CICIMAR Oceánides 29 (1) 2014 by CICIMAR Oceánides

ISSN 1870-0713

Volumen 29(1)

Junio 2014

DIRECTORIO INSTITUTO POLITÉCNICO NACIONAL

CENTRO INTERDISCIPLINARIO DE CIENCIAS MARINAS

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CHRISTINE JOHANNA BAND SCHMIDT

MARK S. PETERSON

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RUBÉN ESCRIBANO V.

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U. CONCEPCIÓN DE CHILE

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SANTIAGO FRAGA

INSTITUTO ESPAÑOL DE OCEANOGRAFÍA ESPAÑA

FERNANDO GÓMEZ

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SERGIO GUZMÁN DEL PRÓO

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DOMENICO VOLTOLINA

JAIME GÓMEZ GUTIÉRREZ

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HELMUT MASKE

CARLOS MÁRQUEZ BECERRA UABC MÉXICO OSCAR UBISHA HERNÁNDEZ ALMEIDA

CICESE MÉXICO

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EN MEMORIA Nació el 9 de octubre de 1941 en el Ingenio Carlos A. Carrillo, en Veracruz, Ver. Por un empeño de su padre, su nombre fue Sarita en lugar de Sara. Llegó a México a los 16 años con la intención de estudiar la carrera de medicina pero optó finalmente por realizar estudios de licenciatura en Biología en la ENCB del IPN de 1959 a1962. Fue una estudiante brillante, siempre apreciada por sus maestros y compañeros de generación. Su tesis de licenciatura fue sobre hongos parásitos de la madera, titulándose en 1965. En la vida profesional laboró para el Instituto Nacional de la Pesca de 1963 a 1981. Fue investigadora del INP en el laboratorio central y en el Centro Regional de Investigación Pesquera en Ensenada, B.C, realizando investigaciones sobre algas marinas y vegetación acuática de 1963 a 1973. En 1972 gozó de una beca de especialización sobre Ictioplancton en los laboratorios del Southwest Marine Fisheries Center de la Jolla California y, desde entonces, su especialidad se orientó hacia ese campo de la biología pesquera. A su regreso a México al laboratorio central del INP fue designada Jefa de La Sección de plancton del INP; un puesto que desempeñó desde 1973 a 1981, donde junto con el grupo de investigadores y técnicos que formó, hicieron las primeras evaluaciones publicadas de la biomasa de sardina y anchoveta en SARITA DE LA CAMPA JEREZ (9 de octubre de 1941-19 de mayo de 2014) el Golfo de California. Participó activamente en Congresos y diferentes foros científicos, particularmente en las Reuniones científicas México-EUA sobre los recursos pesqueros del Golfo de México (MEXUS GOLFO) y los de la Corriente de California (CALCOFI), donde se ganó el respeto y la estimación de sus colegas por su preparación, seguridad y por una simpatía y alegría natural que siempre irradió. De 1981 a 1992 pasó a ser profesora –investigadora de tiempo completo de la Escuela Nacional de Ciencias Biológicas del IPN, donde fue Jefa del Laboratorio de Ecología, Jefa de la Carrera de Biólogo, representante de profesores ante el Consejo General consultivo del IPN, profesora del curso de Ecología de la Carrera de Biólogo y coordinadora de proyectos de investigación de servicio externo de ese laboratorio. Dirigió cerca de 20 tesis de licenciatura, tanto en la ENCB como en la Escuela Superior de Ciencias Marinas de la UABC cuando residió en Ensenada, B.C. Al fundarse la Sociedad Mexicana de Planctología fue presidenta de dicha asociación científica. Después de jubilarse dedicó sus últimos años activos a obtener la Maestría en el CICESE y continuó con estudios de doctorado que por razones de salud no pudo culminar. En dicha institución colaboró por espacio de 10 años como experta de ictioplancton en el Departamento de Ecología Marina, de donde finalmente se retiró en 2003. A lo largo de su carrera supo combinar exitosamente su profesión con el desempeño de madre de 5 hijas, a las cuales formó igual que ella, con un espíritu alegre, independiente y combativo. Donde quiera, gozó siempre del cariño y la simpatía de alumnos y colegas por su carácter festivo y, al mismo tiempo, su fuerza y templanza le ganaron el reconocimiento y el cariño de propios y extraños. Su inesperado fallecimiento nos deja un enorme vacío de su alegría por la vida, de amor, y de su reconocida sapiencia. SAGP 27 de mayo de 2014

SEMBLANZA DR. SERGIO ANTONIO GUZMÁN DEL PRÓO desarrollado la mayor parte de sus investigaciones científicas y pesqueras. Actualmente continúa laborando con la misma convicción llevando a cabo estudios de índole ecológica de largo plazo sobre el abulón, v.gr., investigando los factores ambientales que afectan el reclutamiento del abulón, construyendo modelos acerca de la adecuada explotación del recurso y el pronóstico de su disponibilidad futura basado en series de tiempo construidas desde 1996 a la fecha. Ello incluye estudios sobre el hábitat, genética poblacional y el ecosistema propio de los abulones, así como sus relaciones tróficas, lo que ha implicado su colaboración con colegas ficólogos especialistas en macroalgas, campo explorado por el Dr. Guzmán del Próo en los inicios de su larga carrera, y también en el de microalgas, campo en el que hubo de incursionar al interesarse en la dieta de juveniles de abulón.

El Dr. Sergio Guzmán del Próo nació en el DF el 20 de octubre de 1939. Realizó sus estudios de licenciatura en la Escuela Nacional de Ciencias Biológicas del Instituto Politécnico Nacional entre 1957-1960, logrando ahí mismo su doctorado en 1994. Afirma que tuvo la suerte de participar, junto con un reducido grupo de biólogos, en la fundación de lo que fue originalmente el Instituto Nacional de Investigaciones Biológico Pesqueras, hoy Instituto Nacional de la Pesca, y ser actor y testigo de su desarrollo durante los primeros 20 años de su existencia en donde laboró entre 1962 y 1981. Es miembro del Sistema Nacional de Investigadores desde 1987, actualmente como permanente. Es miembro honorario (permanente) de la Sociedad Ficológica Mexicana; fue Vicepresidente de la International Abalone Society (2002-2004) y Consejero Científico del Instituto Nacional de la Pesca (2007-2008) (2009-2010). La International Abalone Society lo premió en 2012 con un reconocimiento por su larga carrera cientifica y contribución de su investigación al servicio de la industria abulonera, otorgándole además la membresía de por vida a dicha Sociedad Científica. Ha sido pionero en diverso temas de la investigación pesquera mexicana, particularmente en el campo de las macroalgas de interés económico y, posterioremente en la biologia, ecología y dinámica de poblaciones de abulón, langosta y otros organismos bentónicos de la Península de Baja California en donde ha

Ha impartido cerca de cien cursos de licenciatura sobre diversos temas: botánica marina, ecología marina, biología pesquera, recursos naturales, y más recientemente sobre comunicación científica, materia esta última a la

que el Dr. Guzmán del Próo impulsa como un elemento básico en la formación del científico en el discurso oral y escrito. Fue profesor en la Escuela Superior de Ciencias Marinas de la UABC cuando laboraba en Ensenada, B.C para el Instituto Nacional de la Pesca. Posteriormente y por largo tiempo, fue investigador de la Escuela Nacional de Ciencias Biológicas, donde fue Coordinador de la Maestría y Doctorado en Biología, presidente de la Academia de Ecología y jefe del Laboratorio de Ecología. Ha dirigido alrededor de treinta tesis de licenciatura, maestría y doctorado, además de contar con más de ochenta publicaciones nacionales e internacionales; todo ello vinculado con el sector pesquero de México. Como científico mexicano de formación íntegra, aplicado a la ecología pesquera, destaca su posición crítica respecto a la implementación de los estímulos económicos por productividad, que se otorgan a los investigadores desde

hace unas tres décadas y hace un llamado a la recuperación del espíritu y auténtica vocación cient�� í�� fica que han sido desplazados por intereses monetarios. Asimismo, ha resaltado cómo algunos cambios en los sistemas de posgrado como el acortamiento en los tiempos de Maestría y Doctorado han redundando en prácticas poco éticas y en la baja calidad de los posgraduados. El Dr. Guzmán del Próo pugna por recuperar las bases filosóficas de la formación en los científicos mexicanos y el consecuente reconocimiento del componente ético con que debe actuar todo científico en el ejercicio de su carrera como docente y como investigador. Actualmente, el Dr. Guzmán del Próo labora en el CICIMAR-IPN en La Paz, BCS, después de su larga carrera en la ENCB, en donde ya se ha proyectado su vocación científica y como formador de recursos humanos, apelando siempre a la filosofía y ética científicas, mismas que promueve entre sus estudiantes y sus colegas.

CICIMAR Oceánides, 2014

VOL 29(1)

ISSN-1870-0713

CONTENIDO Metabolic balance of the polyp-algae mutualistic symbiosis in the hermatypic coral Porites panamensis in La Paz, Baja California Sur, México. RICO-ESENARO, S.D., M. SIGNORET POILLON, J. ALDECO & H. REYES-BONILLA

Bloom of Gonyaulax spinifera (Dinophyceae: Gonyaulacales) in Ensenada de La Paz lagoon, Gulf of California. GÁRATE-LIZÁRRAGA, I., MA. S. MUÑETÓN-GÓMEZ, B. PÉREZ-CRUZ & J. A. DÍAZORTÍZ.

NOTAS First nesting records of the American Avocet (Recurvirostra americana) and White Ibis (Eudocimus albus) at Laguna Ojo De Liebre, BCS, Mexico. AYALA-PEREZ, V., R. CARMONA, N. ARCE & J. RIVERA.

Distribution of Amylax triacantha and A. triacantha var. buxus nov. comb. (Dinophyceae) along the Pacific coast of México GÁRATELIZÁRRAGA, I.

First record of Reimerothrix floridensis (Fragilariaceae: Bacilla riophyta) for Mé�� xico. HERNÁNDEZ-ALMEIDA, O. U. & J. A. HERRERA-SILVEIRA.

CICIMAR Oceánides 29(1): 1-10 (2014)

METABOLIC BALANCE OF THE POLYP-ALGAE MUTUALISTIC SYMBIOSIS IN THE HERMATYPIC CORAL Porites panamensis IN LA PAZ, BAJA CALIFORNIA SUR, MÉXICO Rico-Esenaro, S.D.1, M. Signoret Poillon✝2, J. Aldeco3 & H. Reyes-Bonilla4

Universidad Autónoma Metropolitana Unidad Xochimilco - Licenciatura en Biología, Departamento del Hombre y su ambiente. 2,3 Universidad Autónoma Metropolitana Unidad Xochimilco - Departamento del Hombre y su Ambiente. 4 Universidad Autónoma de Baja California Sur (UABCS) - Laboratorio de Sistemas Arrecifales. email: jaldeco@correo.xoc.uam.mx; serguevich_r@hotmail.com; hreyes@uabcs.mx 1

ABSTRACT: Studies on metabolic balance in hermatypic corals have been unable to separate the analysis of animal’s respiration from that of plant. The objective of this research was to determine the metabolic balance in the mutualistic symbiosis polyp-algae through incubations in respirometric chambers of twelve fragments of coral. The species studied Porites panamensis (Scleractinia: Poritidae), Verrill, 1866 was collected near La Paz, Baja California Sur, México. Experiments were performed during fall 2009 and winter 2010. Water temperature, salinity, dissolved oxygen, pH, irradiance and photosynthetic pigments were measured every two hours during the incubation times. The concentration of pigments was determined through spectrophotometry. The maximum primary production was at 12:00 h, with 3.80 mg O2∙l-1∙h-1 for fall and 4.92 mg O2∙l-1∙h-1 for winter. According to the P : R (Production : Respiration) ratio of 1.90 for fall and 2.07 for winter, the mutualistic symbiosis in P. panamensis showed a predominantly autotrophic behavior. The relative quotients of chlorophyll concentrations (mg∙polyp-1), Chl a : Chl c2, were 1.0 : 0.69 for fall and 1.0 : 1.22 for winter; while ratio of concentrations chlorophyll a : carotenes , Chl a : carotenes (both in mg∙polyp-1), were 1.0 : 2.13 for fall and 1.0 : 1.88 for winter. The high relative concentrations of Chl c2 and carotenes with respect to Chl a is explained as an adaptive response to high irradiance.

Keywords: Metabolic balance, hermatypic coral, respiration, mutualistic symbiosis, primary production. Balance metabólico en la simbiosis mutualista pólipo-alga en el coral hermatípico Porites panamensis en La Paz, Baja California Sur, México RESUMEN: Estudios del balance metabólico en corales hermatípicos han sido incapaces de separar el análisis de la respiración animal y vegetal. El objetivo en este trabajo fue determinar el balance metabólico en la simbiosis mutualista alga-pólipo a través de incubaciones en cámaras respirométricas en doce fragmentos de coral. Los experimentos se realizaron en otoño del 2009 e invierno del 2010. La especie estudiada fue Porites panamensis (Scleractinia: Poritidae), Verrill, 1866, recolectada en La Paz, Baja California Sur, México. La temperatura del agua, salinidad, oxígeno disuelto, pH, irradiación y pigmentos fotosintéticos fueron registrados cada dos horas durante los tiempos de incubación. Los pigmentos fotosintéticos se determinaron mediante espectrofotometría. La producción primaria máxima fue a las 12:00 h, con 3.80 mg O2∙ l-1∙ h-1∙ para otoño y 4.92 mg O2 l-1∙ h-1∙ para invierno. De acuerdo con el cociente P : R (Producción : Respiración) con valor de 1.90 para el otoño, y 2.07 para el invierno, la simbiosis mutualista en P. panamensis muestra un comportamiento predominantemente autótrofo. Los cocientes relativos de concentración de clorofilas (mg ∙polyp-1), Cl a : Cl c2, fueron 1.0 : 0.69 para otoño y 1.0 : 1.22 para invierno, mientras que la relación de clorofila a : carotenos, Cl a : carotenos (ambos en mg∙polyp-1), fueron de 1.0 : 2.13 para otoño y 1.0 : 1.88 para invierno. Las altas concentraciones relativas de Cl c2 y carotenos con respecto a Cl a se explican como una respuesta adaptativa a una mayor irradiancia.

Palabras clave: Balance metabólico, coral hermatípico, respiración, simbiosis mutualista, producción primaria. Rico-Esenaro, S.D., M. Signoret Poillon, J. Aldeco & H. Reyes-Bonilla. 2014. Metabolic balance of the polypalgae mutualistic symbiosis in the hermatypic coral Porites panamensis in La Paz, Baja California Sur, México. CICIMAR Oceánides, 29(1): 1-10.

INTRODUCTION Hermatypic corals harbor in their tissues microalgae of the genus Symbiodinum. The photosynthetic products of the algal cells consist of short-chain carbohydrates that the algae metabolize for their own growth. Parts of these carbohydrates are translocated to the host coral and represent essential nutrients (McCloskey et al., 1978; Muscatine et al., 1981; Jesser et al., 2000; Apprill et al., 2007). Carbon distribution is determined by the polyp-algae mutualistic symbiosis; however, there is an incomplete understanding of how environmental factors affect these organisms (López-Pérez, 2005). Studies of metabolic balance in hermaFecha de recepción: 14 de junio de 2013

typic corals have been unable to separate the analysis of animal’s respiration from that of the plant. This demands an analysis of the metabolic process in the symbiotic relationship as a system with its own energy flux. The existence of corals under stress conditions generated by temperature change is an adaptive feature of high-latitude coralline formations (Riegl & Piller, 2003; LaJeunesse et al., 2008). The study of coral symbiosis in mid-latitude regions of the eastern Pacific provides important ecological and biogeographic perspectives on the stability and variability of polyp algae mutualistic symbiosis (LaJeunesse et al. 2008). Understanding the natural Fecha de aceptación: 21 de abril de 2014

RICO-ESENARO et al.

variability of photosynthetic pigment ranges and distributions in healthy corals is central to the evaluation of the usefulness of the measurements in assessing the health and status of endosymbiotic reef-building corals (Apprill et al., 2007). In the Californian coral patches the species P. panamensis is one of the most abundant. The metabolic balance in mutualistic symbiosis, such as primary production in reef corals, can be estimated from oxygen yield and carbon dioxide (CO2) incorporation, or indirectly from the organic matter input to the surrounding water (Hatcher, 1990). Despite some uncertain respiration measurements, net primary production values pose a good indicator of the metabolic process. The polyp-algae mutualistic symbiosis forms part of a highly efficient system for recycling matter and energy that is considered a nutritive advantage in hermatypic corals. The coral polyps may be reasoned in literature as herbivores. However, they may present alternative breeding forms. The coral–algae complex can be thought of as a unique entity, like the fungi-algae lichen complex, establishing the coral concept to refer both elements. The mutualistic algae are dinoflagellates. The most conspicuous pigments in this algae are chlorophylls (Chl) a, c2 and beta-carotenes. Nevertheless, other pigments have been considered in the literature such as diadinoxanthin, dinoxanthin, neo-dinoxanthin, peridin, neoperidin and three unidentified pigments (Jeffrey & Haxo, 1968; Hochberg et al., 2006). The shallowest hermatypic corals may present an unidentified pigment of high absorption at short wavelength; this pigment can function as a protection against high irradiances. The transfer of photosynthetic products from the algae to the polyp can supply its metabolic requirements and promote rapid calcification (Goreau & Goreau, 1959; Osinga et al., 2011). The photosynthetic fixation of CO2 and the subsequent calcium carbonate (CaCO3) precipitation are intimately linked on both spatial (cell to ecosystem) and temporal (day–night) scales (Gattuso et al., 1999; Falter et al., 2011). Metabolic balance can be expressed by the quotient between the photosynthetic rate during the daylight (P) divided by the daylight respiration rate (R). Several studies involving metabolic measurements in Porites (Table 1) have been used to infer that the coral is selfsustaining with respect to carbon. The aim of this study was to determine the metabolic balance of the polyp-algae mutu-

Table 1. P: R quotient values for Porites spp., date of determination, bioma location, and author reference. (n/d = not dated). Species

P:R Month

P. divaricata

3.4

n/d

P. sp.

2.9

n/d

P. monticulosa 2.9

n/d

2.1 2.8 1.4

n /d May Sep.

P. lutea

2.3

Nov.

P. furcata

1.5

May

P. compressa P. porites

Location

Authors Kanishwer & Florida, USA Wainwright (1967) Enewetak Roffman Atoll, Marshal (1968) Islands Coles & Hawai, USA Jokiel (1977) Veracruz, México

Signoret et al. (1987)

Sichang, Thailand

Moberg et al. (1997) Manzanello Florida, USA & Lirman (2003)

alistic symbiosis of P. panamensis in the reef area of Pichilingue, Baja California Sur, México. This was done through (1) estimations of primary production by changes in dissolved oxygen (DO) on incubations of P. panamensis fragments, (2) estimations of the algal biomass through photosynthetic pigments, and (3) the determination of the autotrophy - heterotrophy conditions in the mutualistic association. MATERIALS AND METHODS Collection area: Coral samples were obtained at 24° 17’08” N, 110° 19’50” E, near Pichilingue beach and 2 km north of Unidad de Investigación Pichilingue of the Universidad Autónoma de Baja California Sur. There is an approximately 500m strip of coral to the north side of the beach in which P. panamensis is the predominant form. The specimens were collected manually at 1 m depth; they were selected with a similar size and good polyp health (no observable whitening presence). Twelve pieces of coral per season (fall of 2009 and winter of 2010) were collected and moved to the laboratory in marine water containers. To allow acclimation to laboratory conditions, pieces were deposited before the experiment in the experimental pool for 24 hours (h). Physicochemical variables: Water temperature, salinity and dissolved oxygen (DO) in the experimental pool were registered with a multiprobe hand oxymeter YSI-85. The pH was measured with a Conductronic potentiometer, and irradiance with a LI-Cor 9901-sha220 underwater radiation sensor. The precision for water temperature measurements was ±0.05°C, for salinity ±0.01 psu, for DO 0.5 mg∙l-1, for pH ±0.1 pH units and for irradiance ±0.01 μmol∙s1 ∙m-2. Data were tested for normality by the Chisquare test and the null hypothesis as normality; null hypothesis was not rejected in any case (Daniel &Terrel, 1983). Homoscedasticity was

METABOLISM IN POLYP-ALGAE SYMBIOSIS

assumed because the data were grouped (low scatter in Figure 2) and in all cases the ratio of the largest sample variance to the smallest variance did not exceed 1.5. Analysis of variance (ANOVA) was applied for each parameter to evaluate the difference between replicates. Primary production: Primary production was estimated under laboratory conditions for collected fragments of each season (fall of 2009 and winter of 2010). Each coral fragment collected was placed in a respirometric glass chamber, 20 cm diameter and 20 cm height with removable cover. The respirometric chambers were placed on a circular pond of 1.3 m diameter and 50 cm depth with a continuous flow of sea water provided by the pumping-filtering system; this system has a set of filters capable of eliminating 70% of the organic sediment and particulate matter. The 24 h experiment consisted of three incubations of 2 h during the day and four during the night for three consecutive days in fall and one day in winter; in both cases a rest of 1 h between incubations was allowed. During the resting time each chamber was opened to permit water exchange and reduce stress to the coral. The dissolved oxygen concentrations (DO) were measured with a YSI-85 oxygen meter, calibrated with the Winkler method at the start and end of each incubation. Also, water variables were measured from a control chamber (without coral). With the discrete dissolved oxygen values, a best fit fourth degree polynomial graph (Fig. 2a, 2b) provided a daily oxygen release curve and the estimation of the primary gross production in the mutualistic symbiosis for each season. Metabolic balance determination: The dissolved O2 curve obtained from incubations gave rise to a mathematical model that explains the autotrophic-heterotrophic periods. The range of production periods was determined by the change (increase or decrease) of the initial dissolved O2 values from each incubator. Inflection points of the oxygen curve were determined to verify correspondence of the model with the metabolic balance. A best fit oxygen concentration hourly curve was built by the evaluation of the polynomial function obtained. Net production was obtained from the daily photosynthetic and daily respiratory rates calculated from the dissolved oxygen produced or consumed in a given time by a given biomass, according to the following equations (Barreiro & Signoret, 1999):

P=(Oc – O0 ) / t N R=(O0 – Oc ) / t N

(1) (2)

Where: P= Photosynthetic rate (mg O2•polyp-1•day-1); R = Respiratory rate (mg O2•polyp-1•day-1); Oc = O2 released diurnal values (mg O2•L-1•day-1); O0 = O2 consumed nocturnal values (mg O2•L-1•day-1), t = Incubation time (hr) and N = Number of polyps per cm2 of living surface. Biomass estimation and photosynthetic pigments: Once incubations had been achieved, the living surface of the coral was estimated from an impression on aluminum foil (Marsh, 1970). Ten 1 cm2 fragments of each coral were obtained with a Mototool DREMEL-770. Polyps were counted on each 1cm2 while being shield from direct sun-light. Each sample was macerated with a pestle and mortar with 10ml (90%) acetone and centrifuged at 4000 rpm and 4.0°C for 15 minutes. The supernatant was analyzed in a Thermo Scientific Multiskan Spectrum, with wavelengths ranging from 400 to 750nm. Pigment concentration for chlorophylls a and c2 were determined with the spectrophotometric formulas proposed by Jeffrey & Humphrey (1975); for carotenes concentration the formula proposed by Strickland & Parsons (1972) for dinoflagellate carotenes was used: mg Cla ∙ total polyps∙cm-2=(11.85 A664-1.54 A647-0.08 A630)V/P l

(3)

mg Clb ∙ total polyps∙cm-2=(-5.43 A664+21.03 A647-2.66 A630)V/P l (4)

mg Cl c1 y c2∙ total polyps∙cm-2=(-1.67 A664-7.60 A647 +24.52 A630)V/P l (5) mg carotenes ∙ total polyps∙cm-2=(10.0 A480) V/P l (6)

Where: A=Optical density read at the wavelength indicated as subscript; V=Acetone volume (ml); l=Length size of the cell where the light beam passed through (1.0 cm), P=Total polyps per cm-2 and Cl=Chlorophyll. RESULTS Physicochemical parameters: The abiotic parameters (water temperature, salinity, pH, irradiance and DO) did not differ significantly between specimens or between days of incubation (ANOVA, p>0.5). Water temperature inside the respiratory chamber differed between day and night (Table 2); the average temperatures were 22.50°C for fall (range between 19.74°C at 21:00 h to 26.71°C at 15:00 h) and 17.51°C for winter (range 14.05°C at 07:00 h to 22.06 °C at 16:00 h). Average salinity was 36.7 for fall and 37.4 for winter. Water pH increased during daylight and decreased at sunset. Although differences

RICO-ESENARO et al.

Table 2. Season of incubation, time of the day, average values of irradiance, temperature, salinity, and pH. Season

Fall

Winter

Hour 1-3 6-8 9-12 13-15 16-18 19-21 22-00 1-3 6-8 9-12 13-15 16-18 19-21 22-00

Irradiance Temperature Salinity (μmol∙s-1∙m-2) (°C) (psu) 0 1315.62 1482.78 448.95 0 0 0 0 1447.3 1584.0 492.7 0 0 0

were not significant (p>0.05); pH variation was different in the chambers with corals than in the control chamber (Fig. 1). Primary production: The first increase in the DO values with sunlight was registered from 06:00 to 8:00 h, with a primary gross production peaking at 12:00 - 14:00 h. DO values began to fall at 16:00 and were stable since the 18:00 h (Table 3). The lowest average of DO value fell between 22:00 and 03:00 h. Minimum DO values were of 0.5 mg O2∙l-1 in the fall (Fig. 1a) and 1.2 mg O2∙l-1 in winter (Fig. 1b), recorded at dawn (06:00 h) and sunset (18:00 h), under the respiratory effect of the mutualistic symbiosis. The DO curve for each season showed a maximum value of 3.1 mg O2∙l-1 for 12:00 h in the fall and 3.5 mg O2∙l-1 in the winter (Fig. 2A

22.32 24.03 25.75 25.03 21.26 20.95 21.19 16.00 14.30 15.80 18.40 20.40 19.60 18.10

36.39 36.34 36.47 36.43 36.60 36.47 36.85 36.20 38.60 39.50 39.20 37.70 35.30 35.30

pH 8.54 8.51 8.42 8.28 8.29 8.41 8.50 7.97 7.88 7.96 7.95 7.95 8.11 7.99

and 2B). Best fit equations of each drawn curve were computed to elaborate the metabolic balance model for each season. Measurement of irradiance started at dawn around 06:30 h and ended with sunset at 17:30 h. Maximum irradiance was between -1 -2 09:00 and 15:00 h (around 1500 μmol·s ·m ). Mabolic balance: The metabolic balance models assume a constant respiratory rate per hour (r) for the heterotrophic period. A value of 0.8 mgO2∙l-1∙h-1 was determined for fall and 1.5 mgO2∙l-1∙h-1 for winter. Because the nocturnal values did not differ significantly between each hour, and in view of other research on corals metabolism (Muscatine et al., 1981; Signoret et al., 1987) respiratory rates were based on constant values for each hour of the heterotrophic period. Only a best fit straight line was drawn for each season, fall and winter (Fig. 3).

Figure 1. Dissolved Oxygen during the heterotrophic period in the incubation chambers

METABOLISM IN POLYP-ALGAE SYMBIOSIS

Table 3. Season of incubation, time and average dissolved oxygen concentration (mg O2∙L-1) for different specimens incubation. Bold numbers indicate the time of 6-8 and 16-18 hours for values at dawn and sunset. Season

Fall

Winter

Hour

Specimen 6 7 0.73 0.75 2.85 2.69 3.22 3.14 2.30 2.99 0.99 1.10 0.84 0.73 0.74 0.79 1.59 1.92

1-3 6-8 9-12 13-15 16-18 19-21 22-00 1-3

1 0.82 2.85 2.71 2.84 0.98 0.91 0.95 1.27

2 0.75 2.60 2.37 2.03 1.00 0.82 0.69 1.54

3 0.69 3.52 3.80 2.76 0.77 0.35 0.41 1.30

4 0.72 2.7 3.2 2.7 0.9 0.9 0.8 1.41

5 0.81 3.00 3.01 2.45 0.91 0.79 0.83 1.45

6-8

3.25

2.31

3.56

3.24

3.62

3.42

9-12 13-15 16-18 19-21 22-00

3.32 3.13 1.67 2.13 1.71

2.47 2.06 1.68 1.80 1.49

3.97 3.11 1.83 1.91 1.14

3.51 3.37 2.01 1.81 1.28

3.84 3.15 2.03 1.80 1.50

3.53 2.93 1.78 1.87 1.39

The metabolic balance models were built by the hourly evaluations of the polynomial equation (obtained from the DO curve) for each hour of the autotrophic period, and with the hourly respiratory rate (r) determined for the heterotrophic period. This model shows the metabolic balance between heterotrophic and autotrophic periods. Photosynthetic rate (P) was 0.045 mg O2∙l-1∙day-1∙polyp-1 for fall and 0.072 mg O2∙l1 ∙day1∙polyp-1 for winter; while the respiratory rate (R) was 0.023 mg O2∙l-1∙day-1∙polyp-1 for fall and 0.034 mg O2∙l-1∙day-1∙polyp-1 for winter. The P : R ratio was 1.977 for fall and 2.047 for winter.

8 0.91 2.50 3.19 2.55 1.09 0.92 0.89 1.87

9 0.84 2.12 2.38 2.34 1.15 0.96 0.98 1.31

10 0.82 3.18 3.70 3.00 0.92 0.78 0.80 1.44

11 0.89 2.97 3.42 2.92 0.87 0.76 0.69 1.60

2.93

2.98

3.43

3.46

3.47

3.99 3.92 1.61 1.32 1.53

3.32 3.35 1.61 1.42 1.24

4.92 3.89 1.61 1.34 1.66

4.69 3.20 1.61 1.45 1.34

4.34 3.65 1.61 1.49 1.46

Biomass and photosynthetic pigments: The average animal biomass was 36 (±6.0 SD) polyps∙cm-2 for fall in a living surface of 2476 cm2 and 46 (±4.0 SD) polyps∙cm2 in 2066 cm2 of living surface for winter. This contrasts with Glynn et al. (1994) who reported 53 (±2.6 SD) polyps∙cm-2. Measurements of the photosynthetic pigments (Fig. 4) for fall showed an average content of 0.57 (±0.13 SD) mg Chl a∙polyp-1 , 0.40 (±0.13 SD) mg Chl c2∙polyp-1 and 1.23 (±0.31 SD) mg carotenes∙polyp-1. In winter the average contents were 0.86 (±0.18 SD) mg Chl a∙polyp-1, 1.05 (±0.14 SD) mg Chl c2∙polyp-1 , and 1.61 (±0.28 SD) mg carotenes∙polyp-1. The

Figure 2. Hourly dissolved oxygen curves and polynomial best fit equations for each season for incubations of P. panamensis (1A for winter and 1B for fall).

RICO-ESENARO et al.

Table 4. Specimen number, their living surface biomass and average polyps per cm2 for fragment of P. porites utilized in each chamber. Specimen 3 and 10 showed a relation between increased number of polyps per living surface and maximum GP values. Fall Specimen 1 2 3 4 5 6 7 8 9 10 11 12

Live surface Average (cm2) polyps per cm2 248.2 158.0 194.1 193.3 241.0 137.5 220.4 319.0 156.8 289.0 129.2 191.2

31.4 29.8 47.4 38.9 35.4 34.3 28.7 42.2 34.0 44.1 27.9 33.4

Winter GP(mg O2∙L-1∙h-1) Max. Min. 3.6 0.76 3.24 0.41 4.78 0.27 3.80 0.68 4.18 0.6 3.93 0.51 3.39 0.42 3.22 0.91 2.81 0.88 4.31 0.48 3.17 0.70 3.06 0.86

relative quotients of chlorophyll concentrations (mg∙polyp-1) (Chl a : Chl c2) were 1.0 : 0.69 for fall and 1.0 : 1.22 for winter. Meanwhile chlorophyll a : carotenes concentrations (mg∙polyp-1) ratio (Chl a : carotenes) were 1.0 : 2.13 for fall and 1.0 : 1.88 for winter. DISCUSSION Primary production was higher in winter and this difference could be the result of many factors. One is the limitation of light inasmuch irradiance in the fall was lower than normal because the 2009 hurricane season, that generally ends in September, extended until November, bringing cloudy days. Another factor was the high water temperatures in the fall that increased respiratory rates. A comparison of metabolic balance of field observations with laboratory measurements has a strong correlation of a decrease in respiration rates with a decrease in photosynthetic rates on cloudy days and is related to a regulation of the whole system.

GP( mg O2∙L-1∙h-1) Live Surface Average (cm2) polyps per cm2 Max. Min. 255.0 51.3 1.52 1.05 149.5 42.5 0.39 0.14 156.9 46.9 1.59 0.89 231.7 49.3 1.8 0.58 129.2 41.2 1.6 0.89 148.7 36.7 1.37 0.75 132.5 45.3 1.65 0.53 104.2 45.6 1.00 0.42 260.7 51.2 2.22 0.81 196.2 44.1 2.20 0.46 173.5 40.5 1.59 0.78 127.5 45.4 1.45 0.37

Although DO curves did not differ significantly between specimens, there was some relation between the maximum production values and the number of polyps per cm2. Specimens 3 and 10 in the fall, and 9 and 10 in the winter, showed both the highest production levels and the highest number of polyps per living surface (Table 4). This relation did not apply for minimum values because the biomass of polychaetes and other organisms of the association were not considered in this study. As there is no relationship between the size of the polyps and the chlorophyll concentration, animal biomass data were considered in terms of living surface areas. The metabolic balance determined by P : R ratios is consistent with data for other species of the same genus (Table 1). P. panamensis maintain a high metabolic efficiency that can even maintain the metabolic requirements of other integral members of the association such as shrimp larvae, polychaetes, ophiuroids

Figure 3. Average concentration (mg) of photosynthetic pigments per polyp in P. panamensis for each season.

METABOLISM IN POLYP-ALGAE SYMBIOSIS

Figure 4. Mesured pH values for the reference and coral chambers in fall season.

and sea cucumbers which live within the coral framework. The higher concentration of photosynthetic pigments in the winter than in fall suggests that the Symbiodinium population was affected by high irradiance and temperatures in fall. Previous studies have demonstrated that the concentrations of these pigments, as well as symbiont densities, vary in relation to environmental factors. During winter conditions of low temperature and solar irradiance, increased pigments concentrations and symbiont densities are frequently observed (Brown et al., 1999; Fagoonee et al., 1999; Fitt et al., 2000; Apprill et al., 2007). Many studies have shown some variability in pigment concentrations between seasons (Brown et al., 1999; Fitt et al., 2000; Costa et al., 2005); these changes represent some adjustments by mutualistic algae to optimize physiological activity to the environmental changes (Sunagawa et al., 2008). The relative high concentration of carotenes (Fig. 4) is representative of shallow-water corals, because these pigments fulfill a double function, as accessory pigments to absorb light and as a protection for the Chl a at high irradiances. Carotenes are related with the survival of the mutualistic algae; elevated concentrations of Chl c2 and carotenes are indicators of mature and stable communities of dinoflagellates. The mutualistic relationship in the pH behavior can be explained by the marine carbon dynamics. In marine ecosystems pH is regulated by the carbonate synthesis that changes the water alkalinity. This process is thermodynamically regulated and includes a series of substitutive reactions to transform CO2 molecules into H2CO3 and then HCO3 (Millero,

1995). Many marine organisms including corals, can use this HCO-3 to synthesize CaCO3 by the reaction Ca2+ + HCO3 â&#x2020;&#x2019; CaCO3 +H2O. These changes are controlled by chemical factors more than by physical conditions (Gattuso et al., 1999). Both CO2 decrease due to photosynthesis as well as precipitation of CaCO3 contribute in rising the pH values during light periods, and the increase of CO2 by respiration acidifies during darkness (Bold & Winne, 1985) (Fig. 1). The mutualistic associations in hermatypic corals are determinants in this control; investigations related to changes in pH and the supply or access to dissolved inorganic carbon might provide further mechanistic explanation for the host role in protecting its symbionts from environmental stresses (Bahgoli et al., 2008). The light intensity and wavelength reaching the symbiotic algae, and the solute exchange between the coral and the surrounding water are the most important external regulators of photosynthesis in reef corals (Ulstrup, 2006). The metabolic balance in the mutualistic association polyp-algae of Porites panamensis had a predominantly autotrophic behavior in both seasons (fall and winter). The presented results show that the mutualistic association consumes in respiration one third of the total carbon fixed by its own primary production. The relative proportions of photosynthetic pigments suggest an adaptive feature of the species, that allows high-quality photosynthetic material (Chl a) in low proportions, protected by the high presence of accessory pigments (Chl c2 and carotenes); these last pigments increase in fall and protect Chl a at high irradiances. This coral species has shown a high photosynthetic efficiency in the mutualistic association and can regulate the metabolic balance. This efficiency is higher in the winter than in the fall and is de-

RICO-ESENARO et al.

termined by irradiance ACKNOWLEDMENTS We would like to thank Ana Isabel Beltrán and Hermilo Santoyo of the Marine Biology Department of the Autonomous University of Baja California Sur. We also thank the Division of Biological and Health Sciences, the Man and his Environment Department, and the Biology career at the Metropolitan Autonomous University, campus Xochimilco. We thank Etzaguery Janeth Marin Coria for the improvement on the drawings. Special thanks to the editor who substantially improved the manuscript.

Bahgoli, R.A., H. Barid & P.J. Ralph. 2008. Does the coral host protect its algal symbionts from heat and light stresses? 113-117, in: Proceedings of the 11th International Coral Reef Symposium, Ft. Lauderdale. Bold, H.C. & M.J. Wynne. 1985. Introduction to the algae: Structure and reproduction. Prentice-Hall, Englewood Cliffs, 720 p. Brown, B.E., R.P. Dunne, I. Ambarsari, M.D.A. Letissier & U. Satapoomin. 1999. Seasonal fluctuations in environmental factors and variations in symbiotic algae and chlorophyll pigments in four Indo-Pacific coral species. Mar. Ecol. Progr. Ser., 191: 53-69. Coles S.L. & P.L. Jokiel. 1977. Effects of Temperature on Photosynthesis and Respiration in Hermatypic Corals. Mar. Biol., 43: 209-216. Costa, C. F. R. Sassi & F.D. Amaral. 2005. Annual cycle of symbiotic dinoflagellates from three species of scleractinian corals from coastal reefs of northeastern Brazil. Coral Reefs, 24(2): 191-193. Daniel, W. W. & J. C. Terrell, 1983. Business statistics. Houghton Mifflin Company. Boston. 700 p.

Dra. Martha Signoret-Poillon We greatly appreciate the support provi ded by Dra. Martha Signoret-Poillon throughout her stay in the Universidad Autonoma Metropolitana, Xochimilco Unit, Department Man and Environment. We appreciate her friendship and specially her enthusiastic way of life, her teachings and human warmth. REFERENCES Apprill, A.M., R.R. Bidigare & R.D. Gates. 2007. Visibly healthy corals exhibit variable pigment concentrations and symbiont phenotypes. Coral Reefs, 26: 387-397. Barreiro, M.T. & M. Signoret. 1999. Productividad primaria en sistemas acuáticos costeros, métodos de evaluación. Serie Académicos. Universidad Autónoma Metropolitana, Unidad Xochimilco. Ciudad de México, 81p.

Falter, J.L., M.J. Atkinson. D.W. Schar, R.J. Lowe & S.G. Monismith. 2011. Short-term coherency between gross primary production and community respiration in an algaldominated reef flat. Coral Reefs, 30: 53-58. Fagoonee, E., H.B. Wilson, M.P. Hassell, J.R. Turner. 1999. The dynamics of zooxanthellae populations: a long-term study in the Weld. Nature, 283: 843-845. Fitt, W.K., F.K. McFarland, M.E. Warner & G.C. Chilcolat. 2000. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol. Oceanogr., 45(3): 677685. Gattuso, J.P., D. Allemand & M. Frankignoulle. 1999. Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Amer. Zool., 39(1): 160-183.

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Goreau, T. E. & N. Goreau. 1959. The physiology of skeleton formation in corals II. Calcium deposition by hermatypic corals under various conditions in the reef. Biol. Bull., 117: 239-250.

McCloskey, L. R., D.S. Wethey & J.W. Porter. 1978. Measurement of photosynthesis and respiration in reef corals. In: Stoddart D.R. & R. E. Johannes. Coral reefs: research methods. Reino Unido: Unesco Pub. 581 p.

Glynn, P.W., S.B. Colley, C.M. Eakin, D.B. Smith, J. Cortes, N.J. Gassman, H.M. Guzman, J.B. Rosario & S. Feingold. 1994. Reef coral reproduction in the eastern Pacific: Costa Rica, Panamá, and Galápagos Islands (Ecuador). II. Poritidae. Mar. Biol., 118: 191-208.

Millero, F.J. 1995. Thermodynamics of the carbon dioxide system in the oceans. Geochim. Cosmochim. Acta, 4(59): 661-677.

Hatcher, B. 1990. Coral Reef Primary Productivity: A hierarchy of pattern and process trends. Ecol. Evol., 5(5): 149-155. Hochberg, E. J., M. Amy, M Apprill, J. Atkinson & R.R. Bidigare. 2006. Bio-optical modeling of photosynthetic pigments in corals. Coral Reefs, 25: 99-109. Jeffrey, S.W. & F.T. Haxo. 1968. Photosynthetic pigments of symbiotic dinoflagellates (zooxanthellae) from corals and clams. Biol. Bull., 135(1): 149-165. Jeffrey, S.W. & G.F. Humphrey. 1975. New spectrophotometric equations for determining chlorophylls a, b, c1, and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanzen., 167: 191-194.

Muscatine, L., L.R. McCloskey & R.E. Marian. 1981. Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol. Oceanogr., 26(4): 601611. Moberg F., M. Nyström, N. Kautsky, M. Tedengren & P. Jarayabhand (1997). Effects of reduced salinity on the rates of photosynthesis and respiration in the hermatypic corals Porites lutea and Pocillopora damicornis. Mar. Ecol. Prog. Ser., 157: 53-59. Osinga, R., M. Schutter, B. Griffioen, R.H. Wijffels, J.A.J. Verreth, S. Shafir, S. Henard, M. Taruffi, C. Gili & S. Lavorano. 2011. The biology and economics of coral growth. Mar. Biotechnol., 13(4): 658-671. Riegl, B. & W.E. Piller. 2003. Possible refugia for reefs in times of environmental stress. Int. J. Earth Sci., 92: 520-531.

Jesser, M.P., C. Mazel, D. Phinney & C.S. Yentsch. 2000. Light absorption and utilization by colonies of the congeneric hermatypic corals Montastraea faveolata and Montastraea cavernosa. Limnol. Oceanogr., 45: 76–86.

Signoret, M., H. Santoyo & A.G. Zapata. 1987. Balance metabólico de la asociación de corales hermatípicos-productores primarios en el arrecife de Isla Verde, Veracruz. In: 143-167, Memoria del V Simposio de Biología Marina. Universidad. Autónoma de Baja California Sur.

Kanwisher J.W. & S.A. Wainwright. 1967. Oxygen Balance in Some Reef Corals Biol. Bull., 133(2): 378-390.

Roffman B. 1968. Patterns of oxygen exchange in some Pacific corals. Comp. Biochem. Physiol., 27: 405-418.

LaJeunesse, T.C., H. Reyes-Bonilla, M.E. Warner, M. Wills, G.W. Schmidt & W.K. Fitt. 2008. Specificity and stability in high latitude eastern Pacific coral–algal symbioses. Limnol. Oceanogr., 53(2): 719-727.

Strickland, J. & T. Parsons. 1972. A practical handbook of seawater analysis. Bulletin 167, Fisheries Research Board of Canada. 310 p.

López-Pérez, R.A. 2005. The Cenozoic hermatypic corals in the eastern Pacific: History. Earth Sci. Rev., 72: 67-87. Manzello D. & D. Lirman. 2003. The photosynthetic resilience of Porites furcata to salinity disturbance. Coral Reefs, 22: 537-540. Marsh, J. A. Jr. 1970. Primary Productivity of reef-building calcareous red algae. Ecology, 51(2): 255-263.

Sunagawa, S., J. Cortés, C. Jiménez & R. Lara. 2008. Variación en la densidad de células y en las concentraciones de pigmentos de los dinoflagelados simbióticos del coral Pavona clavus en el Pacífico oriental (Costa Rica). Cienc. Mar., 32(2): 113-123. Ulstrup, K.E., J. Ralph, A.W.D. Larkum & M. Kühl. 2006. Intra-colonial variability in light acclimation of zooxanthellae in coral tissues of Pocillopora damicornis. Mar. Biol., 149: 1325-1335.

CICIMAR Oceánides 29(1): 11-18 (2014)

BLOOM OF Gonyaulax spinifera (DINOPHYCEAE: GONYAULACALES) IN ENSENADA DE LA PAZ LAGOON, GULF OF CALIFORNIA

Gárate-Lizárraga, I.1, Ma. S. Muñetón-Gómez1, B. Pérez-Cruz2 & J. A. Díaz-Ortíz2 Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Apartado Postal 592, Col. Centro, La Paz, B.C.S. 23000, México. 2Laboratorio Estatal de Salud Pública “Dr. Galo Soberón y Parra”, Boulevard Vicente Guerrero Esq. Juan R. Escudero s/n, Ciudad Renacimiento, Acapulco 39715, Guerrero, México. Email: igarate@ipn.mx 1

ABSTRACT. During a sampling on 24 September 2012 in the coastal lagoon, Ensenada de La Paz, a small bloom of the dinoflagellate Gonyaulax spinifera was detected. Its abundance varied from 401 to 1342 × 103 cells L–1. Cells of G. spinifera ranged from 34 to 50 µm in length and 22 to 35 µm in width (n = 30). Seawater temperature and salinity were 29 °C and 35.5, respectively. The species composition of the bloom was recorded. The phytoplankton community had high species richness, resulting from a mix of benthic and pelagic diatoms and dinoflagellates, as well as cyanobacteria that occurred with low frequency. This brief proliferation lasted around three hours and may have been caused by tidal water accumulation along the shore. Although G. spinifera is a producer of yessotoxin, no fish or invertebrates were apparently killed by this bloom, which was rapidly dispersed by tides and wind-forcing.

Keywords: Bloom, Dinoflagellates, Gonyaulax spinifera, Protoceratium reticulatum, Gulf of California

Florecimiento de Gonyaulax spinifera (Dinophyceae: Gonyaulacales) en la laguna Ensenada de La Paz, Golfo de California

RESUMEN. Durante un muestreo el 24 de septiembre de 2012 en la laguna costera Ensenada de La Paz se detectó un pequeño florecimiento del dinoflagelado Gonyaulax spinifera. Los valores de abundancia variaron de 401 a 1342 × 103 céls L–1. Los especímenes de G. spinifera presentaron un intervalo de tallas de 34 a 50 µm de longitud y de 22 a 35µm de ancho (n = 30). La temperatura del agua fue de 20 °C y la salinidad fue de 35.5. Se determinó la composición de especies durante este florecimiento. Como resultado de la mezcla de especies bentónicas y pelágicas de diatomeas y dinoflagelados, así como de algunas cianobacterias poco frecuentes, la comunidad del fitoplancton presentó una riqueza de especies alta. Esta pequeña proliferación se observó por alrededor de 3 horas y pudo ser ocasionada por la marea acumulándola en la línea de costa. Aunque G. spinifera es una especie productora de yessotoxinas, no se observaron peces ni invertebrados muertos durante este florecimiento, el cual se dispersó rápidamente por efecto de la marea y la fuerza del viento.

Palabras claves: Florecimiento, Dinoflagelados, Gonyaulax spinifera, Protoceratium reticulatum, Golfo de California. Gárate-Lizárraga, I., Ma. S. Muñetón-Gómez, B. Pérez-Cruz & J. A. Díaz-Ortíz. 2014. Bloom of Gonyaulax spinifera (Dinophyceae: Gonyaulacales) in Ensenada de La Paz Lagoon, Gulf of California. CICIMAR Oceánides, 29(1): 11-18.

INTRODUCTION Dinoflagellate red tides are frequent and periodic throughout the year in Bahía de La Paz in the southwestern part of the Gulf of California (Gárate-Lizárraga et al., 2001). A systematic monitoring of marine microalgae blooms in this bay began in the summer of 2000 because of an extensive bloom of Cochlodinium polykrikoides (Gárate-Lizárraga et al., 2004). Blooms monitoring has been important for knowing the species involved, if they are toxic or not and eventually to predict and manage harmful algal blooms. The majority of red tides in Bahía de La Paz coasts are produced by dinoflagellates species (Gárate-Lizárraga et al., 2001; 2006). Few records of Gonyalax red tides exist. Gonyaulax polygramma (Pouchet) Kofoid, 1911 is the main blooming species in several sites in the Gulf of California: Bahía de Los Ángeles (Millán-Núñez, 1988), Ensenada de La Paz (Gárate-Lizárraga et al., 2001), Bahía de La Paz (Gárate-Lizárraga et al., 2006), and off Isla Espíritu Santo (Gárate-Lizárraga, 2006). Fecha de recepción: 03 de marzo de 2014

Gonyaulax belongs to the order Gonyaulacales F.J.R.Taylor, 1980 and it is one of the most widely represented genera of the dinoflagellates, occurring in temperate and tropical seas and in brackish and fresh water (Kofoid, 1911; Taylor, 1976). This order is characterized by a strongly asymmetrical organization of the thecal plates. The apical pore complex is also asymmetrical and it is never connected to the 1′ by a canal plate as in the case of the Peridiniales. The typical plate formula is 4′, 6″, 6c, 5s, 5″′, 2″″ according to Fensome et al. (1993). Gonyaulax is the representative genus of this order; it has a round to polygonal body, a cingulum strongly cavozone (deeply excavated), median but may be offset ventrally, sulcus distinct, thecal plates may be thick and strongly patterned, antapical spines are often present. Currently, there are 121 species (and infraspecific) names of Gonyaulax in the AlgaeBase database, out of which 72 have been listed as accepted (Guiry & Guiry, 2014). Only a few species in this genus produce toxins and red tides (Rhodes et al., 2006). Fecha de aceptación: 10 de abril de 2014

GÁRATE-LIZÁRRAGA et al.

This report describes the first bloom of Gonyaulax spinifera (Claparède & Lachmann) Diesing, 1866 in the southwestern Gulf of California. The microalgae community present during this bloom is also described. MATERIAL AND METHOD On 24 September 2012 a reddish-coloured phytoplankton patch was observed nearby the CICIMAR-IPN pier in Ensenada de La Paz (Fig. 1), which is a shallow coastal lagoon connected to Bahía de La Paz; the inlet is 1.2 km wide and 4 km long and has an average depth of 7 m (Gómez-Valdés et al., 2003). The sampling station (24.08°N, 110.21°W) is located in the shallow basin of the southernmost part of the bay. Three red tide samples were collected in 250 mL plastic bottles. Samples were fixed with acid Lugol solution and later used for identification and counting cells. The total phytoplankton, nano- (organism <20 μm) and microphytoplankton (organism >20 μm) abundances (cells L–1) were estimated simultaneously with species composition identifications of microphytoplankton. Nanophytoplankton was not identified taxonomically. Subsamples were taken for observations of live phytoplankton. Cell counts were made in 5 mL settling chambers under an inverted Carl Zeiss phase-contrast microscope (Utermöhl, 1958). Sea surface temperature was recorded with a bucket thermometer. Salinity was measured with a refractometer (Model STX3, Vee Gee Scientific, Kirkland, WA). A compound Olympus CH2 microscope was used to measure cells. A digital Konus camera (8.1 MP) was used for recording images. RESULTS AND DISCUSSION The phytoplankton patch (~10 m long, 2 m wide) occurred during high tide. The bloom lasted about 3 h and disappeared during ebb tide. This bloom could be the result of accumulation of cells along the shore, as other red tides that have occurred in the lagoon (Gárate-Lizárraga et al., 2006). The phytoplankton community within this red tide was composed of 69 microalgae taxa, including 33 species of Dinophyta, 30 Bacillariophyta, 4 cyanobacteria, 1 euglenophyte, and 1 prasinophyte. Species richness ranged from 41 to 61 species. The high richness resulted from a mix of benthic and pelagic diatoms and dinoflagellates, as well as cyanobacteria that occurred with a low frequency. The microalgae species list and their abundances are summarized in Table 1. Total phytoplankton abundance in samples varied from 601 to 1496 × 103 cells L–1. Micro-phytoplankton was numerically more important (avg. = 952 × 103 cells L–1) than nano-phytoplankton (avg. = 79 ×

Figure 1. a) Location of bloom dominated by Gonyaulax spinifera; b) tidal variation on 24 September 2012. Arrow indicates the time of sampling.

103 cells L–1). Nano-phytoplankton was mainly composed by small flagellates and naviculoid diatoms. On the basis of abundance and the number of species, dinoflagellates were the most important group, followed by diatoms. Seven species of Gonyaulax were identified and displayed iconographically: Gonyaulax spinifera (Figs. 2, 3, and 4), G. polygramma (Fig. 7), Gonyaulax cochlea Meunier, 1919 (Figs. 9, and 10), G. digitalis (Fig. 15), G. hyalina Ostenfeld & Schmidt, 1901 (Figs. 16, and 17), G. birostris F. Stein, 1883 (Fig. 18), and G. fusiformis H.W.Graham, 1942 (Fig. 19). G. spinifera was the dinoflagellate species responsible for this bloom. At that time seawater temperature was 31 °C and salinity reached 35.5. Cells of G. spinifera were slightly longer than wide. The epitheca had convex sides and a small apical horn. The hypotheca has 2–4 antapical spines. The sulcus extends almost the full length of the cell. The cingulum is deeply excavated. Cell surface is ornate (Fig. 4). Striae are associated with round trichocyst pores. Single cells ranged from 34 to 50 µm in length and 22 to 35µm in width. The shape was variable and made identification difficult. The G. spinifera group (Kofoid, 1911) includes three species with similar morphological features, which can easily be confused: G. spinifera, G. digitalis (Pouchet) Kofoid, 1911, and G. diegensis Kofoid, 1911 (Lewis et al., 1999). During the examination of live samples we observed the formation of temporary resting states or pellicles in some species of Gonyaulax (Figs. 5, 6, 8, 10, 17) and Scrippsiella spinifera (Figs. 12, 13, 14). About 30 min after cells were collected, they began to grow and to undergo ecdysis to form a round pellicle. These temporary cysts could be the result of manipulating samples or a response to the microscope light and heat, which may pause adverse conditions

BLOOM OF Gonyaulax spinifera

Table 1. Abundance of microalgae species recorded in the Ensenada de La Paz, Gulf of California during proliferation of Gonyaulax spinifera on September 2012. Microalgae species Bacillariophyta Arcuatasigma challengeriense (Castracane) G.Reid, 2012 Asterionellopsis glacialis (Castracane) Round, 1990 Asteromphalus arachne (Brébisson) Ralfs, 1861 Asteromphalus heptactis (Brébisson) Ralfs, 1861 Biddulphia tridens (Ehrenberg) Ehrenberg, 1841 Chaetoceros coarctatus H.S. Lauder, 1864 Chaetoceros diversus Cleve, 1983 Chaetoceros didymus Ehrenberg, 1845 Chaetoceros socialis H.S. Lauder, 1864 Chaetoceros sp. Climacodium frauenfeldianum Grunow, 1868 Cylindrotheca closterium (Ehrenberg) Reimann & J.C. Lewin, 1964 Fragilariopsis doliolus (Wallich) Medlin & P. A.Sims, 1993 Grammatophora sp. Guinardia flaccida (Castracane) H. Peragallo, 1892 Helicotheca tamesis (Shrubsole) M. Ricard, 1987 Hemiaulus membranaceus Cleve,1873 Nitzschia longissima (Brébisson) Ralfs, 1861 Odontella aurita var. obtusa (Kützing) Denys, 1982 Odontella rhombus (Ehrenberg) Kützing, 1849 Paralia fenestrata Sawai and Nagumo, 2005 Planktoniella sol (C.G.Wallich) Schütt, 1892 Proboscia alata (Brightwell) Sundström, 1986 Rhizosolenia clevei var. communis Sundström, 1984 Skeletonema costatum (Greville) Cleve, 1873 Stauroneis membranacea (Cleve) Hustedt, 1959 Stephanopyxis palmeriana (Greville) Grunow, 1884 Thalassionema nitzschioides (Grunow) Mereschkowsky, 1902 Thalassiosira eccentrica (Ehrenberg) Cleve, 1904 Toxarium undulatum Bailey, 1854 Total abundance of diatoms Dinophyta Actiniscus pentasterias (Ehrenberg) Ehrenberg, 1854 Akashiwo sanguinea (K. Hirasaka) G. Hansen & Ø. Moestrup in N. Daugbjerg, G. Hansen, J. Larsen, & Ø. Moestrup, 2000 Cochlodinium polykrikoides Margalef, 1961 Dinophysis acuminata Claparède & Lachmann, 1859 Dinophysis caudata Saville-Kent, 1881 Dinophysis tripos Gourret, 1883 Gonyaulax birostris F. Stein, 1883 Gonyaulax cochlea Meunier 1919 Gonyaulax digitalis (Pouchet) Kofoid, 1911 Gonyaulax fusiformis H.W.Graham, 1942 Gonyaulax hyalina Ostenfeld & Schmidt, 1901 Gonyaulax polygramma (Pouchet) Kofoid, 1911 Gonyaulax spinifera (Pouchet) Kofoid, 1911 Lepidodinium chlorophorum (M. Elbrächter & E.Schnepf) Gert Hansen, L.Botes & M. de Salas 2007 Lingulodinium polyedrum (F.Stein) J. D. Dodge, 1989 Metaphalacroma skogsbergii Tai, 1934 Nematodinium armatum (Dogiel) Kofoid & Swezy, 1921 Ornithocercus magnificus Stein, 1883 Peridinium quinquecorne Abé, 1927 Phalacroma favus Kofoid & J. R. Michener, 1911 Prorocentrum gracile Schütt, 1895 Prorocentrum micans Ehrenberg, 1833 Prorocentrum rhathymum Loeblich, Sherley & Schmidt, 1979 Protoceratium reticulatum (Claparède & Lachmann) Bütschli, 1885 Protoperidinium abei (Paulsen) Balech, 1974 Protoperidinium claudicans (Paulsen) Balech, 1974 Protoperidinium longipes Balech, 1974 Protoperidinium sp. 1 Protoperidinium sp. 2 Scrippsiella spinifera G.Honsell & M. Cabrini, 1991 Tripos dens (Ostenfeld & Schmidt) F. Gomez, 2013 Tripos fusus (Ehrenberg) F. Gómez, 2013

Sample A cells L−1 1600 400 400 200 2400 1400 18200 3200 1000 200 1200 400 400 200 400 400 200 1200 1200 200 200 200 2400 400 1200 1200 400 400 41200 200 2800 200 600 200 200 2400 600 200 4200 401200 200 200 600 200 2200 200 200 200 400 400

4200 200 200

Sample B cells L−1

Sample C cells L−1

200

400

200 200

600 200 200 2800

2400 1200 24600 1800 800 600 200 400 200 400

1600

2800 800 200 200 200 200 200 200 400 200

200 400 1200 400 2400 2000

1200 800 1600

39800

14800

200 400 4400 1400 200 3600 400 400 2400 892800 200 200 200 200 400 400 200 400 200 200 400 200 200 400 1200 200 400

1600 7200 200 3200 1200 5200 1200 200 1200 1342600 400 400 400 600 200 200 600 400 5600 200

GÁRATE-LIZÁRRAGA et al.

Table 1. Continued. Microalgae species Tripos furca (Ehrenberg) F. Gómez, 2013 Total abundance of dinoflagellates Cyanobacteria Anabaena sp. Merismopedia sp. Lyngbya majuscula (Dillwyn), Harvey, 1833 Richelia intracellularis J. Schmidt in Ostenfeld & J. Schmidt, 1901 Euglenophyta Euglena sp. Prasinophyta Pterosperma sp. Total abundance of cyanobacteria, euglenophytes and prasinophytes Microphytoplankton Nanophytoplankton Phytoplankton total abundance

for these species. In G. spinifera, G. polygramma (Fig. 7), Lingulodinium polyedrum (F.Stein) J.D. Dodge, 1989 (Fig. 21), and perhaps others members of the group, ecdysis is frequently seen (Kofoid, 1911; Marasovic, 1989). Temporary cysts quickly turn into a vegetative, motile state when conditions become again favorable, thus allowing cells to withstand short-term environmental fluctuations (Anderson, 1998). Abundances of G. spinifera in the three samples were 401, 892, and 1342 × 103 cells L–1, respectively. Densities of G. spinifera in this report were high, compared to a previous record (Gárate-Lizárraga, 2013), but lower than that of Margalef (1956) from blooms in Ría de Vigo (Spain), by Riaux-Gobin & Lassus (1989) in the Riviere de Morlaix in Brittany, or that of Praseno et al. (1999) off the coast of western Sumatra in the Indian Ocean. Although this is the first bloom of G. spinifera in the eastern Pacific along the coast of Mexico, this species is widely distributed in the Gulf of California (Okolodkov & Gárate-Lizárraga, 2006; Esqueda-Lara & Hernández-Becerril, 2010). Blooms of G. spinifera are responsible for mass die-offs of marine biota and cause severe damage to fisheries (Praseno et al., 1999; Fukuyo et al., 2003; Riccardi et al., 2009). A massive bloom of G. spinifera (9 × 106 cells L–1) formed on the west coast of Vancouver Island, BC, Canada, caused a substantial shellfish dieoff due to hypoxia in Barkley Sound (Forbes et al., 1990). Many mussel farms along the Emilia Romagna coast of Italy (northwestern Adriatic Sea) were closed due to excessive levels of yessotoxin (>1 mg YTX equivalents/ kg mussels; Riccardi et al., 2009). Yessotoxin (YTX) is a disulfated polyether toxin that was ﬁrst isolated from the yesso scallop (Patinopecten yessoensis Jay, 1857) collected in Japan (Murata et al., 1987). A bloom of G. spinifera occurred recently north of San Francisco in Au-

Sample A cells L−1

Sample B cells L−1

Sample C cells L−1

200 422400

200 912000

1372800

4200 8200 5200 4000

1600 3800 10200 4800

2200 8600

200

200 22000 485800 115600 601400

20600 972400 23200 995600

400 11200 1398800 97600 1496400

gust 2011, and extended 80 km along the coast causing a massive die-off of wild marine invertebrates (Rogers-Bennett et al., 2012). YTX is produced by G. spinifera and other plankton, including Protoceratium reticulatum (Claparède & Lachmann) Bütschli, 1885 and L. polyedrum (Rhodes et al., 2006). Although these three species were found in our samples, no fish or invertebrates were apparently killed by this bloom, which was very short and was rapidly dispersed by tides and wind-forcing. On the other hand, four species producers of domoic acid were recorded: Dinophysis acuminata, D. caudata, D. tripos (Fig. 29), and Phalacroma favus (Fig. 30). These species occurred in low densities and could also represent a health public if they proliferate. Microalgae blooms are still monitored at permanent monitoring stations in Bahía de La Paz. This monitoring program provides data on the occurrence, distribution, and possible causes of harmful microalgae blooms. New records During this bloom, several taxa of microalgae were new records for the Gulf of California coasts: the dinoflagellates Gonyaulax hyalina (Figs.16–17), Gonyaulax birostris (Fig. 18), and Gonyaulax fusiformis (Fig. 19); the dinoflagellates Gonyaulax cochlea (Fig. 9) and Lepidodinium chlorophorum (M. Elbrächter & E. Schnepf) Gert Hansen, L. Botes & M. de Salas 2007 (Fig. 24), the prasinophyte Pterosperma sp. (Fig. 40) and the diatom Arcuatasigma challengeriense (Fig. 52) are new records for the Mexican Pacific. The diatom Asteromphalus arachne (Fig. 50) is a new record for Bahía de La Paz. Because the samples were taken close to the shore, some uncommon species of cyanobacteria, such as Merismopedia sp. (Fig. 59), Anabaena sp. (Fig. 60) and Lyngbya majuscula (Fig. 61), were also collected.

BLOOM OF Gonyaulax spinifera

Figures 2–21. Vegetative cells (2–4) and temporary cysts (5–6) of Gonyaulax spinifera, vegetative cells (7) and temporary cyst (8) of G. polygramma, vegetative cells (9) and temporary cysts (10) of Gonyaulax cochlea, vegetative cells (11–12) and temporary cysts of Scrippsiella spinifera (13–14), Gonyaulax digitalis (15), vegetative cell (16) and temporary cyst (17) of Gonyaulax hyalina, G. birostris (18), G. fusiformis (19), Protoceratium reticulatum (20), and Lingulodinium polyedrum (21). White arrows indicate the broken theca and the temporary cysts.

ACKNOWLEDGMENTS

REFERENCES

The project was funded by Instituto Politécnico Nacional (SIP-20121152, SIP-20130549). I.G.L. is a COFAA and EDI fellow. We thank M.C. Ramírez-Jáuregui (ICMyL-UNAM, Mazatlán) for the literature search. Thanks to José Ochoa (CICESE Unidad La Paz) for the data on tides. We also thank two anonymous referees for their helpful comments and suggestions.

Anderson, D.M. 1998. Physiology and bloom dynamics of toxic Alexandrium species, with emphasis on life cycle transitions, 29–48 In: Anderson, D.M., A.D. Cembella, & G.M. Hallegraeff, (Eds.). Physiological Ecology of Harmful Algal Blooms. NATO ASI Series. Series G: Ecological Sciences, Vol. 41. Berlin: Springer.

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Figures 22–41. Cochlodinium polykrikoides (22), Akashiwo sanguinea (23), Lepidodinium chlorophorum (24), Ceratoperidinium falcatum (25), Actiniscus pentasterias (26), Nematodinium armatum, white arrow indicates the ocelloid (27), Metaphalacroma skogsbergii (28), Dinophysis tripos (29), Phalacroma favus (30), Ornithocercus steinii with abundant coccoid cyanobacteria cf. Synechococcus (31), Prorocentrum rhathymum (32), P. micans (33), Protoperidinium sp. 1 (34), P. abei (35), Protoperidinium sp. 2 (36), P. claudicans (37), P. longipes (38), Peridinium quinquecorne, white arrow indicates the bright red stigma in the sulcal area (39), phycoma-stage of Pterosperma sp. (40), and Euglena sp. (41).

Esqueda-Lara, K. & D.U. Hernández-Becerril. 2010. Dinoflagelados microplanctónicos marinos del Pacífico central de México (Isla Isabel, Nayarit y costas de Jalisco y Colima). Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México. 206 p. Fensome, R.A., F.J.R. Taylor, G. Norris, W.A.S. Sarjeant, D.I. Wharton & G. L. Williams. 1993. A classification of living and fossil

dinoflagellates. Micropaleontology Special Publication 7, Hanover, PA: Sheridan Press, 351 p. Forbes, J.R., G. A. Borstad & R.E. Waters. 1990. Massive bloom of Gonyaulax spinifera along the west coast of Vancouver Island. Red Tide Newsletter, 3(4): 2–3. Fukuyo, Y., Y. Sako, K. Matsuoka, I. Imai, M. Takahasi & M. Watanabe. 2003. Biological

BLOOM OF Gonyaulax spinifera

Figures 42–61. Chaetoceros diversus (42), C. socialis, with of epiphytic diatoms (white arrow) (43), C. coarctatus, white arrow indicates to Vorticella oceanica (44), Chaetoceros sp. (45), C. didymys (46), Hemiaulus membranaceus, white arrow indicates the cyanobacteria Richelia intracellularis (47), Asterionellopsis glacialis (48), Stauroneis membranacea (49), Asteromphalus arachne (50), Fragilariopsis doliolus with Vorticella sp. (51), Arcuatasigma challengeriense (52), Nitzschia longissima (53), Helicotheca tamensis (54), Toxarium undulatum (55), Biddulphia tridens (56), Odontella alternans (57), Odontella aurita var. obtusa (58), Merismopedia sp. (59), Anabaena sp. (60), and Lyngbya majuscula (61).

character of red-tide organisms, 61–153 In: Okaichi, T. (Ed.), Red Tides. Terra Scientific Publishing Company, Tokyo.

2001. Red tides along the coasts of Baja California Sur, México (1984 to 2001). Oceánides, 16(2):127–134.

Gárate-Lizárraga, I. 2013. Bloom of Cochlodinium polykrikoides (Dinophyceae: Gymnodiniales) in Bahía de La Paz, Gulf of California. Mar. Poll. Bull., 67: 217–222.

Gárate-Lizárraga, I., D.J. López-Cortés, J.J. Bustillos-Guzmán & F. Hernández-Sandoval. 2004. Blooms of Cochlodinium polykrikoides (Gymnodiniaceae) in the Gulf of California, Mexico. Rev. Biol. Trop., 52: (1):51–58.

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Gárate-Lizárraga, I., M.S. Muñetón-Gómez. & V. Maldonado-López. 2006. Florecimiento del dinoflagelado Gonyaulax polygramma frente a la Isla Espíritu Santo, Golfo de California (Octubre 2004). Rev. Inv. Mar., 27(1): 31–39. Gárate-Lizárraga, I., C.J. Band-Schmidt, F. Aguirre-Bahena & T. Grayeb-del Álamo. 2009. A multi-species microalgae bloom in Bahía de La Paz, Gulf of California, Mexico (June 2008). CICIMAR Oceánides, 24(1): 1−15. Gómez-Valdés, J., J.A. Delgado & J.A. Dwora. 2003. Overtides, compound tides, and tidal-residual current in Ensenada de La Paz lagoon, Baja California Sur, Mexico. Geof. Inter., 42(4): 623–634. Guiry, M.D. & Guiry, G.M. 2014. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www. algaebase.org; (accessed 25 February 2014). Kofoid, C.A. 1911. Dinoflagellata of the San Diego Region, IV. The genus Gonyaulax with notes on the skeletal morphology. University of California Publications in Zoology, 8: 187–300. Lewis, J., A. Rochon & I. Harding. 1999. Preliminary observations of cyst-theca relationships in Spiniferites ramosus and Spiniferites membranaceus (Dinophyceae). Grana, 38: 113–124. Marasovic, I. 1989. Encystment and excystment of Gonyaulax polyedra during a red tide. Est. Coast. Shelf Sci., 28: 35-41 Margalef, R. 1956. Estructura y dinámica de la “purga de mar” en la Ría de Vigo. Inv. Pesq., 5: 113–134. Millán-Núñez, E. 1988. Marea roja en Bahía de Los Ángeles. Cienc. Mar., 14: 51–55.

Murata, M., A.M. Legrand, Y. Ishibashi, T. Yasumoto. 1987. Isolation and structure of yessotoxin, a novel polyether compound implicated in diarrhetic shellﬁsh poisoning. Tetrahedron Letter, 28: 5869–5872. Okolodkov, Y.B. & I. Gárate-Lizárraga. 2006. An annotated checklist of dinoflagellates from the Mexican Pacific. Acta Bot. Mex., 74(1): 1–154. Riccardi, M., F. Guerrini, F. Roncarati, A. Milandri, M. Cangini, S. Pigozzi E. Riccardi, A. Ceredi, P. Ciminiello & C. Dell’Aversano. 2009. Gonyaulax spinifera from the Adriatic Sea: Toxin production and phylogenetic analysis. Harmful Algae, 8: 279–290. Rhodes, L., P. McNabb, M. de Salas, L. Briggs, V. Beuzenberg & M. Gladstone. 2006. Yessotoxin production in Gonyaulax spinifera. Harmful Algae, 5: 148–155. Riaux-Gobin, C. & P. Lassus. 1989. Conditions hydroclimatiques d’une eau colorée à Gonyaulax spinifera (dinoflagellé) dans une ria du Nord-Finistère. Bot. Mar., 32: 491–498. Rogers-Bennett, L., R. Kudela, K. Nielsen, A. Paquin, C. O’Kelly, G. Langlois, D. Crane & J. Moore. 2012. Dinoflagellate bloom coincides with marine invertebrate mortalities in northern California. Harmful Algae News, 46: 10–11. Taylor, F.J.R. 1976. Dinoﬂagellates from the International Indian Ocean Expedition-A report on material collected by the R.V. ‘Anton Brun’ 1963–1964. Bibliotheca Botanica, Vol. 132, E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart. Utermöhl, H. 1958. Zur Vervollkommung der quantitativen Phytoplankton Methodik. Mitte. Int. Ver. Theor. Angew. Limnol., 9: 1–38.

CICIMAR Oceánides 29(1): 19-22 (2014)

NOTA FIRST NESTING RECORDS OF THE AMERICAN AVOCET (Recurvirostra americana) AND WHITE IBIS (Eudocimus albus) AT LAGUNA OJO DE LIEBRE, BCS, MÉXICO Primer registro de anidación de Avoceta americana (Recurvirostra americana) e Ibis blanco (Eudocimus albus) en Laguna Ojo de Liebre, BCS, México. Resumen: El humedal de Guerrero Negro es uno de los sitios de mayor relevancia para las aves acuáticas en México y es un sitio importante para su reproducción. Esta nota describe los primeros registros de anidación de Avoceta americana (Recurvirostra americana) e Ibis blanco (Eudocimus albus) en este humedal, incrementando con esto a 24 el número de especies cuya anidación se ha registrado en la zona. Ayala-Perez, V.1, R. Carmona1, N. Arce1 & J. Rivera2. 1Departamento de Biología Marina. Universidad Autónoma de Baja California Sur. A.P. 19-B. 23080. La Paz, Baja California Sur, México. 2Exportadora de Sal, S. A. de C. V., Guerrero Negro, Baja California Sur, México. email. ayala.vic@hotmail.com Ayala-Perez, V., R. Carmona, N. Arce & J. Rivera. 2014. First nesting records of the american avocet (Recurvirostra americana) and white ibis (Eudocimus albus) at Laguna Ojo de Liebre, BCS, México. CICIMAR Oceánides, 29(1): 19-22.

The Guerrero Negro wetland complex (GN hereinafter) is an important breeding area for several species of waterbirds (Bancroft, 1927; Grinnell, 1928; Danemann & Carmona, 2000; Castellanos et al., 2001). Bancroft (1927) recorded the presence of 18 species of reproductive waterbirds at Ojo de Liebre lagoon. Subsequently, two new records were included: the Great Egret, Ardea alba (Massey & Palacios, 1994) and the Laughing Gull (Leucophaeus atricilla; Castellanos et al., 1994). While for the artificial wetland created by Exportadora de Sal (ESSA), Danemann and Carmona (2000) included the record of the Gull-billed Tern (Gelochelidon nilotica) and the Black Skimmer (Rynchops niger). Thus 22 species of waterbirds have been registered as breeders in GN. In this note we report the breeding of two species of waterbirds in Ojo de Liebre lagoon: the American Avocet (Recurvirostra americana) and the White Ibis (Eudocimus albus). This wetland has an extension of 57,000 ha and is located in the midwestern portion of the Baja California peninsula, within the Sebastian Vizcaíno bay, in northwestern Mexico. Adjacent to this wetland there is an artificial wetland created by ESSA (33,000 ha, Fig. 1). Both wetFecha de recepción: 11 de abril de 2013

lands are surrounded by the Vizcaíno Desert, and is part of the “El Vizcaino” Biosphere Reserve, a federal protected area (D.O.F., 1988). As part of a constant monitoring of waterbirds in GN, the Birds Laboratory of the Universidad Autónoma de Baja California Sur and ESSA, we have conducted monthly visits to the study area from 2006 to date. We go through the area in established routes, identifying and counting the birds using 10x binoculars and 1560x scopes. On June 24, 2007 we found three nests of American Avocet in ESSA, in the area called Salitrales 1-A (S1-A 27 ° 35’8 .18 “N, 114 ° 6’46 .23” W). The area is a mud flat with similar characteristics to the natural wetland, widely used by shorebirds (Ayala-Perez et al., 2012). The three nests were close to each other, in an area no greater than 16 m2. They consist of small cavities in the ground, with some branches of pickleweed (Salicornia spp.) and Iodine Bush (Allenrolfea occidentalis) arranged around these. Two of the nests had eggs, one with one egg and another with two. In the area we observed 16 adults, some of whom were displaying a distracting behavior typical of these birds when they are nesting (Robinson et al., 1997). The American Avocet is a common wintering species in GN (Howell & Webb, 2005), but their numbers are not high. A winter peak of 380 individuals has been observed, with around 60 individuals summering in the area (Carmona

Figure 1. Study Area. Sites are indicated where the nests of American Avocet and White Ibis were observed.. Fecha de aceptación: 12 de febrero de 2014

AYALA-PEREZ et al.

et al., 2011). Until 1998, nesting records of this species in the Baja California peninsula were restricted to the north in San Quintin Bay (Massey & Palacios 1994). The first nesting record of this species is for the summer of 1998 in La Paz, in the southern part of the peninsula, where at least five active nests were observed (Carmona et al., 2000). Guerrero Negro is located between those sites, so there exists the possibility that the species used the area as a breeding ground, but given the little ornithological effort in summer, and the large size of the wetland, it had not been located previously. With respect to the second record, we sighted a couple of White Ibis each time on July 27, 2010 and July 23, 2011, at Isla Piedra located in the middle of Ojo de Liebre lagoon (27°42’20.70”N, 114° 9’33.18”W), apparently they were nesting. However, these records could not be verified, because there were significant numbers of nests of other birds, such as the Reddish Egret (Egretta rufescens) and the Western Gull (Larus occidentalis); besides our presence may have disturbed the birds. On May 22, 2012 we again sighted a couple of White Ibis on the same place, this time the nest was observed directly. The nest was located on a scrub of Iodine Bush and pickleweed, and it

was built with the same material. We also observed both parents and two chicks (Fig. 2a and b). Considering that the nearest breeding site to GN is located about 150 km south in Laguna San Ignacio (Massey & Palacios, 1994; Howell & Webb, 2005), this record could signify a northern extension of its breeding range. The White Ibis in GN is considered a common winter visitor (Howell & Webb, 2005). In 2004 we started to document sporadic observations of juveniles of the species. Since 2008 its sightings have been more common and include adult birds. The White Ibis is a nomadic species with high dispersion after the breeding season, mainly juveniles (Heath et al., 2009). Different studies (Heath, 2009; Frederick et al., 1996) document that the White Ibis is a nomad breeding species adapted to exploit food resources available in a given site. These nomadic tendencies and opportunistic features explain the settlement of a breeding pair in GN because of the available resources in the area. Guerrero Negro is one of the most important sites for waterbirds in the Baja California peninsula and one of the most relevant in México, both during migration and wintering periods (SEMARNAT, 2008; Carmona et al.,

Figure 2. Nest of White Ibis: (a) shows an adult beside the nest, and (b) shows the nest with two chicks.

NEW RECORDS OF BREEDING WATERBIRDS

2011), and integrate also an important breeding area. Although the avifauna of the area is well documented (Page et al., 1997; Carmona et al., 2011), the recording of new species nesting in GN underscores the biological importance of the wetland and requires continuous monitoring. We thank all facilities granted by Exportadora de Sal S.A. de C.V, especially Edmundo Elorduy and Martín Domínguez for their logistic support, both in the field and in their hosting facility. Reviews by Glen Coady, Gerard Binsfeld and anonymous reviewers are greatly appreciated. REFERENCES Ayala-Perez, V., R. Carmona & N. Arce. 2012. Efecto de la Marea en el Uso de Diferentes Zonas por las Aves Playeras: Comparación entre un Humedal Natural y uno Artificial en Guerrero Negro, Baja California Sur, México. Académica Española. 88 p. Bancroft, G. 1927. Breeding birds of Scammon’s Lagoon, Lower California. Condor, 29: 29-57. Carmona, R., C. Carmona, J. A. Castillo-Guerrero & E. M. Zamora-Orozco. 2000. Nesting records of American Avocet and Black-Necked Stilt in Baja California Sur, México. Southwest. Nat., 45: 523-524.

Danemann, G. & R. Carmona. 2000. Breeding birds of the Guerrero Negro saltworks, Baja Califomia Sur, México. Western Birds, 31: 195-199. Diario Oficial de la Federación (D.O.F.). 1988. Decreto de la Reserva de la Biosfera “El Vizcaíno”, ubicada en el Municipio de Mulegé, B.C.S. Noviembre 30 de 1998. México, D. F. Tomo CDXXII, No. 22. Frederick, P. C., K. L. Bildstein, B. Fleury & J. Ogden. 1996. Conservation of large, nomadic populations of White Ibises (Eudocimus albus) in the United States. Conserv. Biol. 10: 203-216. Grinnell, J. 1928. A distributional summation of the omithology of Lower Califomia. Univ. Calif. Publ. Zool., 32: 1-300. Heath, J. A., P. Frederick, J. A. Kushlan & K. L. Bildstein. 2009. White Ibis (Eudocimus albus). In: A. Poole (Ed.). The Birds of North America. Ithaca: Cornell Lab of Ornithology. http://bna.birds.cornell.edu/bna/species/009; última consulta: 18. II. 2013. Howell, S. N. G. & S. Webb. 2005. A Guide to the Birds of Mexico and Northern Central America. Oxford Univ. Press, Oxford, England. 851 p Massey, W. B. & E. Palacios. 1994. Avifauna of the wetlands of Baja California, Mexico: Current status. Studies Avian Biol., 15: 45-57.

Carmona, R., N. Arce, V. Ayala-Pérez & G. D. Danemann. 2011. Seasonal abundance of shorebirds at the Guerrero Negro wetland complex, Baja California Sur, Mexico. Wader Study Group Bull., 118: 40-48.

Page, G. W., E. Palacios, L. Alfaro, S. González, L. E. Stensel & M. Jungers. 1997. Numbers of wintering shorebirds in coastal wetlands of Baja California, México. J. Field Ornithol., 68: 562574.

Castellanos, A., F. Salinas & A. Ortega-Rubio. 2001. Inventory and conservation of breeding waterbirds at Ojo de Liebre and Guerrero Negro lagoons, Baja California Sur, México. Cienc. Mar., 27: 351-373.

Robinson, J., A. Lewis, W. Oring, J. P. Skorupa & R. Boettcher. 1997. American Avocet (Recurvirostra americana). In: A. Poole (Ed.). The Birds of North America. Ithaca: Cornell Lab. of Ornithology. http://bna.birds.cornell.edu/bna/species/275. última consulta: 18. II.2013.

Castellanos, A., F. Salinas-Zavala & A. Ortega-Rubio. 1994. First nesting record of the laughing gull for the west coast of Baja California, Mexico. Western Birds, 25: 203–205.

SEMARNAT. 2008. Estrategia para la Conservación, Manejo y Aprovechamiento Sustentable de las Aves Acuáticas y su Hábitat en México. Dirección General de Vida Silvestre. México D.F. 92 p.

CICIMAR Oceánides 29(1): 23-28 (2014)

NOTA DISTRIBUTION OF Amylax triacantha AND A. triacantha var. buxus nov. comb. (DINOPHYCEAE) ALONG THE PACIFIC COAST OF MEXICO Distribución de Amylax triacantha y A. triacantha var. buxus nov. comb. (Dinophyceae) a lo largo de la costa Pacífico de México RESUMEN. El género Amylax está conformado por dos especies, A. triacantha y A. buxus, las cuales se encuentran principalmente distribuidas en aguas frías y templadas del hemisferio norte. En este estudio se presenta la distribución de ambos taxones a lo largo del Pacífico mexicano y se propone una nueva combinación para A. buxus, i.e. , A. triacantha var. buxus. Se utilizaron muestras de fitoplancton de botella y red obtenidas en diferentes áreas de la costa del Pacífico mexicano durante el periodo 2006-2013. Se registró A. triacantha por primera vez en Bahía de Los Ángeles, Bahía San Lucas, Loreto, Bahía de Acapulco y Salina Cruz, Oaxaca. En tanto que A. triacantha var. buxus se presenta por primera ocasión en Cuenca Alfonso, Bahía de Los Ángeles, Bahía San Lucas y Salina Cruz. Ambos taxones se presentaron en un intervalo de temperatura de 21 a 25 °C. De acuerdo con estos resultados, se concluye que estos taxones también están presentes en aguas tropicales y subtropicales.

Gárate-Lizárraga, I. Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Departamento de Plancton y Ecología Marina, Apartado postal 592, La Paz, Baja California Sur 23096, México. email: igarate@ipn.mx Gárate-Lizárraga, I. 2014. Distribution of Amylax triacantha and A. triacantha var. buxus nov. comb. (Dinophyceae) along the Pacific coast of Mexico. CICIMAR Oceánides, 29(1): 23-28.

Dinoflagellates are unicellular protists that exhibit a great diversity of forms. Two cell types can be distinguished on the basis of the cell wall covering or theca. The naked or unarmored forms have an outer plasmalemma surrounding a single layer of flattened vesicles. Armored dinoflagellates have cellulose or other polysaccharides within each vesicle, giving the cells a more rigid, inflexible wall. These cellulose plates are arranged in distinct patterns named tabulations (Fensome et al., 1993). The species of the order Gonyaulacales F.J.R. Taylor, 1980 exhibit an asymmetrical plate pattern. The plate tabulation is critical for identification and they lack the characteristic channel plate of the peridinoids (Steidinger & Tangen, 1997). The genus Amylax Meunier, 1910 belongs to the order Gonyaulacales: small, fairly delicate cells with a distinct apical horn and two to several antapical spines. The typical plate formula is Po, 3′, 3a, 6″, 6c, 7–8s, 6′′′ 1p, 1′′′′ according to Hoppenrath et al. (2010). Plate 1′ shows ventral pore on its right side near the posterior end. Six species have Fecha de recepción: 10 de marzo de 2014

been assigned to the genus in the past but currently only two species that are morphologically very similar are recognized, i.e., A. buxus (Balech) Dodge, 1989 and A. triacantha (J�� ö�� rgensen) Sournia, 1984 (Hoppenrath et al., 2010). Some authors consider that A. buxus is just a form of A. triacantha (Hoppenrath et al., 2010). Koike and Takishita (2008) determined the nuclear SSU rRNA gene sequence for the Amylax species. They found that the two Amylax species have identical nuclear SSU rRNA gene sequences. A proposal for a new variety of A. triacantha is made here. An extended range for the two taxa is also reported for the Pacific coast of Mexico. Samples were collected with van Dorn bottles and a phytoplankton net with 20 µm mesh. Samples were collected at Station 1 (off the PEMEX landing) in Bahía de La Paz (Fig. 1) from January 2009 through December 2013 using surface tows, and vertical hauls of shallow depth (15 m) with a 20 µm mesh hand net. A portion of each collection from each tow was immediately fixed with acidified Lugol solution and later preserved in 4% formalin. A sub-sample was taken for live phytoplankton observations. Additional surface water samples were collected for identification and cell counting. At Station 2 (Cuenca Alfonso), nine vertical net hauls were conducted from 60 m to surface from February through December 2010 (Fig. 1). Eight net phytoplankton samples were collected in Loreto from February to December 2008. Ten samples were collected in Bahía de Los �� Á�� ngeles from February through December 2006. Nine vertical net hauls were made from 25 m depth to the surface at Stations 3 and 4

Figure 1. ) Sampling sites located at different areas from the Mexican Pacific. 1-2) Bahía de La Paz, 3) Bahía San Lucas, 4) Loreto, 5) Bahía de Los Ángeles, 6) Bahía Magdalena, 7) Bahía de Acapulco, and 8) Salina Cruz. ) Previous records of Amylax triacantha by Alonso-Rodríguez et al. (2003), Ceballos-Corona (2006), Okolodkov & GárateLizárraga (2006), Poot-Delgado (2006), Gárate-Lizárraga et al. (2007). Fecha de aceptación: 07 de mayo de 2014

GÁRATE-LIZÁRRAGA

from November 2012 to July 2013. Three samples were collected in Bahía de Acapulco in November 2009. Four samples were collected from 26 through 29 May 2008 offshore Puerto Salina Cruz, Oaxaca. Seawater temperature was recorded at all sampling stations with a bucket thermometer. Temperature at Station 2 (Cuenca Alfonso) was recorded with a data recorder (SeaBird 19 CTD). Cell counts were made in 5 mL settling chambers (Utermöhl, 1958) with an inverted Carl Zeiss phase-contrast microscope. Cells were measured under a compound Olympus CH2 microscope. A digital Konus camera (8.1 MP) was used for recording images. Description: Amylax triacantha (Jörgensen) Sournia, 1984; p. 350; Dodge, 1989, p. 292, figs. l (J, K) p. 29, 30–33; Hoppenrath et al., 2010; p. 18, fig. 73o-p, Omura et al., 2012; p. 103, figs. a-b. Basionym: Gonyaulax triacantha Jörgensen 1899: p 39. Synonym: Amylax lata Meunier, 1910: p 51, figs 24–27. Amylax triacantha was observed only in phytoplankton net samples, therefore no quantitative data are shown here. This species occurred at temperatures ranging from 21 to 25 °C in most of the areas, and at 29 °C in Bahía de Acapulco. A. triacantha cells are small and delicate (Figs. 2–4), somewhat flattened with a prominent apical horn and two or five antapical spines. In some specimens only one antapical spine is observed. Sides of the epitheca are concave leading to the long tapering apical horn. Sides of the hypotheca are almost straight and the antapex is squared to slightly round, with spines of various lengths arising from the antapical and other plates. The girdle is cavozone (deeply excavated); displaced by just over one girdle width and the two ends do not overlap. The sulcus is straight, wide posteriorly, and narrows in the vicinity of the girdle, but not invading the epitheca. A. triacantha possess a ventral pore, between the 1′ and 6′ plates, which is a criterion that distinguishes it from A. buxus (Balech, 1967; Koike & Takishita, 2008). Single cells ranged from 40 to 62 µm in length without spines and 30– 45µm in width (n=30). It is well known that observations of live cells of A. tricantha in epifluorescence microscopy they emitted bright yellow-orange fluorescence under blue light excitation, typical of cryptophycean phycoerythrin (Okolodkov, 1999; Koike & Takishita, 2008; Park et al., 2013). In this study, some cells of A. tricantha clearly contain plastids of the cryptophyte (Fig. 4) Local distribution: First records of A. triacantha are misidentifications of Peridinium quinquecorne (Cortés-Altamirano, 2002; Cortés-Altamirano et al., 2006), which caused red tides in Bahía de Mazatlán. Therefore, A. triacantha is not a causative agent of red tides along the coasts of Mexico. Alonso-Rodríguez et al. (2003: p. 114, Fig. 2) first reported A. tria-

cantha in Bahía de Mazatlán. Okolodkov & GárateLizárraga (2006) and Gárate-Lizárraga et al. (2007) reported it in Bahía de La Paz and Bahía Magdalena. It was also recorded in Laguna Macapule, Sinaloa (Poot-Delgado, 2006: p. 143, Fig. 1, pl. 6). Recently, A. triacantha (Fig. 18, p. 74) was observed in the coast of Michoacán (Ceballos-Corona, 2006). In this study, I observed for the first time A. triacantha in Bahía de Los Ángeles, Bahía San Lucas, at Loreto, Bahía de Acapulco, and Salina Cruz. This species is rare along the Mexican coast, observed mainly in phytoplankton net samples (Ceballos-Corona, 2006; this study). According to Meave del Castillo (2014), A. triacantha is an invasive species along the Pacific coast of Mexico. I regard this hypothesis as untenable because there are insufficient studies of marine phytoplankton in this area and because it is not a common species. General distribution: Mainly observed in cold to temperate waters of the Northern Hemisphere (Lebour, 1925; Balech, 1967, 1977; Dodge, 1982; Okolodkov, 1996; Bérard-Therriault et al., 1999; Koike & Takishita, 2008; Omura et al., 2012). The first finding of A. triacantha in the Northeastern Pacific (California) was recorded by Kofoid (1911) and later recorded in British Columbia, Canada by Wiles (1928). Description: Amylax triacantha var. buxus (Dodge) Gárate-Lizárraga, 2014, nov. comb.: Dodge, 1989, Fig. 1 (L) 29; Balech, 1967: p. 106, figs. 100–107; Hoppenrath et al., 2010: p. 181, fig. 73q-r: Omura et al., 2012: p. 103, figs. a-f. Basionym: Gonyaulax buxus Balech, 1967: p. 106, figs. 100–107. Synonym: Amylax buxus (Balech) Dodge, 1989, Fig. 1 (L) 29; Main part of the epitheca of A. triacantha var. buxus cells is truncated with convex sides leading to an extended apical horn (Figs. 5–7). The hypotheca is rounded with one large antapical spine arising from the 1′′′′ plate and one or two small spines. Girdle bounded by protruding lists, sulcus, and tabulation, as in A. triacantha. Thecal plates are thick and ornamented by a series of depressions, some of which contain trichocyst pores. A. triacantha var. buxus does not possess a ventral pore between the 1′ and 6′ plates (Balech, 1967; Koike & Takishita, 2008). This characteristic and the high similarity in the nuclear SSU rRNA gene sequence for the Amylax species (Koike and Takishita, 2008; Park et al., 2013) allow me to propose the new combination: A. triacantha var. buxus. In single cells the length without spines ranged from 34 to 48 µm and the width from 26 to 30 µm (n=30). Cells of A. tricantha var. buxus also contain plastids of a cryptophyte (Fig. 6). A. triacantha var. buxus was mainly observed in samples for phytoplankton net. Quantitative data (200–800 cells L–1) were previously reported by Gárate-Lizárraga

DISTRIBUTION OF Amylax triacantha

Figures 2–7. Specimens of Amylax. Cells of A. triacantha (Figs. 2–4) and A. triacantha var. buxus (Figs. 5–7) observed under the light microscope. White arrowheads indicate plastids of cryptophytes.

(2012). Similar densities were observed in Bahía San Lucas in samples collected in March 2013. This species occurred within a temperature range of 22– 25 °C. Local distribution: First records of A. triacantha var. buxus are from Bahía de La Paz (Gárate-Lizárraga, 2012). A wide range extension for A. triacantha var. buxus along the Mexican Pacific is reported here because it was found in Cuenca Alfonso, Bahía de La Paz, Bahía de Los Ángeles, Bahía San Lucas, and Salina Cruz. General distribution: Mainly observed in cold to temperate and waters of the Northern Hemisphere (Balech, 1967, 1977; Koike & Takishita, 2008; Hoppenrath et al., 2010; Omura et al., 2012). In the past, it is possible that Amylax species were confused with certain Gonyaulax species.

For this reason, the geographical distribution of Amylax species is not well known. In this study, Amylax triacantha was easily distinguished by its peculiar angular body outline. A. triacantha var. buxus is more rounded. According to these results, it is possible to conclude that they are also distributed in tropical and subtropical waters.

ACKNOWLEDGMENTS The study was partially funded by Instituto Politécnico Nacional (SIP-20100870, SIP-20100192, SIP-20121152, and 20130549) and CONACYT (grant 47310F). The author is a COFAA-IPN and EDI-IPN fellow. I thank M.C. Ramírez-Jáuregui (ICMyL-UNAM, Mazatlán) for the literature search. Fig. 4 was taken from Alonso-Rodríguez et al. (2003). I also thank two anonymous referees for their helpful comments and suggestions.

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REFERENCES Alonso-Rodríguez, R., F. Páez-Osuna & I. GárateLizárraga. 2004. El fitoplancton en la camaronicultura y larvicultura: importancia de un buen manejo. Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México y Comité Estatal de Sanidad Acuícola de Sinaloa, México. 147 p. Balech, E. 1967. Dinoflagelados nuevos o interesantes del Golfo de México y Caribe. Hidrobiología, 2: 77 -126. Balech, E. 1977. Cuatro especies de Gonyaulax sensu lato y consideraciones sobre el género (Dinoflagellata). Hidrobiología, 5(6): 115-136. Bérard-Therriault, L., M. Poulin & L. Bossé. 1999. Guide d’identification du phytoplancton marin de l’estuaire et du Golfe du Saint-Laurent incluant également certains protozoaires. Publication Spéciale Canadienne des Sciences Halieutiques et Aquatiques. 387 p. Ceballos-Corona, J.G.A. 2006. Análisis de los dinoflagelados potencialmente nocivos en el fitoplancton de la zona nerítica de la costa michoacana (enero-mayo 2004). Universidad Michoacana de San Nicolás de Hidalgo. Morelia, Michoacán, 165 p. Cortés-Altamirano, R. 2002. Mareas rojas: biodiversidad de microbios que pintan el mar. 29-41, In: Cifuentes, J. L. & J. Gaxiola-López (Eds.). Atlas de biodiversidad de Sinaloa. Colegio de Sinaloa. Guadalajara, Jalisco. Cortés-Altamirano R., M.F. Lavín, A.P. Sierra-Beltrán & M.C. Cortés-Lara. 2006. Una hipótesis sobre el transporte de microalgas invasoras desde el Pacífico oeste tropical hasta el Golfo de California por las corrientes marinas. Ciencias del Mar, UAS, 18: 19–26. Dodge, J.D. 1982. Marine dinoflagellates of the British Isles. Her Majesty’s Stationery Office, London. 303 p. Fensome, R.A., F.J.R. Taylor, G. Norris, W.A.S. Sarjeant, D.I. Wharton & G.L. Williams. 1993. A classification of living and fossil dinoflagellates. Am. Mus. Nat. Hist., Micropal. Spec. Publ., 7. 351 p.

Gárate-Lizárraga, I., C.J. Band-Schmidt, G. Verdugo-Díaz, M.S. Muñetón-Gómez & E.F. Félix– Pico. 2007. Dinoflagelados (Dinophyceae) del sistema lagunar Magdalena-Almejas. 141−170, In: Funes-Rodríguez, R., J. Gómez-Gutiérrez & J.R. Palomares-García (Eds.). Estudios ecológicos en Bahía Magdalena. CICIMAR-IPN, La Paz, Baja California Sur, México. Gárate-Lizárraga, I. 2012. Proliferation of Amphidinium carterae (Gymnodiniales: Gymnodiniaceae) in Bahía de La Paz, Gulf of California. CICIMAR Oceánides 27(2): 37–49. Hoppenrath, M., M. Elbrächter & G. Drebes. 2010. Marine phytoplankton: Selected microphytoplankton species from the North Sea around Helgoland and Sylt. 264 p., 87 figs. Koike, K. & Takishita, K. 2008. Anucleated cryptophyte vestiges in the gonyaulacalean dinoflagellates Amylax buxus and Amylax triacantha (Dinophyceae). Phycol. Res., 56(4): 301–311. Lebour, M.V. 1925. The dinoflagellates of Northern seas. Marine Biol. Assoc. U.K., Plymouth. 250 p. Meave del Castillo, M.E. 2014. Plancton marino introducido por agua de lastre. 289-308, In: Mendoza R. & P. Koleff (Eds.), Especies acuáticas invasoras en México. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, México. Okolodkov, Y.B. 1996. Biogeography of Arctic-boreal and bipolar dinoflagellates. Bot. J. Russ. Acad. Sci., 81: 18–30. Okolodkov, Y.B. 1999. Differentiation of phototrophic and heterotrophic dinoflagellates (Dinophyceae) by epifluorescence microscopy in the northern Greenland Sea. Bot. J. Russ. Acad. Sci., 84: 53–61. Okolodkov, Y.B. & I. Gárate-Lizárraga. 2006. An annotated checklist of dinoflagellates (Dinophyceae) from the Mexican Pacific. Acta Bot. Mex., 74: 1–154. Omura, T., M. lwataki, V.M. Borja, H. Takayama &Y. Fukuyo. 2012. Marine phytoplankton of the western Pacific. Kouseisha Kouseikaku, Tokyo, 160 p.

DISTRIBUTION OF Amylax triacantha

Park, M. G., M. Kim & M. Kang. 2013. A dinoflagellate Amylax triacantha with plastids of the Cryptophyte origin: Phylogeny, feeding mechanism, and growth and grazing responses. J. Eukariot Microbiol., 60: 363–376. Poot-Delgado, C.A. 2006. Estructura de la comunidad fitoplanctónica con énfasis en las especies tóxicas y/o nocivas de la laguna de Macapule, Sinaloa. Tesis de Maestría. Centro Interdisciplinario de Ciencias Marinas. La Paz, Baja California Sur, México. 145 p.

Steidinger, K.A. & K. Tangen. 1997. Dinoflagellates. 387–584, In: Tomas C.R. (Ed.). Identifying marine phytoplankton. Academic Press, New York. Utermöhl, H. 1958. Zur Vervollkommung der quantitativen Phytoplankton Methodik. Mitte. Int. Ver. Theor. Angew. Limnol., 9: 1–38. Wiles, G.H. 1928. Dinoflagellates and Protozoa from British Columbia. Vancouver Mus. Notes, 3: 1–41.

CICIMAR Oceánides 29(1): 29-31 (2014)

NOTA FIRST RECORD OF Reimerothrix floridensis (FRAGILARIACEAE: BACILLARIOPHYTA) FOR MÉXICO Primer registro de Reimerothrix floridensis (Fragilariaceae: Bacillariophyta) para México Resumen. Reimerothrix floridensis forma parte de un grupo de diatomeas con forma arqueada que generalmente son confundidas con Cylindrotheca closterium, Psammosynedra closterioides y Nitzschia longissima var. reversa. En este trabajo se presenta el primer registro de la diatomea arqueada Reimerothrix floridensis, recolectada en Dzilam de Bravo (costa norte de la Península de Yucatán) en el extremo sur del Golfo de México. Este hallazgo se realizó en el marco de la identificación de las especies de diatomeas que conformaron una proliferación de fitoplancton suscitada en las costas de la Península de Yucatán durante 2011, y en donde C. closterium y N. longissima var. reversa fueron especies dominantes. Las características de R. floridensis coinciden con la descripción original de la especie, excepto por las areolas asociadas al sternum. Dado que esta especie solo había sido registrada en la Bahía de Florida, su observación en México en la costa norte de la Península de Yucatán representa su registro más sureño, lo cual extiende el rango geográfico de esta especie. Por otra parte, debido a que la observación de R. floridensis se realizó durante la presencia de una proliferación de C. closterium y N. longissima, especies con las que generalmente es confundida, se pone de manifiesto la importancia de realizar determinaciones taxonómicas cuidadosas acompañadas de descripciones detalladas que den certeza a los estudios ecológicos.

Hernández-Almeida, O. U.1 & J. A. Herrera-Silveira2. 1Laboratorio de Oceanografía Biológica, Universidad Autónoma de Nayarit, Secretaria de Investigación y Posgrado, Edificio CEMIC 01, Ciudad de la Cultura “Amado Nervo”, C.P. 63000, Tepic, Nayarit. 2Laboratorio de Producción Primaria CINVESTAV-IPN, Unidad Mérida, Carretera Antigua a Progreso km 6. C.P. 97310 Mérida, Yucatán, México. email: ubisha78@hotmail.com Hernández-Almeida, O. U. & J. A. Herrera-Silveira. 2014. First record of Reimerothrix floridensis (Fragilariaceae: Bacillariophyta) for México. CICIMAR Oceánides, 29(1): 29-31.

Reimerothrix floridensis A.K.S.K. Prasad, belongs to a group of diatoms with arcuate form whose taxonomic diversity has been discussed by Prasad et al. (2001). This author agrees with Round (1993) in that species with said morphology are easily confused with Cylindrotheca closterium (Ehrenberg) Reimer & Lewin, a common taxón in coastal phytoplankton. According to Prasad et al. (2001) these species can be discriminated live by observing the number and form of the chloroplasts. In C. closterium there are two plate form organelles; whilst in Fecha de recepción: 30 de abril de 2014

Psammosynedra closterioides and R. floridensis there is only one with a similar form. Another way to distinguish between them is on the basis of their movement. In C. closterium it consist of directional gliding, while P. closterioides (Round, 1993) and R. floridensis (Prasad et al., 2001) are sessil forms. However, in ecological studies of coastal phytoplankton when blooms of arcuate species are present, such as C. closterium, Nitzschia longissima and N. longissima var. reversa, this observations are very difficult to perform, mainly because samples are generally fixed with acid lugol solution, that modifies the plastids and precludes the motility of cells. An alternative is to rely on general morphology and of the apex, nonetheless, the great amount of mucilage produced by the cells and the organic matter from re-suspension make their distinction difficult. Thus, a better alternative to identify R. floridensis with certainity is to examine acid-cleaned material under SEM (Prasad et al., 2001). Based on the above, the aim of our work is to present the first record of the arcuate diatom Reimerothrix floridensis during a bloom of C. closterium off the coasts of the Yucatán peninsula in 2011, as well as to provide a brief description of this taxon relying on electron microscopy. Our study area, Dzilam de Bravo, Yucatán shows three climate seasons: dry (March-May), rainy (June-October), and nortes or norths from November to February (Capurro, 2002). This locality registers underground water discharge into the sea, which derives in high nutrient concentrations and low salinities (Troccoli-Ghinaglia et al., 2004). Environmental conditions in the study area promote phytoplankton blooming, such the one that occurred in 2011, when C. closterium, N. logissima and Nitzschia longissima var. reversa were recorded as the most important taxa. In order to monitor this phytoplankton bloom monthly samplings were carried out by taking surficial water samples with 250 ml bottles and fixing them with lugol solution. Simultaneously, hydrological variables such as salinity, temperature, and nitrate, phosphate and silicate concentrations were measured. In order to observe and identify the bloom forming diatom species, their frustules were cleaned following Siqueiros-Beltrones & Voltolina (2000). Afterwards, the samples were observed under a Jeol JSM-7600F field emission electron microscope. In this manner Reimerothrix floridensis was observed for the first time in Mexico in the northern coasts of the Yucatán peninsula�� . �� The species occurred in September, 500 m from the coast-line off Dzilam de Bravo. Hydrological variables reached the following values: salinity 28.9 ups, temperature 30 °C, nitrate concentration 1.8 mmol/l-1, phosphate Fecha de aceptación: 20 de mayo de 2014

HERNÁNDEZ-ALMEIDA & HERRERA-SILVEIRA

0.38 mmol/l-1 and silicates 0.89 mmol/l-1. Description. The described specimens showed the following characteristics: narrow, elongated cells at the center of the valve, from which arcuate valval extensions are projected (Fig. 1). The apex of the valval extensions slightly rostrated (Fig. 1, arrows). Length of the apical axis 172 µm; transapical 4.5 µm (at the elongated part). Valval extensions 0.6 µm in width and up to 1 µm at the ápex. The distance from the center of the valve to the end of the valval extensions was 95 µm. The central area of the valve shows a wide sternum with a single line of poroid areolae (31 in 10 µm) associated to the union between the mantle and the valval face (Fig. 2). The valval extensions had 35-36 uniseriate poroid areolae in 10 µm (Fig. 3), whilst in the area near the apex these became biseriate (Fig. 4). Each apex presented a rimoportula (Fig. 4, arrow), a rectangular pore field, and four poroid areolae between the field and the rimoportula (Fig. 4). Except for the density of the areolae associated to the sternum, the above description depicts Reimerothrix floridensis as described by Prasad et al. (2001). Such variation in striae density could be explained as adaptations to nutrient and salinity conditions in the study area, as it has been observed for

different species of Nitzschia (Trobajo et al., 2011) and was attributed to variations at species level. On the other hand, Prasad et al. (2001) outline that in spite the occurrence of R. floridensis in various densities in the water column it is mainly a benthicepiphytic form, and it is generally associated to Climaconeis koenigii, C. colemaniae, Synedra bacillaris and Cocconeis scutellum. Although in this study no samples of Thalassia testudinum were examined, earlier Hernández-Almeida et al. (2013) observed that on said host Climaconeis aff. coxii, Synedra bacillaris and Cocconeis scutellum were common, thus suggesting the likely presence of R. floridensis within the epiphytic assemblages along the coasts of the Yucatán peninsula. This range extension on the distribution of R. floridensis underlines the need for more taxonomic efforts that allow us to know with a higher degree of certainty which species may develop blooms along the coastal waters of México. This work was done as part of the Estancias Posdoctorales Nacionales program with a grant by CONACyT for the first author. We acknowledge projects FOMIX-CONACyT 2008-108160 and CONACyT LAB-2009-01 No. 123931, and the coastal monitoring program of the Laboratorio de Productividad Primaria of CINVESTAV- IPN, for providing the samples of coastal phytoplankton. Also, we thank EM

Figures 1-4. Reimerothrix floridensis. Fig. 1. Complete frustule of R. floridensis showing arcuate form and rostrate apexes (arrows). Scale bar = 50 mm. Fig. 2. Sternum with uniseriate line of areolae assciated to the union between mantle and valval face; scale bar = 10 mm. Fig. 3. Detail of valval extension with uniseriate areolae; scale bar = 5 mm. Fig. 4. Detail of apex showing the rimoportula (arrow) and pore field; scale bar = 2.5 mm.

FIRST RECORD OF Reimerothrix floridensis

technicians Dora Huerta and Ana Ruth Cristóbal of the Laboratorio Nacional para el análisis de Nano y Biomateriales. We likewise acknowledge the reviews by two anonymous referees to an earlier manuscript. English translation by D. Siqueiros Beltrones.

REFERENCES Capurro, L. 2002. A Large Coastal Ecosystem: The Yucatan Peninsula. Advances and Perspectives, 22: 69–75. Hernández-Almeida, O. U., J. A. Herrera-Silveira & F. del C. Merino-Virgilio. 2013. Nine New Records of Benthic Diatoms of the Genera Climaconeis, Cocconeis, Licmophora, Talaroneis, Oestrupia, Petroneis and Synedrophenia from the Northern Coast of the Yucatan Peninsula, Mexico. Hidrobiológica, 23 (2): 154–168. Prasad, A. K. S. K., J. A. Nienow & K. A. Riddle. 2001. Fine Structure, Taxonomy and Systematics of Reimerothrix (Fragilariaceae: Bacillariophyta), a New Genus of Synedroid Diatoms from Florida Bay, USA.” Phycologia, 40 (1): 35–46.

Round, F. E. 1993. The Identity of Synedra closterioides Grun. and Its Transference to a New Genus Psammosynedra. Diatom Research, 8 (1): 209–213. Siqueiros-Beltrones, D. A. & D. Voltolina. 2000. Grazing Selectivity of Red Abalone Haliotis rufescens Postlarvae on Benthic Diatom Films under Culture Conditions. Journal of the World Aquaculture Society, 31 (2): 239–246. Trobajo, R., L. Rovira, D. G. Mann & E. J. Cox. 2011. Effects of Salinity on Growth and on Valve Morphology of Five Estuarine Diatoms. Phycological Research, 59 (2): 83–90. Troccoli-Ghinaglia, L., J. A. Herrera-Silveira & F. A. Comín. 2004. Structural Variations of Phytoplankton in the Coastal Seas of Yucatan, Mexico. Hydrobiologia, 519: 85–102.

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