We compared the responses of two estuarine phytoplankton communities, one from a temperate (Chubut River estuary (CH), Argentina) and one from a sub-tropical site (Babitonga Bay (BB), Brazil), in a scenario of nutrient enrichment under solar ultraviolet radiation (UVR) exposure. Seawater samples were exposed in microcosms to two nutrients, ambient vs. enriched, and two radiation conditions, with and without UVR, and exposed to solar radiation for 4 days. We evaluated the short- (PSII photochemistry, during 90 min light and 90 min dark cycles, before and after the 4 days of acclimation) and mid-term effects (growth and taxonomic changes) of the phytoplankton communities. Before acclimation, short-term UVR effects were dominant in CH, whereas in BB, nutrient effects prevailed. Such differences were related to the previous light history of the cells and to the ambient nutrient status. After acclimation, an overall improvement of the photosynthetic performance was observed at both sites, either by reducing the relative inhibition or by increasing the recovery of the effective photochemical quantum yield. Interactive effects of UVR and nutrients on growth at CH were antagonistic, while at BB, no differences were observed between the interactive and the sum of effects. Part of the differences in the mid-term observed responses can be attributed to taxonomic changes, with the CH community dominated by diatoms throughout the experiment, but with a shift from a diatom to a flagellate-dominated community in BB. Temperature differences between both sites might have favored higher growth rates and flagellates dominance in BB under the nutrient enriched conditions.
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Aidar, E., S.A. Gaeta, S.M.F. Gianesella-Galvão, M.B.B. Kutner, and C. Teixeira. 1993. Ecossistema costeiro subtropical: nutrients dissolvidos, fitoplâncton e clorofila-a e suas relações com as condições oceanográficas na região de Ubatuba, SP. Publicação Especial do Instituto Oceanografico Sao Paulo 10: 9–43.
Ayoub, L.M., P. Hallock, P.G. Coble, and S.S. Bell. 2012. MAA-like absorbing substances in Florida Keys phytoplankton vary with distance from shore and CDOM: Implications for coral reefs. Journal of Experimental Marine Biology and Ecology 420-421: 91–98.
Banaszak, A.T., and M.P. Lesser. 2009. Effects of solar ultraviolet radiation on coral reef organisms. Photochemical and Photobiological Sciences 8: 1276–1294.
Barbieri, E.S., V.E. Villafañe, and E.W. Helbling. 2002. Experimental assessment of UV effects upon temperate marine phytoplankton when exposed to variable radiation regimes. Limnology and Oceanography 47: 1648–1655.
Beardall, J., C. Sobrino, and S. Stojkovic. 2009. Interactions between the impacts of ultraviolet radiation, elevated CO2, and nutrient limitation on marine primary producers. Photochemical and Photobiological Sciences 8: 1257–1265.
Bergmann, T., T.L. Richardson, H.W. Paerl, J.L. Pinckney, and O. Schofield. 2002. Synergy of light and nutrients on the photosynthetic efficiency of phytoplankton populations from the Neuse River Estuary, North Carolina. Journal of Plankton Research 24: 923–933.
Björn, L.O., and T.M. Murphy. 1985. Computer calculation of solar ultraviolet radiation at ground level. Physiologie Vegetale 23: 555–561.
Brandini, F.P., F. Alquini, R.B. Pereira, and R.L. Leite. 2006. Abundância e estrutura populacional da comunidade planctônica na Baía da Babitonga: Subsídios para a avaliação de impactos ambientais. In Diagnóstico Ambiental da Baía da Babitonga, ed. M.J. Cremer, P.R.D. Moralo, and T.M.N. Oliveira, 112–134. Joinville: Univille.
Bricker, S.B., B. Longstaff, W. Dennison, A. Jones, K. Boicourt, C. Wicks, and J. Woerner. 2008. Effects of nutrient enrichment in the nation's estuaries: A decade of change. Harmful Algae 8: 21–32.
Buma, A.G.J., P. Boelen, and W.H. Jeffrey. 2003. UVR-induced DNA damage in aquatic organisms. In UV effects in aquatic organisms and ecosystems, ed. E.W. Helbling, and H.E. Zagarese, 291–327. Cambridge: The Royal Society of Chemistry.
Carrillo, P., J.A. Delgado-Molina, J.M. Medina-Sánchez, F.J. Bullejos, and M. Villar-Argaiz. 2008. Phosphorus inputs unmask negative effects of ultraviolet radiation on algae in a high mountain lake. Global Change Biology 14: 423–439.
Chapin, F.S. III, E.S. Zavaleta, V.T. Eviner, R.L. Naylor, P.M. Vitousek, H.L. Reynolds, D.U. Hooper, S. Lavorel, O.E. Sala, S.E. Hobbie, M.C. Mack, and S. Díaz. 2000. Consequences of changing biodiversity. Nature 405: 234–242.
Christensen, M.R., M.D. Graham, R.D. Vinebrooke, D.L. Findlay, M.J. Paterson, and M.A. Turner. 2006. Multiple anthropogenic stressors cause ecological surprises in boreal lakes. Global Change Biology 12: 2316–2322.
Cloern, J.E. 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210: 223–253.
Cloern, J.E., S.Q. Foster, and A.E. Fleckner. 2014. Phytoplankton primary production in the world’s estuarine-coastal ecosystems. Biogeosciences 11: 2477–2501.
Crain, C.M., K. Kroeker, and B.S. Halpern. 2008. Interactive and cumulative effects of multiple human stressors in marine systems. Ecology Letters 11: 1304–1315.
Cremer, M.J., T.M.N. Oliveira, and P.R.D. Morales. 2006. Diagnóstico ambiental da Baía da Babitonga. Joinville: Editora da UNIVILLE.
de Groot, R., M.A. Wilson, and R.M.J. Boumans. 2002. A typology for the classification, description and evaluation of ecosystem functions, goods and services. Ecological Economics 41: 393–408.
Dimier, C., S. Giovanni, T. Ferdinando, and C. Brunet. 2009. Comparative ecophysiology of the xanthophyll cycle in six marine phytoplankton species. Protist 160: 397–411.
Eppley, R.W. 1972. Temperature and phytoplankton growth in the sea. Fishery Bulletin 70: 1063–1085.
Fernandes, L.F., and F. Pereira Brandini. 2010. The potentially toxic diatom Pseudo-nitzschia H. Peragallo in the Paraná and Santa Catarina States, Southern Brazil. Iheringia Ser.Bot. 65: 47–62.
Genty, B.E., J. Harbinson, and N.R. Baker. 1990. Relative quantum efficiencies of the two photosystems of leaves in photorespiratory and non-photorespiratory conditions. Plant Physiology and Biochemistry 28: 1–10.
Goss, R., and T. Jakob. 2010. Regulation and function of xantophyll cycle-dependent photoprotection in algae. Photosynthesis Research 106: 103–122.
Häder, D.-P., M. Lebert, M. Schuster, L. del Ciampo, E.W. Helbling, and R. McKenzie. 2007. ELDONET—A decade of monitoring solar radiation on five continents. Photochemistry and Photobiology 83: 1348–1357.
Häder, D.-P., E.W. Helbling, C.E. Williamson, and R.C. Worrest. 2011. Effects of UV radiation on aquatic ecosystems and interactions with climate change. Photochemical and Photobiological Sciences 10: 242–260.
Häder, D.P., V.E. Villafañe, and E.W. Helbling. 2014. Productivity of aquatic primary producers under global climate change. Photochemical and Photobiological Sciences 13: 1370–1392.
Häder, D.-P., C.E. Williamson, S.-A. Wängberg, M. Rautio, K.C. Rose, K. Gao, E.W. Helbling, R.P. Sinha, and R. Worrest. 2015. Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors. Photochemical and Photobiological Sciences 14: 108–126.
Harrison, J.W., and R.E.H. Smith. 2013. Effects of nutrients and irradiance on PSII variable fluorescence of lake phytoplankton assemblages. Aquatic Sciences 75: 399–411.
Harrison, J.W., G.M. Silsbe, and R.H. Smith. 2015. Photophysiology and its response to visible and ultraviolet radiation in freshwater phytoplankton from contrasting light regimes. Journal of Plankton Research 37: 472–488.
Helbling, E.W., V.E. Villafañe, M.E. Ferrario, and O. Holm-Hansen. 1992. Impact of natural ultraviolet radiation on rates of photosynthesis and on specific marine phytoplankton species. Marine Ecology Progress Series 80: 89–100.
Helbling, E.W., E.S. Barbieri, M.A. Marcoval, R.J. Gonçalves, and V.E. Villafañe. 2005. Impact of solar ultraviolet radiation on marine phytoplankton of Patagonia, Argentina. Photochemistry and Photobiology 81: 807–818.
Helbling, E.W., D.E. Pérez, C.D. Medina, M.G. Lagunas, and V.E. Villafañe. 2010. Phytoplankton distribution and photosynthesis dynamics in the Chubut River estuary (Patagonia, Argentina) throughout tidal cycles. Limnology and Oceanography 55: 55–65.
Helbling, E.W., A.T. Banaszak, and V.E. Villafañe. 2015. Differential responses of two phytoplankton communities from the Chubut river estuary (Patagonia, Argentina) to the combination of UVR and elevated temperature. Estuaries and Coasts 38: 1134–1146.
Hernando, M., I. Schloss, S. Roy, and G. Ferreyra. 2006. Photoacclimation to long-term ultraviolet radiation exposure of natural sub-Antarctic phytoplankton communities: Fixed surface incubations versus mixed mesocosms. Photochemistry and Photobiology 82: 923–935.
Holm-Hansen, O., and B. Riemann. 1978. Chlorophyll a determination: Improvements in methodology. Oikos 30: 438–447.
Hüner, N.P.A., G. Öquist, and F. Sarhan. 1998. Energy balance and acclimation to light and cold. Trends in Plant Science 3: 224–230.
IPCC. 2013. Climate Change 2013. The Physical Science Basis. New York, USA: Cambridge University Press.
Kulk, G., W.H. van de Poll, R.J.W. Visser, and A.G.J. Buma. 2011. Distinct differences in photoacclimation potential between prokaryotic and eukaryotic oceanic phytoplankton. Journal of Experimental Marine Biology and Ecology 398: 63–72.
Lavaud, J., R.F. Strzepek, and P.G. Kroth. 2007. Photoprotection capacity differs among diatoms: Possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnology and Oceanography 52: 1188–1194.
Liang, Y., J. Beardall, and P. Heraud. 2006. Effects of nitrogen source and UV radiation on the growth, chlorophyll fluorescence and fatty acid composition of Phaeodactylum tricornutum and Chaetoceros muelleri (Bacillariophyceae). Journal of Photochemistry and Photobiology, B: Biology 82: 161–172.
Litchman, E., and P.J. Neale. 2005. UV effects on photosynthesis, growth and acclimation of an estuarine diatom and cryptomonad. Marine Ecology Progress Series 300: 53–62.
Longhi, M.L., G. Ferreyra, I. Schloss, and S. Roy. 2006. Variable phytoplankton response to enhanced UV-B and nitrate addition in mesocosm experiments at three latitudes (Canada, Brazil and Argentina). Marine Ecology Progress Series 313: 57–72.
Marcoval, M.A., V.E. Villafañe, and E.W. Helbling. 2007. Interactive effects of ultraviolet radiation and nutrient addition on growth and photosynthesis performance of four species of marine phytoplankton. Journal of Photochemistry and Photobiology, B: Biology 89: 78–87.
Martins, C.C., A.C. Cabral, S.C.T. Barbosa-Cintra, A.L.L. Dauner, and F.M. Souza. 2014. An integrated evaluation of molecular marker indices and linear alkylbenzenes (LABs) to measure sewage input in a subtropical estuary (Babitonga Bay, Brazil). Environmental Pollution 188: 71–80.
Maxwell, D.P., S. Falk, and N.P.A. Huner. 1995. Photosystem II excitation pressure and development of resistance to photoinhibition. Plant Physiology 107: 687–694.
Ogbebo, F.E., and C. Ochs. 2008. Bacterioplankton and phytoplankton production rates compared at different levels of solar ultraviolet radiation and limiting nutrient ratios. Journal of Plankton Research 30: 1271–1284.
Paerl, H.W., and T.G. Otten. 2013. Harmful cyanobacterial blooms: Causes, consequences, and controls. Microbial Ecology 65: 995–1010.
Pájaro, M., G.J. Macchi, and P. Martos. 2005. Reproductive pattern of the Patagonian stock of Argentine hake (Merluccius hubbsi. Fisheries Research 72: 97–108.
Parizzi, R.A. 2013. Variação sazonal do fitoplâncton e parâmetros ambientais no Canal do Rio Palmital, Baía da Babitonga, Sul do Brasil. Ciência e Natura 35: 41–53.
Parizzi, R.A. 2014. Produtividade primária e dinâmica do fitoplâncton em um estuário subtropical: Uma abordagem em diferentes escalas temporais, Universidade Federal do Paraná Pontal do Paraná
Parkhill, J.-P., G. Maillet, and J.J. Cullen. 2001. Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. Journal of Phycology 37: 517–529.
Pereira Camacho, F., and J.M. Souza-Conceição. 2007. Distribuição espaço-temporal da clorofila a e das variáveis ambientais em praias estuarinas da Ilha de São Francisco do Sul (Baía da Babitonga, sul do Brasil). Boletim Técnico-científico do CEPENE 15: 9–16.
Piccolo, M.C., and G.M.E. Perillo. 1999. Estuaries of Argentina: A review. In Estuaries of South America: Their geomorphology and dynamics, ed. G.M.E. Perillo, M.C. Piccolo, and M. Pino Quivira, 101–132. Berlin: Springer.
Porra, R.J. 2002. The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynthesis Research 73: 149–156.
Rabalais, N.N., R.E. Turner, R.J. Díaz, and D. Justic. 2009. Global change and eutrophication of coastal waters. ICES Journal of Marine Science 66: 1528–1537.
Ruban, A.V., J. Lavaud, B. Rousseau, G. Guglielmi, P. Horton, and A.-L. Etienne. 2004. The super-excess energy dissipation in diatom algae: Comparative analysis with higher plants. Photosynthesis Research 82: 165–175.
Ruggaber, A., R. Dlugi, and T. Nakajima. 1994. Modelling of radiation quantities and photolysis frequencies in the troposphere. Journal of Atmospheric Chemistry 18: 171–210.
Schreiber, U., W. Bilger, and C. Neubauer. 1994. Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. In Ecophysiology of photosynthesis, ed. E.-D. Schulze, and M.M. Caldwell, 49–70. Berlin: Springer.
Skewgar, E., P.D. Boersma, G. Harris, and G. Caille. 2007. Sustainability: Anchovy fishery threat to Patagonian Ecosystem. Science 315: 45.
Sobrino, C., M.L. Ward, and P.J. Neale. 2008. Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: Effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnology and Oceanography 53: 494–505.
Staehr, P.A., P. Henriksen, and S. Markager. 2002. Photoacclimation of four marine phytoplankton species to irradiance and nutrient availability. Marine Ecology Progress Series 238: 47–59.
Strickland, J.D.H., and T.R. Parsons. 1972. A practical handbook of seawater analysis. Fisheries Research Board of Canada Bull. 167: 1–310.
Thomas, M.K., C.T. Kremer, C.A. Klausmeier, and E. Litchman. 2012. A global pattern of thermal adaptation in marine phytoplankton. Science 338: 1085–1088.
Tittensor, D.P., C. Mora, W. Jetz, H.K. Lotze, D. Ricard, E. Vanden Berghe, and B. Worm. 2010. Global patterns and predictors of marine biodiversity across taxa. Nature 466: 1098–1101.
van de Poll, W., A.G.J. Buma, R.J. Visser, P.J. Janknegt, V.E. Villafañe, and E.W. Helbling. 2010. Xanthophyll cycle activity and photosynthesis of Dunaliella tertiolecta (Chlorophyceae) and Thalassiosira weissflogii (Bacillariophyceae) during fluctuating solar radiation. Phycologia 49: 249–259.
Villafañe, V.E., and F.M.H. Reid. 1995. Métodos de microscopía para la cuantificación del fitoplancton. In Manual de Métodos Ficológicos, ed. K. Alveal, M.E. Ferrario, E.C. Oliveira, and E. Sar, 169–185. Concepción, Chile: Universidad de Concepción.
Villafañe, V.E., E.S. Barbieri, and E.W. Helbling. 2004. Annual patterns of ultraviolet radiation effects on temperate marine phytoplankton off Patagonia, Argentina. Journal of Plankton Research 26: 167–174.
Villafañe, V.E., A.T. Banaszak, S.D. Guendulain-García, S.M. Strauch, S.R. Halac, and E.W. Helbling. 2013. Influence of seasonal variables associated with climate change on photochemical diurnal cycles of marine phytoplankton from Patagonia (Argentina). Limnology and Oceanography 58: 203–214.
Villafañe, V.E., G.S. Erzinger, S.M. Strauch, and E.W. Helbling. 2014. Photochemical activity of PSII of tropical phytoplankton communities of Southern Brazil exposed to solar radiation and nutrient addition. Journal of Experimental Marine Biology and Ecology 459: 199–207.
Villafañe, V.E., M.S. Valiñas, M.J. Cabrerizo, and E.W. Helbling. 2015. Physio-ecological responses of Patagonian coastal marine phytoplankton in a scenario of global change: Role of acidification, nutrients and solar UVR. Marine Chemistry 177: 411–420.
Weis, E., and A. Berry. 1987. Quantum efficiency of photosystem II in relation to the energy dependent quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 894: 198–208.
Zar, J.H. 1999. Biostatistical analysis. Englewood Cliffs, NJ: Prentice Hall.
We thank the help of C. Machado, C. Hack Gumz Correia, and R. Parizzi for their help with analysis of samples and setup of experiments in BB. We also thank the comments and suggestions of three anonymous reviewers that helped us to improve this manuscript. This work was supported by Consejo Nacional de Investigaciones Científicas y Técnicas—CONICET (PIP No. 112-201001-00228), Agencia Nacional de Promoción Científica y Tecnológica—ANPCyT (PICT 2012-0271 and PICT 2013-0208), Fundaçao de Apoio à Pesquisa Científica e Tecnológica do Estado de Santa Catarina (FAPESC), National Counsel of Technological and Scientific Development (CNPQ), Universidade da Região de Joinville, and Fundación Playa Unión. We also thank Cooperativa Eléctrica y de Servicios de Rawson for providing building’ infrastructure in CH. MCJ was supported by the Ministerio de Educación, Cultura y Deporte of Spain through a “Formación de Profesorado Universitario” Ph.D. fellowship (FPU12/01243) and a short-term fellowship (EST13/0666) at EFPU. This is Contribution No. 164 of Estación de Fotobiología Playa Unión.
Communicated by Hans W. Paerl
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Villafañe, V.E., Cabrerizo, M.J., Erzinger, G.S. et al. Photosynthesis and Growth of Temperate and Sub-Tropical Estuarine Phytoplankton in a Scenario of Nutrient Enrichment under Solar Ultraviolet Radiation Exposure. Estuaries and Coasts 40, 842–855 (2017). https://doi.org/10.1007/s12237-016-0176-z
- PSII photochemistry
- Global change
- Ultraviolet radiation
- Taxonomic changes
- Nutrients enrichment
- Specific growth rates