Influence of salinity on the growth of Akashiwo sanguinea and Prorocentrum micans (Dinophyta) under acclimated conditions and abrupt changes

References

• Abreu PC, Bergesch M, Proença LA, Garcia CAE, Odebrecht C. 2010. Short- and long-term chlorophyll a variability in the shallow microtidal Patos Lagoon Estuary, Southern Brazil. Estuaries and Coasts 33:554–69.
   Web of Science ®Google Scholar
• Alkawri AAS, Ramaiah N. 2010. Spatio-temporal variability of dinoflagellate assemblages in different salinity regimes in the west coast of India. Harmful Algae 9:153–62.
   Web of Science ®Google Scholar
• Anselmo TPA. 2007. Monitorização do Fitoplâncton no Estuário do Tejo: Contagem e Identificação de Espécies, Índice de Biomassa, Análise Pigmentar e Resposta Fotossintética. Master’s Thesis. Universidade de Lisboa, Portugal. 78 pages.
   Google Scholar
• Balech E. 1988. Los Dinoflagelados del Atlântico Sudoccidental. Madrid: Instituto Español de Oceanografia. 310 pages.
   Google Scholar
• Balkis HAN. 2003. Seasonal variations in the phytoplankton and nutrient dynamics in the neritic water of Büyükçekmece Bay, Sea of Marmara. Journal of Plankton Research 25:703–17.
   Web of Science ®Google Scholar
• Balzano S, Sarno D, Kooistra W. 2011. Effects of salinity on the growth rate and morphology of ten Skeletonema strains. Journal of Plankton Research 33:937–945.
   Web of Science ®Google Scholar
• Bollmann M, Bosch T, Colijin F, Ebinghaus R, Froese R, Güssow K, et al. 2010. World Ocean Review 1. Hamburg: Maribus. 232 pages.
   Google Scholar
• Braarud T. 1961. Cultivation of marine organisms as a means of understanding environmental influences on populations. In: Sears M, editor. Oceanography. Washington, DC: American Association for Advancement of Science Publication 67, p 271–98.
   Google Scholar
• Cardoso LS. 1998. Dinoflagelados da Ilha do Arvoredo e da Praia de Ponta das Canas, Santa Catarina, Brasil. Biociências 6:3–54.
   Google Scholar
• Cullen JJ, Horrigan SG. 1981. Effects of nitrate on the diurnal vertical migration, carbon to nitrogen ratio, and the photosynthetic capacity of the dinoflagellate Gymnodinium splendens. Marine Biology 62:81–89.
   Web of Science ®Google Scholar
• Darley WM. 1982. Algal Biology: A Physiological Approach. Oxford: Blackwell Scientific Publications. 168 pages.
   Google Scholar
• Du X, Peterson W, McCulloch A, Liu G. 2011. An unusual bloom of the dinoflagellate Akashiwo sanguinea off the central Oregon, USA, coast in autumn 2009. Harmful Algae 10:784–93.
   Web of Science ®Google Scholar
• Durham WM, Stocker R. 2012. Thin phytoplankton layers: Characteristics, mechanisms, and consequences. Annual Review of Marine Science 4:177–207.
   PubMed Web of Science ®Google Scholar
• Errera RM, Campbell L. 2012. Correction for Errera and Campbell, Osmotic stress triggers toxin production by the dinoflagellate Karenia brevis. Proceedings of the National Academy of Sciences 109:17723–24.
   Web of Science ®Google Scholar
• Figueroa RI, Vázquez JA, Massanet A, Murado MA, Bravo I. 2011. Interactive effects of salinity and temperature on planozygote and cyst formation of Alexandrium minutum (Dinophyceae) in culture. Journal of Phycology 47:13–24.
   Web of Science ®Google Scholar
• Flöder S, Burns CW. 2004. Phytoplankton diversity of shallow tidal lakes: Influence of periodic salinity changes on diversity and species number of a natural assemblage. Journal of Phycology 40:54–61.
   Web of Science ®Google Scholar
• Flöder S, Jaschinski S, Wells G, Burns CW. 2010. Dominance and compensatory growth in phytoplankton communities under salinity stress. Journal of Experimental Marine Biology and Ecology 395:223–31.
   Web of Science ®Google Scholar
• Fodorpataki L, Bartha C. 2004. Salt stress tolerance of a freshwater green alga under different photon flux densities. Studia Universitatis Babes Bolyai Biology 2:86–93.
   Google Scholar
• Fujita CCO, Odebrecht C. 2007. Short-term variability of chlorophyll a and phytoplankton composition in a shallow area of the Patos Lagoon estuary (Southern Brazil). Atlântica 29:93–107.
   Google Scholar
• Gameiro C, Cartaxana P, Cabrita MT, Brotas V. 2004. Variability in chlorophyll and phytoplankton composition in an estuarine system. Hydrobiologia 525:113–24.
   Web of Science ®Google Scholar
• Gayoso AM, Fulco VK. 2006. Occurrence patterns of Alexandrium tamarense (Lebour) Balech populations in the Golfo Nuevo (Patagonia, Argentina), with observations on ventral pore occurrence in natural and cultured cells. Harmful Algae 5:233–41.
   Web of Science ®Google Scholar
• Guillard RRL, Hargraves PE. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycology 32:234–36.
   Web of Science ®Google Scholar
• Guimarães SCP, Rorig LR. 2004. Efeito da salinidade no crescimento dos dinoflagelados Prorocentrum micans Ehrenberg e Prororcentrum cf. obtusum Ostenfeld isolados da costa Catarinense – Brasil. Revista Estudos de Biologia 54:29–36.
   Google Scholar
• Hoek VD, Mann DG, Jahns HM. 1995. Algae: An Introduction to Phycology. Cambridge: Cambridge University Press. 627 pages.
   Google Scholar
• Hoppenrath M, Elbrachter M, Drebes G. 2009. Marine Phytoplankton: Selected Microphytoplankton Species from the North Sea around Helgoland and Sylt. Stuttgart: E. Schweizerbart’sche Verlagsbuchhandlung (Nagele U. Obermiller). 264 pages.
   Google Scholar
• Ignatiades L, Gotsis-Skretas O. 2010. A review on toxic and harmful algae in Greek coastal waters (E. Mediterranean Sea). Toxins 2:1019–37.
   PubMed Web of Science ®Google Scholar
• IPCC. 2013. Climate Change 2013. The Physical Science Basis. Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press. 222 pages.
   Google Scholar
• Jauffrais T, Sécheta V, Herrenknecht C, Truquet P, Véronique S, Tillmann U, et al. 2013. Effect of environmental and nutritional factors on growth and azaspiracid production of the dinoflagellate Azadinium spinosum. Harmful Algae 27:138–48.
   Web of Science ®Google Scholar
• Jeong HJ, Yoo YD, Park JY, Song JY, Kim ST, Lee SH, et al. 2005. Feeding by phototrophic red-tide dinoflagellates: Five species newly revealed and six species previously known to be mixotrophic. Aquatic Microbial Ecology 40:133–50.
   Web of Science ®Google Scholar
• Jessup DA, Miller MA, Ryan JP, Nevins HM, Kerkering HA, Mekebri A, et al. 2009. Mass stranding of marine birds caused by a surfactant-producing red tide. PloS One 4:e4550. 8 pages.
   Web of Science ®Google Scholar
• Kain JM, Fogg GE. 1960. Studies on the growth of marine phytoplankton. III. Prorocentrum micans. Journal of the Marine Biological Association of the United Kingdom 39:33–50.
   Web of Science ®Google Scholar
• Katano T, Yoshida M, Yamaguchi S, Hamada T, Yoshino K, Hayami Y. 2011. Diel vertical migration and cell division of bloom-forming dinoflagellate Akashiwo sanguinea in the Ariake Sea, Japan. Plankton and Benthos Research 6:92–100.
   Google Scholar
• Kim D, Matsuyama Y, Nagasoe S, Yamaguchi M, Yoon Y, Oshima Y, et al. 2004. Effects of temperature, salinity and irradiance on the growth of the harmful red tide dinoflagellate Cochlodinium polykrikoides Margalef (Dinophyceae). Journal of Plankton Research 26:61–66.
   Web of Science ®Google Scholar
• Kim G, Lee YW, Joung DJ, Kim KR, Kim K. 2006. Real-time monitoring of nutrient concentrations and red-tide outbreaks in the southern sea of Korea. Geophysical Research Letters 33:1–4.
   Google Scholar
• Kirst GO. 1989. Salinity tolerance of eukaryotic marine algae. Annual Review of Plant Physiology and Plant Molecular Biology 40:21–53.
   Google Scholar
• Kremer LM, Rosa ZM. 1983. Dinoflagelados do microplâncton de Tramandaí, Rio Grande do Sul, Brasil. Iheringia 30:3–35.
   Google Scholar
• Licea S, Zamudio ME, Luna R, Soto J. 2004. Free-living dinoflagellates in the southern Gulf of Mexico: Report of data (1979–2002). Physiological Research 52:419–28.
   Google Scholar
• Lim P, Ogata T. 2005. Salinity effect on growth and toxin production of four tropical Alexandrium species (Dinophyceae). Toxicon 45:699–710.
   PubMed Web of Science ®Google Scholar
• Lizárraga IG, Orozco MLH, Schmidt CB, Casillas GS. 2001. Red tides along the coasts of Baja California Sur, México (1984 to 2001). Oceanides 16:127–34.
   Google Scholar
• Macedo CX. 2007. Dinâmica Temporal de Microalgas de Zona de Arrebentação na Praia dos Navegantes – SC. Master’s Thesis. Universidade Federal do Paraná, Brazil. 95 pages.
   Google Scholar
• Manjarrez JLP, Castro GG, Escamilla JH, Cepeda EO. 2001. Cysts of Lingulodinium polyedrum, red tide producing organism in the Todos Santos Bay (winter-spring, 2000). Ciencias Marinas 27:543–58.
   Web of Science ®Google Scholar
• Marshall HG. 1995. Succession of dinoflagellate blooms in the Chesapeake Bay, USA. In: Lassus P, Arzul G, Erard E, Gentien P, Marcaillou C, editors. Harmful Marine Algal Blooms. Paris: Lavoisier Publishing, p 615–20.
   Google Scholar
• Marshall HG. 2005. A review of phytoplankton composition within Chesapeake Bay and its tidal estuaries. Journal of Plankton Research 27:1083–102.
   Web of Science ®Google Scholar
• Marshall HG, Cohn MS. 1982. Seasonal Phytoplankton Assemblages in Northeastern Coastal Waters of the United States. NOAA Technical Memorandum nmfs-f/nec-15. 36 pages.
   Google Scholar
• Matsubara T, Nagasoe S, Yamasaki Y, Shikata T, Shimasaki Y, Oshima Y, et al. 2007. Effects of temperature, salinity, and irradiance on the growth of the dinoflagellate Akashiwo sanguinea. Journal of Experimental Marine Biology and Ecology 342:226–30.
   Web of Science ®Google Scholar
• Nakamura H, Kobayashi J, Hirata Y. 1982. Separation of mycosporine-like amino acids in marine organisms using reversed-phase high-performance liquid chromatography. Journal of Chromatography 250:113–18.
   Web of Science ®Google Scholar
• Neale PJ, Banaszak AT, Jarriel CR. 1998. Ultraviolet sunscreens in Gymnodinium sanguinium (Dinophyceae): Micosporine-like amino acids protect against inhibition of photosynthesis. Journal of Phycology 34:928–38.
   Web of Science ®Google Scholar
• Odebrecht C, Rörig L, Garcia VMT, Abreu PC. 1995. Shellfish mortality and a red tide event in southern Brazil. In: Lassus P, Arzul G, Erard E, Gentien P, Marcaillou C, editors. Harmful Marine Algal Blooms. Paris: Lavoisier Publishing, p 213–18.
   Google Scholar
• Odebrecht C, Bergesch M, Rörig LR, Abreu PC. 2010. Phytoplankton interannual variability at Cassino Beach, Southern Brazil (1992–2007), with emphasis on the surf zone diatom Asterionellopsis glacialis. Estuaries and Coasts 33:570–83.
   Web of Science ®Google Scholar
• Park M, Cooney S, Kim J, Coats D. 2002. Effects of parasitism on diel vertical migration, phototaxis/geotaxis, and swimming speed of the bloom-forming dinoflagellate Akashiwo sanguinea. Aquatic Microbial Ecology 29:11–18.
   Web of Science ®Google Scholar
• Peterson TD, Toews HNJ, Robinson CLK, Harrison PJ. 2007. Nutrient and phytoplankton dynamics in the Queen Charlotte Islands (Canada) during the summer upwelling seasons of 2001–2002. Journal of Plankton Research 29:219–39.
   Web of Science ®Google Scholar
• Phillips EM, Zamon JE, Nevins HN, Gibble CM, Duerr RS, Kerr LH. 2011. Summary of birds killed by a harmful algal bloom along the South Washington and North Oregon coasts during October 2009. Northwestern Naturalist 92:120–26.
   Google Scholar
• Qasim SZ, Bhattathiri PMA, Devassy VP. 1972. The influence of salinity on the rate of photosynthesis and abundance of some tropical phytoplankton. Marine Biology 12:200–06.
   Web of Science ®Google Scholar
• Quinlan EL, Phlips EJ. 2007. Phytoplankton assemblages across the marine to low-salinity transition zone in a blackwater dominated estuary. Journal of Plankton Research 29:401–16.
   Web of Science ®Google Scholar
• R Development Core Team. 2014. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. ISBN 3-900051-07-0. http://www.R-project.org. (accessed June 2015). Computer program.
   Google Scholar
• Radchenko IG, Il’yash LV. 2006. Growth and photosynthetic activity of diatom Thalassiosira weissflogii at decreasing salinity. Biology Bulletin 33:242–47.
   Web of Science ®Google Scholar
• Resende P, Azeiteiro UM, Gonçalves F, Pereira MJ. 2007. Distribution and ecological preferences of diatoms and dinoflagellates in the west Iberian Coastal zone (North Portugal). Acta Oecologia 32:224–35.
   Web of Science ®Google Scholar
• Röder K, Hantzsche MF, Gebühr C, Miene C, Helbig T, Krock B, et al. 2012. Effects of salinity, temperature and nutrients on growth, cellular characteristics and yessotoxin production of Protoceratium reticulatum. Harmful Algae 15:59–70.
   Web of Science ®Google Scholar
• Rojas de Mendiola R. 1979. Red tide along the Peruvian coast. In: Taylor DL, Seliger HH, editors. Toxic Dinoflagellate Blooms (Proceedings of the 2nd International Conference). North Holland: Elsevier, p 183–90.
   Google Scholar
• Sahraoui I, Bouchouicha D, Mabrouk HH, Halaili AS. 2013. Driving factors of the potentially toxic and harmful species of Prorocentrum Ehrenberg in a semi-enclosed Mediterranean lagoon (Tunisia, SW Mediterranean). Mediterranean Marine Science 14:353–62.
   Web of Science ®Google Scholar
• Shankle AM, Mayali X, Franks PJS. 2004. Temporal patterns in population genetic diversity of Prorocentrum micans (Dinophyceae). Journal of Phycology 40:239–47.
   Web of Science ®Google Scholar
• Sigaud-Kutner TC, Aidar E. 1995. The influence of osmotic shocks on the growth rate and chlorophyll-a content of planktonic algae species. Boletim do Istituto Oceanográfico 43:89–98.
   Google Scholar
• Silva A, Palma S, Oliveira PB, Moita MT. 2009. Composition and interannual variability of phytoplankton in a coastal upwelling region (Lisbon Bay, Portugal). Journal of Sea Research 62: 238–49.
   Web of Science ®Google Scholar
• Smayda TJ. 1980. Phytoplankton species succession. In: Morris I, editor. The Physiological Ecology of Phytoplankton. Oxford: Blackwell Scientific Publications, p 493–570.
   Google Scholar
• Smayda TJ. 2002. Turbulence, watermass stratification and harmful algal blooms: An alternative view and frontal zones as ‘pelagic seed banks’. Harmful Algae 1:95–112.
   Google Scholar
• Smayda TJ, Bienfang PK. 1983. Suspension properties of various phyletic groups of phytoplankton and tintinnids in an oligotrophic, subtropical system. Marine Ecology 4:289–300.
   Google Scholar
• Smayda TJ, Reynolds CS. 2001. Community assembly in marine phytoplankton: Application of recent models to harmful dinoflagellate blooms. Journal of Plankton Research 23:447–61.
   Web of Science ®Google Scholar
• Smayda TJ, Reynolds CS. 2003. Strategies of marine dinoflagellate survival and some rules of assembly. Journal of Sea Research 49:95–106.
   Web of Science ®Google Scholar
• Stat Soft. 2004. Statistica (data analysis software system), version 7. Stat Soft. Inc. www.statsoft.com (accessed June 2015). Computer program.
   Google Scholar
• Sunda WG, Burleson C, Hardson DR, Morey JS, Wang Z, Wolney J, et al. 2013. Osmotic stress does not trigger brevetoxin production in the dinoflagellate Karenia brevis. Proceedings of the National Academy of Sciences 110:10223–28.
   PubMed Web of Science ®Google Scholar
• Thomas WH, Dodson AN, Linden C. 1973. Optimum light and temperature requirements for Gymnodinium splendens, a larval fish food organism. Fishery Bulletin 71:599–601.
   Web of Science ®Google Scholar
• Uchida T. 1981. The relationships between Prorocentrum micans growth and its ecological environment. Scientific Papers of the Institute of Algological Research, Faculty of Science, Hokkaido University 7:17–76.
   Google Scholar
• Utermöhl H. 1958. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitteilungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 9:1–8.
   Google Scholar
• Vázquez EJN, Lizarraga IG, Schmidt CJB, Tapia AC, Cortes DJL, Sandoval FEH, et al. 2011. Impact of harmful algal blooms on wild and cultured animals in the Gulf of California. Journal of Environmental Biology 34:413–23.
   Google Scholar
• Venables WN, Ripley BD. 2002. Modern Applied Statistics with S. 4th edition. New York: Springer. 495 pages.
   Google Scholar
• Voltolina D. 1993. The origin of recurrent blooms of Gymnodinium sanguineum (Hirasaka) in a shallow lagoon. Journal of Experimental Marine Biology and Ecology 168:217–22.
   Web of Science ®Google Scholar
• Wolmarans K. 2012. The Influence of Nutrients on Surf-zone Phytoplankton Dynamics. Master’s Thesis. Nelson Mandela Metropolitan University, Port Elizabeth, South Africa. 136 pages.
   Google Scholar
• Wood AM, Everroad RC, Wingard LM. 2005. Measuring growth rates in microalgal cultures. In: Andersen R, editor. Algal Culturing Techniques. Oxford: Elsevier Academic Press, p 269–85.
   Google Scholar
• Yamaguchi H, Yoshimatsu T, Tanimoto Y, Sato S, Nishimura T, Uehara K, et al. 2012. Effects of temperature, salinity and their interaction on growth of the benthic dinoflagellate Ostreopsis cf. ovate (Dinophyceae) from Japanese coastal waters. Phycological Research 60:297–304.
   Web of Science ®Google Scholar
• Yamamoto K, Tsujimura H, Nakajima M, Harrison PJ. 2013. Flushing rate and salinity may control the blooms of the toxic dinoflagellate Alexandrium tamarense in a river/estuary in Osaka Bay, Japan. Journal of Oceanography 69:727–36.
   Web of Science ®Google Scholar
• Yamamoto T, Oh SJ, Kataoka Y. 2002. Effects of temperature, salinity and irradiance on the growth of the toxic dinoflagellate Gymnodinium catenatum (Dinophyceae) isolated from Hiroshima Bay, Japan. Fisheries Science 68:356–63.
   Web of Science ®Google Scholar
• Xin L, Ying HH, Ping ZY. 2011. Growth and lipid accumulation properties of a freshwater microalga Scenedesmus sp. under different cultivation temperature. Bioresource Technology 102: 3098–102.
   PubMed Web of Science ®Google Scholar
• Zar JH. 1996. Biostatistical Analysis. 3rd edition. Upper Saddle River, NJ: Prentice Hall. 663 pages.
   Google Scholar