Use of pulse-amplitude-modulated fluorescence to assess the physiological status of Cladophora sp. along a water quality gradient

Journal of Phycology

Volumn 44, Issue 6, 2008, Pages 1604-1613

  Hiriart Baer, Véronique P ^a   Arciszewski, Tim J ^b   Malkin, Sairah Y ^c   Guildford, Stephanie J ^c   Hecky, Robert E ^c  

^a ENVIRONMENT CANADA   (Canada)

^b UNIVERSITY OF NEW BRUNSWICK   (Canada)

^c UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Cladophora sp.; Fv Fm; Great Lakes; Nutrient limitation; Pulse amplitude modulated fluorescence

Indexed keywords

ALGAE; CLADOPHORA;

EID: 57449101869     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2008.00588.x     Document Type: Article

References (64)

1. Atkinson, M. J. Smith, S. V. 1983. C:N:P ratios of benthic marine plants. Limnol. Oceanogr. 28 : 568 74.
2. Barbiero, R. P., Tuchman, M. L. Millard, E. S. 2006. Post-dreissenid increases in transparency during summer stratification in the offshore waters of Lake Ontario: is a reduction in whiting events the cause? J. Gt. Lakes Res. 32 : 131 41.
3. Berges, J. A., Charlebois, D. O., Mauzerall, D. C. Falkowski, P. G. 1996. Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiol. 110 : 689 96.
4. Björkman, O. 1981. Responses of different quantum flux densities. In Lange, O. L., Nobel, P. S., Osmond, C. B. Ziegler, H. Eds Physiological Plant Ecology I. Responses to the Physical Environment. Springer-Verlag, Heidelberg, Germany, pp. 57 107.
5. Cleveland, W. S. 1979. Robust locally weighted regression and smoothing scatterplots. J. Am. Stat. Assoc. 74 : 829 36.
6. Cullen, J. J., Yang, X. MacIntyre, H. L. 1992. Nutrient limitation of marine photosynthesis. In Falkowski, P. G. Woodhead, A. D. Eds Primary Productivity and Biogeochemical Cycles in the Sea. Plenum Press, New York, pp. 69 88.
7. Dodds, W. K. Gudder, D. A. 1992. The ecology of Cladophora. J. Phycol. 28 : 415 27.
8. Ensminger, I., Hagen, C. Braune, W. 2000. Strategies providing success in a variable habitat: II. Ecophysiology of photosynthesis of Cladophora glomerata. Plant Cell Environ. 23 : 1129 36.
9. Ensminger, I., Xylander, M., Hagen, C. Braune, W. 2001. Strategies providing success in a variable habitat: III. Dynamic control of photosynthesis in Cladophora glomerata. Plant Cell Environ. 24 : 769 79.
10. Falkowski, P. G. Raven, J. A. 2007. Aquatic Photosynthesis, 2nd ed. Princeton University Press, Princeton, New Jersey, 500 pp.
11. Geider, R. J., Greene, R. M., Kolber, Z., MacIntyre, H. L. Falkowski, P. G. 1993a. Fluorescence assessment of the maximum quantum efficiency of photosynthesis in the western North Atlantic. Deep-Sea Res. Part I Oceanogr. Res. Pap. 40 : 1205 24.
12. Geider, R. J., La Roche, J., Greene, R. M. Olaizola, M. 1993b. Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate and iron starvation. J. Phycol. 29 : 755 66.
13. Geider, R. J., MacIntyre, H. L., Graziano, L. M. McKay, R. M. L. 1998. Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation. Eur. J. Phycol. 33 : 315 32.
14. Genty, B., Briantais, J.-M. Baker, N. R. 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 990 : 87 92.
15. Graziano, L. M., La Roche, J. Geider, R. J. 1996. Physiological responses to phosphorus limitation in batch and steady-state cultures of Dunaliella tertiolecta (Chlorophyta): a unique stress protein as an indicator of phosphate deficiency. J. Phycol. 32 : 825 38.
16. Häder, D.-P. 1997. Penetration and effects of solar UV-B on phytoplankton and macroalgae. Plant Ecol. 128 : 4 13.
17. Harris, V. 2004. Cladophora confounds coastal communities: public perceptions and management dilemmas. In Bootsma, H. A., Jensen, E. R., Young, E. B. Berges, J. A. Eds Cladophora Research and Management in the Great Lakes. Proceedings of a workshop held at the Great Lakes WATER Institute, University of Wisconsin, Milwaukee, pp. 5 13.
18. Hautman, D. P. Munch, D. J. 1997. Determination of Inorganic Anions in Drinking Water by Ion Chromatography. Method 300.1. U. S. EPA, Cincinnati, Ohio.
19. Hecky, R. E., Smith, R. E. H., Barton, D. R., Guildford, S. J., Taylor, W. D., Charlton, M. N. Howell, T. 2003. The near shore phosphorus shunt: a consequence of ecosystem engineering by dreissenids in the Laurentian Great Lakes. Can. J. Fish. Aquat. Sci. 61 : 1285 93.
20. Heinz Walz GmbH 1998. Underwater Fluorometer DIVING-PAM: Submersible Photosynthesis Yield Analyzer, 1st ed. Heinz Walz GmbH, Effeltrich, Germany, 104 pp.
21. Higgins, S. N., Hecky, R. E. Guildford, S. J. 2005a. Modeling the growth, biomass, and tissue phosphorus concentration of Cladophora glomerata in Eastern Lake Erie: model description and field testing. J. Gt. Lakes Res. 31 : 439 55.
22. Higgins, S. N., Hecky, R. E. Guildford, S. J. 2006. Environmental controls of Cladophora growth dynamics in Eastern Lake Erie: application of the Cladophora growth model (CGM). J. Gt. Lakes Res. 32 : 629 44.
23. Higgins, S. N., Howell, E. T., Hecky, R. E., Guildford, S. J. Smith, R. E. H. 2005b. The wall of green: the status of Cladophora glomerata on the northern shores of Lake Erie's eastern basin, 1995-2002. J. Gt. Lakes Res. 31 : 547 63.
24. Holmes, R. M., Aminot, A., Kérouel, R., Hooker, B. A. Peterson, B. J. 1999. A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can. J. Fish. Aquat. Sci. 56 : 1801 8.
25. Howell, E. T., Marvin, C. H., Bilyea, R. W., Kauss, P. B. Somers, K. 1996. Changes in environmental conditions during Dreissena colonization of a monitoring station in eastern Lake Erie. J. Gt. Lakes Res. 22 : 744 56.
26. Jassby, A. D. Platt, R. 1976. Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol. Oceanogr. 21 : 540 1.
27. Kirk, J. T. O. 1994. Optics of UV-B radiation in natural waters. Arch. Hydrobiol. 43 : 1 16.
28. Kolber, Z., Wyman, K. D. Falkowski, P. G. 1990. Natural variability in photosynthetic energy conversion efficiency: a field study in the Gulf of Maine. Limnol. Oceanogr. 35 : 72 9.
29. Kolber, Z., Zehr, J. Falkowski, P. 1988. Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in photosystem II. Plant Physiol. 88 : 923 9.
30. Krause, G. H. Weis, E. 1984. Chlorophyll fluorescence as a tool in plant physiology 2. Interpretation of fluorescence signals. Photosynth. Res. 5 : 139 57.
31. Kruskopf, M. Flynn, K. J. 2006. Chlorophyll content and fluorescence responses cannot be used to gauge reliably phytoplankton biomass, nutrient status or growth rate. New Phytol. 169 : 525 36.
32. Lapointe, B. E. Tenore, K. R. 1981. Experimental outdoor studies with Ulva fasciata Delile. I. Interaction of light and nitrogen on nutrient uptake, growth, and biochemical composition. J. Exp. Mar. Biol. Ecol. 53 : 135 52.
33. Lembi, C. A. 2003. Control of nuisance algae. In Wehr, J. D. Sheath, R. G. Eds Freshwater Algae of North America: Ecology and Classification. Academic Press, Elsevier Science, San Diego, California, pp. 805 34.
34. Lippemeier, S., Frampton, D. M. F., Blackburn, S. I., Geier, S. C. Negri, A. P. 2003. Influence of phosphorus limitation on toxicity and photosynthesis of Alexandrium minutum (Dinophyceae) monitored by in-line detection of variable chlorophyll fluorescence. J. Phycol. 39 : 320 31.
35. Lippemeier, S., Hintze, R., Vanselow, K. H., Hartig, P. Coljin, F. 2001. In-line recording of PAM fluorescence of phytoplankton cultures as a new tool for studying effects of fluctuating nutrient supply on photosynthesis. Eur. J. Phycol. 36 : 89 100.
36. Lohman, K. Priscu, J. C. 1992. Physiological indicators of nutrient deficiency in Cladophora (Chlorophyta) in the Clark Fork of the Columbia River, Montana. J. Phycol. 28 : 443 8.
37. Malkin, S. Y., Guildford, S. J. Hecky, R. E. 2008. Modeling the growth response of Cladophora in a Laurentian Great Lake to the exotic invader Dreissena and to lake warming. Limnol. Oceanogr. 53 : 1111 24.
38. Marwood, C. A., Smith, R. E. H., Furgal, J. A., Charlton, M. N., Solomon, K. R. Greenberg, B. M. 2000. Photoinhibition of natural phytoplankton assemblages in Lake Erie exposed to solar ultraviolet radiation. Can. J. Fish. Aquat. Sci. 57 : 371 9.
39. Maxwell, K. Johnson, G. N. 2000. Chlorophyll fluorescence - a practical guide. J. Exp. Bot. 51 : 659 68.
40. Nicholls, K. H., Hopkins, G. J., Standke, S. J. Nakamoto, L. 2001. Trends in total phosphorus in Canadian near-shore waters of the Laurentian Great Lakes: 1976-1999. J. Gt. Lakes Res. 27 : 402 22.
41. Niyogi, K. K. 2000. Safety valves for photosynthesis. Curr. Opin. Plant Biol. 3 : 455 60.
42. Painter, D. S. Kamaitis, G. 1987. Reduction of Cladophora biomass and tissue phosphorus in Lake Ontario, 1972-83. Can. J. Fish. Aquat. Sci. 44 : 2212 5.
43. Parkhill, J.-P., Maillet, G. Cullen, J. J. 2001. Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J. Phycol. 37 : 517 29.
44. Perkins, R. G., Mouget, J. L., Lefebvre, S. Lavaud, J. 2006. Light response curve methodology and possible implications in the application of chlorophyll fluorescence to benthic diatoms. Mar. Biol. 149 : 703 12.
45. Pillsbury, R. W., Lowe, R. L., Pan, Y. D. Greenwood, J. L. 2002. Changes in the benthic algal community and nutrient limitation in Saginaw Bay, Lake Huron, during the invasion of the zebra mussel (Dreissena polymorpha). J. N. Am. Benthol. Soc. 21 : 238 52.
46. Planas, D., Maberly, S. C. Parker, J. E. 1996. Phosphorus and nitrogen relationships of Cladophora glomerata in two lake basins of different trophic status. Freshw. Biol. 35 : 609 22.
47. Ralph, P. J. Gademann, R. 2005. Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat. Bot. 82 : 222 37.
48. Roberts, J. 1997. Control of the supply line. Science 278 : 2073 4.
49. Rubin, A. B., Venediktov, P. S., Krendeleva, T. E. Paschenko, V. Z. 1986. Influence of the physiological state of plants on primary events of photosynthesis. Photobiochem. Photobiophys. 12 : 185 9.
50. Schreiber, U. 1986. Detection of rapid induction kinetics with a new type of high-frequency modulated chlorophyll fluorometer. Photosynth. Res. 9 : 261 72.
51. Schreiber, U., Bliger, W. Neubauer, C. 1994. Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In Schulze, E.-D. Caldwell, M. M. Eds Ecophysiology of Photosynthesis. Springer, Berlin, pp. 49 70.
52. Schreiber, U., Schliwa, U. Bilger, W. 1986. Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth. Res. 10 : 51 62.
53. Smith, R. E. H., Furgal, J. A., Charlton, M. N., Greenberg, B. M., Hiriart, V. Marwood, C. 1999. Attenuation of ultraviolet radiation in a large lake with low dissolved organic matter concentrations. Can. J. Fish. Aquat. Sci. 56 : 1351 61.
54. Smith, J. E., Runcie, J. W. Smith, C. M. 2005. Characterization of a large-scale ephemeral bloom of the green alga Cladophora sericea on the coral reefs of West Maui, Hawai'i. Mar. Ecol. Prog. Ser. 302 : 77 91.
55. Stainton, M. P., Capel, M. J. Armstrong, F. A. J. 1977. The Chemical Analysis of Fresh Water. 2nd ed. Can. Fish. Mar. Serv. Misc. Spec. Publ. 25, 18 pp.
56. Stankovich, W. S. 2004. The interaction of two nuisance species in Lake Michigan: Cladophora glomerata and Dreissena polymorpha. In Bootsma, H. A., Jensen, E. R., Young, E. B. Berges, J. A. Eds Cladophora Research and Management in the Great Lakes. Proceedings of a workshop held at the Great Lakes WATER Institute, University of Wisconsin, Milwaukee, pp. 31 5.
57. Toohey, B., Kendrick, G. A., Wernber, T., Phillips, J. C., Malkin, S. Prince, J. 2004. The effects of light and thallus scour from Ecklonia radiata canopy on an associated foliose algal assemblage: the importance of photoacclimation. Mar. Biol. 144 : 1019 27.
58. Van Leeuwe, M. A. De Baar, H. J. W. 2000. Photoacclimation by the Antarctic flagellate Pyramimonas sp. (Prasinophyceae) in response to iron limitation. Eur. J. Phycol. 35 : 295 303.
59. Walsby, A. E. 1997. Numerical integration of phytoplankton photosynthesis through time and depth in a water column. New Phytol. 136 : 189 209.
60. Wetzel, R. G. 2001. Limnology: Lake and River Ecosystems, 3rd ed. Academic Press, San Diego, California, 1006 pp.
61. White, A. J. Critchley, C. 1999. Detection of rapid induction kinetics with a new type of high-frequency modulated chlorophyll fluorometer. Photosynth. Res. 59 : 63 72.
62. Wong, S. L. Clark, B. 1976. Field determination of the critical nutrient concentrations for Cladophora in streams. J. Fish. Res. Board Can. 33 : 85 92.
63. Yentsch, C. S., Yentsch, C. M., Phinney, D. A., Lapointe, B. E. Yentsch, S. F. W. 2004. The odyssey of new production. J. Exp. Mar. Biol. Ecol. 300 : 15 30.
64. Zimmermann, C. F., Keefe, C. W. Bashe, J. 1997. Determination of Carbon and Nitrogen in Sediments and Particulates of Estuarine/Coastal Waters Using Elemental Analysis. Method 440.0. U. S. EPA, Cincinnati, Ohio.