Differential Responses of Two Phytoplankton Communities from the Chubut River Estuary (Patagonia, Argentina) to the Combination of UVR and Elevated Temperature

Estuaries and Coasts

Volumn 38, Issue 4, 2015, Pages 1134-1146

  Helbling, E Walter ^a   Banaszak, Anastazia T ^b   Villafañe, Virginia E ^a  

^a Universidad Nacional de Río Cuarto Consejo Nacional de Investigaciones Científicas y Técnicas   (Argentina)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Global change; Patagonia; Photosynthesis; Phytoplankton; Temperature; Ultraviolet radiation

Indexed keywords

EID: 84931956473     PISSN: 15592723     EISSN: 15592731     Source Type: Journal    
DOI: 10.1007/s12237-013-9752-7     Document Type: Article

References (62)

1. Banaszak, A.T. 2003. Photoprotective physiological and biochemical responses of aquatic organisms. In UV effects in aquatic organisms and ecosystems, ed. E.W. Helbling and H.E. Zagarese, 329–356. Cambridge: The Royal Society of Chemistry.
2. Banaszak, A.T., and P.J. Neale. 2001. Ultraviolet radiation sensitivity of photosynthesis in phytoplankton from an estuarine environment. Limnology and Oceanography 46: 592–603.
3. 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.
4. 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.
5. Branco, A.B., and J. Kremer. 2005. The relative importance of chlorophyll and colored dissolved organic matter (CDOM) to the prediction of the diffuse attenuation coefficient in shallow estuaries. Estuaries 28: 643–652.
6. 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.
7. Buma, A.G.J., R.J. Visser, W. Van de Poll, V.E. Villafañe, P.J. Janknegt, and E.W. Helbling. 2009. Wavelength-dependent xanthophyll cycle activity in marine microalgae exposed to natural ultraviolet radiation. European Journal of Phycology 44: 515–524.
8. Dunne, R.P. 2010. Synergy or antagonism—interactions between stressors on coral reefs. Coral Reefs 29: 145–152.
9. Eilers, P.H.C., and J.C.H. Peeters. 1988. A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecological Modelling 42: 199–215.
10. Ferreyra, G.A., B. Mostajir, I.R. Schloss, K. Chatila, M.E. Ferrario, P. Sargian, S. Roy, J. Prod'homme, and S. Demers. 2006. Ultraviolet-B radiation effects on the structure and function of lower trophic levels of the marine planktonic food web. Photochemistry and Photobiology 82: 887–897.
11. Finazzi, G., G.N. Johnson, L. Dall'Osto, F. Zito, G. Bonente, R. Bassi, and F.A. Wollman. 2006. Nonphotochemical quenching of chlorophyll fluorescence in Chlamydomonas reinhardtii. Biochemistry 45: 1490–1498.
12. Fiorda Giordanino, M.V., S.M. Strauch, V.E. Villafañe, and E.W. Helbling. 2011. Influence of temperature and UVR on photosynthesis and morphology of four species of cyanobacteria. Journal of Photochemistry and Photobiology, B: Biology 103: 68–77.
13. Folt, C.L., C.Y. Chen, M.V. Moore, and J.L. Burnaford. 1999. Synergism and antagonism among multiple stressors. Limnology and Oceanography 44: 864–877.
14. Forster, R., and H. Schubert. 2001. The effects of ultraviolet radiation on the planktonic community of a shallow, eutrophic estuary: Results of mesocosm experiments. Helgoland Marine Research 55: 23–34.
15. Garcia-Pichel, F., and R.W. Castenholz. 1993. Occurence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Applied and Environmental Microbiology 59: 163–169.
16. Genty, B.E., J.M. Briantais, and N.R. Baker. 1989. Relative quantum efficiencies of the two photosystems of leaves in photorespiratory and non-photorespiratory conditions. Plant Physiology and Biochemistry 28: 1–10.
17. 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.
18. Halac, S., E. García-Mendoza, and A.T. Banaszak. 2009. Ultraviolet radiation reduces the photoprotective capacity of the marine diatom Phaeodactylum tricornutum (Bacillariophyceae, Heterokontophyta). Photochemistry and Photobiology 85: 807–815.
19. Halac, S.R., V.E. Villafañe, and E.W. Helbling. 2010. Temperature benefits the photosynthetic performance of the diatoms Chaetoceros gracilis and Thalassiosira weissflogii when exposed to UVR. Journal of Photochemistry and Photobiology, B: Biology 101: 196–205.
20. Halac, S.R., S.D. Guendulain-García, V.E. Villafañe, E.W. Helbling, and A.T. Banaszak. 2013. Responses of tropical plankton communities from the Mexican Caribbean to solar ultraviolet radiation exposure and increased temperature. Journal of Experimental Marine Biology and Ecology 445: 99–107.
21. Hansen, D.V., and M. Rattray Jr. 1965. Gravitational circulation in straits and estuaries. Journal of Marine Research 23: 104–122.
22. Helbling, E.W., J.M. Santamarina, and V.E. Villafañe. 1992. Chubut river estuary (Argentina): Estuarine variability under different conditions of river discharge. Revista de Biologia Marina 27: 73–90.
23. Helbling, E.W., V.E. Villafañe, and O. Holm-Hansen. 1994. Effects of ultraviolet radiation on Antarctic marine phytoplankton photosynthesis with particular attention to the influence of mixing. In Ultraviolet radiation in Antarctica: Measurements and biological effects, ed. C.S. Weiler and P.A. Penhale, 207–227. Washington, D.C.: American Geophysical Union.
24. Helbling, E.W., B.E. Chalker, W.C. Dunlap, O. Holm-Hansen, and V.E. Villafañe. 1996. Photoacclimation of antarctic marine diatoms to solar ultraviolet radiation. Journal of Experimental Marine Biology and Ecology 204: 85–101.
25. Helbling, E.W., K. Gao, R.J. Gonçalves, H. Wu, and V.E. Villafañe. 2003. Utilization of solar UV radiation by coastal phytoplankton assemblages off SE China when exposed to fast mixing. Marine Ecology Progress Series 259: 59–66.
26. 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.
27. 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.
28. Helbling, E.W., A.G.J. Buma, P. Boelen, H.J. van der Strate, M.V. Fiorda Giordanino, and V.E. Villafañe. 2011. Increase in Rubisco activity and gene expression due to elevated temperature partially counteracts ultraviolet radiation–induced photoinhibition in the marine diatom Thalassiosira weissflogii. Limnology and Oceanography 56: 1330–1342.
29. Helbling, E.W., P. Carrillo, J.M. Medina-Sánchez, C. Durán, G. Herrera, M. Villar-Argaiz, and V.E. Villafañe. 2013. Interactive effects of vertical mixing, nutrients and ultraviolet radiation: In situ photosynthetic responses of phytoplankton from high mountain lakes in Southern Europe. Biogeosciences 10: 1037–1050.
30. Heraud, P., and J. Beardall. 2000. Changes in chlorophyll fluorescence during exposure of Dunaliella tertiolecta to UV radiation indicate a dynamic interaction between damage and repair processes. Photosynthesis Research 63: 123–134.
31. Holm-Hansen, O., and E.W. Helbling. 1995. Técnicas para la medición de la productividad primaria en el fitoplancton. In Manual de Métodos Ficológicos, ed. K. Alveal, M.E. Ferrario, E.C. Oliveira, and E. Sar, 329–350. Concepción: Universidad de Concepción.
32. Holm-Hansen, O., and B. Riemann. 1978. Chlorophyll a determination: Improvements in methodology. Oikos 30: 438–447.
33. Holm-Hansen, O., C.J. Lorenzen, R.W. Holmes, and J.D.H. Strickland. 1965. Fluorometric determination of chlorophyll. Journal du Conseil permanent International pour l' Exploration de la Mer 30: 3–15.
34. Houghton, J.T., Y. Ding, D.J. Griggs, M. Noguer, P.J. van der Linden, X. Dai, K. Maskell, and C.A. Johnson. 2001. Climate Change 2001: The scientific basis. Cambridge: Cambridge University Press.
35. IPCC. 2007. Climate Change 2007: The physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. New York, USA: Cambridge University Press.
36. Kana, M., R.J. Geider, and C. Critchley. 1997. Regulation of photosynthetic pigments in micro-algae by multiple environmental factors: A dynamic balance hypothesis. New Phytologist 137: 629–638.
37. Lesser, M.P. 1996. Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnology and Oceanography 41: 271–283.
38. 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.
39. Marcoval, M.A., V.E. Villafañe, and E.W. Helbling. 2008. Combined effects of solar ultraviolet radiation and nutrients addition on growth, biomass and taxonomic composition of coastal marine phytoplankton communities of Patagonia. Journal of Photochemistry and Photobiology, B: Biology 91: 157–166.
40. Müller, P., X.-P. Li, and K.K. Niyogi. 2001. Non-photochemical quenching. A response to excess light energy. Plant Physiology 125: 1558–1566.
41. Neale, P.J. 2000. Spectral weighting functions for quantifying effects of UV radiation in marine ecosystems. In The effects of UV radiation on marine ecosystems, ed. S.J. de Mora, S. Demers and M. Vernet, 72–100. Cambridge: Cambridge University Press.
42. Neale, P.J., A.T. Banaszak, and C.R. Jarriel. 1998. Ultraviolet sunscreens in Gymnodinium sanguineum (Dinophyceae); Mycosporine-like amino acids protect against inhibition of photosynthesis. Journal of Phycology 34: 928–938.
43. Neale, P.J., E.W. Helbling, and H.E. Zagarese. 2003. Modulation of UVR exposure and effects by vertical mixing and advection. In UV effects in aquatic organisms and ecosystems, ed. E.W. Helbling and H.E. Zagarese, 108–134. Royal Society of Chemistry.
44. 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-Verlag.
45. 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.
46. Rundel, R.D. 1983. Action spectra and estimation of biologically effective UV radiation. Physiologia Plantarum 58: 360–366.
47. Sastre, A.V., N.H. Santinelli, S.H. Otaño, and M.E. Ivanissevich. 1998. Water quality in the lower section of the Chubut River, Patagonia, Argentina. Internationale Vereinigung fur Theoretische und Angewandte Limnologie 26: 951–955.
48. Skewgar, E., P.D. Boersma, G. Harris, and G. Caille. 2007. Sustainability: Anchovy fishery threat to Patagonian ecosystem. Science 315: 45.
49. Sobrino, C., and P.J. Neale. 2007. Short-term and long-term effects of temperature on photosynthesis in the diatom Thalassiosira pseudonana under UVR exposures. Journal of Phycology 43: 426–436.
50. Steemann Nielsen, E. 1952. The use of radio-active carbon (C14) for measuring organic production in the sea. Journal du Conseil permanent International pour l' Exploration de la Mer 18: 117–140.
51. Thyssen, M., G. Ferreyra, S. Moreau, I. Schloss, M. Denis, and S. Demers. 2011. The combined effect of ultraviolet B radiation and temperature increase on phytoplankton dynamics and cell cycle using pulse shape recording flow cytometry. Journal of Experimental Marine Biology and Ecology 406: 95–107.
52. Van de Poll, W.H., and A.G.J. Buma. 2009. Does ultraviolet radiation affect the xanthophyll cycle in marine phytoplankton? Photochemical and Photobiological Sciences 8: 1295–1301.
53. 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.
54. Villafañe, V.E., K. Sundbäck, F.L. Figueroa, and E.W. Helbling. 2003. Photosynthesis in the aquatic environment as affected by UVR. In UV effects in aquatic organisms and ecosystems, ed. E.W. Helbling and H.E. Zagarese, 357–397: Royal Society of Chemistry.
55. Villafañe, V.E., E.S. Barbieri, and E.W. Helbling. 2004a. Annual patterns of ultraviolet radiation effects on temperate marine phytoplankton off Patagonia, Argentina. Journal of Plankton Research 26: 167–174.
56. Villafañe, V.E., A.G.J. Buma, P. Boelen, and E.W. Helbling. 2004b. Solar UVR-induced DNA damage and inhibition of photosynthesis in phytoplankton from Andean lakes of Argentina. Archiv für Hydrobiologie 161: 245–266.
57. Villafañe, V.E., M.A. Marcoval, and E.W. Helbling. 2004c. Photosynthesis versus irradiance characteristics in phytoplankton assemblages off Patagonia (Argentina): Temporal variability and solar UVR effects. Marine Ecology Progress Series 284: 23–34.
58. Villafañe, V.E., P.J. Janknegt, M. de Graaff, R.J.W. Visser, W.H. van de Poll, A.G.J. Buma, and E.W. Helbling. 2008. UVR-induced photoinhibition of summer marine phytoplankton communities from Patagonia. Marine Biology 154: 1021–1029.
59. Villafañe, V.E., A.T. Banaszak, S.D. Guendulain-García, S.M. Strauch, S.R. Halac, and E.W. Helbling. 2013a. Influence of seasonal variables associated with climate change on photochemical diurnal cycles of marine phytoplankton from Patagonia (Argentina). Limnology and Oceanography 58: 203–214.
60. Villafañe, V.E., G.S. Erzinger, S.M. Strauch, and E.W. Helbling. 2013b. Photochemical activity of PSII under UVR exposure and nutrient addition of phytoplankton communities from Babitonga Bay (Santa Catarina, Southern Brazil). Journal of Experimental Marine Biology and Ecology. Submitted for publication.
61. Zar, J.H. 1999. Biostatistical analysis. Englewood Cliffs, NJ: Prentice Hall.
62. Zhou, W., K. Yin, X. Yuan, and X. Ning. 2009. Comparison of the effects of short-term UVB radiation exposure on phytoplankton photosynthesis in the temperate Changjiang and subtropical Zhujiang estuaries of China. Journal of Oceanography 65: 627–638.