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Mixotrophic phytoplankton is enhanced by UV radiation in a low altitude, P-limited Mediterranean lake

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Abstract

UV radiation promotes harmful effects on phytoplankton populations, but it is influenced by the degree of sensitivity of different populations to the ultraviolet:photosynthetically active radiation ratio (UVR:PAR), part of which is P-dependent. Given the expected increase of UV radiation along with global change, one may ask if phytoplankton populations are able to adapt to the expectedly higher UVR:PAR ratio. If so, how would phytoplankton communities be affected? The main goal of this study is to answer these questions. Field and laboratory experiments were carried out with phytoplankton populations of an oligotrophic, low altitude lake in Central Spain. No changes were observed in abundance of phytoplankton fractions after UVR removal in the lake. However, autotrophic picoplankton underwent lower growth and contribution to total phytoplankton biomass when UVR increased. Phytoplankton biomass under enhanced UVR was one-third lower than the biomass reached under only PAR. UV-related growth changes were species-specific and linked to cell size and metabolism. An UVR increase would then promote phytoplankton assemblages who resulted from a trade-off between competitive advantages of picoplankton in a P-limited system and selected larger algae. Under these circumstances, the mixotrophic character of these larger species happened to be an evolutionary advantage.

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References

  • Álvarez-Cobelas, M., S. Cirujano, E. Montero, C. Rojo, M. A. Rodrigo, E. Piña, J. C. Rodríguez, O. Soriano, M. A. Aboal, J. P. Marín & R. Araujo, 2007. Ecología acuática y sociedad de las lagunas de Ruidera. CSIC Editorial, Madrid.

    Google Scholar 

  • American Public Health Association, 1998. Standard Methods for the Examination of Water and Wastewater, 20th ed. APHA, American Water Works Association, Water Environment Federation, Washington.

    Google Scholar 

  • Banaszak, A. T., 2003. Photoprotective physiological and biochemical responses of aquatic organisms. In Helbling, E. W. & H. Zagarese (eds), UV Effects in Aquatic Organisms and Ecosystems. Royal Society of Chemistry, Cambridge: 329–356.

    Chapter  Google Scholar 

  • Bell, T. & J. Kalff, 2001. The contribution of picophytoplankton in marine and freshwater systems of different trophic status and depth. Limnology and Oceanography 46: 1243–1248.

    Article  Google Scholar 

  • Berman-Frank, I. & Z. Dubinsky, 1999. Balanced growth of photosynthesizing aquatic organisms: myth and reality. BioScience 49: 29–37.

    Article  Google Scholar 

  • Bertoni, R. & C. Callieri, 1999. Effects of UVB radiation on freshwater autotrophic and heterotrophic picoplankton in a subalpine lake. Journal of Plankton Research 21: 1373–1388.

    Article  Google Scholar 

  • Buma, A. G. J., P. Boelen & W. H. Jeffrey, 2003. UVR induced DNA damage in aquatic organisms. In Helbling, E. W. & H. E. Zagarese (eds), UV Effects in Aquatic Organisms and Ecosystems. The Royal Society of Chemistry, Cambridge: 291–327.

    Chapter  Google Scholar 

  • Callieri, C., 2008. Picophytoplankton in freshwater ecosystems: the importance of small-sized phototrophs. Freshwater Revue 1: 1–28.

    Google Scholar 

  • Callieri, C., G. Morabito, Y. Huot, P. Neal & E. Lichman, 2001. Photosynthetic response of pico- and nanoplanktonic algae to UVB, UVA and PAR in a high mountain lake. Aquatic Science 63: 286–293.

    Article  Google Scholar 

  • Callieri, C., B. Modenutti, C. Queimaliños, R. Bertoni & E. Balseiro, 2007. Production and biomass of picoplankton and larger autotrophs in Andean ultraoligotrophic lakes: differences in light harvesting efficiency in deep layers. Aquatic Ecology 41: 511–523.

    Article  CAS  Google Scholar 

  • Carignan, R., D. Planas & C. Vis, 2000. Planktonic production and respiration in oligotrophic Shield lakes. Limnology and Oceanography 45: 189–199.

    Article  Google Scholar 

  • Carrillo, P., J. A. Delgado-Molina, J. M. Medina-Sánchez, F. J. Bullejos & 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.

    Article  Google Scholar 

  • de Mora, S., S. Demers & M. Vernet, 2000. The Effects of UV Radiation in the Marine Environment. Cambridge Environmental Chemistry Series 10. Cambridge University Press, Cambridge.

  • Delgado-Molina, J. A., P. Carrillo, J. M. Medina-Sanchez, M. Villar-Argaiz & F. J. Bullejos, 2009. Interactive effects of phosphorus loads and ambient ultraviolet radiation on the algal community in a high-mountain lake. Journal of Plankton Research 31: 619–634.

    Article  CAS  Google Scholar 

  • Eilertsen, H. C. & O. Holm-Hansen, 2000. Effects of high latitude UV radiation on phytoplankton and nekton modelled from field measurements by simple algorithms. Polar Research 19: 173–182.

    Article  Google Scholar 

  • Gallardo, C., A. Arribas, J. A. Prego, M. A. Gaertner & M. Castro, 2001. Multi-year simulations with a high resolution regional climate model over the Iberian Peninsula. Current climate and 2xCO2 scenario. Quarterly Journal of the Royal Meteorological Society 127: 1659–1682.

    Google Scholar 

  • García-Pichel, F. & R. W. Castenholz, 1993. Occurrence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Applied and Environmental Microbiology 59: 163–169.

    PubMed  Google Scholar 

  • Häder, D., H. Kumar, R. Smith & R. Worrest, 2007. Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochemical & Photobiological Sciences 6: 267–285.

    Article  Google Scholar 

  • Halac, S., M. Felip, Ll. Camarero, S. Sommaruga-Wögrath, R. Psenner, J. Catalan & R. Sommaruga, 1997. An in situ enclosure experiment to test the solar UV-B impact on microplankton in a high altitude mountain lake: 1) lack of effect on phytoplankton species composition and growth. Journal of Plankton Research 11: 1671–1687.

    Article  Google Scholar 

  • Harrison, J. W. & R. E. H. Smith, 2009. Effects of ultraviolet radiation on the productivity and composition of freshwater phytoplankton communities. Photochemical & Photobiological Sciences 8: 1218–1232.

    Article  CAS  Google Scholar 

  • Hayhome, B. A., T. Brei & R. C. Tuttle, 1981. Photoreactivation of far U.V. damage in the dinoflagellate Peridinium cinctum. Environmental and Experimental Botany 21: 121–125.

    Article  Google Scholar 

  • Helbling, E. W. & H. Zagarese, 2003. UV Effects in Aquatic Organisms and Ecosystems. Royal Society of Chemistry, Cambridge.

    Book  Google Scholar 

  • Helbling, E. W., V. Villafañe, A. Buma, M. Andrade & F. Zaratti, 2001. DNA damage and photosynthetic inhibition induced by solar ultraviolet radiation in tropical phytoplankton (Lake Titicaca, Bolivia). European Journal of Phycology 36: 157–166.

    Article  Google Scholar 

  • Hessen, D. O., E. Leu, P. J. Faerovig & S. F. Petersen, 2008. Light and spectral properties as determinants of C:N:P-ratios in phytoplankton. Deep Sea Research LPABt II: Topical Studies in Oceanography 55: 2169–2175.

    Article  CAS  Google Scholar 

  • Hudson, J. J., W. D. Taylor & D. W. Schindler, 2000. Phosphate concentration in lakes. Nature 406: 54–56.

    Article  PubMed  CAS  Google Scholar 

  • Kaczmarska, I., T. A. Clair, J. M. Ehrman, S. L. MacDonald, D. Lean & K. E. Day, 2000. The effect of UV-B on phytoplankton populations in clear and brown temperate Canadian lakes. Limnology and Oceanography 45: 651–663.

    Article  CAS  Google Scholar 

  • Karentz, D., J. E. Cleaver & D. L. Mitchell, 1991. Cell survival characteristics and molecular responses of Antarctic phytoplankton to ultraviolet-B radiation. Journal of Phycology 27: 326–341.

    Article  CAS  Google Scholar 

  • Kasai, F., M. J. Waiser, R. D. Robarts & M. T. Arts, 2001. Size-dependent UVR sensitivity in Redberry Lake phytoplankton communities. International Association of Theoretical and Applied Limnology Proceedings 27: 2018–2023.

    Google Scholar 

  • Klausmeier, C. A., E. Litchman, T. Daufresne & S. A. Levin, 2008. Phytoplankton stoichiometry. Ecological Research 23: 479–485.

    Article  Google Scholar 

  • Laurion, I. & W. F. Vincent, 1998. Cell size versus taxonomic composition as determinants of UV-sensitivity in natural phytoplankton communities. Limnology and Oceanography 43: 1774–1779.

    CAS  Google Scholar 

  • Laybourn-Parry, J., W. A. Marshall & H. J. Marchant, 2005. Flagellate nutritional versatility as a key to survival in two contrasting Antarctic saline lakes. Freshwater Biology 50: 830–838.

    Article  Google Scholar 

  • Leech, D. M. & C. E. Williamson, 2000. Is tolerance to UV radiation in zooplankton related to body size, taxon, or lake transparency? Ecological Applications 10: 1530–1540.

    Article  Google Scholar 

  • Litchman, E. & C. A. Klausmeier, 2008. Trait-based community ecology of phytoplankton. Annual Review of Ecology Evolution and Systematics 39: 615–639.

    Article  Google Scholar 

  • Lund, J., C. Kipling & E. D. Le Cren, 1958. The inverted method of estimating algal numbers and the statistical basis of estimation by counting. Hydorobiologia 11: 143–170.

    Article  Google Scholar 

  • Madronich, S., 1994. Increases in biologically damaging UV-B radiation due to stratospheric ozone reductions: a brief review. Archiv für Hydrobiologie Beiheft Ergebnisse der Limnologie 43: 17–30.

    Google Scholar 

  • Marañón, E., 2009. Phytoplankton size structure. In Steele, J. H., K. K. Turekian & S. A. Thorpe (eds), Encyclopedia of Ocean Sciences, 2nd ed. Academic Press, Oxford.

    Google Scholar 

  • Mauchly, J. W., 1940. Significance test for sphericity of a normal n-variate distribution. The Annals of Mathematical Statistics 11: 204–209.

    Article  Google Scholar 

  • Medina-Sánchez, J. M., M. Villar-Argaiz & P. Carrillo, 2004. Neither with nor without you: a complex algal control on bacterioplankton in a high mountain lake. Limnology and Oceanography 49(5): 1722–1733.

    Article  Google Scholar 

  • Medina-Sánchez, J. M., M. Villar-Argaiz & P. Carrillo, 2006. Solar radiation-nutrient interaction enhances the resource and predation algal control on bacterioplankton: a short-term experimental study. Limnology and Oceanography 51(2): 913–924.

    Article  Google Scholar 

  • Menden-Deuer, S. & E. J. Lessard, 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography 45: 569–579.

    Article  CAS  Google Scholar 

  • Orce, V. I. & E. W. Helbling, 1997. Latitudinal UVR-PAR measurements in Argentina: extent of the “ozone hole”. Global and Planetary Change 15: 113–121.

    Article  Google Scholar 

  • Popovsky, J. & L. A. Préster, 1990. Dinophyceae (Dinoflagellida). Süsswasserflora von Mitteleuropa. Springer, Jena.

    Google Scholar 

  • Quesada, A. & W. F. Vincent, 1997. Strategies of adaptation by Antarctic cyanobacteria to ultraviolet radiation. European Journal of Phycology 32(4): 335–342.

    Google Scholar 

  • Quesada, A., J. L. Mouget & W. F. Vincent, 1995. Growth of Antarctic cyanobacteria under ultraviolet radiation: UVA counteracts UVB inhibition. Journal of Phycology 31: 242–248.

    Article  Google Scholar 

  • Raven, J. A., 1998. The twelfth Tanseley lecture. Small is beautiful: the picophytoplankton. Functional Ecology 12: 503–513.

    Article  Google Scholar 

  • Ravishankara, A. R., J. S. Daniel & R. W. Portmann, 2008. Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326: 123–125.

    Article  Google Scholar 

  • Redfield, A. C., 1958. The biological control of chemical factors in the environment. American Scientist 46: 205–221.

    CAS  Google Scholar 

  • Reynolds, C. S., 1997. Vegetation Processes in the Pelagic: A Model for Ecosystem Theory. Ecology Institute, Oldendorf, Luhe, Germany.

    Google Scholar 

  • Rodrigo, M. A., C. Rojo & M. Álvarez-Cobelas, 2003. Autotrophic and heterotrophic picoplankton in wetlands: differences with lake patterns. International Revue Hydrobiologie 88: 464–481.

    Article  Google Scholar 

  • Rodrigo, M. A., C. Rojo, M. Segura & J. Larrosa, 2009. Mechanisms of microalgae selection during the assembly of a planktonic community. Aquatic Ecology 43: 61–72.

    Article  Google Scholar 

  • Rott, E., 1981. Some results from phytoplankton counting intercalibrations. Schweizerische Zeitschrift für Hydrologie 43: 34–62.

    Google Scholar 

  • Sereda, J. M., D. M. Vandergucht & J. J. Hudson, 2011. Disruption of planktonic phosphorous cycling by ultraviolet radiation. Hydrobiologia 665: 205–217.

    Article  CAS  Google Scholar 

  • Solomon, S., 1999. Stratospheric ozone depletion: a review of concepts and history. Reviews of Geophysics 37: 275–316.

    Article  CAS  Google Scholar 

  • Sommaruga, R. & A. G. J. Buma, 2000. UV-induced cell damage is species-specific among aquatic phagotrophic protists. Journal of Eukaryotic Microbiology 47: 450–455.

    Article  PubMed  CAS  Google Scholar 

  • Souza, M. S., B. E. Modenutti, P. Carrillo, M. Villar-Argaiz, J. M. Medina-Sánchez, F. Bullejos & E. G. Balseiro, 2010. Stoichiometric dietary constraints influence the response of copepods to ultraviolet radiation-induced oxidative stress. Limnology and Oceanography 55: 1024–1032.

    Article  CAS  Google Scholar 

  • Sterner, R. W., J. J. Elser & E. J. Fee, 1997. The light:nutrient ratio in lakes: the balance of energy and materials affects ecosystem structure and process. American Naturalist 150: 663–684.

    Article  PubMed  CAS  Google Scholar 

  • Stockner, J. G., 1991. Autotrophic picoplankton in freshwater ecosystems: the view from the summit. International Revue der Gesamten Hydrobiologie 76: 483–492.

    Article  Google Scholar 

  • van Donk, E., B. A. Faafeng, H. J. de Lange & D. O. Hessen, 2001. Differential sensitivity to natural ultraviolet radiation among phytoplankton species in Arctic lakes (Spitsbergen, Norway). Plant Ecology 154: 247–259.

    Article  Google Scholar 

  • Villafañe, V., C. Sunfbäck, F. L. Figueroa & E. W. Helbling, 2003. Photosynthesis in the aquatic environment as affected by ultraviolet radiation. In Helbling, E. W. & H. Zagarese (eds), UV Effects in Aquatic Organisms and Ecosystems. Royal Society of Chemistry, Cambridge: 357–399.

    Chapter  Google Scholar 

  • Villar-Argaiz, M., J. M. Medina-Sánchez, L. Cruz-Pizarro & P. Carrillo, 2001. Inter- and intraannual variability in the phytoplankton community of a high mountain lake: the influence of external (atmospheric) and internal (recycled) sources of P. Freshwater Biology 46: 1121–1138.

    Article  Google Scholar 

  • Villar-Argaiz, M., J. M. Medina-Sánchez, F. J. Bullejos, J. A. Delgado-Molina, O. Ruiz-Pérez, J. C. Navarro & P. Carrillo, 2009. UV radiation and phosphorus interact to influence the biochemical composition of phytoplankton. Freshwater Biology 54: 1233–1245.

    Article  CAS  Google Scholar 

  • Weisse, T., 1988. Dynamics of autotrophic picoplankton in lake constance. Journal of Plankton Research 10: 1179–1188.

    Article  Google Scholar 

  • Wetzel, R. G., 2001. Limnology Lakes and River Ecosystems, 3rd ed. Academic Press, New York, NY, USA.

    Google Scholar 

  • Wild, M., A. Ohmura & K. Makowski, 2007. Impact of global dimming and brightening on global warming. Geophysical Research Letters 34: L04702. doi:10.1029/2006GL028031.

  • Winder, M., 2009. Photosynthetic picoplankton dynamics in Lake Thahoe: temporal and spatial niche partitioning among prokaryotic and eukaryotic cells. Journal of Plankton Research 31: 1307–1320.

    Article  Google Scholar 

  • Xenopoulos, M. A. & P. C. Frost, 2003. UV radiation, phosphorus, and their combined effects on the taxonomic composition of phytoplankton in a boreal lake. Journal of Phycology 39: 291–302.

    Article  CAS  Google Scholar 

  • Xenopoulos, M. A., P. C. Frost & J. J. Elser, 2002. Joint effects of UV radiation and phosphorus supply on algal growth rate and elemental composition. Ecology 83: 423–435.

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank the Spanish Ministry of the Environment and Ministry of the Science and Innovation for projects CGL2011-23681 and CGL2009-10292, respectively. This research was also supported by the ‘Consejería de Innovación, Ciencia y Empresa' of the ‘Junta de Andalucía' (Project P07-CVI-02598). We also thank Clara Andrés and Andrea Campos (ICBIBE, University of Valencia, Spain) for their careful assistance in laboratory work. Dr. Mario Sendra (Department of Biostatistics, University of Valencia, Spain) proved the suitability of the statistics used. The English used in the manuscript has been corrected by a native English reviewer of scientific texts.

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Authors and Affiliations

  1. Integrative Ecology Group, Institute Cavanilles of Biodiversity and Evolutionary Biology, University of Valencia, c/ Catedrático José Beltrán, No. 2, 46980, Paterna, Spain

    Carmen Rojo & María A. Rodrigo

  2. Functional Ecology Group, Institute of Water, University of Granada, c/ Ramón y Cajal 4, 18071, Granada, Spain

    Guillermo Herrera & Presentación Carrillo

  3. Aquatic Ecology Group, National Museum of Natural History, CSIC, c/ Serrano 115 dpdo., 28006, Madrid, Spain

    María José Ortíz-Llorente

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  1. Carmen Rojo
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  2. Guillermo Herrera
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  3. María A. Rodrigo
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  4. María José Ortíz-Llorente
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Correspondence to Carmen Rojo.

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Guest editors: N. Salmaso, L. Naselli-Flores, L. Cerasino, G. Flaim, M. Tolotti & J. Padisák / Phytoplankton responses to human impacts at different scales: 16th workshop of the International Association of Phytoplankton Taxonomy and Ecology (IAP)

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Rojo, C., Herrera, G., Rodrigo, M.A. et al. Mixotrophic phytoplankton is enhanced by UV radiation in a low altitude, P-limited Mediterranean lake. Hydrobiologia 698, 97–110 (2012). https://doi.org/10.1007/s10750-012-1214-x

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