Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-24T05:38:14.211Z Has data issue: false hasContentIssue false

Distribution of Gymnodinium catenatum Graham cysts and its relation to harmful algae blooms in the northern Gulf of California

Published online by Cambridge University Press:  08 December 2021

Rigel Castañeda-Quezada
Affiliation:
Posgrado de Ecología Marina, Centro de Investigación Científica y de Educación Superior de Ensenada, Carr. Ensenada-Tijuana #3918, CP 22860, Ensenada, Baja California, México
Ernesto García-Mendoza*
Affiliation:
Departamento de Oceanografía Biológica, Centro de Investigación Científica y de Educación Superior de Ensenada, Carr. Ensenada-Tijuana #3918, CP 22860, Ensenada, Baja California, México
Rafael Ramírez-Mendoza
Affiliation:
Departamento de Oceanografía Física, Centro de Investigación Científica y de Educación Superior de Ensenada, Carr. Ensenada-Tijuana, #3918, CP 22860, Ensenada, Baja California, México
Javier Helenes
Affiliation:
Departamento de Geología, Centro de Investigación Científica y de Educación Superior de Ensenada, Carr. Ensenada-Tijuana, #3918, CP 22860, Ensenada, Baja California, México;
David Rivas
Affiliation:
Departamento de Oceanografía Biológica, Centro de Investigación Científica y de Educación Superior de Ensenada, Carr. Ensenada-Tijuana #3918, CP 22860, Ensenada, Baja California, México
Alfonsina E. Romo-Curiel
Affiliation:
Departamento de Oceanografía Biológica, Centro de Investigación Científica y de Educación Superior de Ensenada, Carr. Ensenada-Tijuana #3918, CP 22860, Ensenada, Baja California, México
Asunción Lago-Lestón
Affiliation:
Departamento de Innovación Biomédica, Centro de Investigación Científica y de Educación Superior de Ensenada, Carr. Ensenada-Tijuana, #3918, CP 22860, Ensenada, Baja California, México
*
Author for correspondence: Ernesto García-Mendoza, E-mail: [email protected]

Abstract

Germination of cysts serves as inoculum for the proliferation of some dinoflagellates, and cyst abundance in sediments represents crucial information to understand and possibly predict Harmful Algae Blooms (HABs). Cyst distribution is related to the physical characteristics of the sediments and the hydrodynamics (circulation) of a particular region. In the northern Gulf of California (nGC) several Gymnodinium catenatum HABs have been recorded. However, the presence of resting cysts and the effect of hydrodynamics on their distribution in the nGC have not been investigated. This study evaluated cyst abundance, distribution and their relation to local circulation in surface sediments during two periods that coincided with a non-bloom year condition (July 2016) and after a major HAB registered in the nGC that occurred in January 2017. Also, a numerical ocean model was implemented to characterize the transport and relocation of cysts and sediments in the region. Gymnodinium catenatum cysts were heterogeneously distributed with some areas of high accumulation (as high as 158 cyst g−1, and 27% of total cyst registered). Cysts seemed to be transported in an eastward direction after deposition and accumulated in an extensive area that probably is the seedbed responsible for the initiation of HABs in the region. The nGC is a retention area of cysts (and sediments) that permit the formation of seedbeds that could be important for G. catenatum HAB development. Our results provide key information to understand G. catenatum ecology and specifically, to understand the geographic and temporal appearance of HABs in the nGC.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Álvarez-Borrego, S, Flores-Baéz, BP and Galindo-Bect, LA (1975) Hidrología del Alto Golfo de California II. Condiciones durante invierno, primavera y verano. Ciencias Marinas 2, 2136.CrossRefGoogle Scholar
Amorim, A and Dale, B (1998) Distribution of cysts from toxic or potentially toxic dinoflagellates along the Portuguese coast. In Reguera B, Blanco J, Fernandez M and Wyatt T (eds), Harmful Algae, Proceedings of the VIII International Conference on Harmful Algae. Santiago de Compostela: Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, pp. 6465.Google Scholar
Amorim, A, Dale, B, Godinho, R and Brotas, V (2001) Gymnodinium catenatum-like cysts (Dinophyceae) in recent sediments from the coast of Portugal. Phycologia 40, 572582.CrossRefGoogle Scholar
Anderson, DM, Jacobson, DM, Bravo, I and Wrenn, JH (1988) The unique, microreticulate cyst of the naked dinoflagellate Gymnodinium catenatum. Journal of Phycology 24, 255262.CrossRefGoogle Scholar
Anderson, DM, Stock, CA, Keafer, BA, Nelson, AB, Thompson, B, McGillicuddy, DJ Jr, Keller, M, Matrai, PA and Martin, J (2005) Alexandrium fundyense cyst dynamics in the Gulf of Maine. Deep Sea Research Part II: Topical Studies in Oceanography 52, 25222542.CrossRefGoogle Scholar
Anderson, DM, Keafer, BA, Kleindinst, JL, McGillicuddy, DJ Jr, Martin, JL, Norton, K, Pilskaln, CH, Smith, JL, Sherwood, CR and Butman, B (2014) Alexandrium fundyense cysts in the Gulf of Maine: long-term time series of abundance and distribution, and linkages to past and future blooms. Deep Sea Research Part II: Topical Studies in Oceanography 103, 626.CrossRefGoogle ScholarPubMed
Aretxabaleta, AL, Butman, B, Signell, RP, Dalyander, PS, Sherwood, CR, Sheremet, VA and McGillicuddy, DJ Jr (2014) Near-bottom circulation and dispersion of sediment containing Alexandrium fundyense cysts in the Gulf of Maine during 2010–2011. Deep Sea Research Part II: Topical Studies in Oceanography 103, 96111.CrossRefGoogle ScholarPubMed
Argote, ML, Amador, A, Lavín, MF and Hunter, JR (1995) Tidal dissipation and stratification in the Gulf of California. Journal of Geophysical Research: Oceans (1978–2012) 100, 1610316118.CrossRefGoogle Scholar
Band-Schmidt, CJ, Morquecho, L, Lechuga-Devéze, CH and Anderson, DM (2004) Effects of growth medium, temperature, salinity and seawater source on the growth of Gymnodinium catenatum (Dinophyceae) from Bahía Concepción, Gulf of California, México. Journal of Plankton Research 26, 14591470.CrossRefGoogle Scholar
Band-Schmidt, CJ, Bustillos-Guzmán, J, Gárate-Lizárraga, I, Lechuga-Devéze, CH, Reinhardt, K and Luckas, B (2005) Paralytic shellfish toxin profile in strains of the dinoflagellate Gymnodinium catenatum Graham and the scallop Argopecten ventricosus GB Sowerby II from Bahia concepción, Gulf of California, Mexico. Harmful Algae 4, 2131.CrossRefGoogle Scholar
Band-Schmidt, CJ, Bustillos-Guzmán, JJ, López-Cortés, DJ, Gárate-Lizárraga, I, Núñez-Vázquez, EJ and Hernández-Sandoval, FE (2010) Ecological and physiological studies of Gymnodinium catenatum in the Mexican Pacific: a review. Marine Drugs 8, 19351961.CrossRefGoogle ScholarPubMed
Band-Schmidt, CJ, Duran-Riveroll, LM, Bustillos-Guzman, JJ, Leyva-Valencia, I, Lopez-Cortes, DJ, Nuñez-Vazquez, EJ, Hernández-Sandoval, FE, Ramirez-Rodriguez, DV (2019) Paralytic toxin producing dinoflagellates in Latin America: ecology and physiology (a review). Frontiers in Marine Science 6, 42.CrossRefGoogle Scholar
Beier, E and Ripa, P (1999) Seasonal gyres in the northern Gulf of California. Journal of Physical Oceanography 29, 305311.2.0.CO;2>CrossRefGoogle Scholar
Benninghoff, WS (1962) Calculations of pollen and spore density in sediments by addition of exotic pollen in known quantities. Pollen Spores 4, 332.Google Scholar
Blackburn, SI, Hallegraeff, GM and Bolch, CJ (1989) Vegetative reproduction and sexual life cycle of the toxic dinoflagellate Gymnodinium catenatum from Tasmania, Australia. Journal of Phycology 25, 577590.CrossRefGoogle Scholar
Blanco, J (1995) The distribution of dinoflagellate cysts along the Galician (NW Spain) coast. Journal of Plankton Research 17, 283302.CrossRefGoogle Scholar
Blott, S and Pye, K (2001) Gradistat: a grain size distribution and statistic package for the analysis of unconsolidated sediments. Earth Surface Processes and Landforms 26, 12371248.CrossRefGoogle Scholar
Bolch, CJ and Hallegraeff, GM (1990) Dinoflagellate cysts in recent marine sediments from Tasmania, Australia. Botanica Marina 33, 173192.CrossRefGoogle Scholar
Bolch, CJ, Negri, AP and Hallegraeff, GM (1999) Gymnodinium microreticulatum sp. nov. (Dinophyceae): a naked, microreticulate cyst-producing dinoflagellate, distinct from Gymnodinium catenatum and Gymnodinium nolleri. Phycologia 38, 301313.CrossRefGoogle Scholar
Bray, NA and Robles, JM (1991) Physical oceanography of the Gulf of California. Chapter 25: Part V. Physical Oceanography, Primary Productivity, Sedimentology. In The Gulf and Peninsular Province of the Californias, Memoir of the American association of Petroleum Geologists, 47, 511553.Google Scholar
Brusca, RC, Álvarez-Borrego, S, Hastings, PA and Findley, LT (2017) Colorado River flow and biological productivity in the northern Gulf of California, México. Earth-Science Reviews 164, 130.CrossRefGoogle Scholar
Butman, B, Aretxabaleta, AL, Dickhudt, PJ, Dalyander, PS, Sherwood, CR, Anderson, DM, Keafer, BA and Signell, RP (2014) Investigating the importance of sediment resuspension in Alexandrium fundyense cyst population dynamics in the Gulf of Maine. Deep Sea Research Part II: Topical Studies in Oceanography 103, 7995.CrossRefGoogle ScholarPubMed
Carriquiry, JD, Sánchez, A and Camacho-Ibar, VF (2001) Sedimentation in the northern Gulf of California after cessation of the Colorado river discharge. Sedimentary Geology 144, 3762.CrossRefGoogle Scholar
Cochran, WG (1963) Sampling Techniques, 2nd Edn. New York, NY: John Wiley & Sons.Google Scholar
COFEPRIS (2015) Comisión Federal para la Protección contra Riesgos Sanitarios. Presencia de marea roja en México durante 2015. Secretaría de Salud. Available at http://www.cofepris.gob.mx/ (Accessed online 29 January 2021).Google Scholar
Cruz-Rico, J and Rivas, D (2018) Physical and biogeochemical variability in Todos Santos Bay, northwestern Baja California, derived from a numerical NPZD model. Journal of Marine Systems 183, 6375.CrossRefGoogle Scholar
Dale, B (1983) Dinoflagellate resting cysts: benthic plankton. In Fryxell, GA (ed.), Survival Strategies of the Algae. Cambridge: Cambridge University Press, pp. 69136.Google Scholar
Duque-Herrera, AF, Helenes, J, Flores-Trujillo, JG, Ruiz-Fernández, AC and Sánchez-Cabeza, JA (2020) Dinoflagellate cysts and ENSO-PDO climate forcing in the southern Gulf of California. Palaeogeography, Palaeoclimatology, Palaeoecology 560, 110055.CrossRefGoogle Scholar
Erdner, DL, Percy, L, Keafer, B, Lewis, J and Anderson, DM (2010) A quantitative real-time PCR assay for the identification and enumeration of Alexandrium cysts in marine sediments. Deep Sea Research Part II: Topical Studies in Oceanography 57, 279287.CrossRefGoogle ScholarPubMed
Espinosa-Carreón, TL and Valdez-Holguín, E (2007) Variabilidad interanual de clorofila en el Golfo de California. Ecología Aplicada 6, 8392.CrossRefGoogle Scholar
Fairall, CW, Bradley, EF, Rogers, DP, Edson, JB and Young, GS (1996) Bulk parameterization of air-sea fluxes for tropical ocean global atmosphere coupled-ocean atmosphere response experiment. Journal of Geophysical Research: Oceans 101, 37473764.CrossRefGoogle Scholar
Figueroa, RI and Bravo, I (2005) Sexual reproduction and two different encystment strategies of Lingulodinium polyedrum (Dinophyceae) in culture. Journal of Phycology 41, 370379.CrossRefGoogle Scholar
Figueroa, RI, Bravo, I and Garcés, E (2005) Effects of nutritional factors and different parental crosses on the encystment and excystment of Alexandrium catenella (Dinophyceae) in culture. Phycologia 44, 658670.CrossRefGoogle Scholar
Figueroa, RI, Bravo, I, Ramilo, I, Pazos, Y and Moroño, A (2008) New life-cycle stages of Gymnodinium catenatum (Dinophyceae): laboratory and field observations. Aquatic Microbial Ecology 52, 1323.CrossRefGoogle Scholar
Gárate-Lizárraga, I, Band-Schmidt, CJ, López-Cortés, DJ, Bustillos-Guzmán, JJ and Erler, K (2007 a) Bloom of Pseudo-nitzschia fraudulenta in Bahía de La Paz, Gulf of California (June–July 2006). Harmful Algae News 33, 67.Google Scholar
Gárate-Lizárraga, I, Arellano-Martínez, M, Ceballos-Vázquez, BP, Bustillos-Guzmán, JJ, López-Cortés, DJ and Hernández-Sandoval, F (2007 b) Fitoplancton tóxico y presencia de toxinas paralizantes en la almeja mano de león (Nodipecten subnodosus, Sowerby, 1835) en la Bahía de Los Ángeles, B.C. In Resúmenes del II Taller sobre Florecimientos Algales Nocivos, Ensenada, México, 21–23 Noviembre. Ensenada: CICESE-CETMAR, p. 20.Google Scholar
Graham, HW (1943) Gymnodinium catenatum, a new dinoflagellate from the Gulf of California. Transactions of the American Microscopical Society 62, 259261.CrossRefGoogle Scholar
Hallegraeff, GM, McCausland, MA and Brown, RK (1995) Early warning of toxic dinoflagellate blooms of Gymnodinium catenatum in southern Tasmanian waters. Journal of Plankton Research 17, 11631176.CrossRefGoogle Scholar
Hallegraeff, GM, Blackburn, SI, Doblin, MA and Bolch, CJS (2012) Global toxicology, ecophysiology and population relationships of the chainforming PST dinoflagellate Gymnodinium catenatum. Harmful Algae 14, 130143.CrossRefGoogle Scholar
Hammer, Ø, Harper, DAT and Ryan, PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 9.Google Scholar
Harland, R, Nordberg, K and Filipsson, H (2004) The seasonal occurrence of dinoflagellate cysts in surface sediments from Koljö Fjord, west coast of Sweden – a note. Review of Palaeobotany and Palynology 128, 107117.CrossRefGoogle Scholar
Horner, RA, Greengrove, CL, Davies-Vollum, KS, Gawel, JE, Postel, JR and Cox, AM (2011) Spatial distribution of benthic cysts of Alexandrium catenella in surface sediments of Puget Sound, Washington, USA. Harmful Algae 11, 96105.CrossRefGoogle Scholar
Hwang, CH, Kim, KY, Lee, Y and Kim, CH (2011) Spatial distribution of dinoflagellate resting cysts in Yellow Sea surface sediments. Algae 26, 4150.CrossRefGoogle Scholar
Lavín, MF, Durazo, R, Palacios, E, Argote, ML and Carrillo, L (1997) Lagrangian observations of the circulation in the northern Gulf of California. Journal of Physical Oceanography 27, 22982305.2.0.CO;2>CrossRefGoogle Scholar
Lavín, MF, Godínez, VM and Alvarez, LG (1998) Inverse-estuarine features of the upper Gulf of California. Estuarine, Coastal and Shelf Science 47, 769795.CrossRefGoogle Scholar
Liu, D, Shi, Y, Di, B, Sun, Q, Wang, Y, Dong, Z and Shao, H (2012) The impact of different pollution sources on modern dinoflagellate cysts in Sishili Bay, Yellow Sea, China. Marine Micropaleontology 84, 113.CrossRefGoogle Scholar
Liu, M, Gu, H, Krock, B, Luo, Z and Zhang, Y (2020) Toxic dinoflagellate blooms of Gymnodinium catenatum and their cysts in Taiwan Strait and their relationship to global populations. Harmful Algae 97, 101868.CrossRefGoogle ScholarPubMed
López-Cortés, DJ, Hernández-Sandoval, FE, Band-Schmidt, CJ, Bustillos-Guzmán, JJ and Núñez-Vázquez, EJ (2016) Condiciones ambientales asociadas a florecimientos algales nocivos en el Golfo de California. In García-Mendoza, E, Quijano-Scheggia, SI, Olivos-Ortiz, A and Nuñez-Vazquez, EJ (eds), Florecimientos Algales Nocivos en México. CICESE: Ensenada, México, p. 438.Google Scholar
MacKenzie, AL (2014) The risk to New Zealand shellfish aquaculture from paralytic shellfish poisoning (PSP) toxins. New Zealand Journal of Marine and Freshwater Research 48, 430465.CrossRefGoogle Scholar
Maher, LJ Jr. (1981) Statistics for microfossil concentration measurements employing samples spiked with marker grains. Review of Palaeobotany and Palynology 32, 153191.CrossRefGoogle Scholar
Marinone, SG (2012) Seasonal surface connectivity in the Gulf of California. Estuarine, Coastal and Shelf Science 100, 133141.CrossRefGoogle Scholar
Marinone, SG, Lavín, MF and Parés-Sierra, A (2011) A quantitative characterization of the seasonal Lagrangian circulation of the Gulf of California from a three-dimensional numerical model. Continental Shelf Research 31, 14201426.CrossRefGoogle Scholar
Medina-Elizalde, J (2021) Effects of Paralytic Shellfish Toxins on marine mammals, seabirds and geoduck fisheries in the Northern Gulf of California during 2015–2019. PhD thesis. Centro de Investigación Científica y de Educación de Ensenada, Baja California, México, 83 pp.Google Scholar
Medina-Elizalde, J, García-Mendoza, E, Turner, AD, Sánchez-Bravo, YA and Murillo Martínez, R (2018) Transformation and depuration of paralytic shellfish toxins in the geoduck clam Panopea globosa from the northern Gulf of California. Frontiers in Marine Science 5, 335.CrossRefGoogle Scholar
Mee, LD, Espinosa, M and Diaz, G (1986) Paralytic shellfish poisoning with a Gymnodinium catenatum red tide on the Pacific coast of Mexico. Marine Environmental Research 19, 7792.CrossRefGoogle Scholar
Mertens, KN, Verhoeven, K, Verleye, T, Louwye, S, Amorim, A, Ribeiro, S, Deaf, AS, Harding IC, De Schepper S, Gonzáles C, Kodrans-Nsiah M, De Vernal A, Henry M, Radi T, Dybkjaer K, Poulsen NE, Feist-Burkhardt S, Chitolie J, Heilmann-Clausen C, Londeix L, Turon J-L, Marret F, Matthiesen J, McCarthy FMG, Prasad V, Pospelova V, Kyffin Hughes JE, Riding JB, Rochon, A, Sangiorgi F, Welters N, Sinclair N, Thun C, Soliman A, Van Nieuwenhove N, Vink A and Young M (2009) Determining the absolute abundance of dinoflagellate cysts in recent marine sediments: the Lycopodium marker-grain method put to the test. Review of Palaeobotany and Palynology 157, 238252.CrossRefGoogle Scholar
Mertens, KN, Price, AM and Pospelova, V (2012) Determining the absolute abundance of dinoflagellate cysts in recent marine sediments II: further tests of the Lycopodium marker-grain method. Review of Palaeobotany and Palynology 184, 7481.CrossRefGoogle Scholar
Mesinger, F, DiMego, G, Kalnay, E, Mitchell, K, Shafran, PC, Ebisuzaki, W, Jovic, D, Woollen, J, Rogers, E, Berbery, EH, Ek, MB, Fan, Y, Grumbine, R, Higgins, W, Li, H, Lin, Y, Manikin, G, Parrish, D and Shi, W (2006) North American regional reanalysis. Bulletin of the American Meteorological Society 87, 343360.CrossRefGoogle Scholar
Millán-Núñez, R, Santamaría del Ángel, E, Cajal-Medrano, R and Barocio-León, OA (1999) The Colorado river Delta: a high primary productivity ecosystem. Ciencias Marinas 25, 509524.CrossRefGoogle Scholar
Montes, JM, Lavín, MF and Parés-Sierra, AF (2016) Seasonal heat and salt balance in the upper Gulf of California. Journal of Coastal Research 32, 853862.CrossRefGoogle Scholar
Morquecho, L and Lechuga-Devéze, CH (2003) Dinoflagellate cysts in recent sediments from Bahía Concepción, Gulf of California. Botanica Marina 46, 132141.CrossRefGoogle Scholar
Morquecho, L and Lechuga-Devéze, CH (2004) Seasonal occurrence of planktonic dinoflagellates and cyst production in relationship to environmental variables in subtropical Bahía Concepción, Gulf of California. Botanica Marina 47, 313322.CrossRefGoogle Scholar
Nehring, S (1994) Spatial distribution of dinoflagellate resting cysts in recent sediments of Kiel Bight, Germany (Baltic Sea). Ophelia 39, 137158.CrossRefGoogle Scholar
Orozco-Durán, A, Daesslé, LW, Camacho-Ibar, VF, Ortiz-Campos, E and Barth, JAC (2015) Turnover and release of P-, N-, Si-nutrients in the Mexicali Valley (Mexico): interactions between the lower Colorado River and adjacent ground-and surface water systems. Science of the Total Environment 512, 185193.CrossRefGoogle ScholarPubMed
Palacios-Hernández, E, Beier, E, Lavín, MF and Ripa, P (2002) The effect of the seasonal variation of stratification on the circulation of the northern Gulf of California. Journal of Physical Oceanography 32, 705728.2.0.CO;2>CrossRefGoogle Scholar
Peña-Manjarrez, JL, Flores-Trujillo, JG and Helenes-Escamilla, J (2016) Quistes de dinoflagelados de pared orgánica en las costas de México. In García-Mendoza, E, Quijano-Scheggia, SI, Olivos-Ortiz, A and Nunez-Vazquez, EJ (eds), Florecimientos Algales Nocivos en México. Ensenada: CICESE, p. 438.Google Scholar
Penna, A, Perini, F, Dell'Aversano, C, Capellacci, S, Tartaglione, L, Giacobbe, MG, … Scardi, M (2015) The sxt gene and paralytic shellfish poisoning toxins as markers for the monitoring of toxic Alexandrium species blooms. Environmental Science & Technology 49, 1423014238.CrossRefGoogle ScholarPubMed
Pospelova, V and Kim, SJ (2010) Dinoflagellate cysts in recent estuarine sediments from aquaculture sites of southern South Korea. Marine Micropaleontology 76, 3751.CrossRefGoogle Scholar
Pospelova, V, de Vernal, A and Pedersen, TF (2008) Distribution of dinoflagellate cysts in surface sediments from the northeastern Pacific Ocean (43–25 N) in relation to sea-surface temperature, salinity, productivity and coastal upwelling. Marine Micropaleontology 68, 2148.CrossRefGoogle Scholar
Ramírez Castillo, AM (2020) Comunidad fitoplanctónica y presencia de Gymnodinium catenatum con relación a la temperatura en la Bahía de San Felipe, Baja California, México, Tesis de Licenciatura. Universidad de Colima, 70 pp.Google Scholar
Ramírez-León, MR, Álvarez-Borrego, S, Turrent Thompson, C, Gaxiola Castro, G and Heckel Dziendzielewski, G (2015) Nutrient input from the Colorado River to the northern Gulf of California is not required to maintain a productive pelagic ecosystem. Ciencias Marinas 41, 169188.CrossRefGoogle Scholar
Ravichandran, M, Behringer, D, Sivareddy, S, Girishkumar, MS, Chacko, N and Harikumar, R (2013) Evaluation of the Global Ocean data assimilation system at INCOIS: the tropical Indian ocean. Ocean Model 69, 113.CrossRefGoogle Scholar
Rees, AJJ and Hallegraeff, GM (1991) Ultrastructure of the toxic dinoflagellate Gymnodinium catenatum Graham. Phycologia 30, 90105.CrossRefGoogle Scholar
Ribeiro, S and Amorim, A (2008) Environmental drivers of temporal succession in recent dinoflagellate cyst assemblages from a coastal site in the North-East Atlantic (Lisbon Bay, Portugal). Marine Micropaleontology 68, 156178.CrossRefGoogle Scholar
Rio, MH, Pascual, A, Poulain, PM, Menna, M, Barceló, B and Tintoré, J (2014) Computation of a new mean dynamic topography for the Mediterranean Sea from model outputs, altimeter measurements and oceanographic in situ data. Ocean Science 10, 731744.CrossRefGoogle Scholar
Rivas, D and Samelson, RM (2011) A numerical modeling study of the upwelling source waters along the Oregon coast during 2005. Journal of Physical Oceanography 41, 88112.CrossRefGoogle Scholar
Schlitzer, R (2021) Ocean Data View. https://odv.awi.de.Google Scholar
Shin, HH, Yoon, YH, Kim, YO and Matsuoka, K (2011) Dinoflagellate cysts in surface sediments from southern coast of Korea. Estuaries and Coasts 34, 712725.CrossRefGoogle Scholar
Siegel, S and Castellan, NJ (1988) Nonparametric Statistics for the Behavioural Sciences, 2nd Edn. New York, NY: McGraw-Hill Book Company, pp. 144151.Google Scholar
Singh, AS and Masuku, MB (2013) Fundamentals of applied research and sampling techniques. International Journal of Medical and Applied Sciences 2, 124132.Google Scholar
StatSoft, Inc. (2014) STATISTICA (data analysis software system), version 12. http://www.statsoft.com/.Google Scholar
Stock, G.G. (1976) Modeling of Tides and Tidal Dissipation in the Gulf of California. PhD dissertation, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California, 102 pp.Google Scholar
Tahvanainen, P, Alpermann, TJ, Figueroa, RI, John, U, Hakanen, P, Nagai, S, Blomster, J and Kremp, A (2012) Patterns of post-glacial genetic differentiation in marginal populations of a marine microalga. PLoS ONE 7, e53602.CrossRefGoogle ScholarPubMed
Triki, HZ, Laabir, M, Lafabrie, C, Malouche, D, Bancon-Montigny, C, Gonzalez, C, Deidun, A, Pringault, O and Daly-Yahia, OK (2017) Do the levels of industrial pollutants influence the distribution and abundance of dinoflagellate cysts in the recently-deposited sediment of a Mediterranean coastal ecosystem? Science of the Total Environment 595, 380392.CrossRefGoogle ScholarPubMed
Wang, Z, Matsuoka, K, Qi, Y and Chen, J (2004) Dinoflagellate cysts in recent sediments from Chinese coastal waters. Marine Ecology 25, 289311.CrossRefGoogle Scholar
Wentworth, CK (1922) A scale of grade and class terms for clastic sediments. Journal of Geology 30, 377392.CrossRefGoogle Scholar
Wiese, M, D'agostino, PM, Mihali, TK, Moffitt, MC and Neilan, BA (2010) Neurotoxic alkaloids: saxitoxin and its analogs. Marine Drugs 8, 21852211.CrossRefGoogle ScholarPubMed
Wood, GD, Gabriel, AM and Lawson, JC (1996) Palynological techniques-processing and microscopy. In Jasonius, J and McGregor, DC (eds), Palynology: Principles and Application. Dallas: American Association of Stratigraphic Palynologists Foundation, vol. 1, pp. 2950.Google Scholar
Supplementary material: File

Castañeda-Quezada et al. supplementary material

Castañeda-Quezada et al. supplementary material

Download Castañeda-Quezada et al. supplementary material(File)
File 1.2 MB