Scaling of growth rate and mortality with size and its consequence on size spectra of natural microphytoplankton assemblages in the East China Sea

Biogeosciences

Volumn 10, Issue 8, 2013, Pages 5267-5280

  Chang, F H ^a   Marquis, E C ^b   Chang, C W ^c   Gong, G C ^d,e   Hsieh, C H ^a,b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c NATIONAL CENTRAL UNIVERSITY   (Taiwan)

^d NATIONAL TAIWAN OCEAN UNIVERSITY   (Taiwan)

^e NATIONAL APPLIED RESEARCH LABORATORIES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOMETRY; BODY SIZE; GRAZING; GROWTH RATE; IMAGING METHOD; MACROECOLOGY; MICROPLANKTON; MORTALITY; PHYTOPLANKTON; SIZE STRUCTURE; TOP-DOWN CONTROL;

EAST CHINA SEA; PACIFIC OCEAN;

EID: 84881432481     PISSN: 17264170     EISSN: 17264189     Source Type: Journal    
DOI: 10.5194/bg-10-5267-2013     Document Type: Article

References (92)

1. Agawin, N. S. R., Duarte, C. M., and Agusti, S.: Nutrient and temperature control of the contribution of picoplankton to phyto-plankton biomass and production, Limnol. Oceanogr., 45, 591-600, 2000.
2. Allen, A. P., Gillooly, J. F., and Brown, J. H.: Linking the global carbon cycle to individual metabolism, Funct. Ecol., 19, 202-213, 2005.
3. Alvarez, E., Lopez-Urrutia, A., Nogueira, E., and Fraga, S.: How to effectively sample the plankton size spectrum? A case study using FlowCAM, J. Plankton Res., 33, 1119-1133, 2011.
4. Banavar, J. R., Damuth, J., Maritan, A., and Rinaldo, A.: Supply-demand balance and metabolic scaling, P. Natl. Acad. Sci. USA, 99, 10506-10509, 2002.
5. Barnes, C., Irigoien, X., De Oliveira, J. A. A., Maxwell, D., and Jennings, S.: Predicting marine phytoplankton community size structure from empirical relationships with remotely sensed variables, J. Plankton Res., 33, 13-24, 2011.
6. Berner, T., Dubinsky, Z., Wyman, K., and Falkowski, P. G.: Photoadaptation and the "package effect" in Dunaliella tertiolecta (Chlorophyceae), J. Phycol., 25, 70-78, 1989.
7. Bissinger, J. E., Montagnes, D. J. S., Sharples, J., and Atkinson, D.: Predicting marine phytoplankton maximum growth rates from temperature: Improving on the Eppley curve using quantile regression, Limnol. Oceanogr., 53, 487-493, 2008.
8. Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H., and White, J.-S. S.: Generalized linear mixed models: a practical guide for ecology and evolution, Trends Ecol. Evol., 24, 127-135, 2009.
9. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M., and West, G. B.: Toward a metabolic theory of ecology, Ecology, 85, 1771-1789, 2004.
10. Brucet, S., Boix, D., Quintana, X. D., Jensen, E., Nathansen, L. W., Trochine, C., Meerhoff, M., Gascon, S., and Jeppesen, E.: Factors influencing zooplankton size structure at contrasting temperatures in coastal shallow lakes: Implications for effects of climate change, Limnol. Oceanogr., 55, 1697-1711, 2010.
11. Burkill, P. H., Mantoura, R. F. C., Llewellyn, C. A., and Owens, N. J. P.: Microzooplankton grazing and selectivity of phytoplankton in coastal waters, Mar. Biol., 93, 581-590, 1987.
12. Calbet, A.: The trophic roles of microzooplankton in marine systems, ICES J. Mar. Sci., 65, 325-331, 2008.
13. Calbet, A. and Landry, M. R.: Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems, Limnol. Oceanogr., 49, 51-57, 2004.
14. Calbet, A., Landry, M. R., and Nunnery, S.: Bacteria-flagellate interactions in the microbial food web of the oligotrophic subtropical North Pacific, Aquat. Microb. Ecol., 23, 283-292, 2001.
15. Calbet, A., Trepat, I., Almeda, R., Salo, V., Saiz, E., Movilla, J. I., Alcaraz, M., Yebra, L., and Simo, R.: Impact of micro-and nanograzers on phytoplankton assessed by standard and size-fractionated dilution grazing experiments, Aquat. Microb. Ecol., 50, 145-156, 2008.
16. Cavender-Bares, K. K., Rinaldo, A., and Chisholm, S. W.: Micro-bial size spectra from natural and nutrient enriched ecosystems, Limnol. Oceanogr., 46, 778-789, 2001.
17. Cermeño, P., Marañón, E., Rodríguez, J., and Fernádez, E.: Large-sized phytoplankton sustain higher carbon-specific photosynthesis than smaller cells in a coastal eutrophic ecosystem, Mar. Ecol.-Prog. Ser., 297, 51-60, 2005.
18. Chan, Y.-F., Tsai, A.-Y., Chiang, K.-P., and Hsieh, C.-h.: Pigmented nanoflagellates grazing on Synechococcus: seasonal variations and effect of flagellate size in the coastal ecosystem of subtropical western pacific, Microb. Ecol., 58, 548-557, 2009.
19. Chang, J., Lin, K. H., Chen, K. M., Gong, G. C., and Chiang, K. P.: Synechococcus growth and mortality rates in the East China Sea: range of variations and correlation with environmental factors, Deep-Sea Res. Pt. II, 50, 1265-1278, 2003.
20. Chen, B. Z. and Liu, H. B.: Relationships between phytoplank-ton growth and cell size in surface oceans: Interactive effects of temperature, nutrients, and grazing, Limnol. Oceanogr., 55, 965-972, 2010.
21. Chen, B. Z., Liu, H. B., Landry, M. R., Dai, M. H., Huang, B. Q., and Sun, J.: Close coupling between phytoplankton growth and microzooplankton grazing in the western South China Sea, Lim-nol. Oceanogr., 54, 1084-1097, 2009.
22. Dolan, J. R. and McKeon, K.: The reliability of grazing rate estimates from dilution experiments: Have we over-estimated rates of organic carbon consumption by microzooplankton?, Ocean Sci., 1, 1-7, doi:10.5194/os-1-1-2005, 2005.
23. Dolan, J. R., Gallegos, C. L., and Moigis, A.: Dilution effects on microzooplankton in dilution grazing experiments, Mar. Ecol.-Prog. Ser., 200, 127-139, 2000.
24. Edwards, K. F., Thomas, M. K., Klausmeier, C. A., and Litchman, E.: Allometric scaling and taxonomic variation in nutrient utilization traits and maximum growth rate of phytoplankton, Limnol. Oceanogr., 57, 554-566, 2012.
25. Eppley, R. W.: Temperature and phytoplankton growth in the sea, Fish. B.-NOAA, 70, 1063-1085, 1972.
26. Finkel, Z. V.: Light absorption and size scaling of light-limited metabolism in marine diatoms, Limnol. Oceanogr., 46, 86-94, 2001.
27. Finkel, Z. V., Irwin, A. J., and Schofield, O.: Resource limitation alters the 3/4 size scaling of metabolic rates in phytoplankton, Mar. Ecol.-Prog. Ser., 273, 269-279, 2004.
28. Froneman, P. W. and McQuaid, C. D.: Preliminary investigation of the ecological role of microzooplankton in the Kariega Estuary, South Africa, Estuar. Coast. Shelf S., 45, 689-695, 1997.
29. Gaul, W. and Antia, A. N.: Taxon-specific growth and selective microzooplankton grazing of phytoplankton in the Northeast Atlantic, J. Marine Syst., 30, 241-261, 2001.
30. Glazier, D. S.: Beyond the '3/4-power law': variation in the intra-and interspecific scaling of metabolic rate in animals, Biol. Rev., 80, 611-662, 2005.
31. Glazier, D. S.: A unifying explanation for diverse metabolic scaling in animals and plants, Biol. Rev., 85, 111-138, 2010.
32. Gong, G. C., Chen, Y. L. L., and Liu, K. K.: Chemical hydrography and chlorophyll a distribution in the East China Sea in summer: Implications in nutrient dynamics, Cont. Shelf Res., 16, 1561-1590, 1996.
33. Gong, G. C., Shiah, F. K., Liu, K. K., Wen, Y. H., and Liang, M. H.: Spatial and temporal variation of chlorophyll a, primary productivity and chemical hydrography in the southern East China Sea, Cont. Shelf Res., 20, 411-436, 2000.
34. Gong, G. C., Wen, Y. H., Wang, B. W., and Liu, G. J.: Seasonal variation of chlorophyll a concentration, primary production and environmental conditions in the subtropical East China Sea, Deep-Sea Res. Pt. II, 50, 1219-1236, 2003.
35. Gutiérrez-Rodríguez, A., Latasa, M., Mourre, B., and Laws, E. A.: Coupling between phytoplankton growth and microzooplankton grazing in dilution experiments: potential artefacts, Mar. Ecol.-Prog. Ser., 383, 1-9, 2009.
36. Gutiérrez-Rodríguez, A., Latasa, M., Scharek, R., Massana, R., Vila, G., and Gasol, J. M.: Growth and grazing rate dynamics of major phytoplankton groups in an oligotrophic coastal site, Estuar. Coast. Shelf S., 95, 77-87, 2011.
37. Hendriks, A. J.: The power of size: A meta-analysis reveals consistency of allometric regressions, Ecol. Model., 205, 196-208, 2007.
38. Huete-Ortega, M., Calvo-Díaz, A., Graña, R., Mouriño-Carballido, B., and Marañón, E.: Effect of environmental forcing on the biomass, production and growth rate of size-fractionated phy-toplankton in the central Atlantic Ocean, J. Marine. Syst., 88, 203-213, 2011.
39. Huete-Ortega, M., Cermeño, P., Calvo-Díaz, A., and Marañón, E.: Isometric size-scaling of metabolic rate and the size abundance distribution of phytoplankton, P. Roy. Soc. B-Biol. Sci., 279, 1815-1823, 2012.
40. Ide, K., Takahashi, K., Kuwata, A., Nakamachi, M., and Saito, H.: A rapid analysis of copepod feeding using FlowCAM, J. Plankton Res., 30, 275-281, 2008.
41. Irwin, A. J., Finkel, Z. V., Schofield, O. M. E., and Falkowski, P. G.: Scaling-up from nutrient physiology to the size-structure of phy-toplankton communities, J. Plankton Res., 28, 459-471, 2006.
42. Jiao, N. Z., Yang, Y. H., Koshikawa, H., and Watanabe, M.: Influence of hydrographic conditions on picoplankton distribution in the East China Sea, Aquat. Microb. Ecol., 30, 37-48, 2002.
43. Juhl, A. R. and Murrell, M. C.: Interactions between nutrients, phy-toplankton growth, and microzooplankton grazing in a Gulf of Mexico estuary, Aquat. Microb. Ecol., 38, 147-156, 2005.
44. Key, T., McCarthy, A., Campbell, D. A., Six, C., Roy, S., and Finkel, Z. V.: Cell size trade-offs govern light exploitation strategies in marine phytoplankton, Environ. Microbiol., 12, 95-104, 2010.
45. Kiørboe, T.: Turbulence, phytoplankton cell size, and the structure of pelagic food webs, Adv. Mar. Biol., 29, 1-72, 1993.
46. Landry, M. R. and Calbet, A.: Reality checks on microbial food web interactions in dilution experiments: responses to the comments of Dolan and McKeon, Ocean Sci., 1, 39-44, 2005, http://www.ocean-sci.net/1/39/2005/.
47. Landry, M. R. and Hassett, R. P.: Estimating the grazing impact of marine micro-zooplankton, Mar. Biol., 67, 283-288, 1982.
48. Landry, M. R., Kirshtein, J., and Constantinou, J.: A refined dilution technique for measuring the community grazing impact of microzooplankton, with experimental tests in the central equatorial Pacific, Mar. Ecol.-Prog. Ser., 120, 53-63, 1995.
49. Landry, M. R., Constantinou, J., Latasa, M., Brown, S. L., Bidi-gare, R. R., and Ondrusek, M. E.: Biological response to iron fertilization in the eastern equatorial Pacific (IronEx II), III. Dynamics of phytoplankton growth and microzooplankton grazing, Mar. Ecol.-Prog. Ser., 201, 57-72, 2000.
50. Latasa, M., Morán, X. A. G., Scharek, R., and Estrada, M.: Estimating the carbon flux through main phytoplankton groups in the northwestern Mediterranean, Limnol. Oceanogr., 50, 1447-1458, 2005.
51. Legendre, P. and Legendre, L.: Numerical ecology, 2nd English Edn., Elsevier Science B. V., Amsterdam, the Netherlands, i-xv, 1-853, 1998.
52. Lessard, E. J. and Murrell, M. C.: Microzooplankton herbivory and phytoplankton growth in the northwestern Sargasso Sea, Aquat. Microb. Ecol., 16, 173-188, 1998.
53. Li, W. K. W.: Macroecological patterns of phytoplankton in the northwestern North Atlantic Ocean, Nature, 419, 154-157, 2002.
54. Lie, A. A. Y. and Wong, C. K.: Selectivity and grazing impact of microzooplankton on phytoplankton in two subtropical semi-enclosed bays with different chlorophyll concentrations, J. Exp. Mar. Biol. Ecol., 390, 149-159, 2010.
55. Litchman, E., Klausmeier, C. A., Schofield, O. M., and Falkowski, P. G.: The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level, Ecol. Lett., 10, 1170-1181, 2007.
56. Lopez-Urrutia, A., San Martin, E., Harris, R. P., and Irigoien, X.: Scaling the metabolic balance of the oceans, P. Natl. Acad. Sci. USA, 103, 8739-8744, 2006.
57. Maguer, J. F., L'Helguen, S., Waeles, M., Morin, P., Riso, R., and Caradec, J.: Size-fractionated phytoplankton biomass and nitrogen uptake in response to high nutrient load in the North Biscay Bay in spring, Cont. Shelf Res., 29, 1103-1110, 2009.
58. Marañón, E.: Inter-specific scaling of phytoplankton production and cell size in the field, J. Plankton Res., 30, 157-163, 2008.
59. Marañón, E., Cermeno, P., Rodriguez, J., Zubkov, M. V., and Harris, R. P.: Scaling of phytoplankton photosynthesis and cell size in the ocean, Limnol. Oceanogr., 52, 2190-2198, 2007.
60. Marañón, E., Cermeño, P., Latasa, M., and Tadonléké, R. D.: Temperature, resources, and phytoplankton size structure in the ocean, Limnol. Oceanogr., 57, 1266-1278, 2012.
61. Marañón, E., Cermeño, P., López-Sandoval, D. C., Rodríguez-Ramos, T., Sobrino, C., Huete-Ortega, M., Blanco, J. M., and Rodríguez, J.: Unimodal size scaling of phytoplankton growth and the size dependence of nutrient uptake and use, Ecol. Lett., 16, 371-379, 2013.
62. Marba, N., Duarte, C. M., and Agusti, S.: Allometric scaling of plant life history, P. Natl. Acad. Sci. U. S. A., 104, 15777-15780, 2007.
63. Marquis, E., Niquil, N., and Dupuy, C.: Does the study of microzooplankton community size structure effectively define their dynamics? Investigation in the Bay of Biscay (France), J. Plankton Res., 33, 1104-1118, 2011.
64. McCoy, M. W. and Gillooly, J. F.: Predicting natural mortality rates of plants and animals, Ecol. Lett., 11, 710-716, 2008.
65. McManus, G. B., Costas, B. A., Dam, H. G., Lopes, R. M., Gaeta, S. A., Susini, S. M., and Rosetta, C. H.: Microzooplankton grazing of phytoplankton in a tropical upwelling region, Hydrobiologia, 575, 69-81, 2007.
66. Montagnes, D. J. S., Barbosa, A. B., Boenigk, J., Davidson, K., Jur-gens, K., Macek, M., Parry, J. D., Roberts, E. C., and Simek, K.: Selective feeding behaviour of key free-living protists: avenues for continued study, Aquat. Microb. Ecol., 53, 83-98, 2008.
67. Moran, X. A. G., Lopez-Urrutia, A., Calvo-Diaz, A., and Li, W. K. W.: Increasing importance of small phytoplankton in a warmer ocean, Global Change Biol., 16, 1137-1144, 2010.
68. Murrell, M. C., Stanley, R. S., Lores, E. M., DiDonato, G. T., and Flemer, D. A.: Linkage between microzooplankton grazing and phytoplankton growth in a Gulf of Mexico estuary, Estuaries, 25, 19-29, 2002.
69. Platt, T. and Denman, K.: Organization in pelagic ecosystem, Helgoländer wissenschaftliche Meeresuntersuchungen, 30, 575-581, 1977.
70. Power, M. E.: Top-down and bottom-up forces in food webs-do plants have primacy?, Ecology, 73, 733-746, 1992.
71. Reckermann, M. and Veldhuis, M. J. W.: Trophic interactions between picophytoplankton and micro-and nanozooplankton in the western Arabian Sea during the NE monsoon 1993, Aquat. Mi-crob. Ecol., 12, 263-273, 1997.
72. Reich, P. B., Tjoelker, M. G., Machado, J. L., and Oleksyn, J.: Universal scaling of respiratory metabolism, size and nitrogen in plants, Nature, 439, 457-461, 2006.
73. Reul, A., Rodriguez, V., Jimenez-Gomez, F., Blanco, J. M., Bautista, B., Sarhan, T., Guerrero, F., Ruiz, J., and Garcia-Lafuente, J.: Variability in the spatio-temporal distribution and size-structure of phytoplankton across an upwelling area in the NW-Alboran Sea, (W-Mediterranean), Cont. Shelf Res., 25, 589-608, 2005.
74. Reul, A., Rodriguez, J., Guerrero, F., Gonzalez, N., Vargas, J. M., Echevarria, F., Rodriguez, V., and Jimenez-Gomez, F.: Distribution and size biomass structure of nanophytoplankton in the Strait of Gibraltar, Aquat. Microb. Ecol., 52, 253-262, 2008.
75. Ricklefs, R. E.: Evolutionary theories of aging: Confirmation of a fundamental prediction, with implications for the genetic basis and evolution of life span, Am. Nat., 152, 24-44, 1998.
76. Safi, K. A., Brian Griffiths, F., and Hall, J. A.: Microzooplankton composition, biomass and grazing rates along the WOCE SR3 line between Tasmania and Antarctica, Deep-Sea Res. Pt. I, 54, 1025-1041, 2007.
77. Savage, V. M., Deeds, E. J., and Fontana, W.: Sizing up al-lometric scaling theory, PLoS Comput. Biol., 4, e1000171, doi:10.1371/journal.pcbi. 1000171, 2008.
78. Seibel, B. A.: On the depth and scale of metabolic rate variation: scaling of oxygen consumption rates and enzymatic activity in the Class Cephalopoda (Mollusca), J. Exp. Biol., 210, 1-11, 2007.
79. Sheldon, R. W., Sutcliff, W. H., and Prakash, A.: Size distribution of particles in the ocean, Limnol. Oceanogr., 17, 327-340, 1972.
80. Shurin, J. B., Clasen, J. L., Greig, H. S., Kratina, P., and Thompson, P. L.: Warming shifts top-down and bottom-up control of pond food web structure and function, Philos. T. Roy. Soc.-B., 367, 3008-3017, 2012.
81. Stolte, W., McCollin, T., Noordeloos, A. A. M., and Riegman, R.: Effect of nitrogen-source on the size distribution within marine-phytoplankton populations, J. Exp. Mar. Biol. Ecol., 184, 83-97, 1994.
82. Strom, S. L.: Novel interactions between phytoplankton and microzooplankton: their influence on the coupling between growth and grazing rates in the sea, Hydrobiologia, 480, 41-54, 2002.
83. Strom, S. L. and Welschmeyer, N. A.: Pigment-specific rates of phy-toplankotn growth and micrzooplankton grazing in the open subarctic pacific-ocean, Limnol. Oceanogr., 36, 50-63, 1991.
84. Teixeira, I. G., Figueiras, F. G., Crespo, B. G., and Piedracoba, S.: Microzooplankton feeding impact in a coastal upwelling system on the NW Iberian margin: The Ría de Vigo, Estuar. Coast. Shelf S., 91, 110-120, 2011.
85. Thingstad, T. F., Ovreas, L., Egge, J. K., Lovdal, T., and Heldal, M.: Use of non-limiting substrates to increase size; a generic strategy to simultaneously optimize uptake and minimize predation in pelagic osmotrophs?, Ecol. Lett., 8, 675-682, 2005.
86. Tilman, D., Hillerislambers, J., Harpole, S., Dybzinski, R., Far-gione, J., Clark, C., and Lehman, C.: Does metabolic theory apply to community ecology? It's a matter of scale, Ecology, 85, 1797-1799, 2004.
87. Tsai, A. Y., Gong, G. C., Sanders, R. W., Chen, W. H., Chao, C. F., and Chiang, K. P.: Importance of bacterivory by pigmented and heterotrophic nanoflagellates during the warm season in a subtropical western Pacific coastal ecosystem, Aquat. Microb. Ecol., 63, 9-18, 2011.
88. Verdy, A., Follows, M., and Flierl, G.: Optimal phytoplankton cell size in an allometric model, Mar. Ecol.-Prog. Ser., 379, 1-12, 2009.
89. Wong, G. T. F., Gong, G. C., Liu, K. K., and Pai, S. C.: "Excess nitrate" in the East China Sea, Estuar. Coast. Shelf S., 46, 411-418, 1998.
90. Yvon-Durocher, G., Montoya, J. M., Trimmer, M., and Woodward, G. U. Y.: Warming alters the size spectrum and shifts the distribution of biomass in freshwater ecosystems, Global Change Biol., 17, 1681-1694, 2011.
91. Zhang, J., Liu, S. M., Ren, J. L., Wu, Y., and Zhang, G. L.: Nutrient gradients from the eutrophic Changjiang (Yangtze River) Estuary to the oligotrophic Kuroshio waters and re-evaluation of budgets for the East China Sea Shelf, Prog. Oceanogr., 74, 449-478, 2007.
92. Zhang, L. Y., Sun, J., Liu, D. Y., and Yu, Z. S.: Studies on growth rate and grazing mortality rate by microzooplankton of size-fractionated phytoplankton in spring and summer in the Jiaozhou Bay, China, Acta. Oceanol. Sin., 24, 85-101, 2005.