The annual cycles of phytoplankton biomass

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1555, 2010, Pages 3215-3226

  Winder, Monika ^a,c   Cloern, James E ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b U S GEOLOGICAL SURVEY   (United States)

^c GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

Author keywords

Aquatic systems; Chlorophyll a; Periodicity; Phenology; Primary producer; Wavelet analysis

Indexed keywords

ANNUAL CYCLE; AQUATIC ECOSYSTEM; BIOMASS; CHLOROPHYLL A; CLIMATE EFFECT; GROWTH RATE; PERIODICITY; PHENOLOGY; PHYTOPLANKTON; PRIMARY PRODUCTION; SIGNAL-TO-NOISE RATIO; TEMPERATE ENVIRONMENT; TROPHIC INTERACTION; WAVELET ANALYSIS;

EID: 77958043933     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0125     Document Type: Article

References (84)

1. Abreu, P. C., Bergesch, M., Proença, L. A., Garcia, C. A. E. & Odebrecht, C. 2010 Short-and long-term chlorophyll a variability in the shallow microtidal Patos Lagoon Estuary, Southern Brazil. Estuaries and Coasts 33, 554-569. (doi:10. 1007/s12237-009-9181-9)
2. Alheit, J., Mollmann, C., Dutz, J., Kornilovs, G., Loewe, P., Mohrholz, V. & Wasmund, N. 2005 Synchronous ecological regime shifts in the central Baltic and the North Sea in the late 1980s. ICES J. Mar. Sci. 62, 1205-1215. (doi:10. 1016/j.icesjms.2005.04.024)
3. Alpine, A. E. & Cloern, J. E. 1992 Trophic interactions and direct physical effects control phytoplankton biomass and production in an estuary. Limnol. Oceanogr. 37, 946-955. (doi:10.4319/lo.1992.37.5.0946)
4. Anneville, O., Gammeter, S. & Straile, D. 2005 Phosphorus decrease and climate variability: mediators of synchrony in phytoplankton changes among European peri-alpine lakes. Freshwater Biol. 50, 1731-1746. (doi:10.1111/j. 1365-2427.2005.01429.x)
5. Behrenfeld, M. J. et al. 2006 Climate-driven trends in contemporary ocean productivity. Nature 444, 752-755. (doi:10.1038/nature05317)
6. Beninca, E., Huisman, J., Heerkloss, R., Jöhnk, K. D., Branco, P., Van Nes, E. H., Scheffer, M. & Ellner, S. P. 2008 Chaos in a long-term experiment with a plankton community. Nature 451, 822-827. (doi:10.1038/ nature06512)
7. Borkman, D. G. & Smayda, T. 2009 Multidecadal (1959-1997) changes in Skeletonema abundance and seasonal bloom patterns in Narragansett Bay, Rhode Island, USA. J. Sea Res. 61, 84-94. (doi:10.1016/j.seares.2008. 10.004)
8. Briceño, H. O. & Boyer, J. N. 2010 Climatic controls on phytoplankton biomass in a sub-tropical estuary, Florida Bay, USA. Estuaries and Coasts 33, 541-553. (doi:10. 1007/s12237-009-9189-1)
9. Calbet, A. & Landry, M. 2004 Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol. Oceanogr. 49, 51-57.
10. Casini, M., Hjelm, J., Molinero, J. C., Lovgren, J., Cardinale, M., Bartolino, V., Belgrano, A. & Kornilovs, G. 2009 Trophic cascades promote threshold-like shifts in pelagic marine ecosystems. Proc. Natl Acad. Sci. USA 106, 197-202. (doi:10.1073/pnas.0806649105)
11. Chatfield, J. R. 1989 The analysis of time series: an introduction. London, UK: Chapman & Hall.
12. Cleland, E. E., Chuine, I., Menzel, A., Mooney, H. A. & Schwartz, M. D. 2007 Shifting plant phenology in response to climate change. Trends Ecol. Evol. 22, 357-365. (doi:10.1016/j.tree.2007.04.003)
13. Cloern, J. E. 1996 Phytoplankton bloom dynamics in coastal ecosystems: a review with some general lessons from sustained investigation of San Francisco Bay, California. Rev. Geophys. 34, 127-168. (doi:10.1029/96RG00986)
14. Cloern, J. E. & Jassby, A. D. 2008 Complex seasonal patterns of primary producers at the land-sea interface. Ecol. Lett. 11, 1294-1303. (doi:10.1111/j.1461-0248. 2008.01244.x)
15. Cloern, J. E. & Jassby, A. 2010 Patterns and scales of phytoplankton variability in estuarine-coastal ecosystems. Estuaries and Coasts 33, 230-241. (doi:10.1007/s12237-009-9195-3)
16. Cloern, J. E., Jassby, A. D., Thompson, J. K. & Hieb, K. A. 2007 A cold phase of the East Pacific triggers new phytoplankton blooms in San Francisco Bay. Proc. Natl Acad. Sci. USA 104, 18 561-18 565. (doi:10.1073pnas. 0706151104)
17. Cushing, D. H. 1959 The seasonal variation in oceanic production as a problem in population dynamics. J. Cons. Cons. Perm. Int. Explor. Mer. 24, 455-464.
18. Dakos, V., Benincà, E., van Nes, E. H., Philippart, C. J. M., Scheffer, M. & Huisman, J. 2009 Interannual variability in species composition explained as seasonally entrained chaos. Proc. R. Soc. B 276, 2871-2880. (doi:10.1098/rspb.2009.0584)
19. Daubechies, I. 1992 Ten lectures on wavelets. SIAM monographs. Philadelphia, PA: SIAM.
20. Edwards, M. & Richardson, A. J. 2004 Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430, 881-884. (doi:10.1038/nature02808)
21. Fahnenstiel, G. L., Bridgeman, T. B., Lang, G. A., McCormick, M. J. & Nalepa, T. F. 1995 Phytoplankton productivity in Saginaw Bay, Lake Huron: effects of zebra mussel (Dreissena polymorpha) colonization. J. Great Lakes Res. 21, 465-475.
22. Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. 1998 Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237-242. (doi:10.1126/science.281.5374.237)
23. Frank, K. T., Petrie, B., Choi, J. S. & Leggett, W. C. 2005 Trophic cascades in a formerly cod-dominated ecosystem. Science 308, 1621-1623. (doi:10.1126/science.1113075)
24. Garcia-Soto, C. & Pingree, R. D. 2009 Spring and summer blooms of phytoplankton (SeaWiFS/MODIS) along a ferry line in the Bay of Biscay and western English Channel. Continental Shelf Res. 29, 1111-1122. (doi:10.1016/j. csr.2008.12.012)
25. Grinsted, A., Moore, J. C. & Jevrejeva, S. 2004 Application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlinear Process. Geophys. 11, 561-566. (doi:10.5194/npg-11-561-2004)
26. Guinder, V. A., Popovich, C. A. & Perillo, G. M. E. 2009 Particulate suspended matter concentrations in the Bahia Blanca Estuary, Argentina: implication for the development of phytoplankton blooms. Estuarine Coastal Shelf Sci. 85, 157-165. (doi:10.1016/j.ecss.2009.05.022)
27. Hall, N. S., Litaker, R. W., Fensin, E., Adolf, J. E., Bowers, H. A., Place, A. R. & Pearl, H. W. 2008 Environmental factors contributing to the development and demise of a toxic dinoflagellate (Karlodinium veneficum) bloom in a shallow, eutrophic, lagoonal estuary. Estuaries and Coasts 31, 1559-2723. (doi:10.1007/s12237-008-9035-x)
28. Harding, L. W. & Perry, E. S. 1997 Long-term increase of phytoplankton biomass in Chesapeake Bay, 1950-94. Mar. Ecol. Progr. Ser. 157, 39-52. (doi:10.3354/meps157039)
29. Harris, G. P. 1986 Phytoplankton ecology: structure, function, and fluctuation. London, UK: Chapman and Hall.
30. Havens, K. E., Elia, A. C., Taticchi, M. I. & Fulton, R. S. 2009 Zooplankton-phytoplankton relationships in shallow subtropical versus temperate lakes Apopka (Florida, USA) and Trasimeno (Umbria, Italy). Hydrobiologia 628, 165-175. (doi:10.1007/s10750-009-9754-4)
31. Hays, G. C., Richardson, A. J. & Robinson, C. 2005 Climate change and marine plankton. Trends Ecol. Evol. 20, 337-344. (doi:10.1016/j.tree.2005.03. 004)
32. Huisman, J., Sharples, J., Stroom, J. M., Visser, P. M., Kardinaal, W. E. A., Verspagen, J. M. H. & Sommeijer, B. 2004 Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85, 2960-2970. (doi:10.1890/03-0763)
33. Ibáñez, I., Primack, R. B., Miller-Rushing, A. J., Ellwood, E., Higuchi, H., Don Lee, S., Kobori, H. & Silander, J. A. 2010 Forecasting phenology under global warming. Phil. Trans. R. Soc. B 365, 3247-3260. (doi:10.1098/rstb. 2010.0120)
34. 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. Cambridge, UK: Cambridge University Press.
35. Jassby, A. D., Müller-Solger, A. B. & Vayssières, M. 2004 Short-term variability of chlorophyll and implications for sampling frequency in the San Joaquin River. IEP Newsletter 18, 21-28.
36. Jenouvrier, S., Weimerskirch, H., Barbraud, C., Park, Y. H. & Cazelles, B. 2005 Evidence of a shift in the cyclicity of Antarctic seabird dynamics linked to climate. Proc. R. Soc. B 272, 887-895. (doi:10.1098/rspb. 2004.2978)
37. Jeppesen, E., Sondergaard, M., Jensen, A. P., Havens, K. et al. 2005 Lakes' response to reduced nutrient loading-an analysis of contemporary data from 35 European and North American long term studies. Freshwater Biol. 50, 1747-1771. (doi:10.1111/j.1365-2427.2005.01415.x)
38. Jöhnk, K. D., Huisman, J., Sharples, J., Sommeijer, B., Visser, P. M. & Stroom, J. M. 2008 Summer heatwaves promote blooms of harmful cyanobacteria. Global Change Biol. 14, 495-512. (doi:10.1111/j.1365-2486. 2007.01510.x)
39. Jolly, W., Nemani, R. & Running, S. 2005 A generalized, bioclimatic index to predict foliar phenology in response to climate. Global Change Biol. 11, 619-632. (doi:10. 1111/j.1365-2486.2005.00930.x)
40. Kahru, M., Kudela, R., Manzano-Sarabia, M. & Mitchell, B. G. 2009 Trends in primary production in the California current detected with satellite data. J. Geophys. Res.-Oceans 114, C02004. (doi:10.1029/2008JC004979)
41. Karentz, D. & Smayda, T. J. 1998 Temporal patterns and variations in phytoplankton community organization and abundance in Narragansett Bay during 1959-1980. J. Plankton Res. 20, 145-168. (doi:10.1093/plankt/20.1. 145)
42. Keitt, T. H. & Fischer, J. 2006 Detection of scale-specific community dynamics using wavelets. Ecology 87, 2895-2904. (doi:10.1890/0012-9658 (2006) 87[2895: DOSCDU]2.0.CO;2)
43. Kromkamp, J. C. & Van Engeland, T. 2010 Changes in phytoplankton biomass in the Western Scheldt Estuary during the period 1978-2006. Estuaries and Coasts 33, 270-285. (doi:10.1007/s12237-009-9215-3)
44. Li, W. K. W., Lewis, M. W. & Harrison, W. G. 2010 Multiscalarity of the nutrient-chlorophyll relationship in coastal phytoplankton. Estuaries and Coasts 33, 440-447. (doi:10.1007/s12237-008-9119-7)
45. Lieh, H. 1974 Phenology and seasonality modelling. New York, NY: Springer.
46. Liu, Y., Liang, X. S. & Weisberg, R. H. 2007 Rectification of the bias in the wavelet power spectrum. J. Atmos. Oceanic Technol. 24, 2093-2102. (doi:10.1175/2007JTECHO511.1)
47. Longhurst, A. 1995 Seasonal cycles of pelagic production and consumption. Progr. Oceanogr. 36, 77-167. (doi:10. 1016/0079-6611 (95) 00015-1)
48. Lunetta, R. S., Knight, J. F., Paerl, H. W., Streicher, J. J., Peierls, B. L., Gallo, T., Lyon, J. G., Mace, T. H. & Buzzelli, C. P. 2009 Measurement of water colour using AVIRIS imagery to assess the potential for an operational monitoring capability in the Pamlico Sound Estuary, USA. Int. J. Remote Sensing 30, 3291-3314. (doi:10. 1080/01431160802552801)
49. Makarewicz, J. C., Lewis, T. W. & Bertram, P. 1999 Phytoplankton composition and biomass in the offshore waters of Lake Erie: pre-and post Dreissena introduction (1983-1993). J. Great Lakes Res. 25, 135-148. (doi:10. 1016/S0380-1330 (99) 70722-7)
50. McQuatters-Gollop, A., Mee, L. D., Raitsos, D. E. & Shapiro, G. I. 2008 Non-linearities, regime shifts and recovery: the recent influence of climate on Black Sea chlorophyll. J. Mar. Systems 74, 649-658. (doi:10.1016/j.jmarsys.2008.06.002)
51. Melack, J. M. 1979 Temporal variability of phytoplankton in tropical lakes. Oecologia 44, 1-7. (doi:10.1007/BF00346388)
52. Menzel, A. & Fabian, P. 1999 Growing season extended in Europe. Nature 397, 659-659. (doi:10.1038/17709)
53. Myneni, R. B., Keeling, C. D., Tucker, C. J., Asrar, G. & Nemani, R. R. 1997 Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386, 698-702. (doi:10.1038/386698a0)
54. Paerl, H. W. & Huisman, J. 2008 Blooms like it hot. Science 320, 57-58. (doi:10.1126/science.1155398)
55. Paerl, H. W., Karen, L., Rossignol, S., Hall, N., Peierls, B. L. & Wetz, M. S. 2010 Phytoplankton community indicators of short-and long-term ecological change in the anthropogenically and climatically impacted Neuse River Estuary, North Carolina, USA. Estuaries and Coasts 33, 485-497. (doi:10.1007/s12237-009-9137-0)
56. Penuelas, J. & Filella, I. 2001 Responses to a warming world. Science 294, 793-794. (doi:10.1126/science.1066860)
57. Percival, D. B. & Walden, A. T. 2000 Wavelet methods for time series analysis. Cambridge, UK: Cambridge University Press.
58. Philippart, C. J. M., van Iperen, J. M., Cadée, G. C. & Zuur, A. F. 2010 Long-term field observations on seasonality in chlorophyll-a concentrations in a shallow coastal marine ecosystem, the Wadden Sea. Estuaries and Coasts 33, 286-294. (doi:10.1007/s12237-009-9236-y)
59. Platt, T., Fuentes-Yaco, C. & Frank, K. T. 2003 Spring algal bloom and larval fish survival. Nature 423, 398-399. (doi:10.1038/423398b)
60. Platt, T., Sathyendranath, S., White, G. N., Fuentes-Yaco, C., Zhai, L., Devred, E. & Tang, C. 2010 Diagnostic properties of phytoplankton time series from remote sensing. Estuaries and Coasts 33, 428-439. (doi:10.1007/s12237-009-9161-0)
61. Pratt, D. M. 1959 The phytoplankton of Narragansett Bay. Limnol. Oceanogr. 4, 425-440. (doi:10.4319/lo.1959.4. 4.0425)
62. R Development Core Team 2009 R: Language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
63. Reynolds, C. S. 2006 Ecology of phytoplankton. Cambridge, UK: Cambridge University Press.
64. Richardson, A. D. et al. 2010 Influence of spring and autumn phenological transitions on forest ecosystem productivity. Phil. Trans. R. Soc. B 365, 3227-3246. (doi:10.1098/rstb.2010.0102)
65. Scheffer, M. 1991 Should we expect strange attractors behind plankton dynamics-and if so, should we bother? J. Plankton Res. 13, 1291-1305. (doi:10.1093/plankt/13.6.1291)
66. Schindler, D. W. 2001 The cumulative effects of climate warming and other human stresses on Canadian freshwaters in the new millennium. Canad. J. Fish. Aquatic Sci. 58, 18-29. (doi:10.1139/cjfas-58-1-18)
67. Schindler, D. W. et al. 1990 Effects of climatic warming on Lakes of the Central Boreal Forest. Science 250, 967-970. (doi:10.1126/science.250.4983.967)
68. Siegel, H., Ohde, T., Gerth, M., Lavik, G. & Leipe, T. 2007 Identification of coccolithophore blooms in the SE Atlantic Ocean off Namibia by satellites and in-situ methods. Continental Shelf Res. 27, 258-274. (doi:10. 1016/j.csr.2006.10.003)
69. Smayda, T. J. 1997 What is a bloom? A commentary. Limnol. Oceanogr. 42, 1132-1136. (doi:10.4319/lo.1997.42. 5-part-2.1132)
70. Smayda, T. J. 1998 Patterns of variability characterizing marine phytoplankton, with examples from Narragansett Bay. ICES J. Mar. Sci. 55, 562-573. (doi:10.1006/jmsc. 1998.0385)
71. Smayda, T. J., Borkman, D., Beaugrand, G. & Belgrano, A. 2004 Ecological effects of climate variation in the North Atlantic: phytoplankton. In Marine ecosystems and climate variation-the North Atlantic (eds N. C. Stenseth, G. Ottersen, J. W. Hurrell, A. Belgrano & B. Planque), pp. 49-58. Oxford, UK: Oxford University Press.
72. Smetacek, V. 1985 The annual cycle of Kiel Bight plankton-a long-term analysis. Estuaries 8, 145-157. (doi:10.2307/1351864)
73. Sommer, U., Gaedke, U. & Schweizer, A. 1993 The first decade of oligotrophication of Lake Constance II. The response of phytoplankton taxonomic composition. Oecologia 93, 276-284. (doi:10.1007/BF00317682)
74. Sommer, U., Gliwicz, Z. M., Lampert, W. & Duncan, A. 1986 The PEG-model of seasonal succession of planktonic events in fresh waters. Arch. Hydrobiol. 106, 433-471.
75. Straile, D. 2002 North Atlantic Oscillation synchronizes food-web interactions in central European lakes. Proc. R. Soc. Lond. B 269, 391-395. (doi:10.1098/rspb.2001. 1907)
76. Thackeray, S. J., Jones, I. D. & Maberly, S. C. 2008 Longterm change in the phenology of spring phytoplankton: species-specific responses to nutrient enrichment and climatic change. J. Ecol. 96, 523-535. (doi:10.1111/j. 1365-2745.2008.01355.x)
77. Torrence, C. & Compo, G. P. 1998 A practical guide to wavelet analysis. Bull. Am. Meteorol. Soc. 79, 61-78. (doi:10.1175/1520-0477 (1998) 079<0061:APGTWA>2.0.CO;2)
78. Vasseur, D. A. & Fox, J. W. 2007 Environmental fluctuations can stabilize food web dynamics by increasing synchrony. Ecol. Lett. 10, 1066-1074. (doi:10.1111/j.1461-0248. 2007.01099.x)
79. Verity, P. G. & Borkman, D. G. 2010 A decade of change in the Skidaway River Estuary. III. Plankton. Estuaries and Coasts 33, 513-540. (doi:10.1007/s12237-009-9208-2)
80. White, M. A. et al. 2009 Intercomparison, interpretation, and assessment of spring phenology in North America estimated from remote sensing for 1982-2006. Global Change Biol. 15, 2335-2359. (doi:10.1111/j.1365-2486. 2009.01910.x)
81. Winder, M. & Schindler, D. E. 2004a Climate change uncouples trophic interactions in a lake ecosystem. Ecology 85, 2100-2106. (doi:10.1890/04-0151)
82. Winder, M. & Schindler, D. E. 2004b Climatic effects on the phenology of lake processes. Global Change Biol. 10, 1844-1856. (doi:10.1111/j.1365-2486. 2004.00849.x)
83. Wittemyer, G., Polansky, L., Douglas-Hamilton, I. & Getz, W. M. 2008 Disentangling the effects of forage, social rank, and risk on movement autocorrelation of elephants using Fourier and wavelet analyses. Proc. Natl Acad. Sci. USA 105, 19 108-19 113. (doi:10.1073/pnas. 0801744105)
84. Zhou, L., Tucker, C., Kaufmann, R., Slayback, D., Shabanov, N. & Myneni, R. 2001 Variations in northern vegetation activity inferred from satellite data of vegetation index during 1981 to 1999. J. Geophys. Res.-Atmos. 106, 20069-20083.