Interactive effects of vertical mixing, nutrients and ultraviolet radiation: In situ photosynthetic responses of phytoplankton from high mountain lakes in Southern Europe

Biogeosciences

Volumn 10, Issue 2, 2013, Pages 1037-1050

  Helbling, E W ^a   Carrillo, P ^b   Medina Sanchez J M ^c   Duran C ^b   Herrera, G ^b   Villar Argaiz, M ^c   Villafane V E ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b UNIVERSITY OF GRANADA   (Spain)

^c UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CLIMATE CHANGE; DUST; GLOBAL CHANGE; HUMAN ACTIVITY; INHIBITION; IRRADIANCE; LACUSTRINE ENVIRONMENT; MOUNTAIN ENVIRONMENT; NUTRIENT AVAILABILITY; ORGANIC CARBON; PHOTOSYNTHESIS; PHOTOSYNTHETICALLY ACTIVE RADIATION; PHYTOPLANKTON; SOLAR RADIATION; TROPHIC INTERACTION; ULTRAVIOLET RADIATION; VERTICAL MIXING;

SPAIN;

EID: 84873905946     PISSN: 17264170     EISSN: 17264189     Source Type: Journal    
DOI: 10.5194/bg-10-1037-2013     Document Type: Article

References (68)

1. APHA: Standard methods for the examination of water and wastew-ater, American Public Health Association, Washington, USA, 1992.
2. Ayoub, L. M., Hallock, P., Coble, P. G., and Bell, S. S.: MAA-like absorbing substances in Florida Keys phytoplankton vary with distance from shore and CDOM: Implications for coral reefs, J. Exp. Mar. Biol. Ecol., 420, 91-98, 2012.
3. Barbieri, E. S., Villafañe, V. E., and Helbling, E. W.: Experimental assessment of UV effects upon temperate marine phytoplankton when exposed to variable radiation regimes, Limnol. Oceanogr., 47, 1648-1655, 2002.
4. 2, and nutrient limitation on marine primary producers, Photochem. Photobiol. Sci., 8, 1257-1265, 2009.
5. Bullejos, F. J., Carrillo, P., Villar-Argaiz, M., and Medina-Sánchez, J. M.: Roles of phosphorus and ultraviolet radiation in the strength of phytoplankton-zooplankton coupling in a Mediterranean high mountain lake, Limnol. Oceanogr., 55, 2549-2562, 2010.
6. Buma, A. G. J., Boelen, P., and Jeffrey, W. H.: UVR-induced DNA damage in aquatic organisms, in: UV effects in aquatic organisms and ecosystems, edited by: Helbling, E. W. and Zagarese, H. E., Series in Photochemical and Photobiological Sciences, The Royal Society of Chemistry, Cambridge, UK, 291-327, 2003.
7. Buma, A. G. J., Visser, R. J., Van de Poll, W., Villafañe, V. E., Janknegt, P. J., and Helbling, E. W.: Wavelength-dependent xan-thophyll cycle activity in marine microalgae exposed to natural ultraviolet radiation, Eur. J. Phycol., 44, 515-524, 2009.
8. Carrillo, P., Reche, I., Sánchez-Castillo, P., and Cruz-Pizarro, L.: Direct and indirect effects of grazing on the phytoplankton seasonal succession in an oligotrophic lake, J. Plankton Res., 17, 1363-1379, 1995.
9. Carrillo, P., Reche, I., and Cruz-Pizarro, L.: Intraspecific stoichio-metric variability and the ratio of nitrogen to phosphorus resup-plied by zooplankton, Freshwat. Biol., 36, 363-374, 1996.
10. Carrillo, P., Medina-Sánchez, J. M., and Villar-Argaiz, M.: The interaction of phytoplankton and bacteria in a high mountain lake: Importance of the spectral composition of solar radiation, Lim-nol. Oceanogr., 47, 1294-1306, 2002.
11. Carrillo, P., Delgado-Molina, J. A., Medina-Sánchez, J. M., Bullejos, F. J., and Villar-Argaiz, M.: Phosphorus inputs unmask negative effects of ultraviolet radiation on algae in a high mountain lake, Global Change Biol., 14, 423-439, 2008.
12. Catalan, J., Camarero, L., Felip, M., Pla, S., Ventura, M., Buchaca, T., Bartumeus, F., de Mendoza, G., Miró, A., Casamayor, E. O., Medina-Sánchez, J. M., Bacardit, M., Altuna, M., Bartrons, M., and de Quijano, D. D.: High mountain lakes: extreme habitats and witnesses of environmental changes, Limnetica, 25, 551-584, 2006.
13. Christensen, M. R., Graham, M. D., Vinebrooke, R. D., Find-lay, D. L., Paterson, M. J., and Turner, M. A.: Multiple anthropogenic stressors cause ecological surprises in boreal lakes, Global Change Biol., 12, 2316-2322, 2006.
14. Crain, C. M., Kroeker, K., and Halpern, B. S.: Interactive and cumulative effects of multiple human stressors in marine systems, Ecol. Lett., 11, 1304-1315, 2008.
15. Delgado-Molina, J. A.: Efectos interactivos de radiación UV y pulsos de nutrientes sobre la red trófica microbiana: aproximación estructural, estequiométrica y funcional, Ph. D. thesis, Departa-mento de Ecoloǵia, University of Granada, Granada, Spain, 246 pp., 2008.
16. Delgado-Molina, J. A., Carrillo, P., Medina-Sánchez, J. M., Villar-Argaiz, M., and Bullejos, F. J.: Interactive effects of phosphorus loads and ambient ultraviolet radiation on the algal community in a high-mountain lake, J. Plankton Res., 31, 619-634, 2009.
17. Escudero, M., Castillo, S., Querol, X., Avila, A., Alarcón, M., Viana, M. M., Alastuey, A., Cuevas, E., and Rodŕiguez, S.: Wet and dry African dust episodes over eastern Spain, J. Geophys. Res., 110, D18S08, doi:10.1029/2004JD004731, 2005.
18. Evans, C. D., Chapman, P. J., Clark, J. M., Monteith, D. T., and Cresser, M. S.: Alternative explanations for rising dissolved organic carbon export from organic soils, Global Change Biol., 12, 2044-2053, 2006.
19. Falkowski, P. G. and Owens, T. G.: Light-shade adaptation, two strategies in marine phytoplankton, Plant Physiol., 66, 592-595, 1980.
20. Falkowski, P. G. and Wirick, C. D.: A simulation model of the effects of vertical mixing on primary productivity, Mar. Biol., 65, 69-75, 1981.
21. Figueroa, F. L., Salles, S., Aguilera, J., Jiménez, C., Mercado, J., Viñegla, B., Flores-Moya, A., and Altamirano, M.: Effects of solar radiation on photoinhibition and pigmentation in the red alga Porphyra leucosticta, Mar. Ecol. Prog. Ser., 151, 81-90, 1997.
22. Findlay, S. E. G.: Increased carbon transport in the Hudson River: Unexpected consequence of nitrogen deposition?, Front. Ecol. Environ., 3, 133-137, 2005.
23. Folt, C. L., Chen, C. Y., Moore, M. V., and Burnaford, J. L.: Synergism and antagonism among multiple stressors, Limnol. Oceanogr., 44, 864-877, 1999.
24. 2 fixation in marine phy-toplankton: A double-edged sword, Plant. Physiol., 144, 54-59, 2007.
25. Garcia-Pichel, F.: A model for internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens, Limnol. Oceanogr., 39, 1704-1717, 1994.
26. Häder, D.-P., Helbling, E. W., Williamson, C. E., and Worrest, R. C.: Effects of UV radiation on aquatic ecosystems and interactions with climate change, Photochem. Photobiol. Sci., 10, 242-260, 2011.
27. Hallegraeff, G. M.: Ocean climate change, phytoplankton community responses, and harmful algal blooms: A formidable predictive challenge, J. Phycol., 46, 220-235, 2010.
28. Harrison, J. W. and Smith, R. E. H.: The spectral sensitivity of phy-toplankton communities to ultraviolet radiation-induced photoinhibition differs among clear and humic temperate lakes, Limnol. Oceanogr., 56, 2115-2126, 2011.
29. Helbling, E. W., Villafañe, V. E., and Holm-Hansen, O.: 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, edited by: Weiler, C. S. and Penhale, P. A., American Geophysical Union, Washington, DC, USA, 207-227, 1994.
30. Helbling, E. W., Gao, K., Gonçalves, R. J., Wu, H., and Villafañe, V. E.: Utilization of solar UV radiation by coastal phytoplankton assemblages off SE China when exposed to fast mixing, Mar. Ecol. Prog. Ser., 259, 59-66, 2003.
31. Hessen, D. O., Leu, E., Færøvig, P. J., and Petersen, S. F.: Light and spectral properties as determinants of C:N:P-ratios in phyto-plankton., Deep-Sea Res. II, 55, 2169-2175, 2008.
32. Hiriart-Baer, V. P. and Smith, R. E. H.: Models for ultraviolet radiation-dependent photoinhibition of Lake Erie phytoplankton, Limnol. Oceanogr., 49, 202-214, 2004.
33. Hiriart-Baer, V. P. and Smith, R. E. H.: The effect of ultraviolet radiation on freshwater planktonic primary production: The role of recovery and mixing processes, Limnol. Oceanogr., 50, 1352-1361, 2005.
34. Holm-Hansen, O. and Riemann, B.: Chlorophyll a determination: Improvements in methodology, Oikos, 30, 438-447, 1978.
35. Holm-Hansen, O., Lorenzen, C. J., Holmes, R. W., and Strickland, J. D. H.: Fluorometric determination of chlorophyll, J. Cons. Perm. Int. Explor. Mer., 30, 3-15, 1965.
36. IPCC: Climate Change 2007: The physical science basis. Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change, edited by: Solomon, S., Quin, D., Manning, M., Marquis, M., Averyt, K., Tignor, M. M. B., Miller, L. R., Jr., and Chen, Z., Cambridge University Press, New York, USA, 996 pp., 2007.
37. Jabalera Cabrerizo, M.: Influencia de la intensidad y frecuencia de pulsos de nutrientes sobre ecosistemas sometidos a estrés por UVR, Master in Ecology, University of Granada, 2012.
38. Köhler, J., Schmitt, M., Krumbeck, H., Kapfer, M., Litchmann, E., and Neale, P. J.: Effects of UV on carbon assimilation of phy-toplankton in a mixed water column, Aquat. Sci., 63, 294-309, 2001.
39. 14C primary productivity samples, Limnol. Oceanogr., 37, 172-178, 1992.
40. Litchman, E., Neale, P. J., and Banaszak, A. T.: Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: Photoprotection and repair, Limnol. Oceanogr., 47, 86-94, 2002.
41. López-Merino, L., Moreno, A., Leira, M., Sigró, J., González-Sampériz, P., Valero-Garcés, B. L., López-Sáez, J. A., Brunet, M., and Aguilar, E.: Two hundred years of environmental change in Picos de Europa National Park inferred from sediments of Lago Enol, northern Iberia, J. Paleolimnol., 46, 453-467, 2011.
42. Maxwell, K. and Johnson, G. N.: Chlorophyll fluorescence-a practical guide, J. Exp. Bot., 51, 659-668, 2000.
43. Medina-Sánchez, J. M., Villar-Argaiz, M., Sánchez-Castillo, P., Cruz-Pizarro, L., and Carrillo, P.: Structure changes in a planktonic food web: Biotic and abiotic controls, J. Limnol., 58, 213-222, 1999.
44. Medina-Sánchez, J. M., Villar-Argaiz, M., and Carrillo, P.: Solar radiation-nutrient interaction enhances the resource and predation algal control on bacterioplankton: A short-term experimental study, Limnol. Oceanogr., 51, 913-924, 2006.
45. Medina-Sánchez, J. M., Carrillo, P., Delgado-Molina, J. A., Bullejos, F. J., and Villar-Argaiz, M.: Patterns of resource limitation of bacteria along a trophic gradient in Mediterranean inland waters, FEMS Microbiol. Ecol., 74, 554-565, 2010.
46. Morales-Baquero, R., Pulido-Villena, E., and Reche, I.: Atmospheric inputs of phosphorus and nitrogen to the southwest Mediterranean region: Biogeochemical responses of high mountain lakes, Limnol. Oceanogr., 51, 830-837, 2006.
47. Neale, P. J., Davis, R. F., and Cullen, J. J.: Interactive effects of ozone depletion and vertical mixing on photosynthesis of Antarctic phytoplankton, Nature, 392, 585-589, 1998.
48. Neale, P. J., Helbling, E. W., and Zagarese, H. E.: Modulation of UVR exposure and effects by vertical mixing and advection, in: UV effects in aquatic organisms and ecosystems, Comprehensive Series in Photochesmitry and Photobiology, 1, edited by: Hel-bling, E. W. and Zagarese, H. E., The Royal Society of Chemistry, Cambridge, UK, 108-134, 2003.
49. Osburn, C. L. and Morris, D. P.: Photochemistry of chromophoric dissolved organic matter in natural waters, in: UV effects in aquatic organisms and ecosystems, Comprehensive Series in Photochesmitry and Photobiology, 1, edited by: Helbling, E. W. and Zagarese, H., The Royal Society of Chemistry, Cambridge, UK, 185-217, 2003.
50. Porra, R. J.: The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b, Photosynth. Res., 73, 149-156, 2002.
51. Raven, J. A., Giordano, M., Beardall, J., and Maberly, S. C.: Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change, Photosynth. Res., 109, 281-296, 2011.
52. Reche, I., Pulido-Villena, E., Conde-Porcuna, J. M., and Carrillo, P.: Photoreactivity of dissolved organic matter from high-mountain lakes of Sierra Nevada, Spain, Arct. Antarct. Alp. Res., 33, 426-434, 2001.
53. Rocha, O. and Duncan, A.: The relationship between cell carbon and cell volume in freshwater algal species used in zooplankton studies, J. Plankton Res., 7, 279-294, 1985.
54. Rose, K. C., Williamson, C. E., Saros, J. E., Sommaruga, R., and Fischer, J. M.: Differences in UV transparency and thermal structure between alpine and subalpine lakes: implications for organisms, Photochem. Photobiol. Sci., 8, 1244-1256, 2009.
55. Shelly, K., Roberts, S., Heraud, P., and Beardall, J.: Interactions between UV-B exposure and phosphorus nutrition. I. Effects on growth, phosphate uptake, and chlorophyll fluorescence, J. Phy-col., 41, 1204-1211, 2005.
56. United Nations Environment Programme, E. E. A. P.: Environmental effects of ozone depletion and its interactions with climate change: progress report, 2011, Photochem. Photobiol. Sci., 11, 13-27, 2012.
57. Van de Poll, W. H. and Buma, A. G. J.: Does ultraviolet radiation affect the xanthophyll cycle in marine phytoplankton?, Photochem. Photobiol. Sci., 8, 1295-1301, 2009.
58. Velasco, J. L., Araujo, R., Alvarez, M., Colomer, M., and Baltanás, A.: Aportación al conocimiento limnológico de ocho lagos y la-gunas de montaña de Asturias (España). Bol. Real Soc. Esp. Hist. Nat. Biol, 95, 181-191, 1999.
59. Villafañe, V. E. and Reid, F. M. H.: Métodos de microscop'ia para la cuantificación del fitoplancton, in: Manual de Métodos Fi-cológicos, edited by: Alveal, K., Ferrario, M. E., Oliveira, E. C., and Sar, E., Universidad de Concepción, Concepción, Chile, 169-185, 1995.
60. Villafañe, V. E., Helbling, E. W., and Holm-Hansen, O.: Phy-toplankton around Elephant Island, Antarctica. Distribution, biomass and composition, Polar Biol., 13, 183-191, 1993.
61. Villafañe, V. E., Sundbäck, K., Figueroa, F. L., and Helbling, E. W.: Photosynthesis in the aquatic environment as affected by UVR, in: UV effects in aquatic organisms and ecosystems, edited by: Helbling, E. W. and Zagarese, H. E., Comprehensive Series in Photochemical and Photobiological Sciences, The Royal Society of Chemistry, Cambridge, UK, 357-397, 2003.
62. Villafañe, V. E., Buma, A. G. J., Boelen, P., and Helbling, E. W.: Solar UVR-induced DNA damage and inhibition of photosynthesis in phytoplankton from Andean lakes of Argentina, Arch. Hydrobiol., 161, 245-266, 2004.
63. Villafañe, V. E., Gao, K., Li, P., and Helbling, E. W.: Vertical mixing within the epilimnion modulates UVR-induced photoinhibition in tropical freshwater phytoplankton from southern China, Freshwat. Biol., 52, 1260-1270, 2007.
64. Villar-Argaiz, M., Medina-Sánchez, J. M., Cruz-Pizarro, L., and Carrillo, P.: Inter-and intra-annual variability in the phytoplank-ton community of a high mountain lake: the influence of external (atmospheric) and internal (recycled) sources of phosphorus, Freshwat. Biol., 46, 1017-1034, 2001.
65. Villar-Argaiz, M., Bullejos, F. J., Medina-Sánchez, J. M., Ramos-Rodŕiguez, E., Delgado-Molina, J. A., and Carrillo, P.: Disentangling food quantity and quality effects in zooplankton response to P-enrichment and UV radiation, Limnol. Oceanogr., 57, 235-250, 2012.
66. Williamson, C. E. and Rose, K. C.: When UV meets freshwater, Science, 329, 637-639, 2010.
67. Williamson, C. E., Saros, J. E., and Schindler, D. W.: Sentinels of change, Science, 323, 887-888, 2009.
68. Xenopoulos, M. A., Frost, P. C., and Elser, J. J.: Joint effects of UV radiation and phosphorus supply on algal growth rate and elemental composition, Ecology, 83, 423-435, 2002.