Ecological stoichiometry: An elementary approach using basic principles

Limnology and Oceanography

Volumn 58, Issue 6, 2013, Pages 2219-2236

  Hessen, Dag O ^a   Elser, James J ^b   Sterner, Robert W ^c   Urabe, Jotaro ^d  

^a UNIVERSITY OF OSLO   (Norway)

^b ARIZONA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOGEOCHEMICAL CYCLE; BIOTIC FACTOR; ECOSYSTEM FUNCTION; ECOSYSTEM MODELING; HOMEOSTASIS; MASS BALANCE; NUTRIENT CYCLING; RECYCLING; STOCHASTICITY; TROPHIC LEVEL;

EID: 84887456923     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2013.58.6.2219     Document Type: Article

References (138)

1. ANDERSEN, T., J. J. ELSER, AND D. O. HESSEN. 2004. Stoichiometry and population dynamics. Ecol. Lett. 7: 884-900, doi:10.1111/ j.1461-0248.2004.00646.x
2. ANDERSEN, T., AND D. O. HESSEN. 1991. Carbon, nitrogen, and phosphorus content of freshwater zooplankton. Limnol. Oceanogr. 36: 807-814, doi:10.4319/lo.1991.36.4.0807
3. ANDERSON, T. R., M. BOERSMA, AND D. RAUBENHEIMER. 2004. Stoichiometry: Linking elements to biochemicals. Ecology 85: 1193-1202, doi:10.1890/02-0252
4. ANDERSON, T. R., AND D. O. HESSEN. 2005. Threshold elemental ratios for carbon versus phosphorus limitation in Daphnia. Freshw. Biol. 50: 2063-2075, doi:10.1111/j.1365-2427.2005.01450.x
5. ANDERSON, T. R., AND D. O. HESSEN, J. J. ELSER, AND J. URABE. 2005. Metabolic stoichiometry and the fate of excess carbon and nutrients in consumers. Am. Nat. 165: 1-15, doi:10.1086/426598
6. ANDERSON, T. R., AND D. O. HESSEN, A. MITRA, D. J. MAYOR, AND A. YOOL. 2013. Sensitivity of secondary production and export flux to choice of trophic transfer formulation in marine ecosystem models. J. Mar. Sys. 125: 41-53, doi:10.1016/j.jmarsys.2012. 09.008
7. AUBERT, A. B., C. SVENSEN, D. O. HESSEN, AND T. TAMELANDER. 2013. CNP stoichiometry of a lipid-synthesizing zooplankton, Calanus finmarchicus, from winter to spring bloom in a sub-Arctic sound. J. Mar. Sys. 111: 19-28, doi:10.1016/j.jmarsys.2012.09.004
8. BAUDOUIN-CORNU, P., Y. SURDIN-KERJAN, P. MARLIERE, AND D. THOMAS. 2001. Molecular evolution of protein atomic composition. Science 293: 297-300, doi:10.1126/science. 1061052
9. BOERSMA, M., AND J. J. ELSER. 2006. Too much of a good thing: On stoichiometrically balanced diets and maximal growth. Ecology 87: 1325-1330, doi:10.1890/0012-9658(2006) 87[1325:TMOAGT]2.0.CO;2
10. BOERSMA, M., AND C. KREUTZER. 2002. Life at the edge: Is food quality really of minor importance at low quantities? Ecology 83: 2552-2561, doi:10.1890/0012-9658(2002)083[2552:LATEIF]2.0.CO;2
11. BRADSHAW, C., U. KAUTSKY, AND L. KUMBLAD. 2012. Ecological stoichiometry and multi-element transfer in a coastal ecosystem. Ecosystems 15: 591-603, doi:10.1007/s10021-012-9531-5
12. BRETT, M. T. 1993. Possibility of N or P limitation for planktonic cladocerans-an experimental test and nutrient element limitation for zooplankton production. Limnol. Oceanogr. 38: 1333-1337, doi:10.4319/lo.1993.38.6.1333
13. CARLSON, R. P., AND R. L. TAFFS. 2010. Molecular-level tradeoffs and metabolic adaptation to simultaneous stressors. Curr. Opin. Biotechnol. 21: 670-676, doi:10.1016/j.copbio.2010.05.011
14. CARRILLO, P., M. VILLAR-ARGAIZ, AND J. M. MEDINA-SÁNCHEZ. 2001. Relationship between N:P ratio and growth rate during the life cycle of calanoid copepods: An in situ measurement. J. Plankton Res., 23: 537-547, doi:10.1093/plankt/23.5.537
15. CEASE, A. J., J. J. ELSER, C. F. FORD, S. HAO, L. KANG, AND J. F. HARRISON. 2012. Livestock overgrazing promotes locust outbreaks by lowering plant nitrogen content. Science 335: 467-469, doi:10.1126/science.1214433
16. CEBRIAN, J. 1999. Patterns in the fate of production in plant communities. Am. Nat. 154: 449-468, doi:10.1086/303244
17. CHEN, X., S. B. BAINES, AND N. S. FISHER. 2011. Can copepods be limited by the iron content of their food? Limnol. Oceanogr. 56: 451-460, doi:10.4319/lo.2011.56.2.0451
18. CHRZANOWSKI, T. H., N. C. LUKOMSKI, AND J. P. GROVER. 2010. Element stoichiometry of a mixotrophic protist grown under varying resource conditions. Eukaryot. Microbiol. 57: 322-327, doi:10.1111/j.1550-7408.2010.00487.x
19. CORNER, E. D. S., R. N. HEAD, C. C. KILVINGSTON, AND L. PENNYCUICK. 1976. On the nutrition and metabolism of zooplankton. J. Mar. Biol. Assoc. U.K. 56: 345-358, doi:10.1017/S0025315400018968
20. COTNER, J. B., E. K. HALL, J. T. SCOTT, AND M. HELDAL. 2010. Freshwater bacteria are stoichiometrically flexible with a nutrient composition similar to seston. Front. Microbiol., doi:10.3389/fmicb.2010.00132
21. DARCHAMBEAU, F., P. J. FAERØVIG, AND D. O. HESSEN. 2003. How Daphnia copes with excess carbon in its food. Oecologia 136: 336-346, doi:10.1007/s00442-003-1283-7
22. DEMOTT, W. R., R. D. GULATI, AND K. SIEWERTSEN. 1998. Effects of phosphorus-deficient diets on the carbon and phosphorus balance of Daphnia magna. Limnol. Oceanogr. 43: 1147-1161, doi:10.4319/lo.1998.43.6.1147
23. DEMOTT, W. R., E. N. MCKINNEY, AND A. J. TESSIER. 2010. Ontogeny of digestion in Daphnia: Implications for the effectiveness of algal defenses. Ecology 91: 540-548, doi:10.1890/08-2103.1
24. DEMOTT, W. R., AND B. J. PAPE. 2005. Stoichiometry in an ecological context: Testing for links between Daphnia P-content, growth rate and habitat preference. Oecologia 142: 20-27, doi:10. 1007/s00442-004-1716-y
25. DEMOTT, W. R., AND A. J. TESSIER. 2002. Stoichiometric constraints vs. algal defenses: Testing mechanisms of zooplankton food limitation. Ecology 83: 3426-3433, doi:10.1890/0012-9658 (2002)083[3426:SCVADT]2.0.CO;2
26. DEMOTT, W. R., AND E. VAN DONK. 2013. Strong interactions between stoichiometric constraints and algal defences: Evidence from population dynamics of Daphnia and algae in phosphoruslimited mesocosms. Oecologia 171: 175-186, doi:10.1007/ s00442-012-2404-y
27. DIEHL, S. 2007. Paradoxes of enrichment: Effects of increased light versus nutrient supply on pelagic producer-grazer systems. Am. Nat. 169: E173-E191, doi:10.1086/516655
28. DOI, H., M. CHERIF, T. IWABUCHI, I. KATANO, J. C. STEGEN, AND M. STRIEBEL. 2010. Integrating elements and energy through the metabolic dependencies of gross growth efficiency and the threshold elemental ratio. Oikos 119: 752-765, doi:10.1111/ j.1600-0706.2009.18540.x
29. ELSER, J. J., C. ACQUISTI, AND S. KUMAR. 2011. Stoichiogenomics: The evolutionary ecology of macromolecular elemental composition. Trends Ecol. Evol. 26: 38-44, doi:10.1016/ j.tree.2010.10.006
30. DOI, H., 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, doi:10.2307/1312897
31. DOI, H., M. M. ELSER, N. A. MACKAY, AND S. CARPENTER. 1988. Zooplankton-mediated transitions between N and P limited algal growth. Limnol. Oceanogr. 33: 1-14, doi:10.4319/ lo.1988.33.1.0001
32. DOI, H., AND R. P. HASSETT. 1994. A stoichiometric analysis of the zooplankton-phytoplankton interaction in marine and freshwater ecosystems. Nature 370: 211-213, doi:10.1038/ 370211a0
33. DOI, H., H. HAYAKAWA, AND J. URABE. 2001. Nutrient limitation reduces food quality for zooplankton: Daphnia response to seston phosphorus enrichment. Ecology 82: 898-903.
34. DOI, H., M. KYLE, M. W. WOJEWODZIC, A. PEACE, M. L. MCCRACKIN, T. ANDERSEN, AND D. O. HESSEN. 2010. Atmospheric nitrogen deposition is associated with elevated phosphorus limitation of lake zooplankton. Ecol. Lett. 13: 1256-1261, doi:10.1111/j.1461-0248.2010.01519.x
35. DOI, H., I. LOLADZE, A. PEACE, AND Y. KUANG. 2012. Lotka reloaded: Modeling trophic interactions under stoichiometric constraints. Ecol. Model. 245: 3-11, doi:10.1016/j.ecolmodel. 2012.02.006
36. DOI, H., AND OTHERS. 2000a. Nutritional constraints in terrestrial and freshwater food webs. Nature 25: 578-580, doi:10.1038/ 35046058
37. DOI, H., AND OTHERS. 2000b. Biological stoichiometry from genes to ecosystems. Ecol. Lett. 3: 540-550, doi:10.1046/j.1461-0248. 2000.00185.x
38. DOI, H., AND OTHERS. 2003. Growth rate-stoichiometry couplings in diverse biota. Ecol. Lett. 6: 936-943, doi:10.1046/j.1461-0248. 2003.00518.x
39. DOI, H., AND OTHERS. 2009. Shifts in lake N:P stoichiometry and nutrient limitation driven by atmospheric nitrogen deposition. Science 326: 835-837, doi:10.1126/science.1176199
40. FÆRØVIG, P. J., AND D. O. HESSEN. 2003. Allocation strategies in crustacean stoichiometry: The potential role of phosphorus in the limitation of reproduction. Freshw. Biol. 48: 1782-1792, doi:10.1046/j.1365-2427.2003.01128.x
41. FLYNN, K. J., J. A. RAVEN, T. A. V. REES, Z. FINKEL, AND A. QUIGG. 2010. Is the growth rate hypothesis applicable to microalgae? J. Phycol. 46: 1-12, doi:10.1111/j.1529-8817.2009.00756.x
42. FRIGSTAD, H., T. ANDERSEN, D. O. HESSEN, L.-J. NAUSTVOLL, T. M. JOHNSEN, AND R. G. J. BELLERBY. 2011. Seasonal variability in marine C:N:P stoichiometry: Can the composition of seston explain stable Redfield ratios? Biogeoscience 8: 2917-2933, doi:10.5194/bg-8-2917-2011
43. FROST, P. E., J. P. BENSTEAD, W. F. CROSS, H. HILLEBRAND, J. H. LARSON, M. A. XENOPOULOS, AND T. YOSHIDA. 2006. Threshold elemental ratios of carbon and phosphorus in aquatic consumers. Ecol. Lett. 9: 774-779, doi:10.1111/j.1461-0248.2006.00919.x
44. FROST, P. E., D. EBERT, AND V. H. SMITH. 2008. Bacterial infection changes the elemental composition of Daphnia magna. J. Anim. Ecol. 77: 1265-2656, doi:10.1111/j.1365-2656.2008.01438.x
45. GAEDKE, U., S. HOCHSTADTER, AND D. STRAILE. 2002. Interplay between energy limitation and nutritional deficiency: Empirical data and food web models. Ecol. Monogr. 72: 251-270, doi:10.1890/0012-9615(2002)072[0251:IBELAN]2.0.CO;2
46. GILLOOLY, J. F., A. P. ALLEN, J. H. BROWN, J. J. ELSER, V. M. SAVAGE, G. B. WEST, W. H. WOODRUFF, AND H. A. WOODS. 2005. The metabolic basis of whole-organism RNA and phosphorus stoichiometry. Proc. Natl. Acad. Sci. USA 102: 11923-11927, doi:10.1073/pnas.0504756102
47. GOROKHOVA, E., T. E. DOWLING, L. J. WEIDER, T. J. CREASE, AND J. J. ELSER. 2002. Functional and ecological significance of rDNA intergenic spacer variation in a clonal organism under divergent selection for production rate. Proc. R. Soc. Lond., B. 269: 2373-2379, doi:10.1098/rspb.2002.2145
48. GREGORY, T. R. 2005. The evolution of the genome. Elsevier.
49. HALL, E. K., F. MAIXNER, O. FRANKLIN, H. DAIMS, A. RICHTER, AND T. BATTIN. 2011a. Linking microbial and ecosystem ecology using ecological stoichiometry: A synthesis of conceptual and empirical approaches. Ecosystems 14: 261-273, doi:10.1007/s10021-010-9408-4
50. HALL, E. K., G. A. SINGER, M. POLZL, I. HAMMERLE, C. SCHWARZ, H. DAIMS, F. MAIXNER, AND T. J. BATTIN. 2011b. Looking inside the box: Using Raman microspectroscopy to deconstruct microbial biomass stoichiometry one cell at a time. ISME J. 5: 196-208, doi:10.1038/ismej.2010.115
51. HALL, S. R. 2009. Stoichiometrically explicit food webs: Feedbacks between resource supply, elemental constraints, and species diversity. Annu. Rev. Ecol. Syst. 40: 503-528, doi:10.1146/annurev.ecolsys.39.110707.173518
52. HALL, S. R., C. J. KNIGHT, C. R. BECKER, M. A. DUFFY, AND A. J. TESSIER. 2009. Quality matters: Resource quality for hosts and the timing of epidemics. Ecol. Lett. 12: 118-128, doi:10.1111/ j.1461-0248.2008.01264.x
53. HALL, S. R., V. H. SMITH, D. A. LYTLE, AND M. A. LEIBOLD. 2005. Constraints on primary producer N: P stoichiometry along N: P supply ratio gradients. Ecology 86: 1894-1904, doi:10. 1890/04-1045
54. HE, X., AND W.-X. WANG. 2008. Stoichiometric regulation of carbon and phosphorus in P-deficient Daphnia magna. Limnol. Oceanogr. 53: 244-254, doi:10.4319/lo.2008.53.1.0244
55. HECKY, R. E., P. CAMPBELL, AND L. L. HENDZEL. 1993. The stoichiometry of carbon, nitrogen and phosphorus in particulate matter of lakes and oceans. Limnol. Oceanogr. 38: 709-724, doi:10.4319/lo.1993.38.4.0709
56. HENDRIXSON, H. A., R. W. STERNER, AND A. D. KAY. 2007. Elemental stoichiometry of freshwater fish in relation to phylogeny, allometry and ecology. J. Fish Biol. 70: 121-140, doi:10.1111/j.1095-8649.2006.01280.x
57. HESSEN, D. O. 1992. Nutrient element limitation of zooplankton production. Am. Nat. 140: 799-814, doi:10.1086/285441
58. HESSEN, D. O. 2008. Efficiency, energy and stoichiometry in pelagic food webs: Reciprocal roles of food quality and food quantity. Freshw. Rev. 1: 43-57.
59. HESSEN, D. O., T. ANDERSEN, P. BRETTUM, AND B. A. FAAFENG. 2003. Phytoplankton contribution to sestonic mass and elemental ratios in lakes: Implications for zooplankton nutrition. Limnol. Oceanogr. 48: 1289-1296, doi:10.4319/lo.2003.48. 3.1289
60. HESSEN, D. O., T. ANDERSEN, S. LARSEN, B. L. SKJELKVÅ LE, AND H. A. DE WIT. 2009. Nitrogen deposition, catchment productivity, and climate as determinants of lake stoichiometry. Limnol. Oceanogr. 54: 2520-2528, doi:10.4319/lo.2009.54.6_part_ 2.2520
61. HESSEN, D. O., AND T. R. ANDERSON. 2008. Excess carbon in aquatic organisms and ecosystems: Physiological, ecological and evolutionary implications. Limnol. Oceanogr. 53: 1685-1696, doi:10.4319/lo.2008.53.4.1685
62. HESSEN, D. O., P. J. 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, doi:10.1890/ 0012-9658(2002)083[1886:LNAPCR]2.0.CO;2
63. HESSEN, D. O., E. LEU, P. J. FÆRØVIG, AND S. F. PETERSEN. 2010. Light and spectral properties as determinants of C:N:P-ratios in phytoplankton. Deep-Sea Res. II 55: 2169-2175, doi:10.1016/ j.dsr2.2008.05.013
64. HESSEN, D. O., M. VENTURA, AND J. J. ELSER. 2008. Do phosphorus requirements for RNA limit genome size in crustacean zooplankton? Genome 51: 685-691, doi:10.1139/G08-053
65. HOOD, J. M., AND R. W. STERNER. 2010. Diet mixing: Do animals integrate growth or resources across temporal heterogeneity? Am. Nat. 176: 651-663, doi:10.1086/656489
66. HUISMAN, J., P. VAN OOSTVEEN, AND F. J. WEISSING. 1999. Species dynamics in phytoplankton blooms: Incomplete mixing and competition for light. Am. Nat. 154: 46-68, doi:10.1086/303220
67. IWABUCHI, T., AND J. URABE. 2012a. Competitive outcomes between herbivorous consumers can be predicted from their stoichiometric demands. Ecosphere 3: art7, doi:10.1890/ES11-00253.1
68. IWABUCHI, T., AND J. URABE. 2012b. Food quality and food threshold: Implications of food stoichiometry to competitive ability of herbivore plankton. Ecosphere 3: art51, doi:10.1890/ES12-00098.1
69. JEYASINGH, P. D., A. RAGAVENDRAN, S. PALAND, J. A. LOPEZ, R. W. STERNER, AND J. K. COLBOURNE. 2011. How do consumers deal with stoichiometric constraints? Lessons from functional genomics using Daphnia pulex. Mol. Ecol. 20: 2341-2352, doi:10.1111/j.1365-294X.2011.05102.x
70. KARIMI, R., N. S. FISHER, AND C. L. FOLT. 2010. Multielement stoichiometry in aquatic invertebrates: When growth dilution matters. Am. Nat. 176: 699-709, doi:10.1086/657046
71. KIM, T.-W., K. LEE, R. G. NAJJAR, H.-D. JEONG, AND H. J. JEONG. 2011. Increasing N abundance in the northwestern Pacific Ocean due to atmospheric nitrogen deposition. Science 334: 505-509, doi:10.1126/science.1206583
72. KLAUSMEIER, C. A., E. LITCHMAN, T. DAUFRESNE, AND S. A. LEVIN. 2004. Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature 429: 171-174, doi:10.1038/nature02454
73. KLAUSMEIER, C. A., E. LITCHMAN, T. DAUFRESNE, AND S. A. LEVIN. 2008. Phytoplankton stoichiometry. Ecol. Res. 23: 479-485, doi:10.1007/s11284-008-0470-8
74. LASPOUMADERES, C., B. MODENUTTI, AND E. BALSEIRO. 2010. Herbivory versus omnivory: Linking homeostasis and elemental imbalance in copepod development. J. Plankton Res. 32: 1573-1582, doi:10.1093/plankt/fbq077
75. LEHMAN, J., AND T. NAUMOSKI. 1985. Content and turnover rates of phosphorus in Daphnia pulex: Effect of food quality. Hydrobiologia 128: 119-125, doi:10.1007/BF00008731
76. LIEBIG, J. 1840. Organic chemistry and its application to agriculture and physiology. Taylor and Walton.
77. LINDEMAN, R. L. 1942. The trophic-dynamic aspect of ecology. Ecology 23: 399-418, doi:10.2307/1930126
78. LOLADZE, I., Y. KUANG, AND J. J. ELSER. 2000. Stoichiometry in producer-grazer systems: Linking energy flow with element cycling. Bull. Math. Biol. 62: 1137-1162, doi:10.1006/ bulm.2000.0201
79. LOLADZE, I., Y. KUANG, AND J. J. ELSER, AND W. F. FAGAN. 2004. Competition and stoichiometry: coexistence of two predators on one prey. J. Theor. Biol. 65: 1-15.
80. MAKINO, W., J. B. COTNER, R. W. STERNER, AND J. J. ELSER. 2003. Are bacteria more like plants or animals? Growth rate and resource dependence of bacterial C:N:P stoichiometry. Funct. Ecol. 17: 121-130, doi:10.1046/j.1365-2435.2003.00712.x
81. MALZAHN, A., M. F. HANTZSCE, K. L. SCHOO, M. BOERSMA, AND N. ABERLE. 2010. Differential effects of nutrient-limited primary production on primary, secondary or tertiary consumers. Oecologia 162: 35-48, doi:10.1007/s00442-009-1458-y
82. MATTHEWS, B., AND A. MAZUMDER. 2005. Temporal variation in body composition (C:N) helps explain patterns of zooplankton delta C-13. Freshw. Biol. 50: 502-515, doi:10.1111/j.1365-2427.2005.01336.x
83. MATZEK, V., AND P. M. VITOUSEK. 2009. N:P stoichiometry and protein:RNA ratios in vascular plants: An evaluation of the growth-rate hypothesis. Ecol. Lett. 12: 765-771, doi:10.1111/ j.1461-0248.2009.01310.x
84. MCCARTHY, S. D. S., S. P. RAFFERTY, AND P. C. FROST. 2010. Responses of alkaline phosphatase activity to phosphorus stress in Daphnia magna. J. Exp. Biol. 213: 256-261, doi:10.1242/jeb.037788
85. MOREHOUSE, R. L., A. R. DZIALOWSKI, AND P. D. JEYASINGH. 2012. Impacts of excessive dietary phosphorus on zebra mussels. Hydrobiologia 707: 73-80, doi:10.1007/s10750-012-1407-3
86. MÜLLER-NAVARRA, D. 1995. Evidence that a highly unsaturated fatty acid limits Daphnia growth in nature. Arch. Hydrobiol. 132: 297-307.
87. NAKAZAWA, T. 2011. The onotogenetic stoichiometric neck stabilizes herbivore-autotroph dynamics. Ecol. Res. 26: 209-216, doi:10.1007/s11284-010-0752-9
88. OLSEN, Y., A. JENSEN, H. REINERTSEN, K. Y. BØRSHEIM, 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. Limnol. Oceanogr. 31: 34-44, doi:10.4319/lo.1986.31.1.0034
89. PERSSON, J., P. FINK, A. GOTO, J. M. HOOD, J. JONAS, AND S. KATO. 2010. To be or not to be what you eat: Regulation of stoichiometric homeostasis among autotrophs and heterotrophs. Oikos 119: 741-751, doi:10.1111/j.1600-0706.2009.18545.x
90. PLATH, K., AND M. BOERSMA. 2001. Mineral limitation of zooplankton: Stoichiometric constraints and optimal foraging. Ecology 82: 1260-1269, doi:10.1890/0012-9658(2001) 082[1260:MLOZSC]2.0.CO;2
91. QUIGG, A., AND OTHERS. 2003. The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425: 291-294, doi:10.1038/nature01953
92. RAUBENHEIMER, D., AND S. A. JONES. 2006. Nutritional imbalance in an extreme generalist omnivore: Tolerance and recovery through complementary food selection. Anim. Behav. 71: 1253-1262, doi:10.1016/j.anbehav.2005.07.024
93. REDFIELD, A. C., B. H. KETCHUM, AND F. A. RICHARDS. 1963. The influence of organisms on the composition of seawater, p. 26-77. In M. N. Hill [ed.], The sea. Interscience.
94. REINERS, W. A. 1986. Complementary models for ecosystems. Am. Nat. 127: 59-73, doi:10.1086/284467
95. ROTHHAUPT, K. O. 1995. Algal nutrient limitation affects rotifer growth rate, but not ingestion rate. Limnol. Oceanogr. 40: 1201-1208, doi:10.4319/lo.1995.40.7.1201
96. SARDANS, J., A. RIVAS-UBACH, AND J. PENUELAS. 2012. The C:N:P stoichiometry of organisms and ecosystems in a changing world: A review and perspectives. Perspect. Plant Ecol. Evol. Syst. 14: 33-47, doi:10.1016/j.ppees.2011.08.002
97. SCHINDLER, D. W., AND S. E. BAYLEY. 1993. The biosphere as an increasing sink for atmospheric carbon-estimates from increased nitrogen deposition. Glob. Biogeochem. Cycles 7: 717-733, doi:10.1029/93GB02562
98. SCHOENER, T. W. 2011. The newest synthesis: Understanding the interplay of evolutionary and ecological dynamics. Science 331: 426-429, doi:10.1126/science.1193954
99. SCOTT, J. T., J. B. COTNER, AND T. M. LAPARA. 2012. Variable stoichiometry and homeostatic regulation of bacterial biomass elemental composition. Front. Microbiol.
100. SEIDENDORF, B., N. MEIER, A. PETRUSEK, M. BOERSMA, B. STREIT, AND K. SCHWENK. 2010. Sensitivity of Daphnia species to phosphorus-deficient diets. Oecologia 162: 349-357, doi:10.1007/s00442-009-1452-4
101. SHIMIZU, Y., AND J. URABE. 2008. Regulation of phosphorus stoichiometry and growth in consumers: Theoretical and experimental analysis with Daphnia. Oecologia 155: 21-31, doi:10.1007/s00442-007-0896-7
102. SHULER, M. L., P. FOLEY, AND J. ATLAS. 2012. Modeling a minimal cell. Methods Mol. Biol. 881: 573-610, doi:10.1007/978-1-61779-827-6_20
103. SIMPSON, S. J., AND D. RAUBENHEIMER. 1995. The geometric analysis of feeding and nutrition: A user's guide. J. Insect Physiol. 41: 545-553, doi:10.1016/0022-1910(95)00006-G
104. SIMPSON, S. J., AND D. RAUBENHEIMER, M. A. CHARLESTON, F. J. CLISSOLD, AND A.-N.V.F. NETWORK. 2010. Modelling nutritional interactions: From individuals to communities. Trends Ecol. Evol. 25: 53-60, doi:10.1016/j.tree.2009.06.012
105. SISTLA, S. A., AND J. P. SCHIMEL. 2012. Stoichiometric flexibility as a regulator of carbon and nutrient cycling in terrestrial ecosystems under change. New Phytol. 196: 68-78, doi:10.1111/j.1469-8137.2012.04234.x
106. SMALL, G., AND C. PRINGLE. 2010. Deviation from strict homeostasis across multiple trophic levels in an invertebrate consumer assemblage exposed to high chronic phosphorus enrichment in a Neotropical stream. Oecologia 162: 581-590, doi:10.1007/s00442-009-1489-4
107. SMITH, V. H., AND R. D. HOLT. 1996. Resource competition and within-host disease dynamics. Trends Ecol. Evol. 11: 386-389, doi:10.1016/0169-5347(96)20067-9
108. SOMMER, U. 1992. Phosphorus-limited Daphnia-interspecific facilitation instead of competition. Limnol. Oceanogr. 37: 966-973, doi:10.4319/lo.1992.37.5.0966
109. SOUZA, M. S., B. E. MODENUTTI, B. E. P. CARRILLO, P. M. VILLARARGAIZ, J.M. MEDINA-SANCHEZ, F. BULLEJOS, AND E. G. BALSEIRO. 2010. Stoichiometric dietary constraints influence the response of copepods to ultraviolet radiation-induced oxidative stress. Limnol. Oceanogr. 55: 1024-1032, doi:10.4319/lo.2010.55.3.1024
110. STERNER, R. W. 1990. The ratio of nitrogen to phosphorus resupplied by herbivores: Zooplankton and the algal competitive arena. Am. Nat. 136: 209-229, doi:10.1086/285092
111. STERNER, R. W., T. ANDERSEN, J. J. ELSER, D. O. HESSEN, J.M. HOOD, E. MCCAULEY, AND J. URABE. 2008. Scale-dependent carbon:nitrogen: phosphorous seston stoichiometry in marine and fresh waters. Limnol. Oceanogr. 53: 1169-1180, doi:10.4319/lo.2008. 53.3.1169
112. STERNER, R. W., AND J. J. ELSER. 2002. Ecological stoichiometry: The biology of elements from molecules to the biosphere. Princeton Univ. Press.
113. STERNER, R. W., AND J. J. ELSER, E. FEE, S. J. GUILFORD, AND T. H. CHRZANOWSKI. 1997. The light:nutrient ratio in lakes: The balance of energy and materials affects ecosystem structure and process. Am. Nat. 150: 663-684, doi:10.1086/286088
114. STERNER, R. W., AND J. J. ELSER, AND D. O. HESSEN. 1992. Stoichiometric relationships among producers, consumers and nutrient cycling in pelagic ecosystems. Biogeochemistry 17: 49-67, doi:10.1007/BF00002759
115. STERNER, R. W., AND D. O. HESSEN. 1994. Algal nutrient limitation and the nutrition of aquatic herbivores. Annu. Rev. Ecol. Syst. 25: 1-29, doi:10.1146/annurev.es.25.110194.000245
116. STERNER, R. W., AND J. L. ROBINSON. 1994. Thresholds for growth in Daphnia magna with high and low phosphorus diets. Limnol. Oceanogr. 39: 1228-1232, doi:10.4319/lo.1994.39.5.1228
117. STERNER, R. W., AND K. L. SCHULZ. 1998. Zooplankton nutrition: Recent progress and a reality check. Aquat. Ecol. 32: 261-279, doi:10.1023/A:1009949400573
118. SUZUKI-OHNO, Y., M. KAWATA, AND J. URABE. 2012. Optimal feeding under stoichiometric constraints: A model of compensatory feeding with functional response. Oikos 121: 569-578, doi:10.1111/j.1600-0706.2011.19320.x
119. URABE, J., J. CLASEN, AND R. W. STERNER. 1997. Phosphorus limitation of Daphnia growth: Is it real? Limnol. Oceanogr. 52: 1436-1443, doi:10.4319/lo.1997.42.6.1436
120. URABE, J., J. J. ELSER, M. KYLE, T. SEKINO, AND Z. KAWABATA. 2002. Herbivorous animals can mitigate unfavorable ratios of energy and material supplies by enhancing nutrient recycling. Ecol. Lett. 5: 177-185, doi:10.1046/j.1461-0248.2002.00303.x
121. URABE, J., M. KYLE, W. MAKINO, T. YOSHIDA, T. ANDERSEN, AND J. J. ELSER. 2002. Reduced light increases herbivore production due to stoichiometric effects of light:nutrient balance. Ecology 83: 619-627, doi:10.1890/0012-9658(2002) 083[0619:RLIHPD]2.0.CO;2
122. URABE, J., AND R. W. STERNER. 1996. Regulation of herbivore growth by the balance of light and nutrients. Proc. Natl. Acad. Sci. USA 93: 8465-8469, doi:10.1073/pnas.93.16.8465
123. URABE, J., AND R. W. STERNER. 2001. Contrasting effects of different type of resource depletion on life history traits in Daphnia. Funct. Ecol. 15: 165-174, doi:10.1046/j.1365-2435.2001.00511.x
124. URABE, J., J. TOGARI, AND J. J. ELSER. 2003. Stoichiometric impacts of increased carbon dioxide on a planktonic herbivore. Glob. Change Biol. 9: 818-825, doi:10.1046/j.1365-2486.2003.00634.x
125. URABE, J., AND Y. WATANABE. 1992. Possibility of N and P limitation for planktonic cladocerans: An experimental test. Limnol. Oceanogr. 37: 244-251, doi:10.4319/lo.1992.37.2.0244
126. VENTURA, M. 2006. Linking biochemical and elemental composition in freshwater and marine crustacean zooplankton. Mar. Ecol. Prog. Ser. 327: 233-246, doi:10.3354/meps327233
127. VILLAR-ARGAIZ, M., J. M. MEDINA-SANCHEZ, AND P. CARILLO. 2002. Linking life history strategies and ontogeny in crustacean zooplankton: Implications for homeostasis. Ecology 83: 1899-1914, doi:10.1890/0012-9658(2002)083[1899: LLHSAO]2.0.CO;2
128. VON ELERT, E., D. MARTIN-CREUZBURG, AND J. R. LE COZ. 2003. Absence of sterols constrains carbon transfer between cyanobacteria and a freshwater herbivore (Daphnia galeata). Proc. R. Soc. B 270: 1209-1214, doi:10.1098/rspb.2003.2357
129. WAGNER, N. D., AND P. C. FROST. 2012. Responses of alkaline phosphatase activity in Daphnia to poor nutrition. Oecologia 170: 1-10, doi:10.1007/s00442-012-2277-0
130. WAGNER, N. D., H. HILLEBRAND, A. WACKER, AND P. C. FROST. 2013. Nutritional indicators and their uses in ecology. Ecol. Lett. 16: 535-544, doi:10.1111/ele.12067
131. WANG, H., R. W. STERNER, AND J. J. ELSER. 2012. On the "strict homeostasis" assumption in ecological stoichiometry. Ecol. Model. 243: 81-88, doi:10.1016/j.ecolmodel.2012.06.003
132. WEIDER, L. J., K. L. GLENN, M. KYLE, AND J. J. ELSER. 2004. Associations among ribosomal (r)DNA intergenic spacer length, growth rate, and C:N:P stoichiometry in the genus Daphnia. Limnol. Oceanogr. 49: 1417-1423, doi:10.4319/lo.2004.49.4_part_2.1417
133. WEIDER, L. J., W. MAKINO, K. ACHYRA, K. L. GLENN, M. KYLE, J. URABE, AND J. J. ELSER. 2005. Genotype x environment interactions, stoichiometric food quality effects, and clonal coexistence in Daphnia pulex. Oecologia 143: 537-547, doi:10.1007/s00442-005-0003-x
134. WHITE, T. C. R. 1993. The inadequate environment: Nitrogen and the abundance of animals. Springer-Verlag.
135. WOJEWODZIC, M. W., M. KYLE, J. J. ELSER, D. O. HESSEN, AND T. ANDERSEN. 2011. Joint effect of phosphorus limitation and temperature on alkaline phosphatase activity and somatic growth in Daphnia magna. Oecologia 165: 837-846, doi:10.1007/s00442-010-1863-2
136. WOODS, H. A., W. MAKINO, J. B. COTNER, S. E. HOBBIE, J. F. HARRISON, K. ACHARYA, AND J. J. ELSER. 2003. Temperature and the chemical composition of poikilothermic organisms. Funct. Ecol. 17: 237-245, doi:10.1046/j.1365-2435.2003.00724.x
137. XENOPOULOS, M. A., P. FROST, AND J. J. ELSER. 2002. The combined effect of ultraviolet radiation and phosphorus supply on phytoplankton growth rates and elemental composition. Ecology 83: 423-435, doi:10.1890/0012-9658(2002)083[0423:JEOURA]2.0.CO;2
138. YU, Q., AND OTHERS. 2010. Linking stoichiometric homoeostasis with ecosystem structure, functioning and stability. Ecol. Lett. 13: 1390-1399, doi:10.1111/j.1461-0248.2010.01532.x