The stoichiometry of consumer-driven nutrient recycling: Theory, observations, and consequences

Ecology

Volumn 80, Issue 3, 1999, Pages 735-751

  Elser, James J ^a   Urabe, Jotaro ^b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

Carbon; Consumer driven nutrient recycling; Food quality; Nitrogen; Nutrient cycling; Phosphorus; Stoichiometry; Zooplankton

Indexed keywords

ECOSYSTEM MODELING; NUTRIENT CYCLING; STOICHIOMETRY;

ALGAE; ANIMALIA;

EID: 0032949222     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/0012-9658(1999)080[0735:TSOCDN]2.0.CO;2     Document Type: Article

References (87)

1. Agren, G. I. 1988. Ideal nutrient productivities and nutrient proportions in plant growth. Plant, Cell, and Environment 11:613-620.
2. Andersen, T. 1997. Pelagic nutrient cycles: herbivores as sources and sinks. Springer-Verlag, New York, New York, USA.
3. Andersen, T., and D. O. Hessen. 1991. Carbon, nitrogen, and phosphorus content of freshwater zooplankton. Limnology and Oceanography 36:807-814.
4. Arnott, D. A., and M. J. Vanni. 1996. Nitrogen and phosphorus recycling by the zebra mussel (Dreissena polymorpha) in the western basin of Lake Erie. Canadian Journal of Fisheries and Aquatic Sciences 53:646-659.
5. Blackman, R. L., and V. F. Eastop. 1994. Aphids on the world's trees. C.A.B., International, Wallingford, UK.
6. Brett, M. T. 1993. Comment on "Possibility of N or P limitation for planktonic cladocerans: an experimental test" (Urabe and Watanabe) and "Nutrient element limitation of zooplankton production" (Hessen). Limnology and Oceanography 38:1333-1337.
7. Carpenter, S. R., and J. F. Kitchell. 1984. Plankton community structure and limnetic primary production. American Naturalist 124:159-172.
8. Carpenter, S. R., J. A. Morrice, P. A. Soranno, J. J. Elser, N. A. MacKay, and A. St. Amand. 1993. Dynamics of primary production and nutrients. Pages 225-251 in S. R. Carpenter and J. F. Kitchell, editors. The trophic cascade in lakes. Cambridge University Press, Cambridge, UK.
9. Chapin, F. S. 1980. The mineral nutrition of wild plants. Annual Review of Ecology and Systematics 11:233-260.
10. Chrzanowski, T. H., M. Kyle, J. J. Elser, and R. W. Sterner. 1997. Element ratios and growth dynamics of bacteria in an oligotrophic Canadian shield lake. Aquatic Microbial Ecology 11:119-125.
11. Coleman, D. C. 1996. Energetics of detritivory and microbivory in soil in theory and practice. Pages 39-50 in G. A. Polis and K. O. Winemiller, editors. Food webs: integration of patterns and dynamics. Chapman and Hall, New York, New York, USA.
12. DeMott, W. R. 1998. Utilization of a cyanobacterium and a phosphorus-deficient green alga as complementary resources by daphnids. Ecology 79:2463-2481.
13. De Ruiter, P. C., A. M. Neutel, and J. C. Moore. 1996. Energetics and stability in belowground food webs. Pages 201-210 in G. A. Polis and K. O. Winemiller, editors. Food webs: integration of patterns and dynamics. Chapman and Hall, New York, New York, USA.
14. Downing, J. A. 1997. Marine nitrogen:phosphorus stoichiometry and the global N:P cycle. Biogeochemistry 37:237-252.
15. Downing, J. A., and E. McCauley. 1992. The nitrogen:phosphorus relationship in lakes. Limnology and Oceanography 37:936-945.
16. Ejsmont-Karabin, J. 1984. Phosphorus and nitrogen excretion by lake zooplankton (rotifers and crustaceans) in relationship to individual body weights of the animals, ambient temperature and presence or absence of food. Ekologia Polska 32:3-42.
17. Elser, J. J., T. H. Chrzanowski, R. W. Sterner, and K. H. Mills. 1998. Stoichiometric constraints on food web dynamics: a whole-lake experiment on the Canadian shield. Ecosystems 1:120-136.
18. Elser, J. J., T. H. Chrzanowski, R. W. Sterner, J. H. Schampel, and D. K. Foster. 1995a. Elemental ratios and the uptake and release of nutrients by phytoplankton and bacteria in three lakes of the Canadian shield. Microbial Ecology 29: 145-162.
19. Elser, J. J., D. Dobberfuhl, N. A. MacKay, and J. H. Schampel. 1996. Organism size, life history, and N:P stoichiometry: towards a unified view of cellular and ecosystem processes. BioScience 46:674-684.
20. Elser, J. J., M. M. Elser, N. A. MacKay, and S. R. Carpenter. 1988. Zooplankton-mediated transitions between N and P limited algal growth. Limnology and Oceanography 33:1-14.
21. Elser, J. J., and D. K. Foster. 1998. N:P stoichiometry of sedimentation in lakes of the Canadian Shield: relationships with seston and zooplankton elemental composition. EcoScience 5:56-63.
22. Elser, J. J., D. K. Foster, and R. E. Hecky. 1995b. Effects of zooplankton on sedimentation in pelagic ecosystems: theory and test in two lakes of the Canadian shield. Biogeochemistry 30:143-170.
23. Elser, J. J., and R. P. Hassett. 1994. A stoichiometric analysis of the zooplankton-phytoplankton interaction in marine and freshwater ecosystems. Nature 370:211-213.
24. Elser, J. J., F. S. Lubnow, M. T. Brett, E. R. Marzolf, G. Dion, and C. R. Goldman. 1995c. Abiotic and biotic factors associated with inter- and intra-annual variation of nutrient limitation on phytoplankton growth in Castle Lake, California. Canadian Journal of Fisheries and Aquatic Sciences 52:93-104.
25. Elser, J. J., E. R. Marzolf, and C. R. Goldman. 1990. Phosphorus and nitrogen limitation of phytoplankton growth in the freshwaters of North America: a review and critique of experimental enrichments. Canadian Journal of Fisheries and Aquatic Sciences 47:1468-1477.
26. 2 in the ocean. Nature 387:272-274.
27. Gulati, R., and W. R. DeMott. 1997. The role of food quality for zooplankton: remarks on the state of the art, perspectives, and priorities. Freshwater Biology 38:753-768.
28. Hassett, R. P., B. Cardinale, L. B. Stabler, and J. J. Elser. 1997. Ecological stoichiometry of N and P in pelagic ecosystems: comparison of lakes and oceans with emphasis on the zooplankton-phytoplankton interaction. Limnology and Oceanography 41:648-662.
29. Hessen, D. O. 1993. The role of mineral nutrients for zooplankton nutrition: reply to the comment by Brett. Limnology and Oceanography 38:1340-1343.
30. _. 1997. Stoichiometry in food webs - Lotka revisited. Oikos 79:195-200.
31. Hessen, D. O., and T. Andersen. 1990. Bacteria as a source of phosphorus for zooplankton. Hydrobiologia 206:217-223.
32. Hessen, D. O., and T. Andersen. 1992. The algae-grazer interface: feedback mechanisms linked to elemental ratios and nutrient cycling. Archiv fuer Hydrobiologie Ergebnisse der Limnologie 35:111-120.
33. Hessen, D., T. Andersen, and B. Faafeng. 1992. Zooplankton contribution to particulate phosphorus and nitrogen in lakes. Journal of Plankton Research 14:937-947.
34. Jones, C., and J. Lawton. 1997. Linking species and ecosystems. Chapman and Hall, New York, New York, USA.
35. Ketchum, B. H. 1962. Regeneration of nutrients by zooplankton. Rapports et Proces-Verbaux des Reunions Conseil International pour l'Exploration de la Mer 152:142-146.
36. LeBorgne, R. P. 1982. Zooplankton production in the eastern tropical Atlantic Ocean: net growth efficiency and P:B in terms of carbon, nitrogen and phosphorus. Limnology and Oceanography 27:681-698.
37. Lehman, J. T. 1980a. Nutrient recycling as an interface between algae and grazers in freshwater communities. American Society of Limnology and Oceanography Special Symposium 3:251-263.
38. _. 1980b. Release and cycling of nutrients between planktonic algae and herbivores. Limnology and Oceanography 25:620-632.
39. _. 1984. Grazing, nutrient release, and their impacts on the structure of phytoplankton communities. Pages 48-72 in D. G. Meyers and J. R. Strickler, editors. Trophic interactions within aquatic ecosystems. American Association tor the Advancement of Science Selected Symposium 85, Westview Press, Boulder, Colorado, USA.
40. Lindeman, R. L. 1942. The trophic dynamic aspect of ecology. Ecology 23:399-418.
41. Lotka, A. J. 1925. Elements of physical biology. Williams and Wilkins, Baltimore, Maryland, USA.
42. 2 fixation by cyanobacteria. Limnology and Oceanography 43:347-354.
43. Main, T., D. R. Dobberfuhl, and J. J. Elser. 1997. N:P stoichiometry and ontogeny in crustacean zooplankton: a test of the growth rate hypothesis. Limnology and Oceanography 42:1474-1478.
44. Moegenburg, S. M., and M. J. Vanni. 1991. Nutrient regeneration by zooplanklon: effects on nutrient limitation of phytoplankton in a eutrophic lake. Journal of Plankton Research 13:573-588.
45. Moen, R., J. Pastor, and Y. Cohen. 1998. Antler growth and extinction of Irish Elk. Evolutionary Ecology: in press.
46. Newbold, J. D., J. W. Elwood, R. V. O'Neill, and A. L. Sheldon. 1983. Phosphorus dynamics in a woodland stream ecosystem: a study of nutrient spiraling. Ecology 64:1249-1265.
47. Olsen, Y., A. Jensen, H. Reinertsen, K. Y. Borsheim, M. Heldal, and A. Langeland. 1986. Dependence of the rate of release of phosphorus by zooplankton on the P:C ratio in the food supply, as calculated by a recycling model. Limnology and Oceanography 31:34-44.
48. Olsen, Y., and K. Ostgaard. 1985. Estimating release rates of phosphorus from zooplankton: model and experimental verification. Limnology and Oceanography 30:844-852.
49. Peters, R. H., and F. H. Rigler. 1973. Phosphorus release by Daphnia. Limnology and Oceanography 18:821-839.
50. Polis, G. A., and D. R. Strong. 1996. Food web complexity and community dynamics. American Naturalist 147:813-846.
51. Redfield, A. C. 1958. The biological control of chemical factors in the environment. American Scientist 46:205-221.
52. Redfield, A. C., B. Ketchum, and F. A. Richards. 1963. The influence of organisms on the composition of seawater. Pages 26-77 in M. N. Hill et al., editors. The sea. Interscience, New York, New York, USA.
53. Reiners, W. A. 1986. Complementary models for ecosystems. American Naturalist 127:59-73.
54. Rhee, G. 1978. Effects of N:P atomic ratios and nitrate limitation on algal growth, cell composition, and nitrate uptake. Limnology and Oceanography 23:10-25.
55. Rothaupt, K. O. 1997. Grazing and nutrient influences of Daphnia and Eudiaptomus on phytoplankton in laboratory microcosms. Journal of Plankton Research 19:125-139.
56. Sarnelle, O. 1992. Contrasting effects of Daphnia on ratios of nitrogen to phosphorus in a eutrophic, hard-water lake. Limnology and Oceanography 37:1527-1542.
57. Scavia, D., and W. S. Gardner. 1982. Kinetics of nitrogen and phosphorus release in varying food supplies by Daphnia magna. Hydrobiologia 96:105-111.
58. Schindler, D. E. 1992. Nutrient regeneration by sockeye salmon (Oncorhynchus nerka) fry and subsequent effects on zooplankton and phytoplankton. Canadian Journal of Fisheries and Aquatic Sciences 49:2498-2506.
59. Schindler, D. E., and L. A. Eby. 1997. Stoichiometry of fishes and their prey: implications for nutrient recycling. Ecology 78:1816-1831.
60. Smith, V. H. 1983. Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science 221:669-671.
61. _. 1992. Effects of nitrogen:phosphorus supply ratios on nitrogen fixation in agricultural and pastoral ecosystems. Biogeochemistry 18:19-35.
62. _. 1993a. Implications of resource-ratio theory for microbial ecology. Advances in Microbial Ecology 13:1-37.
63. _. 1993b. Resource competition between host and pathogen. BioScience 43:21-30.
64. Stadler, B., and T. Müller. 1996. Aphid honeydew and its effect on the phyllosphere microflora of Picea abies (L.) Karst. Oecologia 108:771-776.
65. Sterner, R. W. 1986. Herbivores' direct and indirect effects on algal populations. Science 231:605-607.
66. _. 1989. The role of grazers in phytoplankton succession. Pages 107-170 in U. Sommer, editor. Plankton ecology: succession in plankton communities. Springer-Verlag, Berlin, Germany.
67. _. 1990. The ratio of nitrogen to phosphorus resupplied by herbivores: zooplankton and the algal competitive arena. American Naturalist 136:209-229.
68. _. 1995. Elemental stoichiometry of species in ecosystems. Pages 240-251 in C. Jones and J. Lawton, editors. Linking species and ecosystems. Chapman and Hall, New York, New York, USA.
69. _. 1997. Modeling interactions between food quality and quantity in homeostatic consumers. Freshwater Biology 38:473-482.
70. Sterner, R. W., J. J. Elser, E. J. Fee, S. J. Guildford, and T. H. Chrzanowski. 1997. The light:nutrient ratio in lakes: the balance of energy and materials affects ecosystem structure and function. American Naturalist 150:663-684.
71. Sterner, R. W., J. J. Elser, and D. O. Hessen. 1992. Stoichiometric relationships among producers, consumers, and nutrient cycling in pelagic ecosystems. Biogeochemistry 17: 49-67.
72. 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.
73. Strong, D. R., J. L. Maron, and P. G. Connors. 1996. Top down from underground? The underappreciated influences of subterranean food webs on aboveground ecology. Pages 170-178 in G. A. Polis, and K. O. Winemiller, editors. Food webs: integration of patterns and dynamics. Chapman and Hall, New York, New York, USA.
74. 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.
75. Tilman, D. 1982. Resource competition and community structure. Princeton University Press, Princeton. New Jersey, USA.
76. Urabe, J. 1993. N and P cycling coupled by grazers' activities: food quality and nutrient release by zooplankton. Ecology 74:2337-2350.
77. Urabe, J., J. Classen, and R. W. Sterner. 1997. Phosphorus limitation of Daphnia: is it real? Limnology and Oceanography 42:1436-1443.
78. Urabe, J., M. Nakanishi, and K. Kawabata. 1995. Contribution of metazoan plankton to the cycling of N and P in Lake Biwa. Limnology and Oceanography 40:232-241.
79. Urabe, J., and R. W. Sterner. 1996. Regulation of herbivore growth by the balance of light and nutrients. Proceedings of the National Academy of Sciences 93:8465-8469.
80. Urabe, J., and Y. Watanabe. 1992. Possibility of N or P limitation for planktonic cladocerans: an experimental test. Limnology and Oceanography 37:244-251.
81. Urabe, J., and Y. Watanabe. 1993. Implications of sestonic elemental ratio in zooplankton ecology: reply to the comment by Brett. Limnology and Oceanography 38:1337-1340.
82. Vanni, M. J. 1996. Nutrient transport and recycling by consumers in lake food webs: implications for algal communities. Pages 81-95 in G. A. Polis and K. O. Winemiller, editors. Food webs: integration of patterns and dynamics. Chapman and Hall, New York, New York, USA.
83. Vanni, M. J., and D. L. Findlay. 1990. Trophic cascades and phytoplankton community structure. Ecology 71:921-937.
84. Vanni, M. J., C. D. Layne, and S. E. Arnott. 1997. "Top-down" trophic interactions in lakes: effects of fish on nutrient dynamics. Ecology 78:1-20.
85. Vitousek, P. 1982, Nutrient cycling and nutrient use efficiency. American Naturalist 119:553-572.
86. White, T. C. R. 1993. The inadequate environment: nitrogen and the abundance of animals. Springer-Verlag, New York, New York, USA.
87. Wollast, R., F. T. Mackenzie, and L. Chou. 1993. Interactions of C, N, P, and S biogeochemical cycles and global change. NATO Advanced Science Institute Series Series I, Global environmental change. Springer-Verlag, Berlin, Germany.