19, 31-50. Bursa,.A ., \9(A . Kofoidin ium arcticum, a new dinoflagellate. - M H i M i t i i i M i i i i i i t e Cachon, J., Cachon-Enjumet, M., 1966. Pomatodinium im ­ patiens nov. gen. nov. sp. péridiniens Noctilucidae Kent. Protistologica 2, 23-30. Cachon, J., Cachon, M., 1967a. Cymbodinium elegans nov. gen. nov. sp. péridinien Noctilucidae Saville-Kent. Protis­ tologica 3, 313-318. Cachon, J., Cachon, M., 1967b. Contribution à l'étude des Noctilucidae Saville-Kent, I. Les Kofoidininae Cachon J. et M. Évolution, morphologique et systématique. Protistolo­ gica 3, 427-444. Dodge, J.D., 1982. Marine Dinoflagellates of the British Isles. Her Majesty’s Stationary Office, London, 303pp. Fenaux, R., 1958. Contribution a l’étude de Kofoidinium velelloides. Bull. Inst, océanogr. Monaco., 1118, 11pp. 93 95 97 101 103 105 107 109 1 1 1 Please dte this article as: Gômez, F., Furuya, K., Kofoidinium. Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. European Journal of Protistology (2007), doi:10.1016/j.ejop.2006.12.002 295 10 F. Gômez, K. Furuya / European Journal of Protistology I ( U j i 11 13 15 17 19 21 23 25 27 Gômez, F., Furuya, K., 2005. Leptodiscaceans (Noctilucales, Dinophyceae) from the Pacific Ocean: first records of Petalodinium and Leptodiscus beyond the Mediterranean Sea. Eur. J. Protist. 41, 231-239. Gomez, F., Furuya, K., Takeda, S., 2005. Distribution of the cyanobacterium Richelia intracellularis as an epiphyte of the diatom Chaetoceros compressus in the western Pacific Ocean. J. Plankton Res. 27, 323-330. Halim, Y., 1967. Dinoflagellates of the South-East Caribbean Sea (East-Venezuela). Int. Rev. ges. Hydrobiol. 52, 701-755. Kofoid, C.A., Swezy, O., 1921. The Free-living unarmored Dinoflagellata. University of California Press, Berkeley. Konovalova, G.V., Selina, M.S., 2002. Life cycle o f Spatulo­ dinium pseudonoctiluca (Dinophyta) from Sea of Japan. Bot. Zhurnal. 87, 38-43. Margalef, R., 1969. Composiciôn especifica del fitoplancton de la costa catalano-levantina (Mediterrâneo occidental) en 1962-1967. Inv. Pesq. 33, 345-380. Margalef, R., 1975. Composiciôn y distribuciôn del fitoplanc­ ton marino en la regiôn de afloramiento del NW de Africa, en marzo de 1973 (Campana “Atlor 11” del ‘Comide de Saavedra’). Result. Exped. Cient. B/O Comide 4, 145-170. Parke, M., Dodge, J.D., 1976. Check-list of British marine algae—third revision. J. Mar. Biol. Ass. UK 56, 527-594. Pavillard, J., 1921. Sur le Gymnodinium pseudonoctiluca Pouchet. C. R. Acad. Sci. Paris 172, 86-87. Pavillard, J., 1928. Kofoidinium velleloides n. g. n. spec. Ann. Protistol. Paris 1, 159-161. Pavillard, J., 1937. Les Péridiniens et Diatomées pélagiques de la Mer de Monaco de 1907-1914. Observations générales et conclusions. Bull. Inst. océanogr. M onaco 738, 1-56. Pouchet, G ., 1885. Nouvelle contribution a l ’histoire des Péridiniens marins. J. Anal. Physiol. 21, 28-88. Rampi, L., 1952. Ricerche sul microplancton di superficie del Pacifico tropicale. Bull. Inst. océanogr. Monaco. 1014, 16pp. Sakka, A., Legendre, L., Gosselin, M., Niquil, N., Delesalle, B., 2002. Carbon budget of the planktonic food web in an atoll lagoori (Takapoto, French Polynesia), J. Plankton Res. 24, 301-320. Soumia, A., 1986; Atlas du phytoplancton marin. Vol. I: Introduction, Cyanophycées, Dictyochophycées, Dinophy- cées et Raphidophycées. Editions CNRS, Paris. Taylor, F.J.R., 1976. Dinoflagellates from the Intemational Indian Ocean Expedition. A report on material collected by R/V ‘Anton Bmun’ 1963-64. Bibliotheca Bot. 132, 1-234. Taylor, F .J.R ., 2004. Illumination o r confusion? Dinoflagellate molecular phylogenetic data viewed from a primarily morphological standpoint. Phycol. Res. 52, 308-324. Travers, A., Travers, M., 1975. Observation en Atlantique nord-est de Pomatodinium impatiens Cachon et Cachon- Enjumet, Dinoflagellé Noctilucidae, décrit de M éditerra­ née. Rapport et Procès verbaux des réunions. Comm. Int. Explor. Scient. Mer. Médit. 20, 315-316. Yamaji, I., 1980. Illustrations o f the M arine Plankton of Japan. Hoikusha Press, Osaka. 29 31 33 35 37 39 41 43 45 47 49 51 53 Please cite this article as; Gômez, F., Furuya, K., Kofoidinium. Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. European Journal of Protistology (2007), doi:10.10I6/J.ejop.2006.12.002 296 Ecologie / Ecology On the ecology and unusual life cycle of the dinoflagellate Spatulodinium pseudonoctiluca in the NE English Channel Fernando Gomez*, Sami Souissi Station Marine de Wimereux, Université des Sciences et Technologies de Lille, FRE 2816 ELICO CNRS, 28 Avenue Foch, F-62930 Wimereux, France Abstract The distribution of Spatulodinium (^Gymnodinium) pseudonoctiluca (Pouchet) J. Cachon et M. Cachon has been investigated for 8 years (1998-2005) in the NE English Channel, type locality of the species and its immature stages. The species can be found after the spring diatom bloom fi-om late May to October. The highest abundance was found in June 2004 after the Phaeocystis bloom. Exceptionally, the Phaeocystis bloom was absent in 2005 and only several specimens of S. pseudonoctiluca were observed. The immature and mature stages of Spatulodinium nearly always co­ occurred. No other kofoidiniaceans such as Kofoidinium or Pomatodinium were observed. The first stages of the development of Spatulodinium can easily confuse with gymnodiniaceans. The transformation of the stage “D”, which has been described as Gymnodinium lebouriae (=G. fulgens) or Gymnodinium conicum (=G. viridis), into the mature stage, is illustrated. The stage “D” is longihated froni a cluster of pairs of smal er ce s jome y an e onga e episome. In t e orea Atlantic Ocean, Spatulodinium pseudonoctiluca, a single species which life stages are often reported as separate species, is especially adapted to a strongly fluctuant environment. 297 Résumé Sur l'écologie et le cycle de vie peu commun du dinoflagellé Spatulodinium pseudonoctiluca dans la Manche orientale. Durant 8 années (1998-2005) la distribution de Spatulodinium (^Gymnodinium) pseudonoctiluca (Pouchet) J. Cachon et M. Cachon a été étudiée dans la Manche Orientale qui est un environnent type de cette espèce et de ses stades de développement. S. pseudonoctiluca peut y être observée après le bloom printanier des diatomées de fin mai jusqu’à octobre. Son abondance la plus élevée a été mesurée en juin 2004 après le bloom de Phaeocystis. En 2005 le bloom de Phaeocystis était exceptionnellement absent et seuls plusieurs spécimens de S. pseudonoctiluca ont été observés. Les stades de développement immature ainsi que le stade adulte de Spatulodinium apparaissent souvent en même temps. Aucune autre kofoidiniacea telle que Kofoidinium ou Pomatodinium n’a été observée pendant cette période. Les premiers stades de développement de Spatulodinium peuvent facilement être confondus avec des gymnodiniaceas. La transformation du stade ”D", décrite comme étant le stade immature de Gymnodinium lebouriae (=G. fulgens) ou de Gymnodinium conicum (= G. viridis), en stade adulte est ici illustrée. Le stade "D" provient d’un faisceau de paire de petites cellules jointes par un episome allongé. Dans l'Océan Atlantique boréal, Spatulodinium pseudonoctiluca, une espèce unique dont les stades de développement sont souvent décrit comme étant des espèces différentes, est particulièrement adapté à un environnement fortement fluctuant. Keywords: Spatulodinium pseudonoctiluca', Gymnodinium lebouriae lebouriae; Dinoflagellate; Life cycle; Microbial ecology Mots-clés: Spatulodinium pseudonoctiluca', Gymnodinium lebouriae lebouriae; Dinoflagellé; Cycle mimmmmmÊmaÊÊÊmÊÊÊÊÊÊÊÊÊÊÊÊKm * Corresponding author. E-mail address: fernando.gomez(^itoplancton.com Phone +55 321992926 FAX ̂ 33 321992901 298 1. Introduction The members of the family Kofoidiniaceae F.J.R. Taylor undergo an exceptional morphclogical transformation during their life cycle. This is responsible of the confusion on the identificatioi of the species of the kofodiniaceans. In one of the earlier works on marine dinoflagellates, louchet described Gymnodinium pseudonoctiluca from the coast of Brittany, SE English Charnel [1]. Pouchet found intermediate characteristics between gymnodiniaceans and Noctiluca scirtillans (Macartney) Kofoid. The two flagella, the occurrence of the cingulum and the sulcus is remhiscent of the gymnodiniaceans, especially the immature stage with an anterior cingulum that resenbles a large Amphidinium. The surface of the cell and the radiating fibrils from the perinuclear region resembles N. scintillans [1]. Pouchet illustrated G. pseudonoctiluca as a single species wih two differert forms. One form corresponded to a large Amphidinium-Xike pigmented and the othe form, the mature stage, was a round or oval non-pigmented laterally compressed cell. Off Plymouth (SW English Channel), near the type locality of G. pseudonoctiluca. Labour found 3 specimens of the immature stage of G. pseudonoctiluca [2]. From a single lighly pigmented specimen, she described Gymnodinium viridis Lebour [2]. Kofoid and Swezy reilized that the species name G. viridis was already occupied and they proposed G. conicum Kofrid et Swezy [3]. They considered that Pouchet was mistaken two species as a single one [3, p. 244].They considered that one of the immature stages of G. pseudonoctiluca in Lebour [2] was a separate species. They proposed Gymnodinium fulgens Kofoid et Swezy based on the Lebour’s fgure. Pavillard observed immature stages of kofoidiniaceans in the NW Mediterranean Sea [4. He considered that these forms, similar to the records by Pouchet and Lebour of G. pseudonoctluca, corresponded to a separate species and Pavillard proposed Gymnodinium lebouriae [4] (orignally described as Tebourii’ and commonly misspelled as ‘lebourae’; ICBN: Art. 60.11; Ex. 24.; R«com. 60C.l.b; Art. 23.5 and 32.5; [5]). Later, Pavillard described the type species of Kofoidinium thit at a first sight mainly dififered fix>m mature stage of G. pseudonoctiluca in the lack of the tentacle [6 ]. collected from the coastal Ligurian Sea (NW IVfediterranean) [7]. They recognized six sages labelled from “A” to “F ”. The morphology of the immature stages of the kofoidiniaceans w s too similar to distinguish and the species could only be identified at the sporont stage. In the stage: “A” and “B”, the spores first develop into Gymnodinium-XikQ ovoid motile cells (<35 pm long), vhich resemble non-pigmented gymnodiniaceans. As this stage, the cells ingest small particles sufh as bacteria. In stage “C ”, the hyposome has a globular shape and the cells develop a structure of ibrils radiating from the perinuclear region resembles N. scintillans. This stage was illustrated s G. pseudonoctiluca in Pouchet [1] and Pavillard [4]. Stage “D” has received the names Gymnodnium 299 lebouriae {-G. fulgens) and G. conicum {=G. viridis). In this stage, the globular hyposome transforms into a cylindrical shape that resemble a large Amphidinium-Vke cell. The shape of the episome is highly variable and sometimes a peduncle is observed. The cell develops a marked net of fibrils towards the cystostome and is able to ingest larger particles such as diatoms and silicoflagellates. At this stage, the cells reach the higher degree of pigmentation. According to Cachon and Cachon due to small pigmented lipid droplets and chloroplasts were not observed in any of the life stages [7]. In stage “E”, after the cells get the higher biomass, the cells transform into the sporont flattening laterally (stage “F”). The differences in the morphology of the mature specimens allow die identification of the specimens to species. In the case of mature Spatulodinium a tentacle is projected from the ventral region. The distribution of the kofodiniaceans is mainly restricted to warm to tropical waters, with the exception of Spatulodinium (^Gymnodinium) pseudonoctiluca only known from boreal waters and from the northern Mediterranean [7,8,9] and the Black Sea [10]. In the eutrophic and turbulent waters of the English Channel, the dinoflagellate assemblage has a low diversity. However, after the spring Phaeocystis Lagerheim and diatom bloom, S. pseudonoctiluca and its life stage “D” misidentified as G. lebouriae and G. viridis are highly distinctive species [1,2]. The present study investigated the seasonal and interannual distribution of the life stages of Spatulodinium, often considered as separate species, during 8 years in the proximity of the type locality. Illustrations of the transformation from stage “D” into the mature stage are provided. This study is the first to describe an unusual reproductive stage in Spatulodinium that consisted of a cluster of pairs of small cells that were similar in form to the previously described species G. lebouriae. 2. Material and methods Within the context of the SOMLIT monitoring program (Service d'Observation en Milieu LITtoral) 127 cruises were carried on board RA ̂ Sepia II from November 1997 to December 2005 off Boulogne-sur-Mer (NE English Channel). Two permanent stations were sampled during the station was located at 8 Km offshore (50°40’75 N; 1°24’60 E, 50 m depth). The sampling frequency was planned to be biweekly, but cruises were often cancelled or were restricted to the most coastal station due to meteorological constraints. During the spring and summer of 2003, 2004 and 2005, additional cruises were carried out with a sampling frequency planned to be once a week. Seawater samples were collected with a Niskin bottle at the surface and the bottom. Lugol-fixed samples of 25 or 50 mL were settled in composite settling chambers. The entire chamber was scanned at 200x with an 1X71 inverted Olympus microscope equipped with an Olympus digital camera and each specimen was photographed at 400x with the DP70-BSW software. 300 3. Results 3.1. Temporal distribution in the NE English Channel Spatulodinium was observed from May to October each year from 1998 to 2005 (Fig. 1). The highest abundance, 320 cells L'̂ ( 8 specimens in 25 mL) was observed in June 2004 after the bloom of Phaeocystis and diatoms, mainly Guinardia delicatula (Cleve) Hasle. Anomalously in spring 2005, the bloom of Phaeocystis spp. was not observed and only one specimen of Spatulodinium was observed. The abundance of microplankton as well as Spatulodinium was higher in the coastal stations. No clear differences in the vertical distribution of Spatulodinium were observed in this highly turbulent environment. During and after the spring Phaeocystis-didXom bloom, the dinoftagellate assemblage showed a low diversity. Heterotrophic species such as Gyrodinium spirale (Bergh) Kofoid et Swezy and Protoperidinium spp. were dominant. The only noctilucacean observed was the distinctive sporont of Spatulodinium and its immature stages, with the exception of a very few records oîNoctiluca scintillans. 3.2. Morphology and life stages The mature specimens of S. pseudonoctiluca (80-180 pm long) tend to be more oval than rounder in shape. The elongate tentacle was observed in all the specimens (Figs 11-14). The undulate flagellate often appeared unattached (Figs 12-13). Stage “D”, precursor of the mature stage, was the most distinctive of the immature stages and co-occurred with the sporont in nearly all the samples. This form, described as Gymnodinium lebouriae, showed a cylindrical shape with an anterior cingulum that resembles a large highly pigmented ^mpA/Jm/wm-like cell (Figs 6-10). One of the specimens showed two small “wings” during the transformation from stage “D” into the sporont Spatulodinium (Fig. 9). Coinciding with the period of highest abundance of Spatulodinium in June 2004, a cluster of four pairs of smaller cells of the form G. lebouriae joined at the elongate episome was observed (Figs 4-5). This may be the origin of the elongate episome observed in stage visible net of fibrils was observed. These cells, with variable degrees of pigmentation, may correspond to stages “B” or “C” of Spatulodinium (Figs 2-3). In the case of other smaller Gymnodinium-Xiike cells, it is difficult to discern if they are gymnodiniaceans or immature stages (“A”, “B”) of Spatulodinium. 4. Discussion 4.1. Distribution in boreal-Arctic waters. 301 The complex morphological transformation along the life cycle is responsible of the confusion in the identification of the species of kofoidiniaceans. The morphology of the immature stages of Spatulodinium and Kofoidinium are so similar that it is difficult to identify the genera to which the immature specimens belong. Spatulodinium pseudonoctiluca has been reported along the boreal Atlantic European waters, Russian and Canadian Arctic waters and in the vicinity of the Japan Sea [11]. However in several checklists in the Atlantic European waters Spatulodinium (^Gymnodinium) pseudonoctiluca and G. lebouriae are botlr included as separate species [12,13,14,15,16]. In British waters. Dodge considered G. lebouriae m immature life stàgQ of Kofoidinium [13]. If this consideration is valid, Kofoidinium should appear associated with G. lebouriae in the English Channel. However the only species co-occurring with G. lebouriae is Spatulodinium. All the species, G. pseudonoctiluca, G. lebouriae and G. viridis were described in the English Channel in June or July, which is the period of higher abundance of Spatulodinium as reported in the present study. No species oï Kofoidinium have been reported in the boreal Atlantic Ocean [15,16], Russian Arctic waters [17] or the Japan Sea [18], with a very few exceptions west Ireland [19] and the Norwegian Sea [13, 20]. Bursa [21] described K. arcticum in the Canadian Arctic waters where G. pseudonoctiluca has been reported [22]. As reported by Cachon and Cachon [7, p. 437] and Taylor [23] K. arcticum is a doubtful taxon, described from a single fixed specimen evidently deformed due to the preservation. Records of Kofoidinium in very cold waters of high latitudes are very rare compared to the more common Spatulodinium. 4.2. Records beyond boreal-Arctic waters The records of Kofoidinium in the boreal-Arctic waters are rare. However, Kofoidinium is common in the Mediterranean Sea [23], whereas the records of Spatulodinium are scarce. Cachon and Cachon illustrated the sporont in the Ligurian Sea [7]. In the Adriatic Sea, both Spatulodinium and Kofoidinium have been listed [8,9] as well as G. pseudonoctiluca and G. lebouriae [25], The Sea. In the Black Sea, the only record of S. pseudonoctiluca corresponds to Stoyanova [10]. No records of Kofoidinium exist in the Black Sea [26]. The records of Kofoidinium in temperate to tropical waters are numerous [23] and its immature stages may be referred as G. pseudonoctiluca [27,28]. Following Cachon and Cachon [7], Balech illustrated stage “C” of Kofoidinium pavillardii as G. pseudonoctiluca [27]. He reported K. pavillardii and K. velelloides and he did not find S. pseudonoctiluca. 4.3. Ecological aspects 302 The NE English Channel, near the Strait of Dover, is a shallower environment subjected to intense winds and a tidal flux of 8 meters [29]. A bloom of Phaeocystis dominates this highly turbulent environment in spring and diatoms throughout the year. The early immature stages of Spatulodinium feed on small particles such as bacteria, whereas the large stages, especially stage “D”, feed on larger particles such as diatoms. The Phaeocystis post-bloom conditions, usually around June, provide abundant detritical material from the decomposition of Phaeocystis that may favour the development of immature stages. The present study for the first time illustrates a unique reproduction of the immature stage “D” (Figs 4-5). Cachon and Cachon observed an 8 -cell chain that in only 2 hours divides into a 16-cell chain [7]. Stags “D” seems to develop a strategy of fast division in the short period of favourable conditions. The high abundance of diatoms in late spring and early summer is the source of preys for the larger stages of Spatulodinium. The present study investigates for the first time the ecological distribution of members of the family Kofoidiniaceae. Spatulodinium is especially adapted to the strong phytoplankton fluctuations in the turbulent northern English Channel. The unique mechanism of reproduction, which is here for the first time illustrated, facilitates the fast division and the occurrence of the mature stage in the short period of favourable conditions. Acknowledgements Samples were collected within the context of SOMLIT program on board RA/̂ Sepia II (INSU- CNRS). We thank to D. Degros, E. Lecuyer, D. Devreker and G. Flamme for their help on sample collection. We thank to A. Rhodes for her comments on the manuscript. 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Sarsia 83 (1998) 267̂ 292.̂ ^̂ L -. - - [18] Konovalova G.V., Analysis of the dinophyte (Dinophyceae) flora of the Russian Far East and adjacent waters of the Pacific. Asian Mar. Biol. 17 (2000) 1-14. [19] Raine R., White M., Dodge J.D., 'The summer distribution of net plankton dinoflagellates and their relation to water movements in the NE Atlantic Ocean, west of Ireland. J. Plankton Res. 24 (2002) 1131-1147. [20] 'Throndsen J. Hasle G.R, Tangen K., Norsk krysplanktonflora. Almater forlag, Oslo, 2003. [21] Bursa A., Kofoidinium arcticum, a new dinoflagellate. Phycologia 4 (1964) 1-14. 304 [22] Lovejoy C., Legendre L., Martineau M.J., Bâcle, J. von Quillfeldt C.H., Distribution of phytoplankton and other protists in the North Water. Deep Sea Res. I I22-23 (2002) 5027-5047. [23] Taylor F.J.R., Dinoflagellates from the International Indian Ocean Expedition. A report on material collected by RV ‘Anton Bruun’ 1963-64. Bibliotheca Bot. 132 (1976) 1-234. [24] Gomez F., Checklist of Mediterranean free-living dinoflagellates. Bot. Mar. 46 (2003) 215-242. [25] Schiller, J., Die planktischen Vegetationen des Adriatischen Meeres. Arch. Protistenk. 61 (1928) 119-166. [26] Gomez F., Boicenco L. An annotated checklist of dinoflagellates in the Black Sea. Hydrobiologja 517 (2004) 53-59. [27] Balech E., Los dinoflagelados del Atlantico Sudoccidental. Publ. espec. Inst. Espanol Oceanogr. 1 (1988) 1-310. [28] Ojeda A., Aportacion al conocimiento de los dinoflagelados (Dinophyceae) del orden Gymnodiniales en aguas de las Islas Canarias. Rev. Acad. Canaria Ciencias 12 (2000) 21-44. [29] Seuront L., Schmitt F.G., Lagadeuc Y., Schertzer D., Lovejoy S., Multiffactal analysis as a tool to characterize multiscale inhomogeneous patterns. Example of phytoplankton distribution in turbulent coastal waters. J. Plankton Res. 21 (1999) 877-922. Figure legends Fig. 1. Temporal distribution of the abundance (cell L*) of Spatulodinium pseudonoctiluca in the NE English Channel off Boulogne-sur-Mer from 1998 to 2005. Figs 2-14. Photomicrographs of Spatulodinium pseudonoctiluca. 2-3. Stage “C”, usually reported as Gymnodinium pseudonoctiluca. 4-5. Cluster of pairs of small cells of stage “D”. 6-10. Stage ‘‘D”, usually reported as Gymnodinium lebouriae [=G. fulgens) or G. viridis (=G. conicum). ' - "̂ The aîTOwsrinvfîgït ̂ ... I V " f ir . V T ': Z “ JV V transformation from stage “D”, G. lebouriae, into the mature stage. 11-14. Mature specimens. The arrows indicate the undulate flagellum. Scale bar =50 pm. 305 j 150- I ” -|. I 0- L 150- r 100- 8 Km offshore, surface k |IWWW|I 2 Km offshore, surface T V 150 - j 100 Î 50 I I 0 I ' 1908 1999 2000 2001 2002 2003 2004 ' 2005 1998 1999 2000 2001 2002 ’ 2003 2004 2005 y f r150 I < 0 8 Km offehore, 50 m depth 1998 1999 2000 2001 2002 2003 2004 2005 Date 2 Km offshore, 21 m depth 320 cell L"" I I 1998 1999 2000 2001 2002 2003 2004 2005 Date 100 & . 150 Fig. 1. 306 10* . . — . . / . . " . ' . . . . . / . . . « A g 307 3.2. Taxonomfa y distribuciôn de dinoflagelados poco conocidos: 3.2.5. Dinophyslales: HIstioneis Gômez, F., 2005. Histioneis (Dinophyslales, Dinophyceae) from the western Pacific Ocean. Botanica Marina 48, 421-425. Gomez, P., 2007. Synonymy and biogeography of the dinoflagellate genus Histioneis (Dinophyslales, Dinophyceae). Revista de Biologfa Tropical 55, aceptado. 308 Histioneis (Dinophyslales, Dinophyceae) from the w estern Pacific Ocean Fernando Gomez" Station Marine de Wimereux, Université des Sciences et Technologies de Lille, CNRS UMR 8013 ELICO, 28 avenue Foch, BP 80, F-62930 Wimereux, France, e-mail: fernando.gomez@fitoplancton.com Abstract The distribution of the dinoflagellate Histioneis was stud­ ied in the vicinity of the Kuroshio Current, the Philippine, Celebes, Sulu and South China Seas and the western and central equatorial Pacific Ocean. A total of 65 spec­ imens, assigned to 17 species, was observed. For the first time, photomicrographs of several species are reported. Histioneis cymloalaria and H. longicollis were the most common. Nearly all specimens were recorded from 0-70 m depth, and the highest abundance was recorded in the Philippine Sea in July (32°N, 138°E, 30 m depth) with a maximum of 32 individuals per litre. Keywords: dinoflagellates; Dinophyslales; Histioneis-, Pacific Ocean; phytoplankton. Introduction The tropical dinophycean Histioneis Stein (Histion=wing, neis=vessel) is characterized by an antero-posteriorly flattened, usually rotund to reniform or subreniform cell body with ornate hyaline list and rib systems. The left sulcal list is highly developed, whereas the right sulcal list is vestigial. The cingulum has a very long dorsal edge, is almost horizontal, and very concave. The epitheca has been reduced to a minute disc (Kofoid and Skogsberg 1928). Chloroplasts are absent and symbiotic cyanobac­ teria occur between the two robust lists of a large sin­ gular chamber (Hallegraeff and Jeffrey 1984). The genus Parahistioneis Kofoid et Skogsberg is distinguished from Histioneis mainly by the absence of the submarginal cross-rib of the posterior singular list found in Histioneis (Kofoid and Skogsberg 1928). Parahistioneis, intermedi­ ate between the genera Ornithocercus Stein and Histio­ neis, is considered to be congeneric with Histioneis (Balech 1971, 1988, Sournia 1986). Histioneis is a rare genus; its delicacy, transparency, small size and limited investigations in warm/tropical waters in the last decades contribute to the scarce records. Little is known of its ecological and geographical distribution. Records of Histioneis from the north-western Pacific Ocean are restricted to a few citations along the ̂Present address: Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK. coasts of Japan by Okamura (1912) and Abé (1967). Bohm (1936), Rampi (1952) and Balech (1962) reported several species from the tropical waters of the western and central Pacific Ocean. Wood (1963a,b) described several taxa from the surrounding waters of Australia. For the eastern Pacific Ocean, Kofoid and Skogsberg (1928), in the most complete study on Histioneis to date, described and well illustrated numerous species. The present study describes and illustrates the abun­ dance and composition, geographic and vertical distri­ butions of Histioneis collected in several regions of the tropical and equatorial western Pacific Ocean. Materials and methods Samples were collected during 10 cruises in the western Pacific Ocean (Figure 1 ). • Two cruises were carried out on board RA/ Soyo Maru (13-20 May and 3-10 July 2002) along the meridian 138°E in the vicinity of the Kuroshio Current. Nine sta­ tions were sampled from 30°30'N to 34°15’N in May, and 10 stations from 30°0'N to 34°20'N during the July cruise. At each station, 15 depths from 5-200 m were sampled. • RA/ Hakuho Maru visited the Celebes, Sulu and South China Seas from 7 November to 18 December 2002. Samples were collected from 10 stations at six depths from 0-150 m. • A cruise was carried out on board RA/ Mirai (15-28 January 2003) along the equator from 160°E to 160°W. Samples were collected from 9 stations at 14 depths between 0-200 m. In addition, during the ship transit in returning to Japan, several 5-1 samples were col­ lected by pumping from ca. 5 m depth and filtering through 10-|xm pore size Nylon mesh. • Six cruises were completed at station H (41°30'N, 145°47'E) on board R/V Oshoro Maru and station A7 (41°30'N, 145°30'E) on board R/V Wakataka Maru in the Oyashio area during the spring and summer of 2003. Samples collected by Niskin bottles were preserved with acidified Lugol’s solution and stored at 5°C. Sam­ ples of 400 ml were concentrated via sedimentation in glass cylinders. Over five days, the top 350 ml of each sample was progressively and slowly siphoned off with small-bore tubing. Fifty ml of concentrate from 400 ml of water were settled in composite settling chambers. The entire chamber was scanned at 200x with an inverted Nikon (Tokyo, Japan) microscope equipped with a Nikon digital camera and the specimens of Histioneis were pho­ tographed for further precise identification. Film photo­ graphs were taken during a short period when the digital camera was unavailable. 309 mailto:fernando.gomez@fitoplancton.com 50’N Subarctic Gyro Subtropical Gyre 3 20’N ■ South « < r Chma North EquatonW Cktrrent equMoii0 Counter Cumnt Soaoi taualtxial Cutmtl 120°E 140*E 160*E 180" 1S0“VV Longitude Figure 1 Map of the station locations marked by black circles in tfie western Pacific Ocean. Ttie black squares represent surface net sampling. Results A total of 65 specimens of Histioneis was recorded in the western Pacific Ocean and were tentatively assigned to 17 species (Figures 2-33). All specimens were observed as single cells, never in couplets of dividing cells, triads or tetrads (as occurs in other dinophyceans). Histioneis cymloalaiia Stein sec Balech (1988), with a sulcal list tapering posteriorly to a point, or rounder and with a vari­ able degree of reticulation, was the most common spe­ cies (Figures 3 -4 , 9-13). One specimen with a less com­ plexly ribbed sulcal list was tentatively assigned to H. cleaveri Rampi, being the first record after the original description (Figure 2). Specimens with a sulcal list with several radiating ribs from the main posterior rib and the posterior sulcal list more dorsally extended that H. cym- baiaria were tentatively considered as H. pacifica Kofoid et Skogsberg (Figures 5-7). Figure 8 illustrates a tenta­ tively immature specimen of a species related to the pre­ vious taxa. After H. cymbalaria, the most abundant species was H. longicollis Kofoid, and this species is assumed to show a variable development of the sulcal list (Figures 19-24). Several specimens, with less elon­ gate appearance and shorter sulcal list lacking ornamen­ tation in the posterior rib compared to H. longicollis, were considered to be H. joergensenii Schiller (Figures 17-18). Other species were observed from single or a few specimens, such as Histioneis pietschmannii Bohm in Schiller from the South China Sea, H. mitchellana Murray et Whitting and H. schilleii Bohm in Schiller from the Phil­ ippine Sea (Figures 14-16). Two specimens were identi­ fied as H. elongate Kofoid et Michener (Figures 25-26) and another corresponded to H. costata Kofoid et Mich­ ener (Figure 27). One specimen from the Philippine Sea was tentatively assigned to H. sphaeroldea Rampi (Figure 29), being the first record beyond the Mediterranean Sea (Gomez 2003). The identification of several specimens of the former genus Parahistioneis were more difficult, e.g., H. para Murray et Whitting or H. paraformis (Kofoid et Skogsberg) Balech. The specimen in Figure 30 was assigned to H. para, and a larger specimen to H. para­ formis (Figure 31). Another specimen was tentatively assigned to H. pachypus Bohm in Schiller (Figure 28), and another tentatively identified as H. oxypteris Schiller (Figure 32). In one case, the poor quality of the photo­ micrograph did not allow precise identification (Figure 33). In the vicinity of the Kuroshio Current (138°E) 10 indi­ viduals of Histioneis were found from the 131 samples analysed during the cruise in May. Four specimens were collected at 32°N. The maximum abundance was only two specimens per sample (5 cells M) (Figure 34). During the cruise in July, the stations were re-visited and 38 specimens were observed from 144 samples. As in May, the higher abundance was recorded in the offshore sub­ tropical waters of the Philippine Sea at 32°N. At this sta­ tion, 17 individuals were collected, with 13 specimens at 30 m depth (Figure 35). Nearly all the specimens corre­ sponded to H. cymbalaria, and a few specimens to H. longicollis. During the cruise in the marginal seas of the western Pacific Ocean 9 specimens were recorded from the 81 samples examined. All the specimens were collected in the 0 -30 m depth range, except for one indi­ vidual at 150 m depth in the Sulu Sea (Figure 36). In the western and central equatorial Pacific Ocean, only 8 specimens were observed from the 124 samples analy­ sed. All the specimens were found in the western Pacific warm pool and we have no records in the equatorial upwelling region (Figure 37). Samples from six cruises carried out off Hokkaido (north of Japan) were also ana­ lysed during this study. No specimen of Histioneis was observed in these cold subarctic waters under the influ­ ence of the Oyashio Current. Discussion Two species, Histioneis cymbalaria and H. longicollis, were the most common in the regions of the Pacific Ocean examined. However, previous studies in the area did not report these taxa. In the coastal waters off south­ ern Japan, Okamura (1912) reported H. highleyi Murray et Whitting, H. paraformis (as H. para), H. paulsenii Kofoid {7H. carinata Kofoid or ?H. elongata) and H. reticulata Kofoid. Ab»é (1967) reported H. hippoperoides Kofoid et Michener, H. pietschmanil and H. mitchellana. These authors collected their samples from surface hauls in coastal waters. Net sampling facilitates collection of rare species of phytoplankton, but the smaller and fragile specimens may be inefficiently retained, and their abun­ dances subsequently underestimated in comparison with larger or resistant congeneric taxa. In the present study, small species such as H. cymbalaria (<70 p,m length) were more common in offshore oligotrophic waters (Fig­ ures 34-37). Iriarte and Fryxell (1995) only reported H. longicollis and H. cf. mitchellana in the central equatorial Pacific Ocean. In general, Histioneis is a rare genus. Exceptionally, 13 specimens were found in one sample (32 cells M). The hydrological and trophic conditions (major nutrients), and 310 iE5ü%"i6' & a w 4 ^ 2 1 , . # R \ v 2 2 : 23 24 ma# Ip Figures 2-24 Photom icrographs, bright field optics, of Histioneis in right lateral view (except Figure 6 in dorsal view). (2) Tentatively H. cleaveri (33“N, ISS^E; 50 m depth). (3-4, 9 -13) Several specim ens of H. cymbalaria sec Balech (1988). (5-6) Tentatively H. pacifica (0°, 175”W; 50 m depth). (7) Tentatively H. pacifica (0°, 180°; 80 m depth). (8) Unidentified specim en (0°, 180°; 0 m depth). (14) H. pietschm annii (14°30'N, 118°E; 30 m depth). (15) H. m itchellana (32°30'N, 138°E; 50 m depth). (16) H. schilleri (7°N, 130°E; 30 m depth). (17-18) H. joergensenii. (19-24) H. longicollis. All at the sam e magnification, scale bar=20 |xm. the phytoplankton assemblage at the collection site were investigated, and compared to the surrounding stations. Not one of these factors can be inferred as responsible for the higher abundance of Histioneis at this location. Along the equator, Histioneis was found from 170°E to 175°W, coinciding with high seawater temperatures (>29.5°C ) and very oligotrophic conditions during El Nino in January 2003 (Figure 37). The distribution of Histioneis was different from the autotrophic or mixotrophic species of Dinophysis that can achieve high abundance in eutrophic coastal waters. The apochlorotic Histioneis differs from Dinophysis in having a large singular chamber that seems to be an adaptation for hosting unicellular cyanobacteria. These symbionts, named phaeosomes in early literature, were observed extracellularly in O rnithocercus and Citharistes 311 25 ' 26 2 9 . Figures 2 5 -3 3 Photom icrographs, bright field optics, of Histioneis in right lateral view. (25) H. elongata (32°N, 138°E; 50 m depth). (26) H. elongata (0°, 180°; 0 m depth). (27) H. costata (5"N, 121°E; 10 m depth). (28) Tentatively H. pachypus (7°N, 130°E; 10 m depth). (29) Tentatively H. sphaeroldea (33°30'N, 138°E; 20 m depth). (30) H. para (8'’50'N, 121 °48'E; 150 m depth). (31) H. paraformis (32°30'N, 138^E; 30 m depth). (32) Tentatively H. oxypteris (8°50'N, 121 °48'E; 150 m depth). (33) Unidentified specim en (30°30'N, 138°E; 50 m depth). All at the sam e magnification, except Figure 29 and Figure 33; scale b a rs=20 fxm. Kuroshio Philippine Sea Kuroshio Philippine Sea C1 B1 C6 C9 CIO C11 012 B3 , B2C8 0,7 Q5 0; 100 % May 2002 Jul 2002 33” 32“ 31 Latitude North along 138°E South China Sulu Sea Celet>es Sea Philippine 33“ 32“ 31“ Latitude North along 138°E Western Pacific warm pool Equatorial Upwelling Region 4 T W A. T : 100 150 20“0 150 Nov-Dee 2003 Jan-Feb 2003 2004 160“E 170“E 170“W equator 180' Longitute along the equator Figures 34-37 Section plots of the records of Histioneis in the western Pacific O cean indicated by black triangles (see Figure 1). (34) R ecords along the meridian 138''E in May. (35) Records from the sam e location in July. (36) R ecords from C elebes, Sulu and South China Seas. (37) R ecords from the western and central equatorial Pacific Ocean. The distribution of tem perature is shown. 312 stein and intracellularly \r\ Amphisolenia Stein (Hallegraeff and Jeffrey 1984, Lessard and Swift 1986). In the present study, nearly all the specimens of Histioneis contained symbionts. The few exceptions were probably due to losses through sample treatment or damage to the cin- gular chamber. Norris (1967) described the rod-shaped, purple/pink cyanobacterium in Histioneis as Synecho- coccus carcerarius R.E. Norris. From living material, Lucas (1991) reported the presence of dividing cells in all the populations of symbionts, indicating active growth. He suggested that transmission of the symbiont in His­ tioneis occurs (rather that renewed infection). In the study of Hallegraeff and Lucas (1988), the food contents in Histioneis were not recognizable, but resembled cyanobacteria. During the present study, samples were collected from the surface to 200 m depth. Nearly all the specimens were found in the upper 70 m depth (rarely just in the surface waters) and the highest abundance of Histioneis was at 30 m depth (Figures 34-37). If it is assumed that the cingular chamber functions as a greenhouse in which Histioneis grows symbionts to supplement its diet, the vertical position of Histioneis could be related to the opti­ mal irradiance for the growth of these cyanobacteria. In the upper waters (<70 m depth) of the tropical Pacific Ocean, free-living unicellular cyanobacteria such as Synechococcus Nageli are a ubiquitous component of the picoplankton with abundances of ~ 10x10® cells H (Blanchot et al. 2001). The vertical distribution of Histio­ neis could be related to the depth of maximal availability of potential prey and/or the optimal depth (irradiance) for the growth of the symbiont algae. Histioneis has been reported rarely in the literature of the last three decades, mainly due to the limited taxo- nomical studies carried out in open waters of tropical oceans. Records at the species level are necessary to investigate the distribution and ecology of this genus. Acknowledgements This study was supported by Grant-in-aid for Creative Basic Research (12NP0201, DOBIS) from the MEXT, Japan. I am grate­ ful to the scientists and crew of RA/ Soyo M aru (Nat. Res. Inst. Fish. S ti:), W \/ Hakuho Maru (ORI, Univ. Tokyo) and R/V Mirai (JAMSTEC), R/V Oshoro M aru (Hokkaido Univ.) and R/V Waka­ taka Maru (Tohoku Nat. Fish. Res. Inst.). I was supported by a fellowship of the European Commission (ICB2-CT-2001 -80002) held at the University of Tokyo with Prof. K. Furuya as host. This is a contribution to the French IFB “Biodiversité et Changement Global” programme. References Abé, T.H. 1967. The armoured Dinoflagellata: II. Prorocentridae and Dinophysidae C- Ornithocercus, Histioneis, Amphisole­ nia and others. Publ. Seto Mar. Biol. Lab. 15: 79-116. Balech. E. 1962. Tintinnoidea y Dinoflagellata del Pacifico segun material de las expediciones Norpac y Downwind del Insti­ tute Scripps de Oceanografia. Rev. Mus. Argent. Cienc. Nat. “B. Rivadavia”. Cienc. Zoo/. 7: 1-253. Balech, E. 1971. Microplancton del Atlantico ecuatorial oeste (Equalant I). Servicio Hidrografico Naval. Buenos Aires 654: 1-103. Balech, E. 1988. Los dinoflagelados del Atlantico Sudoccidental. Publ. espec. Inst. Espanol Oceanogr. 7: 1-310. Blanchot, J., J.M. André, C. Navarette, J. Neveux and M.H. Radenac. 2001. Picophytoplankton in the equatorial Pacific: vertical distributions in the warm pool and in the high nutrient low chlorophyll conditions. Deep-Sea Res. I 48: 297-314. Bohm, A. 1936. Dinoflagellates of the coastal waters of the west­ ern Pacific. Bull. Bernice P. Bishop. Mus. Honolulu 137:1 -54. Gomez, F. 2003. Checklist of Mediterranean free-living dinoflag­ ellates. Bot. Mar. 46: 215-242. Hallegraeff, G.M. and S.W. Jeffrey. 1984. Tropical phytoplankton species and pigments of continental shelf waters of north and north-west Australia. Mar. Eco/. Prog. Ser. 20: 59-74. Hallegraeff, G.M. and I.A.N. Lucas. 1988. The marine dinoflag­ ellate genus Dinophysis (Dinophyceae): photosynthetic, nerit- ic and non-photosynthetic, oceanic species. Phycologia 27: 25-42. Iriarte, J .L and G.A Fryxell. 1995. Microplankton at the equa­ torial Pacific (140°W) during the JGOFS EqPac Time Series studies: March to April and October 1992. Deep-Sea Res. II 42: 559-583. Kofoid, C.A. and T. Skogsberg. 1928. The Dinoflagellata: the Dinophysoidea. Harvard Univ., Mus. comp. Zoo/. Mem. 51: 1-708. Lessard, E.J. and E. Swift. 1986. Dinoflagellates from the North Atlantic classified as photctrophic or heterotrophic by epi- fluorescence microscopy. J. Plankton Res. 8: 1209-1215. Lucas, I.A.N. 1991. Symbionts of the tropical Dinophyslales (Dinophyceae). Ophelia 33: 213-224. Norris, R.E. 1967. Algal consortiums in marine plankton. In: (V. Krishnamurthy, ed.) Proc. sem inar on sea, salt and plants. Central Salt and Marine Chemicals Research Institute. Cath­ olic Press, Bharnagar, India, pp. 178-189. Okamura, K. 1912. Plankton organisms from Bonito fishing grounds. Rep. Imp. Bur. Fish. Sci. invest. Tokyo 1: 1-38. Rampi, L. 1952. Ricerche sul microplancton di superficie del Pacifico tropicale. Bull. Inst, océanogr. M onaco 1014: 1-16. Sournia, A. 1986. Atlas du phytoplancton marin. Vol. I: in troduc­ tion, cyanophycées, dictyochophycées, dinophycées et raphidophycées. Ed. CNRS, Paris, pp. 219. Wood, E.J.F. 1963a. Dinoflagellates in the Australian region. II.. Recent collections. C.S.I.R.O. Aust. Div. Fish. Ôceanogr. Rep. 14: 1-55. Wood, E.J.F. 1963b. Dinoflagellates in the Australian region. III. Further collections. C.S.I.R.O. Aust. Div. Fish. Oceanogr. Rep. 17: 1-20. Received 6 March, 2005; accep ted 8 Septem ber, 2005 313 Synonymy and biogeography of the dinoflagellate gtmxs Histioneis (Dinophyslales, Dinophyceae) Fernando Gomez Station M arine de Wimereux, Université des Sciences et Technologies de Lille, FRE 2816 ELICO CNRS, 28 avenue Foch, BP 80, F-62930 Wimereux, France; fem ando.gom ez@ fitoplancton.com A bstract: the genus H is tio n e is (= P a ra h is tio n e is ) contains an excessive num ber o f poorly described species, often based on the observation o f a single specimen and ignoring the intraspecific variability. In order to investigate the validity o f the species and to suggest synonym s, the original illustrations o f all know n species o f H is tio n e is are reproduced and grouped based on the morphological similarity. The scarce records and the uncertainties on the identification at the species level are responsible o f the lack o f biogeographical information. Large and highly ornam ented species tended to appear in tropical waters, whereas sm aller and less ornam ented species showed a w ider distribution and they can also found in tem perate waters such as the M editerranean Sea. Key words: H is tione is , P a ra h is tio ne is , D inophysiales, dinoflagellate, phytoplankton, biogeography. Histioneis Stein is a dinophysoid hetCTOtrophic dinoflagellate especially ad^ted to highly stratified, sub-tropical and tropical oceanic waters. The cingular or phaeosome chamber was modified to harbor unicellular diazotrophic cyanobactora and the orientation of the prominent left sulcal list was speculated to enhance a “feeding currenf ’ towards the sulcal region (Taylor 1980). Kofoid and Skogsberg (1928) elegantly described numerous species in the most complete study on Histioneis to date. Schiller (1933) described several new species and illustrated all the species known at that time. Further species were described by Forti (1932), Bohm (1933,1936), Rampi (1950,1952, see references in Rampi and Bernhard 1980), Osorio-Tafall (1942), Gaarder (1954), Halim (1960) and Wood (1963#)^R W A lÿ^P dl^A d K%##Ô2)"aaèG6rKë^(2005^^ micrographs of species fi*om the Mediterranean Sea and the Pacific Ocean, respectively. Histioneis has a transverse or cross rib in the lower cingular list that is lacking in the genera Parahistioneis Kofoid & Skogsberg and Ornithocercus Stein. According to Wood (1968) more than six radial ribs in the posterior cingular list corresponded to Ornithocercus and less than six radial libs to Parahistioneis. The species Histioneis francescae Murray & Whitting was transferred to Ornithocercus (Balech 1962). The genera Histioneis and Parahistioneis have been considered as synonyms because the cross rib is often hardly visible or it can be considered as a poor taxonomical characteristic for the generic separation (Balech 1988). Balech (1971) transferred Parahistioneis 314 mailto:femando.gomez@fitoplancton.com paraformis whereas P. acuta, P. acutiformis, P. conica, P. gascoynensis, P. pachypus, P. pieltainii, P. sphaeroidea and P. varians have not been formally transferred to Histioneis. Further studies may split the genus Histioneis into several new genera with the re-establishment of Parahistioneis. Consequently at the present, the erection of new combinations, 35 years after the last one, would create more confusion. More than 100 species have been described since the earliest description of the type species {H. remora Stein 1883) to the latest one (Rampi 1969), being one of the most numerous genus of marine dinoflagellates (Gomez 2005a). Nearly all the species were described fiom a single or few specimens and often with no further records after the initial description. Abé (1967), Balech (1971, 1988) and Taylor (1976) discussed on the validity of several species. The hterature was often ancient and scattered, and no revision on the entire genus is available since Kofoid and Skogsberg (1928) and Schiller (1933). The identification at the species level is difficult due to the deficient delimitation of the species and it is uncertain how many species are valid. Within this context, little is known on the biogeography of Histioneis. The present study revises the synonymy of Histioneis in order to facilitate the identification at the species level and discusses on the geographical distribution. MATERIALS AND METHODS The original illustrations of all known species of Histioneis were reproduced and grouped based on the morphological similarity. Key diagnostic characters for the identification of the species include the cell body sh^e, primary ribs of the left sulcal list and the cingular list features (lateral pouch development, inclination of the upper cingular list). Other features such as the areolation of the hypotheca wall are characteristic of only a few taxa (i.e. H. biremis). For the descriptive terminology is important (Fig. 1): R2 (middle rib) the fission rib, at the place where the list is divided by binary fission and R3 (posterior main rib), the list near the posterior end of this list, if more than one rib is present in this region, the best developed of these (Kofoid and Skogsberg 1928). In species such as H. longicollis^ a loop formed by the R2 bending posteriorly and anastomosing with R3 is here named “window”. Several species also showed supplementary ribs (i.e. H. megalocopa). RESULTS AND DISCUSSION Several factors should take into account on the study of the validity of the species based on the original descriptions. Biological factors such as the unknown life cycle and its phenotypic 315 intraspecific variability, difierent degree of development after the division or morphological modifications as an adaptation to aivironmental turbulence conditions may be responsible of the description of morphotypes as separate species. In addition, die transparency of the hyaline structures may be responsible of incomplete descriptions and even new species may be described fiom specimens damaged through sample treatment The scarce records of Histioneis make difficult to assess the intraspecific variability. No species of Histioneis has been cultured and die only existing information on the life cycle of the Dinophysiales came fiom a few toxic specie of Dinophysis Ehrenberg that have been temporally cultured. Dinophysis exhibited a high morphological variability, conplicated by the existence of intermediate forms and the occurrence of “small cells” that have been previously considered to be different species (e.g. Reguera and Gonzalez Gil 2001). The possible phenotypic variability was not considered in the description of the species of Histioneis, often based on single specimens. The size and shape of the sulcal list of Histioneis could vary as an ad^tation to the turbulence conditions as reported for winged dinoflagellates such as Ceratocotys horrida Stein (Zirbel et al. 2000). Immature individuals of Histioneis could be described as new species. The degree of reticulation in the sulcal list probably depends on the maturation following the last division. As reported for Dinophysis the reticulation in the sulcal list was more pronounced on the fully developed-mature specimen and absent in the regaierated half of the list after division (e.g. Reguera and Gonzalez Gil 2001). This factor may he especially relevant in species with supplanentary ribs such as H. megalocopa. Difierent morphology of the sulcal list can be related to the phenotypic variability, whereas the variation in sh^e of the hypotheca is expected to be more conservative. In addition to the incidence of natural factors, the delicate Histioneis, usually collected by net hauls, can be damaged through sample treatment. Incomplete individuals may be described as new species (i.e. H. elegans resembled a damaged individual of H. villafranca). The transparency of the hyaline fins of Histioneis can easily be overlooked being responsible of the incomplete descriptions (i.e. H. elongata). The tine drawings of the original descriptions of some species have been excessively simplified as in Bohm (1933,1936) and Wood (1963a,b) (i.e. H simplex) mà. other illustrationg^#^^^ seem to be over-stylized (i.e. H. josephinae). The cell size as a criterion for the species identification should be considered with caution due to the imprecise size measurements of the early descriptions. For exanple Stein (1883) did not provide information on the magnification of his figures, being misinterpreted by further authors. All these factors, especially the unknown morphological variability in the life cycle, could have been responsible for the excessive proliferation of new species of Histioneis. 316 Delimitation of groups and synonymy: The original descriptions and some illustrations by other authors were grouped based on morphological similarities. In the present study with no phylogenetic purposes and to facilitate the comparisons, the groups of species of Histioneis were mainly delimited by 1 ) the sh^e of the cell body (rotund, reniform, etc) and 2 ) the orientation and shape of the left sulcal list Histioneis cymbalarior^oxsp'. (Figs 2-26) Confusion in the identification of the species of Histioneis began since the first publication. Stein (1883) described the type species, H remora, and H. biremis, H crateriformis, H megalocopa and H. cymbalaria. For this last taxon, he reported three different lateral figures and one ventral view (Figs 3 ,6 ,12). Later, Schiller (1933) described H skogsbergii based on one of the lateral views and the ventral view illustrated by Stein for H cymbalaria (Fig. 3). Kofoid and Skogsberg (1928) considered other of the Schiller’s figures of H cymbalaria as a synonym of H hyalina (Figs 6 ,9). Two further described species, H. depressa and H schilleri (Figs 7, 24), also resembled H cymbalaria. From the observation of a single specimen, Taylor (1976) reported tiiat H. depressa in many respects resembled a very small H. mitchellana in which the reticulation was reduced in conq)lexity (Fig. 5). From abundant material, Balech (1988, p. 237) illustrated 3 morphotypes of H. cymbalaria (Figs 13-15). Balech considered H. depressa as a synonym of H cymbalaria. Histioneis depressa has been illustrated with difierent morphology even by the same author (Fig. 4) (Wood 1963,1968). One of the line drawings by Balech (1988) of H. cymbalaria was similar to Taylor’s (1976) figure oïH depressa (Figs 5,14). None of the illustrations by Taylor or Balech corresponded to Schiller’s figure of H. depressa (Fig. 7). Gomez (2005b) observed several specimens of H cymbalaria fiom the same sanple that allowed the observation of the intraspecific variability. The t^)ering of the sulcal list of difierent specimens was pointed or rounded with variable perforation and the size (-60 pm length) was similar to that for H. cymbalaria sec Balech (1988) or H. depressa sec Taylor (1976). Stein (1883) did not provided information on the size of H. cymbalaria, but Schiller (1933) with no new observations of H. cymbalaria rqx)rted that the length was 130-160 pm. Balech (1988, p. 6 6 ) considered that the - species described by Stein (1883) should be reduced in size to match with the real dimensions. The Schiller’s compilation was commonly referenced for the identification for many authors working in the Mediterranean Sea. Consequently the Mediterranean specimens of H. cymbalaria that really measured 60-65 pm long, instead of 130-160 pm, may be assigned to species of similar morphology and smaller size such as H. depressa. Histioneis depressa, described fi*om the cold waters of the northern Adriatic Sea, was one of the more commonly cited species in the Mediterranean whereas no record of H. cymbalaria existed (Gomez 2003). Beyond the possible H. cymbalaria-depressa synonymy, H. cymbalaria may be present in the Mediterranean Sea because 317 H. speciosa (Fig. 11), only known fiom the original description in the Mediterranean Sea, is here considered as synonym of H. cymbalaria. Histioneis depressa sec Polat and Koray (2002) showed a rounder cell body, the sulcal list was more ventrally deflected and had a lateral pouch compared to the original descriptioii Further research should address VTh&fPsr Histioneis depressa and/7. cymbalaria are conspecific or both co-occur in the Mediterranean Sea. Records beyond the Mediterranean Sea such as H. depressa sec Taylor (1976) corresponded to H. cymbalaria (Table 1). In addition to the confusion between H. cymbalaria and H. depressa, the species H. hyalina is considered a synonym of other of the Stein’s figures of H. cymbalaria (Kofoid and Skogsberg 1928). Stein (1883) could try to show the intraspecific morphological variability of H. cymbalaria with three different illustrations. Stein’s figure showed a specimen with a kidney-shaped cell body, whereas H. hyalina showed a rounder cell body and the sulcal list was more ventrally deflected (Figs 6, 9). Balech (1988, p. 66) already reported that the figures of H. hyalina by Kofoid and Skogsberg and by Stein corresponded to separate species. The illustration of H. hyalina by Wood (1963) was closer to H. depressa (Figs 4, 7). Recently Histioneis cleaveri (Fig. 16) has been tentatively identified finm the Pacific Ocean (Gomez 2005b). Histioneis detonii, only reported by Ranq)i finm the Mediterranean and Pacific waters, showed a sulcal list that resembled members of the c y m b a l a r i a - but it diffaed in having a narrow reniform cell body (Fig. 25). Histioneis rampii, only know by the authority, showed a gibbous ventral margin and the cingular lists inclined (Fig. 17). Histioneis robusta is characterized by a margin extended ventrally (Fig. 18). Histioneis skogsbergii, described by Schiller based on one of Stein’s figures of H. cymbalaria (Fig. 3), with the sulcal list t^reiing posteriorly to a point and highly reticulated, is considered here as a morphotype of H. cymbalaria. Histioneis schilleri (Fig. 24), larger than H. cymbalaria and characterized by a posterior list gibbous and reticulate margin, was a distinctive taxon often reported in the western Pacific Ocean (Table 1). Gomez (2005b) illustrated H. schilleri and H. mitchellana. Histioneis schilleri should not be considered a synonym of H. mitchellana contrary to the opinion by Taylor (1976). In the Caribbean Sea, Paulmier (2004) rqrorted H. cymbalaria, but his figure corresponded to H. schillen, whkMsa& been cited in that location (Diaz-Ramos 2000) (Table 1). Histioneis bougainvillae (Fig. 2), only known by the authority, showed a round cell body and several loops in the sulcal list that differed fiom other members of the cymbalaria-gixiup. Histioneis caminus, with a very sketchy description, would require further research (Fig. 26). A subgroup of species included in the cymbalaria-^up is characterized by a saddle-sh^ed cell body that was higher dorsally. Histioneis pietschmanii was a distinctive taxon commonly reported in the Pacific Ocean (Gomez 2005b, Table 1). Histioneis panaria and H. panda dififered in the size of the cingular list (Figs 19,20). Norris (1969) reported that the hyaline fins of H. panaria could 318 easily go unnoticed. Abé (1967) proposed H. pulchra as a synonym of H. mitchellana (Figs 22, 23). Abé considered that the figures of H. mitchellana by Kofoid and Skogsberg (1928) also illustrated H. pulchra. Both taxa are here considered as separate species until fiirther research. Histioneis longicollis-gyoup: (Figs 27-46) The l o n g i c o l l i s - is characterized by a round cell body and the sulcal list inclined ventrally compared to the cymbalaria-^up. In the cymbalaria- group the hypotheca was kidney or saddle-shaped and the sulcal list was more dorsally deflected. Both groups had a window formed by the R2 bending posteriorly and anastomosing with R3 , quadrangular in members of the c y m b a l a r i a - and circular in the /o«g/co//w-group (quasi triangular for/7 joergensenii). Histioneis longicollis showed a high degree of variability in the development of the sulcal list, including specimens with a short sulcal list (Gomez 2005b). Schiller (1933) did not reproduce the original Kofoid’s figure of H. longicollis (Figs 39,40) and his figure resembled H hyalina (Fig. 9). Halim (1960) reported H. longicollis fiom die Ligurian Sea and he described four close taxa: H. elegans, H. faouzii, H. sublongicollis and 77 villafranca (Figs 27-31). The length of these taxa, 72 pm, agreed with 77 longicollis sec Halim (Fig. 29). The four species, described fi-om single or few specimens, mainly diSered in the distal branches of the sulcal list. These taxa, only known by tiie authority (except 77 faouzii, Rampi 1969), are here considered synonyms of 77 longicollis. Histioneis minuscula (Fig. 32) was akin to specimens of 77 longicollis with a scarcely developed sulcal list and together with 77 kofoidii (Fig. 33) may be considered synonyms of 77 longicollis. Histioneis pacifica is characterized by the sulcal list inclined dorsally and several ribs radiated marginally from the window (Fig. 44). The sulcal list of 77 longicollis was acuter and the cell body was rounder than in H. pacifica. Schiller (1933) suggested that 77 pacifica and 77 hyalina may be synonyms. Histioneis pavillardii dififCTed fiom H. bemhardii in the more elongate appearance (Figs 43, 45). Both taxa were tentatively considered as synonyms of 77 pacifica. Histioneis imbricata (Fig. 46), never reported after the initial description (Table 1), appeared to occupy an intermediate position between 77 longicollis and 77 pacifica. In 77 (Fig; 42)v illustrated by Polat and- Koray (2002), lacked the window, but otherwise resembled the longicollis-^vp. Histioneis aequatorialis with a well-developed dorsal sail and supplementary ribs resembled members of the megalocopa-group. However, 77 aequatorialis was tentatively included in this group due to its rounded cell body (Fig. 41). Histioneis longicollis and H. joergensenii, two of the most common species in the Mediterranean Sea (Gomez 2003), may be synonyms according to fiie illustrations by Rampi and Bernhard (1980) (Figs 37, 38). The shape of the window was rounded in H. longicollis and quasi triangular in 77 joergensenii. Histioneis joergensenii appeared to be intermediate between 77 vouckii and 77 planeta (Figs 34-36). For 77 vouckii the R2 and R3 joined acutely in the margin of 319 the posterior part of a shorter sulcal list. Histioneis planeta showed a larger sulcal list tiiat resembled H longicollis. Histioneis elongata-^ovp: (Figs 47-56) This group is characterized by a long R3 , the cross-rib extended ventrally and a smooth triangular sail extended fiom R2 to R3 . Bohm (1936) illustrated the intraspecific variability of the sulcal fist of H. elongata (Figs 51, 55). Histioneis costata mainly difibed fiom H. elongata in the shorter R3 and it cannot be discarded that both taxa may be conspecific (Figs 55, 56). Histioneis isselii showed an ornamented sulcal fist and in some way resembled the members of the longicollis-gKsup (Fig. 50). Histioneis subcarinata resembled H. elongata sec Bohm (1936) (Figs 49, 51). Histioneis carinata differed fiom other membŒS of this group in the narrow cell body (Fig. 48). Histioneis elongata var. curvata showed a less rotund cell body than H. elongata. Its cell body resembled H. subcarinata and the sulcal fist of H. elongata var. curvata only differed fiom that taxon in the occurrence of the marginal sail that extended dorsally behind R3 (Figs 47,49). Histioneis moresbyensis differed mainly fiom H. costata in the R2 bent sharply backwards and the more ellipsoidal cell body (Fig. 54). I f the bent R3 of H. moresbyensis with a dorsal supplementary rib is projected in the vertical axis of the cell, this taxon resembled H. australiae (Fig. 53). The cell body of Histioneis lanceolata (Fig. 52) was rotund and as in 77 australiae showed a siqjplementary rib branching dorsally behind R3 . These last three species, never reported after the initial descriptions, need fiirther research (Table 1). Histioneis para-group: (Figs 57-62) The species of this group are characterized by a long R3 , almost in the vertical axis of the cell and the cingular fists wide and ribbed Most of the species of this group and several species of the next two groups have been described as Parahistioneis. The hypotheca was hemispherical for 77 paraformis (Figs 59,61) and more triangular for 77 para (Fig. 58). The original description of 77 para and that by Kofoid and Skogsberg (1928) showed slight differences in the sulcal fist (Figs 59, 61). Parahistioneis conica is here considered as a synonym of 77. para (Figs 57, 58) and P. acuta is tentatively considered as-a sync«rym 59-61). Histioneis rotundata is included in this groiq) although it showed a slightly bent R3 and the margin undulated (Fig. 62). Histioneis garrettii-^onpi (Figs 63-74) This group is characterized by a R3 that extended straight almost in the vertical axis of the cell, but the R3 was shorter than in the previous group. Several species had a supplementary rib fix)m R3 dorsally. Histioneis karstenii (Fig. 63) showed a relatively large epitheca, non-pedunculate anterior cingular fist and an elongated margin that in some way resembled Ornithocercus. Histioneis garrettii sec Balech (1988) resembled77 diomedeae'md\R 320 body shape and ventral cross-rib (Figs 6 6 , 67). Histioneis garrettii sec Balech (1988) showed the R2 and R3 more ventrally deflected than in the original description of H. garrettii and showed the anterior cingular list wider and the sail branching dorsally fiom R3 less developed (Fig. 6 6 ). Schiller (1933) included 77 dentata (Fig. 64) in the biremis-gioup. The species P. pachypus and 7*. varians are synonyms (the former has the priority) (Figs 68,69). Histioneis gregoryi (Fig. 70) showed more elongate appearance than P. pachypus. Parahistioneis sphaeroidea and P. pieltainii showed a similar shape of the sulcal list, being more ornamented in P. pieltainii that also showed the upper cingular list inclined (Figs 72,73). Gomez (2005b) illustrated a tentative P. sphaeroidea that, if valid, constituted the first observation after the initial description (Table 1). The original illustration of 77 tubifera was very sketchy and only known by the authority (Fig. 71, Table 1). Parahistioneis pieltainii, P. sphaeroidea and 77 tubifera may be synonyms. Hernandez-Becerril et al. (2003) suggested the synonymy of P. pieltainii and 77 isselii. The type species, 77 remora, with a long R3 is included here only based on the general qjpearance (Fig. 74). According to Bohm (1936), 77 remora illustrated by Jorgensen (1923) could correspond to 77 elongata. The records of the type species have been scarce and often misidentified due to the insufiScient description by Stein (1883). Histioneis crateriformis-gyoup: (Figs 75-84) This group is closely related to the garrettii-gioup, but with a more ventrally deflected R3 . The hypotheca was semicircular and usually the cingulum broad. As in the previous groiç), there was a high number of closely related species and immature specimens may be described as new species. Species such as 77 paulsenii and 77. reticulata were described from single specimens (Figs 78, 83). Histioneis reticulata could correspond to specimens with a scarcely developed sulcal list of 77 crateriformis (Fig. 80). Balech (1971) considered 77 reticulata and 77 crateriformis as synonyms and later as separate species (Balech 1988). The sulcal list of the Balech’s figure of H. reticulata (Fig. 81) was closer to 77 crateriformis (Fig. 80), whereas the Balech’s figure of 77 crateriformis (Fig. 82) was closer to 77 mediterranea (Fig. 84) and 77 mediterranea sec Rampi and Bernhard (1980) (Fig. 85). Histioneis mediterranea resembled 77. reticulata (Figs 83, 84). Balech (1988, p. 63) observed abundant material of 77 crateriformis and he considered that the original Stein’s figure was incomplete. Paulmier (2004, p. 201) illustrated a specimen identified as 77 cf. crateriformis. Histioneis oxypteris (Fig. 79), tentatively identified by Gomez (2005b), resembled 77 crateriformis and 77. paulsenii. According to Balech (1988), 77 paulsenii in Norris (1969) included 77 reticulata and 77 crateriformis. Histioneis crateriformis sec Balech (1988) resembled P. pachypus (Fig. 6 8 ). The small size of the specimens and the short sulcal list made the delimitation of the species of this group especially difficult. Taken into account the high intraspecific variability reported for Dinophysis, 77 reticulata is here considered as 321 synonym of H. crateriformis and also probably H. mediterranea and P. pachypus. Parahistioneis gascoynensis (Fig. 77) is only known by the authority (Table 1). Parahistioneis acutiformis was similar to H. diamantinae in the sulcal list, but the orientation of the R3 was different (Figs 75, 76). Histioneis inclinata-gcoxsp'. (Figs 85-90) This group is characterized by a left sulcal list short, ending ventrally and with a round margin Histioneis mediterranea according to Rampi and Bernhard (1980) resembled H. dubia, being the R3 illustrated in the former taxon (Figs 85, 8 6 ). Histioneis differed fiom H. inclinata in the larger sulcal list, ending more ventrally in H. inclinata. Both taxa, with the R3 absent, may be synonyms (Figs 87, 8 8 ). Histioneis inornata differed fiom other members in the large cingular chamber and a short bent R3 (Fig. 89). The sketchy illustration of H. simplex could correspond to the shape of H. alata, but both taxa differed in the shape of the cell body (Fig. 90). Histioneis gubernans-group: (Figs 91-99) This group is characterized by a rotund cell body and the R3 and R2 deflected ventrally with round margins and forming loops. Tlie four illustrations of H. variabilis reported by Schiller (1933) showed the intraspecific variability. Histioneis steinii Schiller (non H. steinii Lemmermann) is a nomenclatural synonym of H. variabilis. According to Balech (1988) H. variabilis was a synonym of H. striata (Figs 94,95, illustrated by Polat and Koray 2002). Histioneis parallela (Fig. 93) is here also considered as a synonym of H. striata. Histioneis cerasus showed the ^ and R3 almost parallel and branched marginally (Fig. 92). As reported by Taylor (1976), H. fragilis seems to be an immature specimen lacking that part of the left sulcal list posterior to the R2 (Fig. 91). Soumia (1986, p. 153) illustrated an unidentified Histioneis which sulcal list resembled that of H. fragilis, but it differed in having a saddle-shape cell body (Fig. 100). Histioneis ligustica and H. expansa may be considered conspecific based on the original illustrations (Figs 96,97). Polat and Koray (2002) illustrated the latter taxon. Both taxa only showed slight differences in the outline and ornamentation of the sulcal list and they are here considered as syiionyrns ofÆgwèerwû/ts (Fig. 98). Histioneis reginella, with the accessory lis fe th jfe i^ . characterized megalocopa-gtoup, has been included here due to the rotund cell body (Fig. 99). Histioneis megalocopa-gyoup: (Figs 100-106) This groiq) differed fiom the previous one in having a reniform cell body. The sulcal fist achieved the highest degree of development with accessory lists. These ornamented species were likely to suffer breakage of fire accessory fists through sample treatment. There were not reasons to consider Histioneis milneri, H. helenae and H. hippoperoides as separate species {H. milneri has the priority) (Figs 101-103). Histioneis megalocopa and 77 322 dolon are here considered as synonyms contrary to Balech (1988) (Figs 104, 105). Histioneis josephinae (Fig. 106) may be an extremely elaborated form of H. megalocopa. Histioneis navicula-^oup: (Figs 107-108) This group is composed of Histioneis navicula and H. oceanica that were not ascribed to any of the previous groups (Figs 107,108). Both taxa, never reported after the initial descriptions (Table 1), showed a very narrow cell body and a large cingular chamber. Histioneis navicula (Fig. 107) resembled H. panda (Fig. 19). The sulcal hst of H. oceanica (Fig. 108) resembled H. elongata var. curvata (Fig. 47), but it differed in having a narrow subreniform cell body. These rare taxa may be conspecific {H navicula has the priority). Histioneis biremis-gcovapi (Figs 109-111) Histioneis highleyi and 77 biremis showed a distinctive Y-shaped and sigmoid areolated hypotheca, respectively (Figs 109, 110). These species seem to be a transition between Histioneis and Citharistes Stein. Ojeda (1999) illustrated a specimen of Histioneis (Fig. I l l ) with a distinctive pear-shaped hypotheca and the sulcal list as in 77 elongata sec Bohm (1936). The sharper extreme of the hypotheca of 77 biremis was more posteriorly deflected than in Ojeda’s specimen (Figs 110,111). Biogeography : The distribution of Histioneis is restricted to warm waters. The northern records in the NW Pacific appeared associated with the warm waters of the Kuroshio Current (Okamura 1912, Abé 1967). Wood (1964) reported that Histioneis did not occur below 17°C in the southern waters of Australia. Balech (1988) excqrtionally recorded one specimen of 77 cymbalaria at 13°C and other of 77 highleyi at 10°C in the South Atlantic Ocean. In the open north-western Pacific Ocean, the most ubiquitous species were Histioneis longicollis and 77. cymbalaria (Gomez 2005b). It should be taken into account that net sampling does not allow collecting the smaller and fiagile specimens. Consequently historical studies based on net hauls could underestimate the occurrence of these taxa versus larger and resistant species. Histioneis biremis and 77 highleyi are easily identifiable and distinctive species. To the best of my- knowledge, the distribution of 77 biremis is restricted to the Indo-Pacific region with one ancient record in the tropical Atlantic Ocean (Murray and Whitting 1899) (Table 1). Histioneis highleyi, a common species in the coastal waters of the western Pacific Ocean (Bohm 1936), is also known fiom the Atlantic Ocean (Table 1). None of both taxa is known fi*om the Mediterranean Sea. Forty species of Histioneis have been cited in the Mediterranean Sea, being the type locality of 27 species. This substantial species richness can be attributed, in part, to the historical tradition of taxonomic studies. A total of 13 species are exclusively known fi-om the Mediterranean Sea (Gomez 2006). However, the consideration as endemic species should be cautiously considered due to 323 doubts in the validity of these taxa. Histioneis depressa (=?//. cymbalaria), H joergensenii and H longicollis were the most common species, followed by H marchesonii, H inclinata, H mediterranea and H variabilis (Gomez 2003). It can be expected more records of Histioneis in tiie warmer sub-basins of the Mediterranean However, most of the records of Histioneis are reported in the colder sub-basins such as Ligurian and Adriatic Seas (Gomez 2003) because the warmer areas such as the South Ionian Sea are nearly unexplored. Apparently in the Mediterranean Sea were lacking species of Histioneis with accessory ribs such as H megalocopa and H milneri. Other large distinctive ornamented taxa such as H. mitchellana, H. pietschmannii or H. schilleri are known from tropical waters such as the Caribbean Sea, but they are absent from tenperate waters such as Mediterranean Sea. Zirbel et al. (2000) concluded that Ceratocorys horrida increased the length of the extensions under low turbulence conditions as a strategy to reduce the sinking speed. The low turbulence conditions that prevail in stratified tropical waters may favor species of Histioneis with large sulcal lists. In addition, the size and shape of the left sulcal list may be an adaptation for the capture of preys by modulating a feeding current (Taylor 1980). Consequaitly a large sulcal list may reduce the sinking speed and facilitate the capture of picoplankton preys. In addition to the hi^rly developed sulcal list that characterizes Histioneis, all the species have developed an especial chamber to harbor unicellular diazotrophic cyanobacteria that may constitute a simplement of the diet for the dinoflagellate. The miooalgal preys may be found in wide geogr^hical range. However, the requirements of the diazotrophic cyanobacteria could limit the geographical distribution of Histioneis. The dinitrogen fixation tended to be favored at high temperatures and this may explain the warm-water distribution of Histioneis. In cold waters or environments with a h i^ abundance of microalgal preys, the costs of carrying an enmty large cingular chamber would render Histioneis less conmetitive versus other heterotrophic dinoflagellates. When the specimens cannot be illustrated and in case of doubts in the identification, it is recommended that tiie records will be assigned to the closer species of Histioneis by using before the epithet instead of Histioneis sp. This would facilitate further studies on the biogeogr^hy of Histioneis. ACKNOWLEDGMENTS This is a contribution to the French IFB ‘Biodiversité et Changement Global’. 324 Resumen: El género Histioneis {-Parahistioneis) contiene un excesivo numéro de especies, insuficientemente descritas y a menudo a partir de la observaciôn de un solo espécimen ignorando la variabilidad intra-especffica. Con el objetivo de investigar la validez de las especies y sugerir sinônimos, las ilustraciones originales de Histioneis se ban reproducido y agrupado segûn su parecido morfolôgico. Las escasas observaciones de Histioneis y las dudas en la identificaciôn a nivel de especie son responsables de la falta de informaciôn sobre su distribuciôn geogrâfica. Las especies de mayor tamano y mâs omamentadas son tipicas de aguas tropicales, mi entras que especies mas pequenas y menos omamentadas presentan una distribuciôn mâs ampli a y pueden encontrarse también en aguas mâs tempi adas como el Mar Mediterrâneo. Palabras clave: Histioneis, Parahistioneis, Dinophysiales, dinoflagelado, fitoplancton, biogeografïa. REFERENCES Abé, T.H. 1967. The armoured Dinoflagellata: II. Prorocentridae and Dinophysidae C- Omithocercus, Histioneis, Amphisolenia and others. Publ. Seto Mar. Biol. Lab. 15: 79-116. Balech, E 1962. Tintinnoidea y Dinoflagellata del Pacifico segùn material de las expediciones Norpac y Downwind del Instituto Scripps de Oceanografia. Rev. Mus. Argent. Cienc. Nat. “B. Rivadavia”. Cienc. Zool. 7: 1-253. Balech, E. 1971. Microplancton del Atlantico Ecuatorial Oeste (Equalant I). Serv. Hidrogr. Naval. H. Buenos Aires 654: 1-103. Balech, E. 1988. Los dinoflagelados del Atlantico Sudoccidental. Publ. espec. Inst. Espanol Oceanogr. 1: 1-310. Bôhm, A. 1931. Zur Verbreitung einiger Peridineen. Arch. Protistenk. 75: 498-501. Bôhm, A. 1933. Neue Peridineen aus der Adria. Arch. Protistenk. 80: 351-354. Bôhm, A. 1936. Dinoflagellates of the coastal waters of the western Pacific. Bull. Bemice P. Bishop. Mus. Honolulu 137: 1-54. Chen, G. & D. Ni. 1988. Taxonomic studies on three genera of Dinophysiaceae in the South China Sea. Oceanol. Limnol. Sinica 19: 188-248. Diaz-Ramos, J. R 2000. An index of the Venezuelan marine microflora: diatoms, dinoflagellates and coccolithophorids. Rev. Biol. Trop. 48:897-918. Dodge, J.D. 1993. Armoured dinoflagellates in the NE Atlantic during the BOFS cruises 1988-90. J Plankton Res. 15:465-483. Dorgham, M.M. & A. Moftah. 1986. Plankton studies in the Arabian Gulf. I. -Preliminary list of phytoplankton species in Qatari waters. Arab. Gulf. J. Scient. Res. 4: 421-436. Forti, A. 1932. Una rara Dinofisea del Mediterraneo per la prima volta descritta. Arch. Protistenk. 77: 538-542. 325 Gaarder, K.R. 1954. Dinoflagellatae. Rep. Scient. Results “Michael Sars” North Atlantic Deep-Sea Expedition 1910 2(3): 1-62. Gomez, F. 2003. Checklist of Mediterranean free-living dinoflagellates. Bot. Mar. 46: 215-242. Gomez, F. 2005a. A hst of dinoflagellates in the world’s oceans. Acta Bot. Croat. 64: 129-212. Gomez, F. 2005b. Histioneis (Dinophysiales, Dinophyceae) from the wŒtem Pacific Ocean. Bot. Mar. 48: 421-425. Gomez, F. 2006. Endemic and Indo-Pacific plankton in the Mediterranean Sea: A study based on dinoflagellate records. J. Biogeogr. 33: 261-270. Halim, Y. 1960. Étude quantitative et qualitative du cycle écologique des Dinoflagellés dans les eaux de Villefranche-sur-Mer. Ann. Inst, océanogr. Paris 38: 123-232. Halim, Y. 1969. Plankton of the Red Sea. Oceanogr. Mar. Biol. Ann. Rev. 7:231-275. Hallegraefl̂ G.M. 1988. Plankton: A microscopic world. CSIRO, Bathurst, Australia. 112 p. Hallegraeff, G.M. & S.W. Jeffrey. 1984. Tropical phytoplankton species and pigments of continental shelf waters of north and north-west Australia. Mar. Ecol. Prog. Ser. 20: 59-74. HallegraefiF, G.M. & D.D. Reid. 1986. Phytoplankton species successions and their hydrological environment at a coastal station off Sydney. Aust. J. Mar. Fresh. Res. 37: 361-377. Hernandez-Becerril, D.U., M.E. Meave del Castillo & C. Flores-Granados. 2003. Dinoflagelados del orden Dinophysiales en las costas mexicanas, p. 19-42. In M.T. Barreiro et al. (eds). Planctologia Mexicana. Sociedad Mexicana de Planctologfa, Mexico D.F., México. Iriarte, J.L. & G.A Fryxell. 1995. Microplankton at the equatorial Pacific (140°W) during the JGOFS EqPac Time Series studies: March to April and October 1992. Deep-Sea Res. I I 42: 559- 583. Jeffrey, S.W. & G.M. Hallegraeff. 1987. Phytoplankton pigments, species and light climate in a complex warm-core eddy of the East Australian Current. Deep-Sea Res. 34: 649-673. Jorgensen, E. 1923. Mediterranean Dinophysiaceae. Rep. Dan. oceanogr. Exp. Mediterr. 2 (Biol.) J. 2: 1-48. Deutschen Atlantische Exped. “Meteor” 1925-27 12: 165-237. Kofoid, C. A. & T. Skogsbeig. 1928. The Dinoflagellata: the Dinophysoidea. Harvard Univ. Mus. comp. Zool. Mem. 51: 1-708. Konovalova, G. V. 2000. Analysis of the Dinophyte (Dinophyceae) flora of the Russian far East and adjacent waters of the Pacific. Asian Mar. Biol. 17: 1-14. Lessard, E.J. & E. Swift. 1986. Dinoflagellates fix)m the North Atlantic classified as phototrophic or heterotrophic by epiflourescence microscopy. J. Plankton Res. 8 : 1209-1215. 326 Licea, S., M.E. Zamudio, R. Lima & J. Soto. 2004. Free-living dinoflagellates in the southern Gulf of México: Report of data (1979-2002). Phycol. Res. 52: 419-428. Moita, M.T. & M.G. Vilarinho. 1999. Checklist of phytoplankton species off Portugal: 70 years (1929-1998) of studies. Portugahae Acta Biol. Sér. B, Sist. 18: 5-50. Murray, G. & F. Whitting. 1899. New Paidiniaceae from the Atlantic. Trans. Linn. Soc. London. Bottany 5: 321-342. Norris, D .R 1969. Thecal morphology of Omithocercus magnificus (Dinoflagellata) with notes on related species. Bull. Mar. Sci. 19: 175-193. Ojeda, A. 1999. Contribution to the knowledge on dinoflagellates (Dinophyceae) of the order Dinophysiales in the Canary Islands waters. Bol. Mus. Mun. Funchal 51: 53-84. Okamura, K. 1912. Plankton organisms from Bonito fishing grounds. Rep. Imp. Bur. Fish. Sci. invest. Tokyo 1: 1-38. Osorio-Tafall, B.F. 1942. Notas sobre algunos dinoflagelados marinos planctonicos marinos de Mexico, con descripcion de nuevas especies. An. Esc. Nac. Cienc. Biol. México 2: 435-447. Paulmier, G. 2004. Les Dinophycées (Pyrrhophyta, Dinoflagellata) de la Guyane, des Antilles françaises et des aires marines adjacentes. Mém. Inst. océanogr. Paris 20: 1-269. Polat, S. & K. Koray. 2002. New records of the genus Histioneis F.R von Stein (Dinophyceae) from Turkish coastal waters. Turk. J. Bot. 26: 481-484. Rampi, L. 1948. Sur quelques Péiidiniens rares ou intéressants du Pacifique subtropical. Bull. Inst. océanogr. Monaco 937: 1-9. Rampi, L. 1950. Péiidiniens rares ou nouveaux pour le Pacifique Sud-Equatorial. Bull. Inst. océanogr. Monaco 974: 1-12. Rampi, L. 1952. Ricerche sul Microplancton di superficie del Pacifico tropicale. Bull. Inst. océanogr. Monaco 1014: 1-16. Rampi, L. 1969. Péridiniens, Hétérococcales et Pterospermales rares, intéressants ou nouveaux, récoltes dans la mer Ligurienne. Riv. Sci. Nat. “Natura” 60: 313-333. Rampi, L. & M. Bemhard. 1980. Chiave per la determinazione delle peridinee pelagjche mediterranee. Comitato Nazionale Energia Nucleare, CNEN-RT/BIO 8 , Roma, Italia. 193 p. Reguera, B. & S. Gonzalez Gil. 2001. Small cell and intermediate cell formation in species of Dinophysis (Dinophyceae, Dinophysiales). J. Phycol. 37: 318-333. Ricard, M. 1970. Premier inventaire des diatomées et des dinoflagellés du plancton côtier de Tahiti. Cah. Pacifique 14: 244-254. Schiller, J. 1933. Dinoflagellatae (Peridineae) in monographischer Behandlung, p. 1-617. In L. Rabenhorst (ed). Kiyptogamen-Flora von Deutschland, Ôsterreich und der Schweiz. Akademische, Leipzig, Germany. 327 Soumia, A. 1970. A checklist of planktonic diatoms and dinoflagellates from the Mozambique Channel. Bull. Mar. Sci. 20: 678-696. Soumia, A. 1986. Atlas du Phytoplancton Marin. Vol. I: Introduction, Cyanophycées, Dictyochophycées, Dinophycées et Raphidophycées. CNRS, Paris, France. 219 p. Stein, F.R. von. 1883. Der Organisms der Infiisionsthiere. Wilhelm Engelmann, Leipzig, Germany. 31 p. Subrahmanyan, R 1958. Phytoplankton organisms of the Arabian Sea off the west coast of India. J. Ind. Bot. Soc. 37:435-441. Taylor, F.J.R. 1976. Dinoflagellates from the International Indian Ocean Expedition. A report on material collected by R/V '‘"Anton Bruun" 1963-1964. Bibhotheca Bot. 132:1-234. Tong, S.M., K. Nygaard, C. Bernard, N. Vors & D.J. Patterson. 1998. Heterotrophic flagellates from the water column in Port Jackson, Sydney, Australia. Eur. J. ProtistoL 34: 162-194. Venrick, E.L. 1982. Phytoplankton in an oligotrophic ocean: observations and questions. Ecol. Monogr. 52: 129-154. Wood, E.J.F. 1954. Dinoflagellates in the Australian region. Austr. J. Mar. Freshwat. Res. 5:171- 351. Wood, E.J.F. 1963a. Dinoflagellates in the Australian region. H. Recent Collections. Techn. Pap. Div. Fish. Oceanogr. C.S.I.R.O. Austr. 14: 1-55. Wood, E.J.F. 1963b. Dinoflagellates in the Australian region. HI. Further Collections. Techn. Pap. Div. Fish. Oceanogr. C.S.I.R.O. Austr. 17: 1-20. Wood, E.J.F. 1963c. Check-list of dinoflagellates recorded from the Indian Ocean. Rep. Div. Fish. Oceanogr. C.S.I.R.O. Austr. 28: 1-57. Wood, E.J.F. 1964. Studies in microbial ecology of the Australasian Region. Nova Hedwigia 8 : 5- 54. Wood, E.J.F. 1968. Dinoflagellates of the Caribbean Sea and adjacent areas. Univ. Mami, Coral Gables, Florida, USA. 143 p. Jibey^J? Ceratocorys horrida (Peridiniales, Dinophyta). J. Phycol. 36: 46-58. 328 TABLE 1 List of species q/'Histioneis and Parahistioneis and the geographical distribution. Taxa Distribution ‘'F. acutiformis Rampi 1947 (=?//. diamantinae) M(13),P(35) P. acuta Bohm 1931 in Schiller 1933 (=?//. paraformis) A(19,25,49),1(39) aeqiiatorialis Wood 1963 Au (47) *H. alata Rampi 1947 (=//. inclinata) M(13) australiae Wood 1963 (=?//. moresbyensis) Au(47) *H. bernhardii Rampi 1969 (=//. pacifica) M(13) H. biremis Stein 1883 A(28),I(43),P(2,19,31,37) *H. bougainvillae Wood 1963 Au(47) *H. cam//nw Bohm 1931 in Schiller 1933 1(39) H. carinata Kofoid 1907 l(5),Au(46),P(23) H. cerû5i(5 Bôhm 1931 in Schiller 1933 M(13),A(49),I(5,48),Au(47) H. cleaveri Rampi 1952 P(?14,37) P. conica Bohm 1931 in Schiller 1933 (=//. para) I(39)A8) H. costata Kofoid & Michener 1911 (=?//. elongata) l(5,39,48),Au(47),P(5,14,23) H. crateriformis Stein 1883 (=//. reticulata =1 P. pachypus) A(3,4,12,19,26,28,33,41,49),I(15,40),Au(47) H. cym balaria Stein 1883 (=//. skogsbergii,=H. speciosa=H. depressa sec Faylor 1976) A(3,4,19,30,733,41 ),l(?43),Au(46,47),P(14,35,37) •'//. dentata Murray & Whitting 1899 A(28) H. depressa Schiller 1928 (?=//. cymbalaria) M(13,34),A(3,25,49),I(5,15,40,?43),Au(46,47) detonii Rampi 1947 (=?//. cleaveri) M(13),P(36) V. diamantinae Wood 1963 (=?P. acutiformis) Au( 17,46,47) H. dolon Murray & Whitting 1899 (=//. megalocopa) A(4,22,28,29),l(5,39,40,43,48),Au(16,46,47),P(2,23) *H. dubia Bohm 1933 (=?//. mediterranea sec Rampi) M(6) *H. elegans Halim 1960 (=//. longicollis) M(13) ¥. elongata Kofoid & Michener 1911 (=//. subcarinata,=lH. costata) M(34),A(49),I(5,48),Au(47),P(5,14,23,37) *H. elongata var. curvata Wood 1963 (=?//. carinata) Au(47) H. expansa Rampi 1947 (=//. gubernans) M( 13,34) *H. faouzii Halim 1960(=//. longicollis) M(13) *H. fragilis B^^^193fm ^S(^îia^i933 (? . milneri) M 13 ,1(5 H. garrettii Kofoid 1907 A(4),Au(47),P(7,23) *P. gascoynensis Wood 1963 A(49),Au(47) gregoryi Bohm 1936 (=?P. pachypus) P(7) H. gubernans S>c\\nW. 1895 (=//. expansa =H. ligustica) M(13),I(39),P(39) H. helenae Murray & Whitting 1899 (=//. milneri) A(12,28,49),I(48),Au(47),P(2,23,37) H. highleyi Murray & Whitting 1899 A(3,4,22,28,30),I(43),Au(47),P(5,24,31) H. hippoperoides Kofoid & Michener 1911 (=//. milneri) M(13),A(4,19,25,26,29,49),I(5,15,43),Au(46),P(l,23) H. hyalina Kofoid & Michener 1911 M(13),A(3,4,25,49),I(5,40,43,48),Au(47),P(23,45) *//. imbricata Halim 1960 (=?//. longicollis) M(13) 329 H. inclinata Kofoid & Michener 1911 (=//. alata) H. inornata Kofoid & Michener 1911 H. isselii Forti 1932 (=?//. elongata sec Bôhm,=?P. pieltainii) H. joergensenii Schiller 1928 (=?//. vouckii=lH. planeta) josephinae Kofoid 1907 H. karstenii Kofoid & Michener 1911 H. kofoidii Forti & Issel 1925 (=//. longicollis) lanceolata Wood 1963 *H. ligustica Rampi 1940(=//. gubernans=H. expansa) H. longicollis Kofoid 1907 (=// elegans, H. faouzii, H. kofoidii, H. ninuscula, H. sublongicollis, H. villafranca) H. marchesonii Rampi 1941 H. mediterranea Schiller 1928 (=?//. reticulata) Y. megalocopa Stein 1883 (=//. dolon) H. m ilneri Murray & Whitting 1899 (=//. helenae,=H. hippoperoides) *H. minuscula Rampi 1950(=//. longicollis) F/, mitchellana Murray & Whitting 1899 (=?//. pulchra) *H. moresbyensis Wood 1963 (=?//. costata) *H. navicula Kofoid 1907 (=?//. oceanica) *H. oceanica Rampi 1950 (=?//. navicula) H. oxypteris Schiller 1928 (=?//. paulsenii) °, pachypus Bôhm 1931 in Schiller 1933 (=f. varians,=lH. gregoryi,=lH. :rateriformis sec Balech 1988) H. pacifica Kofoid & Skogsberg 1928 (=?//. pavillardii,=lH. bernhardii) H. panaria Kofoid & Skogsberg 1928 (=?//. panda) H. panda Kofoid & Michener 1911 (=?//. panaria) H. para Murray & Whitting 1899 {=P. conica) H. paraform is (Kofoid & Skogsberg 1928) Balech 1971 (=?//. acuta) *H. parallela Gaarder 1954 (=//. striata) H. paulsenii Kofoid 1907 (=?//. crateriformis,^!H. reticulata) H. pavillardii Rampi 1939 (=//. pacifica) *‘P. ieltainU Osorio-Taf 1942 ^!P . s ha roidea =!H. tubi ra sselii) H. pietschm annii Bohm 1931 in Schiller 1933 H. planeta Wood 1963 (=?//. joergensenii,=!H. longicollis) H. pulchra Kofoid 1907 (=?//. mitchellana) *H. rampii Halim 1960 (=?//. cymbalaria) •'//. reginella Kofoid & Michener 1911 ¥. remora Stein 1883 (=?f. sphaeroidea) H. reticulata Kofoid 1907 (=//. crateriformis,=!P. pachypus) H. robusta Rampi 1969 . rotundata Kofoid & Michener 1911 M(13),A(4,26,30,49),l(5,48),Au(47),P(23,37) A(49),Au(47),P(23) M(13),A(9),P(19) M(13),A(19,26,49),Au(47), P(14) P(23) M(13),P(7,23,37) M(13) Au(47) M(13) M(13),A(10,49),I(5,48),Au(47),P(5,7,14,20,23,45) M(13,34) M(13),A(3) 1(5),P(41) A(4,12,28,30,49),I(5,48),Au(47),P(2,7,37) P(36) A(4,12,28,30),1(39,43), Au( 16,17,47),P(1,14,19,20,23,39) Au(47) P(23) P(36) M(13),A(4,30,49),Au(47), P(? 14,45) l(39),Au(16,47),P(5,14) A(29),1(5),P(14,23) A(29,49),l(48),Au(47),P(23) A(19,25,29,49),l(43),Au(47),P(23) M(34),A(4,19,25,28,30,49),l(43),Au(16,17),P(2,14,24) M(13),A(25,29,49),l(5,40),Au(47),P(7,14,19,36,37) A(12) A(29),l(5),Au(47),P(23) M(13),A(27) A(12,49),l(5),Au(47),P(l,2,14,36,37,38) Au(l 8,21,47) A(12,22,26,49),I(40,43),Au(17,47),P(23) M(13) P(23) M(13),A(49),l(48),Au(47) A(4,30),l(5),Au(46),P(7,23,24,31,38,45) M(13),A(27) A(4,19,22,25,26,30,49),I(5,42),Au(46,47),P(23) 330 H. schilleri Bohm 1931 in Schiller 1933 •'//. simplex Wood 1963 *H. skogsbergii Schiller 1933 (=//. cymbalaria) *H. speciosa Rampi 1969 (=//. cymbalaria) R sphaeroidea Rampi 1947 {=1P. pieltainii =1 PI. tubifera) *H. steinii Schiller 1928 (=//. variabilis) H. striata Kofoid & Michener 1911 (=//. variabilis =H. parallela) H. subcarinata Rampi 1947 (=//. elongata) *H. sublongicollis Halim 1960 (=//. longicollis) H. tubifera Bohm 1931 in Schiller 1933 (=??. pieltainii =!P. sphaeroidea) PI. variabilis Schiller 1933 (=//. striata,=H. steinii) *P. varians Bo\\m 1933 {=P. pachypus) *H. villafranca Halim 1960 (=//. longicollis) H. vouckii Schiller 1928 {=!H. joergensenii) A(9),l(5),Au(47),P(5,7,14,24) Au(47) Unknown M(13) M(13), P(?14) M(39) M(34),A(4,19,26,30),1(5),P(23,37) M(13),A(3) M(13) A(49),l(5) M(13),A(25,29,49),l(48),Au(47) M(13) M(13) M(13),A(49),l(5,ll),Au(44,47) (*) Taxa only known by the authority; Bolt type for sufficiently known species; M=Mediterranean, A=Atlantic, I=Indian, Au=Austraha, P=Pacific Ocean. References: 1 = Abe (1967), 2 = Balech (1962), 3 = Balech (1971), 4 = Balech (1988), 5 = Bohm (1931), 6 = Bohm (1933), 7 = Bohm (1936), 8 = Chen and Ni (1988), 9 = Diaz-Ramos (2000), 10 = Dodge (1993), 11 = Dorgham and Moftah (1986), 12 = Gaarder (1954), 13 = Gomez (2003). 14. Gomez (2005b), 15 = Halim (1969), 16 = Hallegraeff (1988), 17 = Hallegraeff and Jeffiey (1984), 18 = Hallegraeff and Reid (1986), 19 - Hernandez-Becerril et a i (2003), 20 = Iriarte and Fryxell (1995), 21 = Jeffrey and Hallegraeff (1987), 22 = Kasler (1938), 23 = Kofoid and Skogsberg (1928), 24 = Konovalova (2000), 25 = Lessard and Swift (1986), 26 = Licea et al. (2004), 27 = Moita and Vilarinho (1999), 28 = Murray and Whitting (1899), 29 = Norris (1969), 30 = Ojeda (1999), 31 = Okamura (1912), 32 = Osorio- Tafall (1942), 33 = Paulmier (2004), 34 = Polat and Koray (2002), 35 = Rampi (1948), 36 = Rampi (1950), 37 = Rampi (1952), 38 = Ricard (1970), 39 = Schiller (1933), 40 = Soumia (1970), 41 = Stein (1883), 42 = Subrahmanyan (1958), 43 = Taylor (1976), 44 = Tong et at. (1998), 45 = Venrick (1982), 46 = Wood (1954), 47 = Wood (1963a,b), 48 = Wood (1963c), 49 = Wood (1968). 331 cross rib eprtheca anterkîror upper dn^lar list pc^terioror lower angular list . right ,sulcal list fission r ib J R j) phaeosome chamber hypotheca window posterior^, main ^ rib (R3) left sulcal list Fig. 1. Descriptive terminology of Histioneis in right lateral view. 332 % ; : , ' c u 1 0 w : | 11 lO W j 17 . a 4;̂ 2 2 % # 2 3 ^ i y 2 4 % % 2 5 W V 26. / ;y ̂ ' y ^ Figs 2-26. Line drawings adapted from the original descriptions of the species morphologically related to the Histioneis cymbalaria-^up in right lateral view. (2) H bougainvillae. (3) H. cymbalaria sec Stein (1883) and H. skogsbergii sec Schiller (1933). (4) H. depressa sec Wood (1963). (5) H. depressa sec Taylor (1976). (6 ) H. cymbalaria sec Stein (1883) and synonym of H. hyalina for Kofoid and Skogsberg (1928). (7) H. depressa. (8 ) H. hyalina sec Wood (1963). (9) H. hyalina. (10) 77 depressa sec Rampi and Bemhard (1980). (11)77 speciosa. (12) 77 cymbalaria sec Stein (1883). (13-15) H. cymbalaria sec Balech (1988). (16)77 cleaveri. (17) 77 rampii. (18) 77. robusta. (19) 77 panda. (20) 77 panaria. (21) 77 pietschmannii. (22) 77 pulchra. (23) 77 'm^aimàr»^mitchellanày{l.^ H.;iSchilleri*^X^SfHik^et^c)pi ■ 333 I Figs 27-46. Histioneis longicollis-gcoup. (27) H villafranca. (28) H. elegans. (29) H. longicollis sec Halim (1960). (30) H. sublongicollis. (31) H. faouzii. (32) H. minuscula. (33) H. kofoidii. (34) H. vouckii. (35) H. joergensenii. (36) H. planeta. (37) H. joergensenii sec Rampi and Bemhard (1980). Schiller (1933). (41)77 aequatorialis. (42)77 marchesonii (43)77 bernhardii. (44)77 pacifica. (45) 77 pavillardii. (46) 77 imbricata. Not to scale. ' Aj; , , I \ / #& ,», / Figs 47-56. Histioneis elongata-^owp. (47) H. elongata var. curvata. (48) H. carinata. (49) H. subcarinata. (50) H. isselii. (51) H. elongata sec Bohm (1936). (52) H. lanceolata. (53) H. australiae. (54) H. moresbyensis. (55) H. elongata. (56) H. costata. Not to scale. Figs 57-62. Histioneis/?^ra-group. (57) P. conica. (58) H. para. (59) H paraformis. (60) H. acuta. (61) Æ paraformis sec Kofoid and Skogsberg (1928). (62) H. rotundata. Not to scale. Figs 63-74. Histioneis garrettii-^o\x^. (63) H. karstenii. (64) H. dentata. (65) H. garrettii. (6 6 ) H. garrettii sec Balech (1988). (67) H. diomedeae. (6 8 ) P. pachypus. (69) P. varians. (70) H. gregoryi. (71)7/. tubifera. (72) P. pieltainii. (73) P. sphaeroidea. (74) H. remora. Not to scale. m 9J> » O m m w / % Figs 75-84. Histioneis crateriformis-gnoup. (75) H. diamantinae. (76) P. acutiformis. (77) P. gascoynensis. (78) H. paulsenii. (79) H. oxypteris. (80) H. crateriformis. (81)7/ reticulata sec Balech (1988). (82) H. crateriformis sec Balech (1988). (83) H. reticulata. (84) H. mediterranea. Not to scale. Figs 85-90. Histioneis inclinata-^ouç. (85) H. mediterranea sec Rampi and Bemhard (1980). (86) H. dubia. (87) H. inclinata. (88) H. alata. (89) H. inornata. (90) H. simplex. Not to scale. Figs 91-99. Histioneis gubemans-^oup. (91) H fragilis. (92) H. cerasus. (93) H. parallela. (94) H. striata. (95) H. variabilis. (96) H. ligustica. (97) H. expansa. (98) H. gubernans. (99) H. reginella. Not to scale. 100 102 ‘'A W 104 - 4 / w / . / > r # C V mgm ' A A5 Figs 100-106. Histioneis megalocopa-^oup. (100) Unidentified specimen illustrated by Soumia (1986, p. 153). (101) //. helenae. (102) H. milneri. (103) H. hippoperoides. (104) H. megalocopa. (105) H. dolon. (106) H. josephinae. Not to scale. 107 108 Figs 107-111. Line drawings adapted from the original descriptions in right lateral view. (107) H. navicula. (108) H. oceanica. (109) H. highleyi. (110)//. biremis. (Ill)Unidentified specimen illustrated by Ojeda (1999). Not to scale. 338 339 4. Discusiôn 4.1 Diversidad y biogeografia 4.1.1. ÂCuantas especies? En términos de riqueza de especies, los dinoflagelados son solo comparables con las diatomeas en el medio marino. Sournia et al. (1991) en su articulo Marine phytoplankton: how many species In the world oceans? no proporclona una llsta de especies, pero propone 1424-1772 especies y 115-131 géneros de dinoflagelados libres marinos. Los valores mayores conslderan a las especies y géneros de dudosa validez. Otros autores dan valores de 4000 especies de dinoflagelados, donde la mitad de las especies son foslles (Taylor, 1987), pero ningun trabajo proporclona una llsta reclente de especies. En la bibliografia pueden encontrarse Inventarios de especies como la revision de Schiller (1931- 1937) que describe e I lustra casi todos los dinoflagelados conocldos en aquel tiempo. Sournia (1973, 1978, 1982a, 1990, 1993) anade llstados en orden alfabético de las especies descrltas tras la revision de Schiller. Segun esta memorla de tesis actuallzada hasta el aho 2004, los dinoflagelados marinos libres conocldos constltuyen un total de 1555 especies, distrlbuldas en 117 géneros. Los géneros mas numerosos son: Protoperldinlum (264 especies), Gymnodinlum (173 especies), DInophysIs+Phalacroma (104+41 especies), Gyrodinlum (87 especies), Amphidinlum (76 especies), Histioneis (65 especies), Ceratlum (64 especies) y Gonyaulax (60 especies) (Fig. 15). Desde 1993 hasta 2004, se han descrito 135 nuevas especies asi como los nuevos géneros: Akashiwo, Amphidinlella, Bysmatrum, Gaarderla, Heterobractum, Karenla, Karlodinlum, Lessardia, Mysticella, Plaglodinlum, Polarella y Takayama. 340 40 354 tn 304 '%254 OJ 204 2 £ 15 -3 ^ 104 g Histioneis ^ CeratiumI I II I CD z Gonyauiax Prorocentrum 0 III I j — 14J ll » . » I ■c&§ . L S .2I 0 c 1 i E 2 I I . I 0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 numéro de especies en cada género Fig. 15. Distrlbuclon de frecuencia del numéro de especies en cada género basado en Gomez (2005). De los 2500 nombres de especies de dinoflagelados marinos aparecidos en la bibliografia, unos 1000 nombres de especies han sido considerados como sinonimos de especies ya descrltas. Sin embargo, si anallzamos los géneros mas Importantes, el numéro de especies validas conocldas podria ser aun menor. Protoperidinium con 264 especies es el género mas numeroso (Fig. 15). Balech transflrio la mayor parte de las especies marinas de Peridinium a Protoperidinium en 1974, y ademàs describlô un total de 100 nuevas especies. Abé (1981) describlô otras 40 especies nuevas. Tanto Balech como Abé se basaron en pequenas diferenclas en la tabulaclôn, principalmente de las plaças sulcales para crear estas nuevas especies. Nadie ha vuelto a realizar estos minuclosos estudios y la mayor parte de las especies descrltas por ambos autores no han vuelto a ser citadas. No hay estudios sobre la varlabllldad Intraespecifica de las plaças sulcales. La cuestlôn esta en si minimas diferenclas en la forma de las plaças sulcales justifican la separaciôn como diferentes especies o al contrario, existe una especlaclôn cnptlca y una misma morfologia enclerra diferentes especies. Al ser Protoperidinium un género heterotrôfico, su cultivo es aùn mas dificll que en el caso de especies autôtrofas y por tanto la varlabllldad morfolôgica, al menos en condiclones de laboratorlo, es dificll de estudiar. La blologia molecular 341 podna ayudar, pero a pesar de lo relative mente fa cl I que résulta capturer estas especies generalmente grandes y resistentes, hasta el présente solo se conocen 10 secuenclas parclales de las 264 especies de Protoperidinium descrltas (YamaguchI y HorIguchI, 2005). Por tanto es aùn prematuro évaluer la validez de las especies del género de dinoflagelados mas numeroso. Gymnodinium es el segundo género mas numeroso, que Incluye a muchos Gyrodinium y en algunos casos descripciones de Amphidinium que corresponden a especies de Gymnodinium giradas 180°. Ambos, Gymnodinium y Gyrodinium tienen un cingulo ecuatorlal, pero Kofoid y Swezy (1921) los separaron, al asignar al género Gyrodinium las especies en las que los extremos del cingulo esta ban desplazados mas del 1/5 de la longitud del cuerpo celular. Evidentemente este criterlo es arbitrarlo y en modo alguno tiene una base fllogenética. La mayor parte de las especies atecadas fueron descrltas a finales del siglo XIX y principles del XX a partir de especimenes fijados, lo que altera drasticamente su morfologia, y ademas en muchos casos descritos a partir de un ûnico espécimen. Incluse aunque se observen Individuos aùn vives, se sabe que la morfologia cambia rapidamente tras su captura (Kofoid y Swezy, 1921). Es muy probable que muchos de esos dinoflagelados descritos a partir de una sola célula correspondan a un espécimen deformado de una especle ya conocida. Los dinoflagelados atecados son a menudo heterôtrofos y tras expulsar los restes de la presa que han Ingerido, présenta n un contorno muy deformado y variable, que puede haber llevado a que se les describe como especies diferentes. Un ejemplo se puede encontrar en Gyrodinium spirale. Schütt (1895) describlô numerosas varledades de Gyrodinium spirale y después Kofoid y Swezy (1921) dieron catégorie de especle a Gyrodinium acutum, G. cornutum, G. m itra , G. obtusum 0 G. pingue. Tamblén Gyrodinium fusiforme, G. lachryma o G. nasutum pueden no ser mas que varledades de Gyrodinium spirale. Mas del 80% de las especies de dinoflagelados atecados descritos por Kofoid y Swezy (1921) no han sIdo citadas por otro au to r y el porcentaje es aùn mayor en géneros como Warnowia. Para Investigar la validez de las especies, una soluclôn pasa por alslar la especle en la localldad tlpo, pero como ocurre con las especies descrltas por Schütt, ni slqulera se conoce la localldad tlpo. La descripciôn de mas de un centenar de especies de estos géneros es claramente Insuficlente. En 1985 HaruyoshI Takayama usando microscopia electrônica de barrido llustra varlos tlpos de surco apical en especies atecadas. Este caracter 342 morfologico, junto la composicion pigmentaria y diferenclas en la secuencla del rADN han justificado la escision del macro-género Gymnodinium (Daugbjerg et al., 2000). SIn embargo, las especies Investigadas son solo aquellas disponibles en cultives y poco se sabe sobre en el ciclo de vida y morfologia de esas especies en condiclones naturales. Tras Protoperidinium y Gymnodinium, el género mas numeroso es Dinophysis. Phalacroma es a menudo considéra do sinônimo de Dinophysis, pero al desconocerse la especle tlpo de Phaiacroma es dificll resolver la cuestlôn. Tan sôlo algunas especies costeras del género Dinophysis causantes de episodios tôxicos han sido Investigadas, mantenléndose en cultivo por algunas generaclones, lo suficlente como para mostrar una alta varlabllldad morfolôgica (Reguera e t ai., 1995). Una de las especies mas comunes en costas atlânticas europeas, Dinophysis acuminata, ha recibido hasta diez nombres diferentes. Estos cambios morfolôgicos no sôlo ocurren en Dinophysiales, y no sôlo debido a cambios en el ciclo de vida. Condiclones amblentales como los niveles de turbulencla son responsables de cambios en la morfologia. Un trabajo publicado por ZIrbel et al. (2000) sirve como ejemplo para llustrar la gran varlabllldad morfolôgica (FIg. 16). Fig. 16. Morfologia de células de Ceratocorys horrida cultivadas a diferentes niveles de turbulencla en ZIrbel et ai. (2000). Podria pensarse en la fig. 16 se llustran très especies diferentes, sIn embargo es la mIsma especle e Incluso la mIsma cepa de Ceratocorys horrida. Las très formas coexisten en cultivos y pueden camblar de una morfologia a otra en cuestlôn de minutes, tan sôlo si se camblan los niveles de turbulencla. Eso ocurre en una especle fuertemente tecada como Ceratocorys, pero la versatllldad morfolôgica puede ser aùn mayor en células atecadas. El conocimlento de la varlabllldad morfolôgica de Dinophysis esta restringida a una docena de especies 343 de costas templadas o boreales, nada se sabe de la varlabllldad de los clentos de especies de Dinophysiales descrltas en aguas ablertas tropicales como Histioneis 0 Amphisolenia, en su mayor parte descrltas a partir de la observaclôn de un solo ejemplar, ces justificable en estos casos que pequenas diferenclas en la aleta sulcal 0 en las espinas antapicales sean criterlo valido para considerarlas como especies diferentes?. Es una Incognita el numéro de especies de Dinophysiales validas en aguas oceanicas. Una gran parte de las nuevas especies descrltas en los ùltimos 15 anos son bénticas, como en el caso de Prorocentrum (Faust, 1993; Hoppenrath, 2000). Es posible que el alslamiento en amblentes bénticos favorezca una mayor especlaclôn frente a las especies planctônicas. La apllcaclôn de la microscopia electrônica a aguas tropicales lleva a Carbonell-Moore (1993) a describir a partir de muestras de red decenas de especies de podolampadaceas, que debido a su baja densidad y escasos caractères distintivos pasaban desapercibldas. Poco se sabe de las abondantes especies atecadas en aguas ablertas de mares tropicales. Si se excluyen todas estas especies dudosas por ser probablemente parte del ciclo de vida de otras especies ya conocldas, el numéro de especies de dinoflagelados validas se quedaria en torno a medIo millar de especies, de las cuales apenas se conocen secuenclas del ADN ribosômico de 100 especies marinas. Cuantas de las especies descrltas de dinoflagelados son validas es dificll de saber. Esta memorla no puede responder a esa pregunta, pero proporclona un Inventarlo de las especies conocldas, Incluyendo los sinônimos mas comùnmente aceptados y correcclones en la nomenclatura segùn el Côdigo botanico vigente. La clasificaclôn usada évita un simple llstado alfabético, pero esta a la espera que la fllogenla molecular llegue al menos a algùn représentante de cada grupo y se pueda realizar una nueva clasificaclôn de las especies conocldas. Gômez, F., 2005. A list of dinoflagellates In the world oceans. Acta Botanica Croatica 64, 129-212. 344 4.1.2 Biogeografia La biogeografia se define como las observaciones, registro y explicacion de los rangos de distrlbuclon geografica de los organlsmos (Plelou, 1979). Los primeros estudios en aguas oceanicas llevaron a Haeckel o Schütt (1897) a conslderar que cada masa de agua estaba caracterlzada por su plancton-flora propla. P.T. Cleve (1903, p. 7) llegaba a deslgnar cada tlpo de agua con el nombre de la especle principal de plancton. Por ejemplo 'Tripos-plankton' para un tlpo de agua donde domlnada por Ceratium tripos. De esta forma se buscaba usar las especies como Indlcadores blologlcos, aportando datos complementarlos a la hidrograffa. A medlda que se ampllô la cobertura geografica de los estudios, se observaba que las especies aparecian en diferentes océanos y por tanto dejaba de tener sentido conslderar que cada masa de agua tuviese su plancton endémico. En general se considéra que los organlsmos de pequeho tamano son muy abundantes y se pueden disperser facllmente, especlalmente en un medio sIn aparentes barreras fisicas como los océanos. Esto ha llevado a asumir que los microorganismos tienen una distrlbuclon cosmopollta (Finlay, 2002). Beljerinck basàndose en cultivos de bacterlas afirma 'todo esta en todas partes, el medio selecclona' (Beljerinck, 1913). Por tanto si se dan las condiclones apropladas, una especle de microorganismo aparecera en cualquler lugar. De estas Ideas surgen dos corrientes: 1) todos los microorganismos tienen una distrlbuclon cosmopollta, con un bajo grado de endemismo y bajo numéro de especies (FInlay et ai., 1996; Fenchel et ai., 1997). Por tanto existirian grandes poblaciones de cada especle de microorganismo y una gran probabllldad de dispersion que previene el alslamiento y la especlaclôn alopatrica (Fenchel et al., 1997); 2) existe un gran endemismo y quedarian muchas especies de protista s por describir, pero las especies no son faciles de diferenclar (Foissner, 1999). En esta ùltima década, el desarrollo blologia molecular deberia clarificar una la Importancla de la especlaclôn cnptlca. En estos microorganismos el concepto de especle no tIene en el mismo sentido que conocemos en animales superlores. MIentras que para microorganismos acuaticos epicontinentales pueden existir barreras ffsicas que separen a sus poblaciones, mas dificll es encontrar claras barreras en aguas oceanicas. Los estudios sobre la biogeografia del fitoplancton han sido escasos. Smayda (1958) se centra en la re-definiclôn de los términos 345 usados en la biogeografia del fitoplancton y tan sôlo cita algunos ejempios, especlalmente de diatomeas bipolares. Margalef (1961), basàndose en la bibliografia de que disponia, sépara las especies de fitoplancton mejor conocldas en 12 grupos en funclôn de su distribuclôn geografica. La mayor parte de las especies resultaban cosmopolites. Hoy en dia, 45 anos tras el trabajo de Margalef, muchas de aquellas especies sehaladas como exclusivamente australes 0 boreales, Indo-Pacificas o atlânticas has sido citadas en otras reglones y por tanto el porcentaje de especies cosmopolites es aùn mayor, siempre asumiendo que las Identificaclones han sido correctes. Evidentemente no todos los protistes son cosmopolites, algunas especies estàn restringidas a zonas cllmàticas particulares. Por ejemplo el género Histioneis esta asoclado con aguas calldas. La morfologia de Histioneis ha evoluclonado hasta crear una camera para albergar clanobacterlas simblontes que fijan nitrôgeno (Foster et ai., 2006) y le proporclonan allmento adiclonal. La fijaclôn de nitrôgeno se Inhibe a baja s temperatures, asi que la distribuclôn de Histioneis se limita a aguas calldas. Tamblén muchas podolampadaceas parecen restringidas a aguas calldas (Carbonell-Moore, 1996). En aguas superficlales tropicales, las especies de género Pyrocystis parecen constituir una excepciôn. NInguna asoclaclôn simblôtica ha sido descrita en la especle y sIn embargo, Pyrocystis pseudonoctiluca, una especle aparentemente autôtrofa, es comùn en aguas oceanicas tropicales. Este fenômeno se explica por migraclones verticales que le permiten explotar nutrientes de aguas profundas, que tan sôlo especies de gran tamano como Pyrocystis pueden realizar (Sukhanova y Radyakov, 1973). En el lado opuesto a las especies pantotropicales, estanan las especies polares (Balech, 1976; Okolodkov y Dodge, 1996). SIn embargo, ta m poco puede descartarse que en algùn caso se trate de especies cosmopolites que modifican su morfologia en condiclones extremes. La diversidad de dinoflagelados en aguas polares es escasa comparada con los trôpicos. A parte de las bajas temperatures, sôlo especies que formen quistes o heterôtrofas pueden adaptarse a los largos perlodos de oscurldad en reglones polares. Existe un gran nùmero de dinoflagelados heterôtrofos como Protoperidinium, que son aparentemente unipolares, simplemente porque E. Balech trabajô en aguas antàrticas (Balech, 1976). Si Balech hublese anallzado muestras del Ârtico, muchas de esas especies serian bipolares. Por ejemplo en 1999 se descubrlô el género Poraliela en el océano Antàrtico, hasta entonces era sôlo conocido en el registro fôsll. Como es 346 un género de interés, se investigô su presencia en el Ârtico y rapidamente se encontre (Montresor et al., 2003). Poraliela glacialls es la misma especle en ambos polos y apenas diflere en 6 pares de bases en su SSU rADN (Montresor et al., 2003). En principle se puede conslderar que las especies bipolares tuvieron una distribuclôn cosmopollta en perlodos mas fnos y que el progresivo calentamiento redujo su distribuclôn a los polos. Es dificll asumir que en la actualldad una especle psicrôflla pueda trasiadarse de un polo a otro, especlalmente las especies fotosintéticas que deberfan resistir a las altas temperaturas en la zona lluminada de los trôpicos. Una divergencla genética muy lenta surge como expllcaclôn a este fenômeno. Las especies del género Ceratium, generalmente grandes y resistentes, facllmente retenidas por muestras de red y relativamente bien identificables, han sido comùnmente usadas como Indlcadores blogeograficos (Dodge y Marshall, 1994). Especies como Ceratium (iongipes) arcticum estàn restringidos a aguas frias y otras como Ceratium dens/divaricatum/balechii parecen restringidas a aguas costeras tropicales. SIn embargo, la dellmitaclôn de las especies de Ceratium es compllcada por la gran varlabllldad intra-especîfica que présenta. Por régla general las especies oceànicas tienden a ser heterôtrofas, mixotrôfas o presentan simblôntes. Por ejemplo, en las aguas ultraollgotrôficas del Giro del Pacifico Sur, las especies màs abundantes pertenecen al género Oxytoxum y especies de Ceratium como C. teres. En aguas oceànicas, las especies tienden a ser màs ornamentadas como en el caso de la Dinophysiales, mientras que las especies neriticas de este orden son menos ornamentadas. Ademàs de una relaclôn con el grado de turbulencla y tasa de sedimentaclôn (ZIrbel et ai., 2000), la ornamentaclôn puede estar destinada a modular corrientes de aguas que dirigen a sus presas hacla la reglôn sulcal, generalmente presas de pequeho tamano como el picoplancton. Las Dinophysiales de aguas costeras donde los nutrientes permiten vida autôtrofa carecen de esta ornamentaclôn. La separaciôn entre especies de afinidad nentlca (paràcticas) y oceànica (anoicticas), màs que geogràfica, es una separaciôn entre condiclones eutrôficas que predominan en las costas frente a la general oligotrofla en aguas oceànicas. La formaclôn de quistes es una ventaja para las especies neriticas, porque un quiste que sedimenta en aguas oceànicas dlficllmente podria volver a la zona fôtica. La ocurrencia de especies coloniales en aguas ablertas es rara, mientras 347 que es mas comùn en especies nenticas como Alexandrium, Pyrodinium bahamense o pseudo-coloniales como Polykrikos. La velocidad de desplazamiento podria ser mayor cuando las células estàn unidas formando colonias, facilitando las migraclones verticales o tamblén podria Incidir en la tasa de mortalldad por depredaclôn. En aguas oceànicas, aunque la formaclôn de colonlas Incrementase la velocidad de ascenso y descenso, la distancla hasta la nutriclina séria tan grande, a menudo màs 200 m, que las especies requeririan grandes vacuolas y varlos dias para completar el ciclo. Algunas especies autôtrofas parecen adaptadas a vivir en aguas profundas. Sournia (1982b) en su estudio de la ^"schatten flora" no encuentra una morfologia comùn entre las especies de aguas profundas. Es esperable que las especies autôtrofas en aguas profundas requlrlesen una mayor concentraclôn de pigmentos y otras adaptaclones como cuerpo y extenslones aplanadas como en el caso de Ceratium piatycorne, C. ranipes o C. praelongum. Los ejempios de endemismo en aguas tropicales y templadas son escasos. Las poblaciones oceànicas de dinoflagelados han estado Interconectadas hasta la formaclôn del Istmo de Panamà hace tan sôlo 6 mlllones de anos. Algunas especies aparecen restringidas a la reglôn Indo-pacifica. Dinophysis miles, una especle que no puede dar ninguna duda en su Identificaclôn, parece restringida a las costas tropicales del Indlco y el sureste asiàtico. Sôlo en esta reglôn del sureste asiàtico, la cosmopollta Noctiluca scintillans presentan simblontes, Pedinomonas noctiiucae. Realmente no podemos asegurar que estas especies estén llmitadas a aguas tropicales del Indlco o Pacifico, porque àreas tropicales como el Goifo de Guinea estàn casI Inexploradas. SI parece exIstIr un mayor grado endemismo en microorganismos que son estrictamente autôtrofos como diatomeas. Los dinoflagelados con una mayor versatllldad trôfica, gran varlabllldad morfolôgica y una gran diversidad genética, podrian adaptarse mejor a diferentes condiclones amblentales y por tanto tener un mayor rango de distribuclôn. El estudio de la biogeografia de las especies de dinoflagelados es dificll, incluso cuando se trata de especies fàcllmente Identificables, debido a la heterogeneldad de los estudios. Asi por ejemplo las costas de Europa, Japôn y Norte América han sido objeto de màs estudios, mientras que vastas reglones de aguas ablertas de mares tropicales y especlalmente del hemisferlo sur han sido escasamente Investigadas. Muchas especies que se citan en trabajos, no son 348 jiustradas o las ilustraciones no son suficientemente detalladas como para confirmar la identificaclôn y por tan to no se pueden sacar conclusiones claras sobre la distribuclôn geogràfica de las especies. En la p resen te memorla se ha estudlado la composiciôn de especies en reglones histôricam ente bien estudladas como la Costa Azul o el Canal de la Mancha y tam blén otras zonas poco conocldas como aguas ablertas del sudeste asiàtico y el océano Paci'flco central y Sur. Por ejemplo, en el océano Pacifico que ocupa 1/3 de la superficie de los océanos, géneros muy distlntlvos como Asterodinium, Brachidinium, Microceratium, Ceratoperidinium, Scaphodinium, Petalodinium, Pomatodinium, Leptodiscus y Spatulodinium, nunca habian sIdo citados. Por tan to géneros como Ceratoperidinium o Petalodinium serian endém icos del m ar Mediterràneo sin los estudios Incluldos en esta memorla. El caràc ter endém ico de e s ta s especies tan sôlo depende de que los escasos Investigadores en activo y con la experlencla suficlente para Identificar a esos grupos Investiguen nuevas à reas geogràficas. Scaphodinium, a parece en cualquler locallzaclôn desde el sur de Japôn a Chile, pero nunca habia sido citado en el Pacifico. El Mediterràneo por sus caracteristicas de alslamiento, pero conectado en las reglones atlânticas e Indo-pacifica es un buen laboratorlo para estudios blogeogràficos. Son m uchas las especies macroscôpicas c laram ente endémicas de aguas m ed ite rràneas o especies de un claro origen Indo-Pacifico (Blanchi y MorrI, 2000). SIn em bargo cuando se estudia la afinidad blogeogràfica en especies de dinoflagelados, no es posible encontrar una especle que se pueda usar como un claro ejemplo de especle endémica o Indo-paciflca. Por ejem plo, surge la duda si es la misma especle un Ceratoperidinium de la Bahia de Palma recogido en aguas con una tem peratu ra de 14°C o en aguas ablertas del Pacifico ecuatorlal a 29°C. No existen diferenclas en la morfologia basado en microscopia ôptica. De mom ento hay que espera r a que los estudios genéticos se extiendan a aguas ablertas oceànicas y asi descarta r una especlaclôn cnptlca y que bajo la misma morfologia tengam os especies diferentes en cada reglôn oceànica. Es esperable que exista un mayor porcentaje de especies endémicas en las cuencas cerradas o sem icerradas. El Mar Mediterràneo cumple estas caracteristicas y ha sido una de las reglones histôricamente mejor Investigada, citàndose al m enos la mitad de especies conocldas de dinoflagelados. Al se r un 349 m ar casi cerrado, con multiples regimenes climaticos e hidrologicos, una compleja historia geologica con episodios de conexiones y alslamiento con los océanos Atlantlco e Indo-Paciflco, el Medlterraneo se présenta como un area Ideal para estudio la biogeografia de los dinoflagelados marinos. Tras un inventarlo de las especies descrltas en las cuencas del Medlterraneo y Mar Negro, e sta memorla ha tra tado de responder a cuestlones como el num éro de especies endém icas o Indo-Paclflcas que podemos encontrar en el Medlterraneo. G o m e z , F., 2 0 0 3 . C h e c k l i s t o f M e d i t e r r a n e a n f r e e - l i v in g d i n o f l a g e l l a t e s . Botanica Marina 4 6 , 2 1 5 - 2 4 2 . G o m e z , F. y B o l c e n c o , L , 2 0 0 4 . An a n n o t a t e d c h e c k l i s t o f d i n o f l a g e l l a t e s In t h e B la ck S e a . Hydrobiologia 5 1 7 , 4 3 - 5 9 . G o m e z , F ., 2 0 0 6 . E n d e m i c a n d I n d o - P a c i f I c p la n k t o n In t h e M e d i t e r r a n e a n S e a : A s t u d y b a s e d o n d i n o f l a g e l l a t e r e c o r d s . Journal of Biogeography 3 3 , 2 6 1 - 2 7 0 . 350 4.2 Taxonomia y distribuciôn de grupos de dinoflagelados poco conocidos Existe una gran heterogeneidad en el estudio de la diversidad de dinoflagelados. Aquellas especies que pueden causar danos en las costas como puede ser el caso de Karenia brevis reciben multitud de fondos para su estudio, mientras que ordenes en te ros como los Noctilucales (excluyendo Noctiluca), a pesar de interés en la evoluclon de los dinoflagelados, no han recibido ninguna atenciôn en las ultimas trè s décadas. Cada época se ha caracterizado por diferentes recursos a la hora de investigar la taxonomia de las especies. En los ùltimos 10 anos, predominan los estudios basados en un solo espécim en aislado durante una proliferaciôn costera y cultivado en condiciones de laboratorio, que ra ram en te reproducen las condiciones naturales. El abundante material permite aplicar los ùltimos adelantos técnicos disponibles. Las especies son desen tas combinando microscopia optica, epifluorescencia, microscopia electron ica de barrido y transmisiôn, perfiles de pigmentos y a veces de toxinas, y adem as la secuencia de regiones del ADN ribosomico. Estas técnicas ra ram en te se aplican a los dinoflagelados de aguas ab iertas sobre todo en m ares tropicales, a lejados de los principales laboratories. Cuando tan solo se dispone de la microscopia optica clasica es dificil realizar estudios taxonômicos que alcancen los requerimientos de las revistas m as reconocidas en la actualidad. En e s te contexte, la falta de recursos se debe suplir incrementando el esfuerzo en la observaciôn, hasta llegar a encontrar especies muy poco conocidas y que sean tan in teresantes que incluse tan solo con microscopia optica los resultados sean compétitives. No es especialm ente necesario irse muy lejos para encontrar especies de interés. Por ejemplo, Ceratoperidinium es casi desconocido, pero se pueden encontrar especim enes en otono cogiendo un cube de agua en las orillas de la Bahia de Raima de Mallorca. Spatulodinlum pseudonoctiluca, une de los pocos dinoflagelados p résen tes en el Canal de la Mancha, tiene un ciclo de vida curioso y poco conocido, pero no recibe ningùn interés. Evidentem ente siem pre se tienen mayores posibilidades de encontrar especim enes in te resan tes en las a reas m as remota s, como puede se r aguas abiertas m ares tropicales de Asia, el Pacifico Central o el Giro del Pacifico Sur. 351 Hoy en dia es dificil que tan solo un estudio taxonômico interese a las Instituclones que financian es tos costosos m uestreos en aguas abiertas, de forma que el analisis de las m uestras tam bién debe contribuir en aspectos ecolôgicos del fitoplancton, mas utiles para estudios biogeoquimicos que financian las cam panas en aguas abiertas. Incluso en las regiones m as rem otas, se han realizado estudios con m uestras de red que permiten recolectar millones de especim enes, en su m ayor parte ya estudiados incluso por microscopia electronica. Aquellos especim enes de m enor tam aho , que no son retenidos por la red de plancton o bien especim enes de mayor tam aho , pero tan delicados que se destruyen durante el filtrado, han sido objeto de m enos estudios y por tan to pueden encontrarse especies poco conocidas. En aguas ab iertas donde la abundancia de células es muy baja y sin usar redes de plancton, se utilizan otros m étodos de concentracion. Es costoso transpo rta r grandes volûm enes de zonas rem otas hasta el laboratorio y la sedimentaciôn de grandes volûmenes de agua es laboriosa. Son escasas las ocasiones en que los organism os pueden investigarse a bordo y por lo tan to es necesaria la fijaciôn para su posterior estudio en laboratorio. Tras una laboriosa sedim entaciôn, el resultado permite observer con microscopia invertida, e specim enes que norm alm ente se dahan o escapan de las redes de plancton y en tonces raras noctilucaceas o pequehas células tecad as con delicada ornam entaciôn como Histioneis aparecen. Cientos de pequehos especim enes in teresan tes, principalmente dinoflagelados a tecados, son aûn m as abondantes. Sin em bargo debido a su pequeho tam aho , la resoluciôn de la microscopia invertida no permite diferenciar su morfologia y sin el auxilio al m enos la microscopia electronica de barrido, estos espec im enes han sido descartados para estudios taxonômicos. En plena era de la biologia molecular, las publicaciones requieren la secuencia de rARN incluso cuando se dispone de un sôlo espécim en, lo cual es casi imposible tra tandose de espec im enes fijados con Lugol. Si es sencillo, sin em bargo, aplicar la técnica desarrollada por el Dr. Takayam a para dinoflagelados, que permite observer mediante microscopia electrônica de barrido el espécimen elegido. Alguna de e s ta s pequehas células gymnodinioides présenta extensiones y eso perm ite distinguirla de o tras como es el caso de dinoflagelados a tecados con ex tensiones como Asterodinium, Brachidinium, Microceratium, Ceratoperidinium y algunos otros no conocidos anteriorm ente . 352 4.2.1. Brachidinium, Asterodinium, Microceratium A pesar de alcanzar dimenslones de m as de 100 pm y llegar a abundancias de h asta 11000 células por litro al sur de Canarias como encontrô Margalef (1975) o Estrada (1976), el género Brachidinium no fue descrito hasta 1963 y Asterodinium y Microceratium hasta 1972. Résulta verdaderam ente anormal que se ta rdera tan to en describir esos géneros tan distintivos. Tan solo puede explicarse porque los estudios anteriores, generalm ente m uestras de red fijadas con formol, utilizaban una metodologia inapropiada. El exceso de formol en la m uestra pudo se r la causa de la descripcion incomplete de Brachidinium por Taylor (1963). Taylor al no observer ni siquiera el cingulo, incluyo a Brachidinium en el orden Dinoccocales, unos dinoflagelados cocoides o parasitos y ce ren tes de flagelos, lo que dio a Brachidinium un halo de misterio. Taylor, sin otras observaciones, continué en sus libros imaginando la morfologia de Brachidinium y proponiendo hasta trè s orientaciones diferentes errôneas (Taylor, 1963, 1980b, 1987; Fensome e t al., 1993). Sournia observé especim enes de Brachidinium capitatum con una morfologia variable en las ex tensiones y describié algunas formas como nuevas especies. En las m ism as estac iones donde Sournia encontraba Brachidinium, pero a mas profundidad, solian aparecer especim enes de Asterodinium con el mismo nûcleo prom inente, una pigmentacién verde-amarilla mas intensa y ex tensiones de Brachidinium, pero con 5 extensiones en diferente posicién y tam bién otro género , Microceratium, con sélo 3 extensiones (Sournia, 1972a,b). Por aquel tiem po, Cachon en Villefranche/Mer habia observado un espécim en de Brachidinium vivo y describié que podia mover sus extensiones (Léger, 1971). Esto Neva a Sournia (1972a) a crear el orden Arthrodiniales 'dinoflagelados articulados' para es to s dos géneros. Loeblich (1982) anadiria m as confusién creando el orden "Brachydiniales", que sin em bargo séria validado por Sournia (1984). Después Taylor (1987, p. 729) incluye a las brachidiniaceas en el orden Kolkwitziellales y poco después en Ptychodiscales (Fensome e t al., 1993). Sournia (1972b), coincidiendo con Asterodinium y Brachidinium y Microceratium, tam bién observé unas células gymnodinioides y anotaba "'poché à Brachidinium". Sournia (1972b) ilustré lo que en 2004 se describié como Karenia papilionacea. En 1986, en su Atlas du Phytoplancton Marin, Sournia escribia que los Brachidiniales quizas eran parte ciclo vida de otros dinoflagelados m as com unes, sin dar m as informacién. 353 En una casi inaccesible publicaciôn, Abboud-Abi Saab (1989) encuentra Brachidinium capitatum y las mismas células gymnodinioides que ya observé Sournia (1972b). Abboud-Abi Saab incluye una nueva especie, Asterodinium libanum, con una pésima fotograffa y sin apenas descripcién. Poco m as se conoce sobre la morfologia de los misteriosos Brachidiniales, pero dcual es la verdadera naturaleza de estos dinoflagelados?,