Torodinium Robustum and T

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n Torodinium robustum and T. teredo

istributio New data on the distribution of D (Dinophyceae: Gymnodiniales) in the Gulf of * raphic g California eo Ismael Gárate-Lizárraga and Rocío Elizabeth Muciño-Márquez G n o Instituto Politécnico Nacional (IPN),[email protected] Centro Interdisciplinario de Ciencias Marinas (CICIMAR), Departamento de Plancton y Ecología Marina, Avenida Instituto Politécnico Nacional s/n, Col. Playa Palo de Santa Rita, La Paz, B.C.S. 23096, México

otes * Corresponding author E-mail: N Abstract: Torodinium robustum and T. teredo Torodinium teredo The gymnodinioid marine dinoflagellatesTorodinium robustum are reported for the Gulf of California.T. robustum This and is the T. teredofirst record of on the Pacific coast of Mexico. Both species were found mainly during the winter-spring in seawater at 19–27.5 °C. was the most frequent species. Morphological features of varied widely and specimens observed in live samples and fixed in Lugol’s solution were easily recognizable. Short description and microphotographs were provided for each species.

The unarmored dinoflagellates of the order sampling stations (Figure 5). Geographic coordinates for Gymnodiniales Lemmermann, 1910 lack cellulose plates, each sampling station are shown in Table 1. From January but have a membranous outer covering of small vesicles. 2009 to April 2012, 42 collections of phytoplankton were Most of the studies of gymnodinioidAkashiwo dinoflagellates sanguinea in taken at the first sampling station (Figure 5). Surface and Mexico have focused on the bloom forming species, Amphidinium which vertical (15 m depth) phytoplankton tows were collected carteraeare common in coastal watersCochlodinium like fulvescens with a 50 cm diameter 20 µm mesh net. Each net tow was (K.Hirasaka) G.Hansen and Ø.MoestrupCochlodinium 2000, polykrikoides immediately preserved with acid Lugol’s solution (5% final Hulburt,Gymnodinium 1957, catenatum Iwataki, concentration). Subsamples were taken for observations GyrodiniumKawami and instriatumMatsuoka, 2008, of live phytoplankton. From February through December KatodiniumMargalef, 1963, glaucum Graham, 1943, 2010, 19 vertical net hauls were monthly taken from 60 Freudenthal andet al Lee, 1963, and m depth at the second sampling station in the northern (Lebour) Loeblich III, 1965 (Cortés- part of Bahía de La Paz. In July 2010 at Los Cabos, 4 Altamirano 1998; Gárate-Lizárraga . 2004;Torodinium 2006; vertical net hauls were conducted from 15 m depth to 2009; Morquecho-Escamilla and Alonso-Rodríguez. 2008; Gárate-Lizárraga; 2012; 2013).Torodinium The genus robustum Kofoid and Swezy 1921T. teredo with two taxonomically accepted species (Brandt 2010; 2011), Kofoid and Swezy, 1921 andTorodinium (Pouchet) Kofoid and Swezy, 1921 belongs to the order Gymnodiniales and family Gymnodiniaceae. species are characterized by a very large episome that occupies most of the cell body, a posterior cingulum, a much-reduced hyposome, and the sulcus extending along theTorodinium episome only (Kofoid and Swezy 1921). Main morphological and taxonomical features are shown in Figures 1–4. species are etmarine al planktonic dinoflagellates, free-living, unicellular, T robustumand apparently cosmopolitan (Gómez 2009; Hoppenrathet al . 2010). Along the Mexican coast of the Pacific, . has rarelyet albeen reported (Gaxiola-Castro . 1987; Morquecho-EscamillaTorodinum robustum and Lechuga-Devéze 2004; Gárate-LizárragaT. teredo . 2009). This report confirms the presence of and registers for the first time at some sites in the Gulf of California. Figures 1-4. Torodinium Torodinium robustum Information about their morphology and ecology is also species diagram taken from Kofoid and Swezy provided. (1921). (1)Torodinium teredo . Left lateral view. (2) Ventral view of Phytoplankton samples were collected at three antapical region. (3) Right lateral view of antapical region of the same figure. (4) . Abbreviations: epi., epicone; (gir., girdle sites: (1) off Petroléos dock in the shallow basin of the or cingulum; hyp., hypocone; long fl., longitudinal flagellum; n., nucleus; southernmost region of the Bahía de La Paz; (2) Cuenca pus., pusule; rod., rodlets or rhabdosomes; sulc., sulcus; tr. fl., transverse flagellum. Alfonso in Bahía de La Paz and (3) off Los Cabos with four 809 Gárate-Lizárraga and Muciño-Márquez | New data on the distribution of Torodinium robustum and T. teredo

the surface at Stations 3, 4, 5 and 6 (Figure 5). Cell counts Mediterranean Sea, and the Pacific (Kofoid and Swezy were made in 5 mL settling chambers under a Carl Zeiss (1921; Lebour 1925; Trégouboff andT robustum Rose 1957). Some inverted microscope (Hasle 1978). Both live and fixed net specimens from NW Africa are related with upwellings phytoplankton samples were analyzed by phase contrast Elbrächter 1979). More recently, . has been microscopy. Sea surface temperature (SST) was recorded reported at La Jolla, California et(Kimor al and Reid 1989), in with a bucket thermometer. Images were recorded (SONY (Japan (Yoshimatsuet al 1990), in the Helgoland and Sylt islands Cyber-shot camera, 8.1 MP) under a Carl Zeiss inverted in the North Sea (Hoppenrath T teredo. 2009), and in Kuwait microscope. Al-Kandari . 2009). A total of 93 specimens of . were indentified only in net phytoplankton haulsT teredo at sampling station 1 (Table 1). This species occurred in seawater with temperature of 19.0–24.5°C. . cells have a very elongated body (Figures 12–14). Cell length is more than 4 transdiameters; there is no loop in the terminal part of the sulcus. The epicone is very long and the hypocone is reduced to a conical structure. The sulcus arises near the apex of the cell with a loop nearly completely around the cell and then curves to meet the girdle. The nucleus is elongated and located along nthe centre of the cell. Cells are aboutT 100–115teredo µm (108.67±4.40 μm) long and 20–27.5 µm (24.43±2.04 μm) wide ( = 30). Gómez (2009) found that . specimens had an elongated protuberance, a peduncle that protrudes from the sulcal-cingular region.

Figure 5.

Sampling stations in Bahía de La Paz, and Los Cabos at the southern endTorodinium of the Baja California Peninsula.

Two species were identified in the samples collected monthly from Bahía de La Paz from January 2009 to April 2012 and in samples of July 2010 collected at Los Cabos. SpecimensTorodinium of both species fit well with the diagnosis and descriptions of KofoidT and robustum Swezy (1921). All samples containing species were listed in Table 1. A total of 167 specimens of . were observed only in net phytoplankton hauls at the three sampling sites in this study (Table 1). Therefore, no quantitative data are presented,–1 however,et densities al from 1000 to 45000 cells L were reported during a multi-species redT tide robustum event (Gárate-Lizárraga . 2009). This species occurred in seawater with temperature of 19.0–27.5 °C. . cells have an elongated body with a very small hypocone, reduced to a conical structure (Figure 2). Cell length is less than 3.5 greatest transdiameters, the sulcus has a reversed terminal apical loop, and the girdle forms a left- (handedn spiral (Figures T6–11). robustum Cells are about 60–75 µm (69.63±2.95 μm) long and 20–37.5 µm (28±3.81 μm) wide = 30). In Figure 9 the . is 60 µm long and 37.5 Figures 6-14. Torodinium µm wide. The nucleus is an elongated rod with rounded end located centrally. A very long and small pusule extended Torodinium robustum Microphotographs of species from the southwestern Gulf of California. Figs. 6, 7, 8, and 9: live specimens of to nearly the same point as the nucleus. Many greenish to Torodinium collected robustum in June 2008, March 2009, June 2010, brownTorodinium chloroplasts, robustum arranged into longitudinal rows, are February 2011 respectively, in Bahía de La Paz. Fig. 10 and Fig. 11: Lugol- present (Figures 6–11). fixed specimenTorodinium of teredo collected in May 2010 at Cuenca Alfonso and in July 2010 at Los Cabos, respectively. Figs. 12 and13: Live is a planktonic species which Torodiniumspecimens of teredo collected in Bahía de La Paz in March has been found at Burnham (Essex) and Plymouth in the 2009 and April 2011, respectively. Fig. 14: Lugol-fixed specimen of United Kingdom. It has been reported in the North Sea, collected in October 2010 at Cuenca Alfonso. 810 Gárate-Lizárraga and Muciño-Márquez | New data on the distribution of Torodinium robustum and T. teredo

Table 1. Torodinium robustum and Torodinium teredo

Geographic coordinates for each station, sampling date, number of specimens of and SST data SAMPLING VERTICAL NET recorded in 17 field samplingsLATITUDE performed (N) atLONGITUDE Bahía de La (W)Paz andDATE Los Cabos. (D/M/Y) SURFACE NET SAMPLES SST (°C) STATION SAMPLES T. robustum T. robustum T. robustum T. robustum 1 24° 21’ 110°31’ 23/01/09 (4) (6) 20 T. teredo T. robustum 1 19/02/09 (8) (2) 21 T. teredo T. teredo 1 26/02/09 (5) (13) 21 T. teredo 1 05/03/09 (6) (7) 22 T. robustum T. robustum 1 17/03/09 (11) T. teredo 22.5 T. robustum (17) 1 24/06/10 T. teredo (16) 25 T. teredo (5) (14) 1 13/12/10 T. teredo (3) T. robustum 21 T. robustum T. teredo (9) (18) (21) 1 23/01/11 T. teredo T. robustum 23.5 T. robustum (6) T. teredo (2) (5) (8) 1 17/02/11 T. robustum T. robustum 19 (7) (14) T. robustum 1 28/04/11 (4) (7) 23 T. robustum 1 24/02/12 (2) T. robustum 1 19/04/12 (2) 24. T. robustum 2 24° 39’ 110°36’ 01/02/10 T. teredo (4) 21.5 (2) 2 01/05/10 T. teredo 24.5 T. robustum (1) (2) 2 16/10/10 T. robustum 27 (2) T. robustum 2 23/01/11 T. teredo (3) 24 (3) 3 22° 55’ 109° 47’ 01/07/10 T. robustum 24.5 (4) T. robustum 4 22° 52’ 109° 45’ 01/07/10 (2) 25.0 T. robustum

5 22° 51’ 109° 31’ 01/07/10 T. teredo (5) 27.5 (9) 6 22° 48’ 109° 40’ 01/07/10 27.3 (1)

ThisTorodinium peduncle was teredo not observed in live or fixed cells in our sequences should be examined more carefully once samples. they could possibly increase the distinction between the is a planktonic species, apparently species. widely distributed in temperate and tropical waters; it Acknowledgments: has been reported from several locations in the North Funding was received from Instituto Politécnico Sea, English Channel, Mediterranean Sea, Pacific Ocean, Nacional of Mexico (IPN grants SIP-20110281, SIP-20110139, SIP- et al 20110590, and SIP-20121153). We thank M.C. Ramírez-Jáuregui and Gulf of Mexico (KofoidT. teredo and Swezy 1921; Lebour (Instituto de Ciencias del Mar y Limnología, Universidad Nacional 1925, Trégouboff and Rose 1957; Steidinger . 1967). Autónoma de México) for help in the literature search. I.G.L. is a COFAA In northwestern Africa is related with water Literatureand EDI fellow. Cited upwelling (Elbrächter 1979) and recently it was reported Marine Phytoplankton Atlas of Kuwait’s Waters in several regions of the open Pacific Ocean: Oyashio and Al-Kandari, M., F. Al-Yamani and K. Al-Rifaie. 2009. Kuroshio currents of East Asia, The Philippines, Celebes, Torodinium teredo. Safat: Kuwait Institute for ScientificIn Research. 354 p. AlgaeBase Sulu, South China Sea, western and central equatorial Brandt, S. 2010. (Pouchet) Kofoid & Swezy, 1921. Pacific, subtropical Pacific in the vicinity of the Marquesas M.D. Guiry and G.M. Guiry. 2010. . World-wide electronic Archipelago, in theTorodinium South Pacific teredo Gyre, and in the Perú- publication, National University of Ireland, Galway. World Register Chile Current (Gómez 2009) and the European Arctic of Marine Species. Electronic Database accessible at http://www. marinespecies.org/aphia.php?p=taxdetails&id=109890.Torodinium robustum In Captured (Okolodkov 2011). is now reported for onAlgaeBase 07 May 2012. the Torodiniumfirst time in teredo the Gulf and of T California robustum in Pacific waters of Brandt, S. 2011. . M.D. Guiry and G.M. Guiry. 2011. . World-wide electronic publication, National University Mexico. of Ireland, Galway. World Register of Marine Species. Electronic . occur together in Database accessible Las at mareas http://www.marinespecies.org/aphia. rojas the North Sea, Mediterranean Sea and Gulf of California php?p=taxdetails&id=109889. Captured on 07 May 2012. Cortés-Altamirano, R. 1998. . México: AGT, Editor, S.A. (Lebour 1925; Trégouboff and Rose 1957; T thisteredo study). 161 p. The species were easily recognizedT robustum in live samples as Elbrächter, M. 1979.Reihe On the taxonomy of unarmored dinophytes well as samples fixed in Lugol’s solution. . is (Dinophyta) from the Northwest African upwellingAmphidinium region. carterae‘Meteor’ easily distinguished from . because its length Forschungs. 30: 1-22. Gárate-Lizárraga,CICIMAR I. 2012. Oceánides Proliferation of is more than four transdiameters, no loop is observed (Gymnodiniales: Gymnodiniaceae) in Cochlodinium Bahía de La polykrikoidesPaz, Gulf of in the terminal part of the sulcus, the larger size, and California. 27(2): 37-49. Gárate-Lizárraga,Marine Pollution I. Bulletin 2013. Bloom of the green pigmentation (Pouchet 1885; Kofoid and (Dinophyceae: Gymnodiniales) in Bahía de La Paz, Gulf of California. Swezy 1921; Steidinger and Tangen 1997; this study). 67: 217-222. Cochlodinium polykrikoides Despite the morphological characteristics to distinguish Gárate-Lizárraga, I., D.J. López-Cortés J.J. Bustillos-Guzmán and F.E. both species, their ultrastructural morphology and DNA Hernández-Sandoval. 2004. Blooms of 811 Gárate-Lizárraga and Muciño-Márquez | New data on the distribution of Torodinium robustum and T. teredo

Revista de Biología Tropical (Gymnodiniaceae) in the Gulf of California, Mexico. Morquecho-Escamilla, L. and C.H. Lechuga-Devéze. 2004. Seasonal 52 (Suppl. 1): 51-58. Gonyaulax polygramma occurrence of planktonic dinoflagellatesBotanica Marina and cyst production Gárate-Lizárraga, I., M.S. Muñetón-Gómez and V. Maldonado-López.Revista in relationship to environmental variables in subtropical Bahía 2006.Investigaciones Florecimiento Marinas del dinoflagelado frente Concepción, Gulf of California. 47(4): In313-322. a la Isla Espíritu Santo, Golfo de California (Octubre 2004). Okolodkov,Protista, Y.B. 2011. part Division 3. Guide-book Dinoflagellata on Zoology (Bütschli) Fensome, Taylor, 27(1): 31-39. Norris, Sarjeant, Wharton et Williams. 1993. p. 7-119 S.A. Karpov Gárate-Lizárraga, I., C.J. Band-Schmidt F. Aguirre-BahenaCICIMAR Oceánides and T. Grayeb- (ed.). . St. Petersburg-Moscow: del Álamo. 2009. A multi-species microalgae bloom in Bahía de La KMK Sci. JournalPress. de l’Anatomie et de la Physiologie Normales et Paz, Gulf of California, Mexico (June 2008). 24(1): Pouchet,Pathologiques G. 1885. de Nouvelle l’Homme contribution et des Animaux a l’histoire des Perediniens 1-15. Ciencias marins. Manuel de planctonologie Gaxiola-Castro,Marinas G., S. Nájera de Muñoz and S. Álvarez-Borrego. 1987. Méditerranéenne, I, II 21(2): 28-88, pls 2-4. Fitoplancton de inviernoTorodinium del océanoand Pavillardia Pacífico Mexicano. Trégouboff, G. and M. Rose. 1957. 13(4): 129-135. . Paris: Centre National In de Red la tide Recherche studies, Gómez, F. 2009. Protistology(Gymnodiniales, Scientifique.Pinellas to Collier I (text) Counties, 587 p. II 1963-1966: (illustrations), a symposium 207 pl. Dinophyceae): two unarmoured dinoflagellates with a body Steidinger, K.A., J.T. Davis and J. Williams. 1967. p. 4-47 extension, collected from the open Pacific Ocean. In 6(2): . Florida BoardIn 131-135.Phytoplankton Manual ConservationIdentifying Marine Laboratory. Marine Phytoplankton Prof. Pap. Ser. No. 9. Hasle, G.R. 1978. Using the inverted microscope; p. 191-196 A. SourniaMarine Steidinger, K.A. and K. Tangen. 1997. Dinoflagellates. p. 387-584 C. phytoplankton:(ed.). Selected microphytoplankton. Paris: UNESCO. species from the North Tomas (ed). Katodinium glaucum , San Diego: Academic Hoppenrath,Sea around M., Helgoland M. Elbrächter and Sylt and G. Drebes. 2009. Press.In Red Tide Yoshimatsu,Organisms S. 1990. in Japan, an Illustrated Taxonomic(Lebour) GuideLoeblich III. p. 60-61 . Stuttgart: E. Schweizerbart’sche Y. Fukuyo, H. Takano, M. Chihara and K. Matsuoka, (ed.). Verlagsbuchhandlung. 264 p. . Tokyo: Uchida Kimor, B. and F.M.H.Institute Reid. of 1989. MarineLarge Resources dinoflagellates of the orders Rokakuho Publ. Co. Gymnodiniales. NoctilucalesThe and free-living Pyrocystales unarmored from the Dinoflagellata west coast of North America. . 19 p. 13 pl. Kofoid, C.A. and O. Swezy.The dinoflagellates 1921. of Northern seas . City: Memoirs of the University of California. 562 p. Lebour, M.V. 1925. . Plymouth:. Marine BiologicalCochlodinium Association fulvescens U.K. 250 p. Harmful Algae News Received: August 2012 Morquecho-Escamilla, M.L. and R. Alonso-Rodríguez. 2008 First record Accepted: July 2013 of in Mexican Pacific. , Published online: August 2013 Paris, France 37: 5-6. Editorial responsibility: Rodrigo Johnsson

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