The metabolic theory of ecology: Prospects and challenges for plant biology

New Phytologist

Volumn 188, Issue 3, 2010, Pages 696-710

  Price, Charles A ^a,e   Gilooly, James F ^b   Allen, Andrew P ^c   Weitz, Joshua S ^a   Niklas, Karl J ^d  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c MACQUARIE UNIVERSITY   (Australia)

^d Cornell University ^*  (United States)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Allometry; Fractal; Metabolic theory of ecology; Scaling; WBE model

Indexed keywords

ALLOMETRY; BIOMASS ALLOCATION; ECOLOGICAL MODELING; FRACTAL ANALYSIS; GROWTH RATE; METABOLISM; NUTRIENT CYCLING; PLANT COMMUNITY; POPULATION GROWTH; THEORETICAL STUDY;

BIOLOGICAL MODEL; BOTANY; ECOLOGY; ECOSYSTEM; ENERGY METABOLISM; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; METABOLISM; METHODOLOGY; PLANT; PLANT PHYSIOLOGY; POPULATION DYNAMICS; REVIEW;

BOTANY; ECOLOGY; ECOSYSTEM; ENERGY METABOLISM; MODELS, BIOLOGICAL; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS; POPULATION DYNAMICS;

EID: 77958527123     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03442.x     Document Type: Review

References (115)

1. Agutter P, Wheatley D. 2004. Metabolic scaling: consensus or controversy? Theoretical Biology and Medical Modelling 1: 1-11.
2. Allen AP, Gillooly JF. 2009. Towards an integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling. Ecology Letters 12: 369-384.
3. Allen AP, Gillooly JF, Brown JH. 2005. Linking the global carbon cycle to individual metabolism. Functional Ecology 19: 202-213.
4. Allen AP, Gillooly JF, Savage VM, Brown JH. 2006. Kinetic effects of temperature on rates of genetic divergence and speciation. Proceedings of the National Academy of Sciences, USA 103: 9130-9135.
5. Allen AP, Pockman WT, Restrepo C, Milne BT. 2008. Allometry, growth and population regulation of the desert shrub Larrea tridentata. Functional Ecology 22: 197-204.
6. Anderson KJ, Allen AP, Gillooly JF, Brown JH. 2006. Temperature-dependence of biomass accumulation rates during secondary succession. Ecology Letters 9: 673-682.
7. Anfodillo T, Carraro V, Carrer M, Fior C, Rossi S. 2006. Convergent tapering of xylem conduits in different woody species. New Phytologist 169: 279-290.
8. Atkin OK, Tjoelker MG. 2003. Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8: 343-351.
9. Bartholomew G. 1966. Interaction of physiology and behavior under natural conditions. In: Bowman RI, ed. The Galapagos. Berkeley, CA, USA: University of California Press, 39-45.
10. Belgrano A, Allen AP, Enquist BJ, Gillooly JF. 2002. Allometric scaling of maximum population density: a common rule for marine phytoplankton and terrestrial plants. Ecology Letters 5: 611-613.
11. Berry J, Bjorkman O. 1980. Photosynthetic response and adaptation to temperature in higher-plants. Annual Review of Plant Physiology and Plant Molecular Biology 31: 491-543.
12. Blum JJ. 1977. On the geometry of four-dimensions and the relationship between metabolism and body mass. Journal of Theoretical Biology 64: 599-601.
13. Brose U, Williams RJ, Martinez ND. 2006. Allometric scaling enhances stability in complex food webs. Ecology Letters 9: 1228-1236.
14. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB. 2004. Toward a metabolic theory of ecology. Ecology 85: 1771-1789.
15. Brown JH, Sibly RM. 2006. Life history evolution under a production constraint. Proceedings of the National Academy of Sciences, USA 103: 17595-17599.
16. Brown JH, West GB, Enquist BJ. 2000. Scaling in biology: patterns and processes, causes and consequences. In: Brown JH, West GB, eds. Scaling in biology. Oxford, UK: Oxford University Press, 1-24.
17. Brown JH, West GB, Enquist BJ. 2005. Yes, West, Brown and Enquist's model of allometric scaling is both mathematically correct and biologically relevant. Functional Ecology 19: 735-738.
18. Calder WA. 1984. Size, function, and life history. Cambridge, MA, USA: Harvard University Press.
19. Cebrian J. 1999. Patterns in the fate of production in plant communities. American Naturalist 154: 449-468.
20. Charnov EL, Gillooly JF. 2004. Size and temperature in the evolution of fish life histories. Integrative and Comparative Biology 44: 494-497.
21. Chesson P. 2000. Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31: 343-366.
22. Clark JS. 2005. Why environmental scientists are becoming bayesians. Ecology Letters 8: 2-14.
23. Clarke A, Fraser KPP. 2004. Why does metabolism scale with temperature? Functional Ecology 18: 243-251.
24. Connell JH. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: Den Bore BJ, Gradwell GR, ed. Dynamics of population. Wageningen, The Netherlands: Centre for Agricultural Publishing and Documentation, 298-312.
25. Coomes D, Duncan R, Allen R, Truscott J. 2003. Disturbances prevent stem size-density distributions in natural forests from following scaling relationships. Ecology Letters 6: 980-989.
26. Coomes DA, Jenkins KL, Cole LES. 2007. Scaling of tree vascular transport systems along gradients of nutrient supply and altitude. Biology Letters 3: 86-89.
27. Damuth J. 1981. Population density and body size in mammals. Nature 290: 699-700.
28. Deng JM, Li T, Wang GX, Liu J, Yu ZL, Zhao CM, Ji MF, Zhang Q, Liu JQ. 2008. Trade-offs between the metabolic rate and population density of plants. PLoS ONE 3: 7.
29. Dietze MC, Wolosin MS, Clark JS. 2008. Capturing diversity and interspecific variability in allometries: a hierarchical approach. Forest Ecology and Management 256: 1939-1948.
30. Dodds PS, Rothman DH, Weitz JS. 2001. Re-examination of the "3/4-law" Of metabolism. Journal of Theoretical Biology 209: 9-27.
31. Duarte CM. 2007. Marine ecology warms up to theory. Trends in Ecology and Evolution 22: 331-333.
32. Elser JJ, Fagan WF, Kerkhoff AJ, Swenson NG, Enquist BJ. 2010. Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytologist 186: 593-608.
33. Enquist BJ, Allen AP, Brown JH, Gillooly JF, Kerkhoff AJ, Niklas KJ, Price CA, West GB. 2007a. Biological scaling: does the exception prove the rule? Nature 445: E9-E10.
34. Enquist BJ, Brown JH, West GB. 1998. Allometric scaling of plant energetics and population density. Nature 395: 163-165.
35. Enquist BJ, Economo EP, Huxman TE, Allen AP, Ignace DD, Gillooly JF. 2003. Scaling metabolism from organisms to ecosystems. Nature 423: 639-642.
36. Enquist BJ, Kerkhoff AJ, Huxman TE, Economo EP. 2007b. Adaptive differences in plant physiology and ecosystem paradoxes: insights from metabolic scaling theory. Global Change Biology 13: 591-609.
37. Enquist BJ, Niklas KJ. 2002. Global allocation rules for patterns of biomass partitioning in seed plants. Science 295: 1517-1520.
38. Enquist BJ, West GB, Brown JH. 2009. Extensions and evaluations of a general quantitative theory of forest structure and dynamics. Proceedings of the National Academy of Sciences, USA 106: 7046-7051.
39. 2 assimilation in leaves of C3 plants. Planta 149: 78-90.
40. Finkel ZV. 2001. Light absorption and size scaling of light-limited metabolism in marine diatoms. Limnology and Oceanography 46: 86-94.
41. Gillooly JF, Allen AP, Brown JH. 2006. Food-web structure and dynamics: reconciling alternative ecological currencies. In: Pasqual M & Dunne JA, eds. Ecological networks: linking structure to dynamics in food webs. Oxford, UK: Oxford University Press, 209-220.
42. Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL. 2001. Effects of size and temperature on metabolic rate. Science 293: 2248-2251.
43. Gillooly JF, Charnov EL, West GB, Savage VM, Brown JH. 2002. Effects of size and temperature on developmental time. Nature 417: 70-73.
44. Harte J. 2004. The value of null theories in ecology. Ecology 85: 1792-1794.
45. Harte J, Zillio T, Conlisk E, Smith AB. 2008. Maximum entropy and the state-variable approach to macroecology. Ecology 89: 2700-2711.
46. Hemmingsen AM. 1960. Energy metabolism as related to body size and respiratory surfaces, and its evolution. Reports of the Steno Memorial Hospital and the Nordisk Insulinlaboratorium 9: 7-95.
47. Hillebrand H, Borer ET, Bracken MES, Cardinale BJ, Cebrian J, Cleland EE, Elser JJ, Gruner DS, Harpole WS, Ngai JT et al. 2009. Herbivore metabolism and stoichiometry each constrain herbivory at different organizational scales across ecosystems. Ecology Letters 12: 516-527.
48. Hubbell SP. 2001. The unified neutral theory of biodiversity and biogeography. Princeton, NJ, USA: Princeton University Press.
49. Huxley JS. 1932. Problems of relative growth. London, UK: Methuen.
50. Janzen DH. 1970. Herbivores and the number of tree species in tropical forests. The American Naturalist 104: 501-528.
51. Jennings S, Mélin F, Blanchard JL, Forster RM, Dulvy NK, Wilson RW. 2008. Global-scale predictions of community and ecosystem properties from simple ecological theory. Proceedings. Biological Sciences 275: 1375-1383.
52. Jones CG, Lawton JH. 1995. Linking species and ecosystems. New York, NY, USA: Chapman and Hall.
53. Kimura M. 1968. Evolutionary rate at molecular level. Nature 217: 624.
54. Kleiber M. 1932. Body size and metabolism. Hilgardia 6: 315-353.
55. Kolokotrones T, Savage V, Deeds EJ, Fontana W. 2010. Curvature in metabolic scaling. Nature 464: 753-756.
56. Kozlowski J, Konarzewski M. 2004. Is West, Brown and Enquist's model of allometric scaling mathematically correct and biologically relevant? Functional Ecology 18: 283-289.
57. Kozlowski J, Konarzewski M. 2005. West, brown and enquist's model of allometric scaling again: the same questions remain. Functional Ecology 19: 739-743.
58. Lambers H, Chapin FS, Pons TL. 1998. Plant physiological ecology. New York, NY, USA: Springer.
59. Latimer AM. 2007. Geography and resource limitation complicate metabolism-based predictions of species richness. Ecology 88: 1895-1898.
60. Lichstein JW, Dushoff J, Levin SA, Pacala SW. 2007. Intraspecific variation and species coexistence. American Naturalist 170: 807-818.
61. Lieth H. 1973. Primary production: terrestrial ecosystems. Human Ecology 1: 303-332.
62. Lopez-Urrutia A. 2008. The metabolic theory of ecology and algal bloom formation. Limnology and Oceanography 53: 2046-2047.
63. Lopez-Urrutia A, San Martin E, Harris RP, Irigoien X. 2006. Scaling the metabolic balance of the oceans. Proceedings of the National Academy of Sciences, USA 103: 8739-8744.
64. Lotka AJ. 1925. Elements of physical biology. Baltimore, MD, USA: Williams and Wilkins.
65. Mandelbrot BB. 1977. The fractal geometry of nature. New York, NY, USA: W. H. Freeman and Co.
66. Marba N, Duarte CM, Agusti S. 2007. Allometric scaling of plant life history. Proceedings of the National Academy of Sciences, USA 104: 15777-15780.
67. McCulloh K, Sperry J, Adler F. 2003. Water transport in plants obeys Murray's law. Nature 421: 939-942.
68. McMahon TA, Kronauer RE. 1976. Tree structures: deducing the principle of mechanical design. Journal of Theoretical Biology 59: 443-466.
69. Meinzer FC, Bond BJ, Warren JM, Woodruff DR. 2005. Does water transport scale universally with tree size? Functional Ecology 19: 558-565.
70. Meinzer FC, Goldstein G, Andrade JL. 2001. Regulation of water flux through tropical forest canopy trees: do universal rules apply? Tree Physiology 21: 19-26.
71. Mori S, Yamaji K, Ishida A, Prokushkin SG, Masyagina OV, Hagihara A, Hoque A, Suwa R, Osawa A, Nishizono T et al. 2010. Mixed-power scaling of whole-plant respiration from seedlings to giant trees. Proceedings of the National Academy of Sciences, USA 107: 1447-1451.
72. Muller-Landau HC, Condit RS, Chave J, Thomas SC, Bohlman SA, Bunyavejchewin S, Davies S, Foster R, Gunatilleke S, Gunatilleke N et al. 2006a. Testing metabolic ecology theory for allometric scaling of tree size, growth and mortality in tropical forests. Ecology Letters 9: 575-588.
73. Muller-Landau HC, Condit RS, Harms KE, Marks CO, Thomas SC, Bunyavejchewin S, Chuyong G, Co L, Davies S, Foster R et al. 2006b. Comparing tropical forest tree size distributions with the predictions of metabolic ecology and equilibrium models. Ecology Letters 9: 589-602.
74. Murray CD. 1926. The physiological principle of minimum work. I. The vascular system and the cost of blood volume. Proceedings of the National Academy of Sciences, USA 12: 207-214.
75. Nielsen SL, Enriquez S, Duarte CM, SandJensen K. 1996. Scaling maximum growth rates across photosynthetic organisms. Functional Ecology 10: 167-175.
76. Niklas KJ. 1994. Plant allometry: the scaling of form and process. Chicago, IL, USA: University of Chicago Press.
77. Niklas KJ. 2004. Plant allometry: is there a grand unifying theory? Biological Reviews 79: 871-889.
78. Niklas KJ. 2007. Maximum plant height and the biophysical factors that limit it. Tree Physiology 27: 433-440.
79. Niklas KJ, Enquist BJ. 2001. Invariant scaling relationships for interspecific plant biomass production rates and body size. Proceedings of the National Academy of Sciences, USA 98: 2922-2927.
80. Niklas KJ, Owens T, Reich PB, Cobb ED. 2005. Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth. Ecology Letters 8: 636-642.
81. O'Connor MI, Piehler MF, Leech DM, Anton A, Bruno JF. 2009. Warming and resource availability shift food web structure and metabolism. PLoS Biology 7: e1000178.
82. O'Dwyer JP, Lake JK, Ostling A, Savage VM, Green JL. 2009. An integrative framework for stochastic, size-structured community assembly. Proceedings of the National Academy of Sciences, USA 106: 6170-6175.
83. Pacala SW. 1997. The dynamics of plant communities. In: Crawley MJ, ed. Plant ecology. Oxford, UK: Blackwell Science, 532-555.
84. Peters RH. 1983. The ecological implications of body size. Cambridge, UK: Cambridge University Press.
85. Petit G, Anfodillo T. 2009. Plant physiology in theory and practice: an analysis of the WBE model for vascular plants. Journal of Theoretical Biology 259: 1-4.
86. Price CA, Enquist BJ. 2006. Scaling mass and morphology in plants with minimal branching: an extension of the WBE model. Functional Ecology 20: 11-20.
87. Price CA, Enquist BJ. 2007. Scaling mass and morphology in leaves: an extension of the WBE model. Ecology 88: 1132-1141.
88. Price CA, Enquist BJ, Savage VM. 2007. A general model for allometric covariation in botanical form and function. Proceedings of the National Academy of Sciences, USA 104: 13204-13209.
89. Price CA, Ogle K, White EP, Weitz JS. 2009. Evaluating scaling theories in biology using hierarchical bayesian approaches. Ecology Letters 12: 641-651.
90. Raven JA, Geider RJ. 1988. Temperature and algal growth. New Phytologist 110: 441-461.
91. Redfield AC. 1958. The biological control of chemical factors in the environment. American Scientist 46: 205-221.
92. Reich PB, Tjoelker MG, Machado JL, Oleksyn J. 2006. Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439: 457-461.
93. Reiners WA. 1986. Complementary models for ecosystems. American Naturalist 127: 59-73.
94. Rosenzweig ML. 1968. Net primary productivity of terrestrial communities: prediction from climatological data. American Naturalist 102: 67-74.
95. Savage VM. 2004. Improved approximations to scaling relationships for species, populations, and ecosystems across latitudinal and elevational gradients. Journal of Theoretical Biology 227: 525-534.
96. Savage VM, Deeds EJ, Fontana W. 2008. Sizing up allometric scaling theory. PLoS Computational Biology 4: 17.
97. Savage VM, Gillooly JF, Brown JH, West GB, Charnov EL. 2004. Effects of body size and temperature on population growth. American Naturalist 163: E429-E441.
98. Schmidt-Nielsen K. 1984. Scaling: why is animal size so important? Cambridge, UK: Cambridge University Press.
99. Shinozaki K, Yoda K, Hozumi K, Kira T. 1964. A quantitative analysis of plant form - the pipe model theory. I. Basic analysis. Japanese Journal of Ecology 14: 97-105.
100. Shipley B, Dion J. 1992. The allometry of seed production in herbaceous angiosperms. American Naturalist 139: 467-483.
101. Skellam JG. 1951. Random dispersal in theoretical populations. Biometrika 38: 196-218.
102. Sousa T, Domingos T, Kooijman SALM. 2008. From empirical patterns to theory: a formal metabolic theory of life. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363: 2453-2464.
103. Stegen JC, Enquist BJ, Ferriere R. 2009. Advancing the metabolic theory of biodiversity. Ecology Letters 12: 1001-1015.
104. Thompson DW. 1942. On growth and form. Cambridge, UK: Cambridge Univ. Press.
105. Tilman D. 1982. Resource competition and community structure. Princeton, NJ, USA: Princeton University Press.
106. Tilman D, HilleRisLambers H, Harpole S, Dybsinski R, Fargione J, Clark C, Lehman C. 2004. Does metabolic theory apply to community ecology? It's a matter of scale. Ecology 85: 1797-1799.
107. Turcotte DL, Pelletier JD, Newman WI. 1998. Networks with side branching in biology. Journal of Theoretical Biology 193: 577-592.
108. Vasseur DA, McCann KS. 2005. A mechanistic approach for modeling temperature-dependent consumer-resource dynamics. American Naturalist 166: 184-198.
109. Weitz JS, Levin SA. 2006. Size and scaling of predator-prey dynamics. Ecology Letters 9: 548-557.
110. Weitz JS, Ogle K, Horn HS. 2006. Ontogenetically stable hydraulic design in woody plants. Functional Ecology 20: 191-199.
111. West GB, Brown JH, Enquist BJ. 1997. A general model for the origin of allometric scaling laws in biology. Science 276: 122-126.
112. West GB, Brown JH, Enquist BJ. 1999. A general model for the structure and allometry of plant vascular systems. Nature 400: 664-667.
113. West GB, Enquist BJ, Brown JH. 2009. A general quantitative theory of forest structure and dynamics. Proceedings of the National Academy of Sciences, USA 106: 7040-7045.
114. White CR, Phillips NF, Seymour RS. 2006. The scaling and temperature dependence of vertebrate metabolism. Biology Letters 2: 125-127.
115. Wullschleger SD, Meinzer FC, Vertessy RA. 1998. A review of whole-plant water use studies in trees. Tree Physiology 18: 499-512.