Carbon sequestration in ecosystems: The role of stoichiometry

Ecology

Volumn 85, Issue 5, 2004, Pages 1179-1192

  Hessen, Dag O ^a   Ågren, Göran I ^b   Anderson, Thomas R ^c   Elser, James J ^d   De Ruiter, Peter C ^e  

^a UNIVERSITY OF OSLO   (Norway)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^c NATIONAL OCEANOGRAPHY CENTRE   (United Kingdom)

^d ARIZONA STATE UNIVERSITY   (United States)

^e UTRECHT UNIVERSITY   (Netherlands)

Author keywords

C sequestration; C use efficiency; Carbon; Ecosystems; Grazing; Nitrogen; Phosphorus; Stoichiometry, role in carbon sequestration

Indexed keywords

CARBON SEQUESTRATION; MASS BALANCE; NUTRIENT LIMITATION; STOICHIOMETRY;

EID: 1642315811     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/02-0251     Document Type: Article

References (128)

1. Aber, J. D., K. J. Nadelhoffer, P. Steudler, and J. M. Melillo. 1989. Nitrogen saturation in northern forest ecosystems: hypothesis and implications. BioScience 39:378-386.
2. Aerts, R. 1996. Nutrient resorption from senescing leaves of perrennials: are there general patterns? Journal of Ecology 84:597-608.
3. Ågren, G. I., and E. Bosatta. 1998. Theoretical ecosystem Ecology - understanding element cycles. Cambridge University Press, Cambridge, UK.
4. Ågren, G. I., E. Bosatta, and A. M. Magill. 2001. Combining theory and experiment to understand effects of inorganic nitrogen on litter decomposition. Oecologia 128:94-98.
5. Aitkenhead, J. A., and W. H. McDowell. 2000. Soil C:N ratio as a predictor of annual riverine DOC flux at local and global scales. Global Biochemical Cycles 14:127-138.
6. Andersen, T., and D. O. Hessen. 1991. Carbon, nitrogen and phosphorus content in common crustacean zooplankton species. Limnology and Oceanography 36:807-814.
7. Anderson, L. A., and J. L. Sarmiento. 1994. Redfield ratios of remineralization determined by nutrient data analysis. Global Biogeochemical Cycles 8:65-80.
8. Anderson, T. R. 1992. Modelling the influence of food C:N ratio and respiration on growth and nitrogen excretion in marine zooplankton and bacteria. Journal of Plankton Research 14:1645-1671.
9. Anderson, T. R. 1994. Relating C:N ratios in zooplankton food and faecal pellets using a biochemical model. Journal of Experimental Marine Biology and Ecology 184:183-199.
10. Anderson, T. R., M. Boersma, and D. Raubenheimer. 2004. Stoichiometry: linking elements to biochemicals. Ecology 85:1193-1202.
11. 1 in the English Channel. Estuarine, Coastal and Shelf Science 46:93-109.
12. Andrews, M., J. A. Raven, and J. J. Sprent. 2001. Environmental effects on dry matter partitioning between shoot and root of crop plants: relations with growth and shoot protein concentration. Annals of Applied Biology 138:57-68.
13. Berman-Frank, I., and Z. Dubinsky. 1999. Balanced growth in aquatic plants: myth or reality? BioScience 49:29-37.
14. 2 availability affects elemental composition (C:N:P) of the marine diatom Skeletonema costatum. Marine Ecology Progress Series 155:67-76.
15. Cao, M., and F. I. Woodward. 1998. Net primary and ecosystem production and carbon stocks of terrestrial ecosystems and their responses to climate change. Global Change Biology 4:185-198.
16. Caron, D. A., and J. C. Goldman. 1988. Dynamics of protistan carbon and nutrient cycling. Journal of Protozoology 35:247-249.
17. Cebrian, J. 1999. Patterns in the fate of production in plant communities. American Naturalist 154:449-468.
18. 2 on woody plants. New Phytologist 127:425-446.
19. Chen, C.-T. A., C.-M. Lim, B.-T. Huang, and L.-F. Chang. 1996. Stoichiometry of carbon, hydrogen, nitrogen, sulfur and oxygen in the particulate matter of the western North Pacific marginal seas. Marine Chemistry 54:179-190.
20. Cole, J. J., N. F. Caraco, G. W. Kling, and T. K. Kratz. 1994. Carbon-dioxide supersaturation in the surface waters of lakes. Science 265:1568-1570.
21. 2 reduces the nitrogen concentration of plant tissues. Global Change Biology 4:43-54.
22. Curtis, P. S. 1996. A meta-analysis of leaf gas exchange and nitrogen in trees grown under elevated carbon dioxide. Plant, Cell and Environment 19:127-137.
23. 2 effects on woody plant mass, form, and physiology. Oecologia 113:299-313.
24. Darchambeau, F., P. Færovig, and D. O. Hessen. 2003. How Daphnia copes with excess carbon in its food. Oecologia 136:336-346.
25. Daly, K. L., D. W. R. Wallace, W. O. Smith, Jr., A. Skoog, R. Lara, M. Gosselin, E. Falck, and P. L. Yager. 1999. Non-Redfield carbon and nitrogen cycling in the Arctic: effects of ecosystem structure and dynamics. Journal of Geophysical Research 104:3185-3199.
26. Dean, W. E., and E. Gorham. 1998. Magnitude and significance of carbon burial in lakes, reservoirs, and peatlands. Geology 26:535-538.
27. del Giorgio, P. A., and R. H. Peters. 1993. Balance between phytoplankton production and plankton respiration in lakes. Canadian Journal of Fisheries and Aquatic Sciences 50: 282-289.
28. DeMott, W. R., R. D. Gulati, and K. Siewertsen. 1998. Effects of phosphorus-deficient diets on the carbon and phosphorus balance of Daphnia magna. Limnology and Oceanography 43:1147-1161.
29. DeMott, W. R., R. D. Gulati, and E. Van Donk. 2001. Effects of dietary phosphorus deficiency on the abundance, phosphorus balance, and growth of Daphnia cucullata in three hypereutrophic Dutch lakes. Limnology and Oceanography 46:1871-1880.
30. Droop, M. R. 1974. The nutrient status of algal cells in continuous culture. Journal of the Marine Biological Association (UK) 54:825-855.
31. Duboc, P., and U. von Stockar. 1998. Dual limitations: kinetic and stoichiometric analysis. Thermochimica Acta 309:121-128.
32. 2 effects on grassland litter decomposition. Global Change Biology 6:145-154.
33. Elser, J. J., M. M. Elser, N. A. Mackay, and S. Carpenter. 1988. Zooplankton-mediated transitions between N-limited and P-limited algal growth. Limnology and Oceanography 33:1-14.
34. Elser, J. J., W. F. Fagan, R. F. Denno, D. R. Dobberfuhl, A. Folarin, A. Huberty, S. Interlandi, S. S. Kilham, E. McCauley, K. L. Schulz, E. H. Siemann, and R. W. Sterner. 2000. Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578-580.
35. Elser, J. J., K. Hayakawa, and J. Urabe. 2001. Nutrient limitation reduces food quality for zooplankton: Daphnia response to seston phosphorus enrichment. Ecology 82:898-903.
36. Elser, J. J., and J. Urabe. 1999. The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80:735-751.
37. Enriquez, S., C. M. Duarte, and K. Sand-Jensen. 1993. Patterns in decomposition rates among photosynthetic organisms - the importance of detritus C:N:P content. Oecologia 94:457-471.
38. Ericsson, T. 1995. Growth and shoot:root ratio of seedlings in relation to nutrient availability. Plant and Soil 168/169:205-214.
39. Ericsson, T., and T. Ingestad. 1988. Nutrition and growth of birch seedlings at varied relative phosphorus addition rates. Physiologia Plantarum 7:227-235.
40. Fagan, W. F., E. H. Siemann, R. F. Denno, C. Mitter, A. Huberty, H. A. Woods, and J. J. Elser. 2002. Nitrogen in insects: implications for trophic complexity and species diversification. American Naturalist 160:784-802.
41. Falkowski, P. G. 2000. Rationalizing elemental ratios in unicellular algae. Journal of Phycology 36:3-6.
42. Falkowski, P. G., et al. 2000. The global carbon cycle: a test of our knowledge of Earth as a system. Science 290:291-296.
43. Follows, M. J., R. G. Williams, and J. C. Marshall. 1996. The solubility pump of carbon in the subtropical gyre of the North Atlantic. Journal of Marine Research 54:605-630.
44. Friedlingstein, P., G. Joel, C. B. Field, and I. Y. Fung. 1999. Toward an allocation scheme for global terrestrial carbon models. Global Change Biology 5:755-770.
45. Galloway, J. N., W. H. Schlesinger, H. L. Levy, A. Michaels, and J. L. Schnoor. 1995. Nitrogen fixation: an anthropogenic enhancement-environmental response. Global Biogeochemical Cycles 9:235-252.
46. Ganeshram, R. S., T. F. Pedersen, S. E. Calvert, G. W. McNeill, and M. R. Fontugne. 2000. Glacial-interglacial variability in denitrification in the world's oceans: causes and consequences. Paleoceanography 15:361-376.
47. Geider, R. J., and J. La Roche. 2002. Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. European Journal of Phycology 37:1-17.
48. Giardina, C. P., and M. G. Ryan. 2000. Biogeochemistry - soil warming and organic carbon content - reply. Nature 408:790.
49. Gismervik, I. 1997. Stoichiometry of some marine planktonic crustaceans. Journal of Plankton Research 19:279-285.
50. Goldman, J. C., D. A. Caron, and M. R. Dennett. 1987. Regulation of gross growth efficiency and ammonium regeneration in bacteria by substrate C:N ratio. Limnology and Oceanography 32:1239-1252.
51. Goldman, J. C., J. J. McCarthy, and D. G. Peavey. 1979. Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature 279:210-214.
52. Goldman, J. C., and D. G. Peavey. 1979. Steady-state growth and chemical composition of the marine chlorophyte Dunaliella tertiolecta in nitrogen-limited continuous cultures. Applied Enviromental Microbiology 38:894-901.
53. 2. Soil Biol. Biochem. 27:117-120.
54. Grace, J., and M. Rayment. 2000. Respiration in the balance. Nature 404:819-820.
55. Griffiths, B. S., K. Ritz, R. D. Bardgett, R. Cook, S. Christensen, F. Ekelund, S. J. Sørensen, E. Bååth, J. Bloem, P. C. de Ruiter, J. Dolfing, and B. Nicolardot. 2000. Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity-ecosystem function relationship. Oikos 90:279-294.
56. Gutschick, V. P. 1981. Evolved strategies in nitrogen acquisition by plants. American Naturalist 118:607-637.
57. Hairston, N. G., Jr., and N. G. Hairston, Sr. 1993. Cause-effect relationships in energy flow, trophic structure, and interspecific interactions. American Naturalist 142:379-411.
58. Hairston, N. G., F. E. Smith, and L. B. Slobodkin. 1960. Community structure, population control, and competition. American Naturalist 94:421-425.
59. Hastings, H. M., and M. Conrad. 1979. Length and evolutionary stability of food webs. Nature 282:838-839.
60. 2 reduction by the world ocean: experiments with the Hamburg carbon cycle model. Paleoceanography 6:395-430.
61. Hessen, D. O. 1992. Nutrient element limitation of zooplankton production. American Naturalist 140:799-814.
62. Hessen, D. O., B. Faafeng, and P. Brettum. 2003. Autotroph: herbivore biomass ratios; carbon deficits judged from plankton data. Hydrobiologia 491:167-175.
63. Hessen, D. O., P. Færøvig, and T. Andersen. 2002. Light, nutrients, and P:C ratios in algae: grazer performance related to food quality and quantity. Ecology 83:1886-1898.
64. Higashi, M., T. Abe, and T. P. Burns. 1992. Carbon-nitrogen balance and termite ecology. Proceedings of the Royal Society of London B 249:303-308.
65. Hutchinson, G. E. 1959. Homage to Santa Rosalia or Why are there so many kinds of animals? American Naturalist 93:145-159.
66. Ingestad, T. 1979. Nitrogen stress in birch seedlings. II. N, K, P, Ca, and Mg nutrition. Physiologia Plantarum 45:149-157.
67. Ingestad, T., and G. I. Ågren. 1995. Plant nutrition and growth - basic principles. Plant and Soil 169:15-20.
68. Ingestad, T., and A.-B. Lund. 1979. Nitrogen stress in birch seedlings. I. Growth technique and growth. Physiologia Plantarum 45:137-148.
69. Jaenike, J., and T. A. Markow. 2003. Comparative elemental stoichiometry of ecologically diverse Drosophila. Functional Ecology 17:115-120.
70. Joffre, R., and G. I. Ågren. 2001. From plant to soil: litter production and decomposition. Pages 83-99 in J. Roy, B. Saugier, and H. A. Mooney, editors. Terrestrial global productivity. Academic Press, San Diego, California, USA.
71. Johnson, K. S., R. M. Gordon, and K. H. Coale. 1997. What controls dissolved iron concentrations in the world ocean? Marine Chemistry 57:137-161.
72. Kähler, P., and W. Koeve. 2001. Marine dissolved organic matter: can its C:N ratio explain carbon overconsumption? Deep-Sea Research 48:49-62.
73. Killingbeck, K. T. 1993. Nutrient resorption in desert shrubs. Revista Chilena de Historia Natural 66:345-355.
74. Killingbeck, K. T. 1996. Nutrients in senescing leaves: key to the search for potential resorption and resorption proficiency. Ecology 77:1716-1727
75. Kirschbaum, M. U. F. 2000. Will changes in soil organic carbon act as a positive or negatiye feedback on global warming? Biogeochemistry 48:21-51.
76. Kooijman, S. A. L. M. 1998. The synthesizing unit as model for the stoichiometric fusion and branching of metabolic fluxes. Biophysical Chemistry 73:179-188.
77. Kooijman, S. A. L. M., T. Anderson, and B. W. Kooi. 2004. Dynamic energy budget representations of stoichiometric constraints on population dynamics. Ecology 85:1230-1243.
78. Lampitt, R. S., W. R. Hillier, and P. G. Challenor. 1993. Seasonal and diel variations in the open ocean concentration of marine snow aggregates. Nature 362:737-739.
79. Lindeman, R. I. 1942. The trophic dynamic aspect of Ecology. Ecology 23:399-418.
80. Mäkipää, R., T. Karjalainen, A. Pussinen, and S. Kellomäki. 1999. Effects of climate change and nitrogen deposition on the carbon sequestration of a forest ecosystem in the boreal zone. Canadian Journal of Forest Research 29:1490-1501.
81. 2 change: the iron hypothesis. Paleoceanography 5:1-13.
82. Melillo, J. M., J. D. Aber, and J. F. Muratore. 1982. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621-626.
83. Moran, N., and W. D. Hamilton. 1980. Low nutritive quality as defence against herbivores. Journal of Theoretical Biology 86:247-254.
84. Myklestad, S. 1977. Production of carbohydrates by marine planktonic diatoms. II. Influence of the N/P ratio in the growth of cellular and extracellular carbohydrates by Chaetocerus affinis var. willei (Gran) Hustedt and Skeletonema costatum (Grev.) Cleve. Journal of Experimental Marine Biology and Ecology 29:161-179.
85. Nagata, T. 2000. Production mechanisms of dissolved organic matter. Pages 121-152 in D. L. Kirchman, editor. Microbial ecology of the oceans. Wiley-Liss, New York, New York, USA.
86. Norby, R. J., and M. F. Cotrufo. 1998. Global change - a question of litter quality. Nature 396:17-18.
87. 2, litter chemistry, and decomposition: a synthesis. Oecologia 127:153-165.
88. 2-enriched atmosphere. Nature 411:469-472.
89. 2 and the mineral content of herbaceous and woody plants. Vegetatio 104/105:403-411.
90. Passow, U., R. F. Shipe, A. Murray, D. K. Pak, M. A. Brzezinski, and A. L. Alldredge. 2001. Origin of transparent exopolymer particles (TEP) and their role in sedimentation of particulate matter. Continental Shelf Research 21:327-346.
91. Paul, E. A., and F. E. Clark. 1989. Soil microbiology and biogeochemistry. Academic Press, San Diego, California, USA.
92. Perkins, M. C., H. A. Woods, J. F. Harrison, and J. J. Elser. 2004. Dietary phosphorus affects the growth of larval Manduca Sexta. Archives of Insect Biochemistry and Physiology, in press.
93. Peterson, B. J., and J. M. Melillo. 1985. The potential storage of carbon caused by eutrophication of the biosphere. Tellus 37B:117-127.
94. 2: a balanced nutrition, coupled-element-cycles model. Ecological Applications 7:444-460.
95. 2 and temperature. Water, Air, and Soil Pollution 64:327-344.
96. 2, climate, and N deposition. Tree Physiology 9:101-126.
97. Redfield, A. C., B. H. Ketchum, and F. A. Richards. 1963. The influence of organisms on the composition of sea water. Pages 26-77 in M. N. Hill, editor. Comparative and descriptive oceanography. Wiley, New York, New York, USA.
98. Schimel, D. S. 1995. Terrestrial ecosystems and the carbon cycle. Global Change Biology 1:77-91.
99. Schimel, D. S., B. H. Braswell, E. A. Holland, R. McKeown, D. S. Ojima, T. H. Painter, W. J. Parton, and A. R. Townsend. 1994. Climatic, edaphic and biotic controls over storage and turnover of carbon in soils. Global Biogeochemical Cycles 8:279-293.
100. Schindler, D. W. 1977. Evolution of phosphorus limitation in lakes. Science 195:260-262.
101. Schindler, D. W., and S. E. Bayley. 1993. The biosphere as an increasing sink for atmospheric carbon - estimates from increased nitrogen deposition. Global Biogeochemical Cycles 7:717-733.
102. Schlesinger, W. H. 1991. Biogeochemistry - an analysis of global change. Academic Press, San Diego, California, USA.
103. Søndergaard, M., P. J. le B. Williams, G. Cauwet, B. Riemann, C. Robinson, S. Terzic, E. M. S. Woodward, and J. Worm. 2000. Net accumulation and flux of dissolved organic carbon and dissolved organic nitrogen in marine plankton communities. Limnology and Oceanography 45:1097-1111.
104. Sterner, R. W., and J. J. Elser. 2002. Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton, New Jersey, USA.
105. Sterner, R. W., and D. O. Hessen. 1994. Algal nutrient limitation and the nutrition of aquatic herbivores. Annual Review of Ecology and Systematics 25:1-29.
106. Stoddard, J. L. 1994. Long term changes in watershed retention of nitrogen. Its causes and aquatic consequences. Pages 223-284 in L. A. Baker, editor. Environmental chemistry of lakes and reservoirs. Advances in Chemistry Series number 237. Americal Chemical Society, Washington, D.C., USA.
107. Swift, M. J., O. W. Heal, and J. M. Anderson. 1979. Decomposition in terrestrial ecosystems. Blackwell, Oxford, UK.
108. Teira, E., M. J. Pazó, P. Serret, and E. Fernández. 2001. Dissolved organic carbon production by microbial populations in the Atlantic Ocean. Limnology and Oceanography 46:1370-1377.
109. Tezuka, Y. 1990. Bacterial regeneration of ammonium and phosphate as affected by the carbon:nitrogen:phosphorus ratio of organic substrates. Microbial Ecology 19:227-238.
110. Thomas, H., V. Ittekkot, C. Osterroht, and B. Schneider. 1999. Preferential recycling of nutrients - the ocean's way to increase new production and to pass nutrient limitation? Limnology and Oceanography 44:1999-2004.
111. Tilman, D. 1988. Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton, New Jersey, USA.
112. Townsend, A. R., B. H. Braswell, E. A. Holland, and J. E. Penner. 1996. Spatial and temporal patterns in terrestrial carbon storage due to deposition of fossil fuel nitrogen. Ecological Applications 6:806-814.
113. Trier, T. M., and W. J. Mattson. 2003. Diet-induced thermogenesis in insects: a developing concept in nutritional ecology. Environmental Entomology 32:1-8.
114. Tyrrell, T. 1999. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400:525-531.
115. Tyrrell, T., and A. H. Taylor. 1996. A modelling study of Emiliania huxleyi in the NE Atlantic. Journal of Marine Systems 9:83-112.
116. Urabe, J., J. Togari, and J. J. Elser. 2003. Stoichiometric impacts of increased carbon dioxide on a planktonic herbivore. Global Change Biology 9:818-825.
117. Vadstein, O. 2000. Heterotrophic, planktonic bacteria and cycling of phosphorus - phosphorus requirements, competitive ability, and food web interactions. Advances in Microbial Ecology 16:115-167.
118. van der Wal, R., N. Madan, S. van Lieshout, C. Dormann, R. Langvatn, and S. D. Albon. 2000. Trading forage quality or quantity: plant phenology and patch choice by Svalbard reindeer. Oecologia 123:108-115.
119. 2 levels. Ecological Applications 1:175-181.
120. Vitousek, P. M., J. D. Aber, R. W. Howarth, G. E. Likens, P. A. Matson, D. W. Schindler, W. H. Schlesinger, and D. G. Tilman. 1997. Human alterations of the global nitrogen cycle: sources and consequences. Ecological Applications 7:737-750.
121. Vitousek, P. M., T. Fahey, D. W. Johnson, and M. J. Swift. 1988. Element interactions in forest ecosystems: succession, allometry and input-output budgets. Biogeochemistry 5:7-34.
122. Vitousek, P. M., and R. W. Howarth. 1991. Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87-115.
123. Vrede, T., D. Dobberfuhl, S. A. L. M. Kooijman, and J. J. Elser. 2004. Fundamental connections among organism C:N:P stoichiometry, macromolecular composition, and growth. Ecology 85:1217-1229.
124. Vrede, T., J. Persson, and G. Aronsen. 2002. The influence on food quality (P:C ratio) on RNA:DNA ratio and somatic growth of Daphnia. Limnology and Oceanography 47:487-494.
125. Wells, M. L., N. M. Price, and K. W. Bruland. 1995. Iron chemistry in seawater and its relationship to phytoplankton: a workshop report. Marine Chemistry 48:157-182.
126. White, T. C. R. 1993. The inadequate environment: nitrogen and the abundance of animals. Springer-Verlag, New York, New York, USA.
127. Williams, P. J. le B. 1995. Seasonal accumulation of carbon-rich dissolved organic material, its scale in comparison with changes in particulate material and the consequential effect on net C/N assimilation ratios. Marine Chemistry 51:17-29.
128. Woods, H. A., W. Makino, J. B. Cotner, S. Hobbie, J. F. Harrison, K. Acharya, and J. J. Elser. 2003. Temperature shifts cause systematic changes in chemical composition of ectothermic organisms. Functional Ecology 17:237-245.