, Volume 85, Issue 3, pp 235–252 | Cite as

C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass?

  • Cory C. ClevelandEmail author
  • Daniel Liptzin
Original Paper


Well-constrained carbon:nitrogen:phosphorus (C:N:P) ratios in planktonic biomass, and their importance in advancing our understanding of biological processes and nutrient cycling in marine ecosystems, has motivated ecologists to search for similar patterns in terrestrial ecosystems. Recent analyses indicate the existence of “Redfield-like” ratios in plants, and such data may provide insight into the nature of nutrient limitation in terrestrial ecosystems. We searched for analogous patterns in the soil and the soil microbial biomass by conducting a review of the literature. Although soil is characterized by high biological diversity, structural complexity and spatial heterogeneity, we found remarkably consistent C:N:P ratios in both total soil pools and the soil microbial biomass. Our analysis indicates that, similar to marine phytoplankton, element concentrations of individual phylogenetic groups within the soil microbial community may vary, but on average, atomic C:N:P ratios in both the soil (186:13:1) and the soil microbial biomass (60:7:1) are well-constrained at the global scale. We did see significant variation in soil and microbial element ratios between vegetation types (i.e., forest versus grassland), but in most cases, the similarities in soil and microbial element ratios among sites and across large scales were more apparent than the differences. Consistent microbial biomass element ratios, combined with data linking specific patterns of microbial element stoichiometry with direct evidence of microbial nutrient limitation, suggest that measuring the proportions of C, N and P in the microbial biomass may represent another useful tool for assessing nutrient limitation of ecosystem processes in terrestrial ecosystems.


Carbon Microbial biomass Nitrogen Phosphorus Soil Stoichiometry 



We thank Loren Sackett and Christine Fairbanks for assistance with the literature search, and Noah Fierer, Alan Townsend, Josh Schimel and two anonymous reviewers for valuable comments on the manuscript. C. C. was supported by a grant from the National Science Foundation (DEB-0515744). D.L. was supported by grants from the NSF Long-Term Ecological Research (LTER) program (DEB-9810128).


  1. Aerts R, Chapin FS III (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 10:402–407Google Scholar
  2. Agbenin JO, Adeniyi T (2005) The microbial biomass properties of a savanna soil under improved grass and legume pastures in northern Nigeria. Agric Ecosyst Environ 109:245–254CrossRefGoogle Scholar
  3. Arunachalam A, Arunachalam K (2000) Influence of gap size and soil properties on microbial biomass in a subtropical humid forest of north-east India. Plant Soil 223:185–193CrossRefGoogle Scholar
  4. Arunachalam A, Maithani K, Pandey HN, Tripathi RS (1996) The impact of disturbance on detrital dynamics and soil microbial biomass of a Pinus kesiya forest in north-east India. For Ecol Manage 88:273–282CrossRefGoogle Scholar
  5. Asner GP, Seastedt TR, Townsend AR (1997) The decoupling of terrestrial carbon and nitrogen cycles. Bioscience 47:226–234CrossRefGoogle Scholar
  6. Badalucco L, DeCesare F, Grego S, Landi L, Nannipieri P (1997) Do physical properties of soil affect chloroform efficiency in lysing microbial biomass? Soil Biol Biochem 29:1135–1142CrossRefGoogle Scholar
  7. Barbhuiya AR, Arunachalam A, Pandey HN, Arunachalam K, Khan ML, Nath PC (2004) Dynamics of soil microbial biomass C, N and P in disturbed and undisturbed stands of a tropical wet-evergreen forest. Eur J Soil Biol 40:113–121CrossRefGoogle Scholar
  8. Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass P in soil. Soil Biol Biochem 14:319–329CrossRefGoogle Scholar
  9. Brookes PC, Powlson DS, Jenkinson DS (1984) Phosphorus in the soil microbial biomass. Soil Biol Biochem 16:169–175CrossRefGoogle Scholar
  10. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842CrossRefGoogle Scholar
  11. Chadwick OA, Derry LA, Vitousek PM, Huebert BJ, Hedin LO (1999) Changing sources of nutrients during four million years of ecosystem development. Nature 397:491–497CrossRefGoogle Scholar
  12. Chen GC, He ZL (2004) Determination of soil microbial biomass phosphorus in acid red soils from southern China. Biol Fertil Soils 39:446–451CrossRefGoogle Scholar
  13. Chen CR, Condron LM, Davis MR, Sherlock RR (2000a) Effects of afforestation on phosphorus dynamics and biological properties in a New Zealand grassland soil. Plant Soil 220:151–163CrossRefGoogle Scholar
  14. Chen GC, He ZL, Huang CY (2000b) Microbial biomass phosphorus and its significance in predicting phosphorus availability in red soils. Commun Soil Sci Plan 31:655–667CrossRefGoogle Scholar
  15. Chen CR, Condron LM, Davis MR, Sherlock RR (2003) Seasonal changes in soil phosphorus and associated microbial properties under adjacent grassland and forest in New Zealand. For Ecol Manage 177:539–557CrossRefGoogle Scholar
  16. Chen CR, Condron LM, Davis MR, Sherlock RR (2004) Effects of plant species on microbial biomass phosphorus and phosphatase activity in a range of grassland soils. Biol Fertil Soils 40:313–322CrossRefGoogle Scholar
  17. Christ MJ, David MB, McHale PJ, McLaughlin JW, Mitchell MJ, Rustad LE, Fernandez IJ (1997) Microclimatic control of microbial C, N, and P pools in Spodosol Oa horizons. Can J For Res 27:1914–1921CrossRefGoogle Scholar
  18. Cleveland CC, Townsend AR (2006) Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proc Natl Acad Sci U S A 103:10316–10321CrossRefGoogle Scholar
  19. Cleveland CC, Townsend AR, Schmidt SK (2002) Phosphorus limitation of microbial processes in moist tropical forests: evidence from short-term laboratory incubations and field experiments. Ecosystems 5:680–691Google Scholar
  20. Cleveland CC, Townsend AR, Constance BC, Ley RE, Schmidt SK (2004) Soil microbial dynamics in Costa Rica: seasonal and biogeochemical constraints. Biotropica 36:184–195Google Scholar
  21. Cooper DJ, Watson AJ, Nightingale PD (1996) Large decrease in ocean-surface CO2 fugacity in response to in situ iron fertilization. Nature 383:511–513CrossRefGoogle Scholar
  22. Devi NB, Yadava PS (2006) Seasonal dynamics in soil microbial biomass C, N and P in a mixed-oak forest ecosystem of Manipur, north-east India. Appl Soil Ecol 31:220–227CrossRefGoogle Scholar
  23. Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LJ (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–550CrossRefGoogle Scholar
  24. Falkowski P, Scholes RJ, Boyle E et al (2000) The global carbon cycle: a test of our knowledge of earth as a system. Science 290:291–296CrossRefGoogle Scholar
  25. Falster DS, Warton DI, Wright IJ (2006) SMATR: standardised major axis tests and routines, ver2.0. Scholar
  26. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240CrossRefGoogle Scholar
  27. Gallardo A, Schlesinger WH (1994) Factors limiting microbial biomass in the mineral soil and forest floor of a warm-temperate forest. Soil Biol Biochem 26:1409–1415CrossRefGoogle Scholar
  28. Galloway JN, Asner G, Boyer EW et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226CrossRefGoogle Scholar
  29. Hecky RE, Kilham P (1988) Nutrient limitation of phytoplankton in freshwater and marine environments: a review of recent evidence on the effects of enrichment. Limnol Oceanogr 33:796–822Google Scholar
  30. Hedin L (2004) Global organization of terrestrial plant-nutrient interactions. Proc Natl Acad Sci U S A 101:10849–10850CrossRefGoogle Scholar
  31. Hedley MJ, Stewart JWB (1982) Method to measure microbial phosphate in soils. Soil Biol Biochem 14:377–385CrossRefGoogle Scholar
  32. Holland KJ (2006) Fate of nitrogen in alpine tundra. Ph.D. Dissertation, University of Colorado, Boulder, COGoogle Scholar
  33. Ingham E, Horton K (1987) Bacterial, fungal, and protozoan responses to chloroform fumigation in stored soils. Soil Biol Biochem 19:545–550CrossRefGoogle Scholar
  34. Jenkinson DS, Powlson DS (1976) The effects of biocidal treatments on metabolism in soil. Soil Biol Biochem 8:209–213CrossRefGoogle Scholar
  35. Jenkinson DS, Brookes PC, Powlson DS (2004) Measuring soil microbial biomass. Soil Biol Biochem 36:5–7CrossRefGoogle Scholar
  36. Jenny H (1941) Factors of soil formation. McGraw Hill, New YorkGoogle Scholar
  37. Joergensen RG, Kubler H, Meyer B, Wolters V (1995) Microbial biomass phosphorus in soils of beech (Fagus-Sylvatica L) forests. Biol Fertil Soils 19:215–219CrossRefGoogle Scholar
  38. Johnson AH, Frizano J, Vann DR (2003) Biogeochemical implications of labile phosphorus in forest soils determined by the Hedley fractionation procedure. Oecologia 135:487–499Google Scholar
  39. Jonasson S, Michelsen A, Schmidt IK, Nielsen EV, Callaghan TV (1996) Microbial biomass C, N and P in two arctic soils and responses to addition of NPK fertilizer and sugar: implications for plant nutrient uptake. Oecologia 106:507–515CrossRefGoogle Scholar
  40. Jonasson S, Castro J, Michelsen A (2006) Interactions between plants, litter and microbes in cycling of nitrogen and phosphorus in the arctic. Soil Biol Biochem 38:526–532CrossRefGoogle Scholar
  41. Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450CrossRefGoogle Scholar
  42. Kopacek J, Kana J, Santruckova H, Picek T, Stuchlik E (2004) Chemical and biochemical characteristics of alpine soils in the Tatra Mountains and their correlation with lake water quality. Water Air Soil Pollut 153:307–327CrossRefGoogle Scholar
  43. Kwabiah AB, Palm CA, Stoskopf NC, Voroney RP (2003) Response of soil microbial biomass dynamics to quality of plant materials with emphasis on P availability. Soil Biol Biochem 35:207–216CrossRefGoogle Scholar
  44. Lorenz K, Feger KH, Kandeler E (2001) The response of soil microbial biomass and activity of a Norway spruce forest to liming and drought. J Plant Nutr Soil Sci 164:9–19CrossRefGoogle Scholar
  45. Maithani K, Tripathi RS, Arunachalam A, Pandey HN (1996) Seasonal dynamics of microbial biomass C, N and P during regrowth of a disturbed subtropical humid forest in north-east India. App Soil Ecol 4:31–37CrossRefGoogle Scholar
  46. McGroddy M, Daufresne T, Hedin L (2004) Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial Redfield-type ratios. Ecology 85:2390–2401CrossRefGoogle Scholar
  47. McIntosh PD, Gibson RS, Saggar S, Yeates GW, McGimpsey P (1999) Effect of contrasting farm management on vegetation and biochemical, chemical, and biological condition of moist steepland soils of the South Island high country, New Zealand. Aust J Soil Res 37:847–865CrossRefGoogle Scholar
  48. Morel C, Tiessen H, Stewart JWB (1996) Correction for P-sorption in the measurement of soil microbial biomass P by CHCl3 fumigation. Soil Biol Biochem 28:1699–1706CrossRefGoogle Scholar
  49. Northup BK, Brown JR, Holt JA (1999) Grazing impacts on the spatial distribution of soil microbial biomass around tussock grasses in a tropical grassland. Appl Soil Ecol 13:259–270CrossRefGoogle Scholar
  50. Oberson A, Friesen DK, Morel C, Tiessen H (1997) Determination of P released by chloroform fumigation from microbial biomass in high P sorbing tropical soils. Soil Biol Biochem 29:1579–1583CrossRefGoogle Scholar
  51. Oberson A, Friesen DK, Rao IM, Buhler S, Frossard E (2001) Phosphorus transformations in an oxisol under contrasting land-use systems: the role of the soil microbial biomass. Plant Soil 237:197–210CrossRefGoogle Scholar
  52. Okin GS, Mahowald N, Chadwick OA, Artaxo P (2004) Impact of desert dust on the biogeochemistry of phosphorus in terrestrial ecosystems. Global Biogeochem Cycles 18, GB2005Google Scholar
  53. Paul EA, Clark FE (1996) Soil microbiology and biochemistry. Academic Press, San DiegoGoogle Scholar
  54. Redfield A (1958) The biological control of chemical factors in the environment. Am Sci 46:205–221Google Scholar
  55. Reed SC, Cleveland CC, Townsend AR (2007) Controls over free-living nitrogen fixation in a lowland tropical rain forest. Biotropica (in press)Google Scholar
  56. Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci U S A 101:11001–11006CrossRefGoogle Scholar
  57. Reiners W (1986) Complementary models for ecosystems. Am Nat 127:59–73CrossRefGoogle Scholar
  58. Reiss MJ (1989) The allometry of growth and reproduction. Cambridge University Press, Cambridge, UKGoogle Scholar
  59. Ross D (1989) Estimation of soil microbial C by a fumigation-extraction procedure: influence of soil moisture content. Soil Biol Biochem 21:767–772CrossRefGoogle Scholar
  60. Ross D (1990) Estimation of soil microbial C by a fumigation-extraction method: influence of seasons, soils, and calibration with the fumigation-incubation procedure. Soil Biol Biochem 22:295–300CrossRefGoogle Scholar
  61. Ross DJ, Speir TW, Tate KR, Feltham CW (1997) Burning in a New Zealand snow-tussock grassland: effects on soil microbial biomass and nitrogen and phosphorus availability. N Z J Ecol 21:63–71Google Scholar
  62. Ross DJ, Tate KR, Scott NA, Feltham CW (1999) Land-use change: effects on soil carbon, nitrogen and phosphorus pools and fluxes in three adjacent ecosystems. Soil Biol Biochem 31:803–813CrossRefGoogle Scholar
  63. Roy S, Singh JS (1994) Consequences of habitat heterogeneity for availability of nutrients in a dry tropical forest. J Ecol 82:503–509CrossRefGoogle Scholar
  64. Saggar S, Parfitt RL, Salt G, Skinner MF (1998) Carbon and phosphorus transformations during decomposition of pine forest floor with different phosphorus status. Biol Fertil Soils 27:197–204CrossRefGoogle Scholar
  65. Saggar S, McIntosh PD, Hedley CB, Knicker H (1999) Changes in soil microbial biomass, metabolic quotient, and organic matter turnover under Hieracium (H-pilosella L.). Biol Fertil Soils 30:232–238CrossRefGoogle Scholar
  66. Santruckova H, Vrba J, Picek T, Kopacek J (2004) Soil biochemical activity and phosphorus transformations and losses from acidified forest soils. Soil Biol Biochem 36:1569–1576CrossRefGoogle Scholar
  67. Sarathchandra SU, Perrott KW, Littler RA (1989) Soil microbial biomass—influence of simulated temperature-changes on size, activity and nutrient-content. Soil Biol Biochem 21:987–993CrossRefGoogle Scholar
  68. Sarig S, Fliessbach A, Steinberger Y (1996) Microbial biomass reflects a nitrogen and phosphorous economy of halophytes grown in salty desert soil. Biol Fertil Soils 21:128–130CrossRefGoogle Scholar
  69. Schilling EB, Lockaby BG (2005) Microsite influences on productivity and nutrient circulation within two southeastern floodplain forests. Soil Sci Soc Am J 69:1185–1195CrossRefGoogle Scholar
  70. Schmidt IK, Jonasson S, Shaver GR, Michelsen A, Nordin A (2002) Mineralization and distribution of nutrients in plants and microbes in four arctic ecosystems: responses to warming. Plant Soil 242:93–106CrossRefGoogle Scholar
  71. Sharma P, Rai SC, Sharma R, Sharma E (2004) Effects of land-use change on soil microbial C, N and P in a Himalayan watershed. Pedobiologia 48:83–92CrossRefGoogle Scholar
  72. Singh S, Singh JS (1995) Microbial biomass associated with water-stable aggregates in forest, savanna and cropland soils of a seasonally dry tropical region, India. Soil Biol Biochem 27:1027–1033CrossRefGoogle Scholar
  73. Singh RS, Srivastava SC, Raghubanshi AS, Singh JS, Singh SP (1991) Microbial-C, microbial-N and microbial-P in dry tropical savanna—effects of burning and grazing. J Appl Ecol 28:869–878CrossRefGoogle Scholar
  74. Singh KP, Mandal TN, Tripathi SK (2001) Patterns of restoration of soil physicochemical properties and microbial biomass in different landslide sites in the sal forest ecosystem of Nepal Himalaya. Ecol Eng 17:385–401CrossRefGoogle Scholar
  75. Sjursen HS, Michelsen A, Holmstrup M (2005) Effects of freeze-thaw cycles on microarthropods and nutrient availability in a sub-Arctic soil. App Soil Ecol 28:79–93CrossRefGoogle Scholar
  76. Sparling G, West A (1989) Importance of soil water content when estimating soil microbial C, N and P by the fumigation-extraction methods. Soil Biol Biochem 21:245–253CrossRefGoogle Scholar
  77. Sparling GP, Hart PBS, August JA, Leslie DM (1994) A comparison of soil and microbial carbon, nitrogen, and phosphorus contents, and macro-aggregate stability of a soil under native forest and after clearance for pastures and plantation forest. Biol Fertil Soils 17:91–100CrossRefGoogle Scholar
  78. Srivastava SC (1998) Microbial contribution to extractable N and P after air-drying of dry tropical soils. Biol Fertil Soils 26:31–34CrossRefGoogle Scholar
  79. Srivastava SC, Singh JS (1988) Carbon and phosphorus in the soil biomass of some tropical soils of India. Soil Biol Biochem 20:743–747CrossRefGoogle Scholar
  80. Srivastava SC, Singh JS (1991) Microbial-C, microbial-N and microbial-P in dry tropical forest soils—effects of alternate land-uses and nutrient flux. Soil Biol Biochem 23:117–124CrossRefGoogle Scholar
  81. Stark S, Grellmann D (2002) Soil microbial responses to herbivory in an arctic tundra heath at two levels of nutrient availability. Ecology 83:2736–2744CrossRefGoogle Scholar
  82. Stark S, Strommer R, Tuomi J (2002) Reindeer grazing and soil microbial processes in two suboceanic and two subcontinental tundra heaths. Oikos 97:69–78CrossRefGoogle Scholar
  83. Sterner RW, Elser JJ (2002) Ecological stoichiometry: The biology of elements from molecules to the biosphere. Princeton University, PrincetonGoogle Scholar
  84. Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007) Controls of foliar N:P ratios in tropical rain forests. Ecology 88:107–118CrossRefGoogle Scholar
  85. Turner BL, Bristow AW, Haygarth PM (2001) Rapid estimation of microbial biomass in grassland soils by ultra-violet absorbance. Soil Biol Biochem 33:913–919CrossRefGoogle Scholar
  86. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and sea: how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  87. Waksman S, Starkey R (1931) The soil and the microbe. Wiley, LondonGoogle Scholar
  88. Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19CrossRefGoogle Scholar
  89. Wang FE, Chen YX, Tian GM, Kumar S, He YF, Fu QL, Lin Q (2004) Microbial biomass carbon, nitrogen and phosphorus in the soil profiles of different vegetation covers established for soil rehabilitation in a red soil region of southeastern China. Nutr Cycl Agroecosys 68:181–189CrossRefGoogle Scholar
  90. Wardle DA (1992) A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biol Rev 67:321–358Google Scholar
  91. Wardle DA (1998) Controls of temporal variability of the soil microbial biomass: a global-scale synthesis. Soil Biol Biochem 30:1627–1637CrossRefGoogle Scholar
  92. Warton DI, Wright DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291CrossRefGoogle Scholar
  93. West AW, Ross DJ, Cowling JC (1986) Changes in microbial C, N, P and ATP contents, numbers and respiration on storage of soil. Soil Biol Biochem 18:141–148CrossRefGoogle Scholar
  94. Wright CJ, Coleman DC (2000) Cross-site comparison of soil microbial biomass, soil nutrient status, and nematode trophic groups. Pedobiologia 44:2–23CrossRefGoogle Scholar
  95. Yavitt JB, Wieder RK, Wright SJ (1993) Soil nutrient dynamics in response to irrigation of a Panamanian tropical moist forest. Biogeochemistry 19:1–25CrossRefGoogle Scholar
  96. Yeates GW, Saggar S (1998) Comparison of soil microbial properties and fauna under tussock-grassland and pine plantation. J Roy Soc New Zeal 28:523–535Google Scholar

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© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Department of Ecosystem and Conservation SciencesUniversity of MontanaMissoulaUSA
  2. 2.INSTAAR: An Earth and Environmental Sciences Institute and Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA

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