, Volume 117, Issue 1, pp 101–113 | Cite as

Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils

  • Bonnie Grace Waring
  • Samantha Rose Weintraub
  • Robert L. Sinsabaugh


The relative activities of soil enzymes involved in mineralizing organic carbon (C), nitrogen (N), and phosphorus (P) reveal stoichiometric and energetic constraints on microbial biomass growth. Although tropical forests and grasslands are a major component of the global C cycle, the effects of soil nutrient availability on microbial activity and C dynamics in these ecosystems are poorly understood. To explore potential microbial nutrient limitation in relation to enzyme allocation in low latitude ecosystems, we performed a meta-analysis of acid/alkaline phosphatase (AP), β-1,4-glucosidase (BG), and β-1,4-N-acetyl-glucosaminidase (NAG) activities in tropical soils. We found that BG:AP and NAG:AP ratios in tropical soils are significantly lower than those of temperate ecosystems overall. The lowest BG:AP and NAG:AP ratios were associated with old or acid soils, consistent with greater biological phosphorus demand relative to P availability. Additionally, correlations between enzyme activities and mean annual temperature and precipitation suggest some climatic regulation of microbial enzyme allocation in tropical soils. We used the results of our analysis in conjunction with previously published data on soil and biomass C:N:P stoichiometry to parameterize a biogeochemical equilibrium model that relates microbial growth efficiency to extracellular enzyme activity. The model predicts low microbial growth efficiencies in P-limited soils, indicating that P availability may influence C cycling in the highly weathered soils that underlie many tropical ecosystems. Therefore, we suggest that P availability be included in models that simulate microbial enzyme allocation, biomass growth, and C mineralization.


Carbon use efficiency Ecological stoichiometry Soil enzymes Nutrient limitation Resource allocation model Tropical forest 



The authors thank Peyton Smith and Colin Averill for thoughtful discussions related to the manuscript. We also thank three anonymous reviewers for comments on an earlier draft of the manuscript.

Conflict of interest

The authors declare no conflicts of interest.

Supplementary material

10533_2013_9849_MOESM1_ESM.pdf (75 kb)
Supplementary material 1 (PDF 75 kb)


  1. Allison SD (2006) Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes. Biogeochemistry 81:361–373CrossRefGoogle Scholar
  2. Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944CrossRefGoogle Scholar
  3. Austin A, Vitousek P (1998) Nutrient dynamics on a precipitation gradient in Hawai’i. Oecologia 113:519–529CrossRefGoogle Scholar
  4. Barantal S, Schimann H, Fromin N, Hattenschwiler S (2012) Nutrient and carbon limitation on decomposition in an Amazonian moist forest. Ecosystems 15:1039–1052CrossRefGoogle Scholar
  5. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) Introduction to Meta-Analysis. Wiley, West SussexCrossRefGoogle Scholar
  6. Brady NC, Weil RR (eds) (2006) The Nature and Properties of Soils. Prentice Hall, USAGoogle Scholar
  7. Bunemann EK, Oberson A, Frossard E (eds) (2011) Phosphorus in Action: Biological Processes in Soil Phosphorus Cycling. Springer-Verlag, BerlinGoogle Scholar
  8. Chadwick O, Derry L, Vitousek P, Huebert B, Hedin L (1999) Changing sources of nutrients during four million years of ecosystem development. Nature 397:491–497CrossRefGoogle Scholar
  9. Chapin FS, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64:149–175CrossRefGoogle Scholar
  10. Chapin FS, Matson PA, Mooney HA (eds) (2002) Principles of Terrestrial Ecosystem Ecology. Springer, New YorkGoogle Scholar
  11. Cleveland C, Liptzin D (2007) C: N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252CrossRefGoogle Scholar
  12. Cleveland C, Townsend A, Taylor P, Alvarez-Clare S, Bustamante M, Chuyong G et al (2011) Relationships among net primary productivity nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecol Lett 14:939–947CrossRefGoogle Scholar
  13. Crews T, Kitayama K, Fownes J, Riley R, Herbert D, Mueller-Dombois D et al (1995) Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76:1407–1424CrossRefGoogle Scholar
  14. Cusack DF, Chou WW, Yang WH, Harmon ME, Silver WL, and the LIDET Team (2009) Controls on long-term root and leaf litter decomposition in neotropical forests. Global Change Biology 15:1339–1355Google Scholar
  15. Frey SD, Lee J, Melillo JM, Six J (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nature Climate Change. doi: 10.1038/NCLIMATE1796 Google Scholar
  16. Galloway J, Dentener F, Capone D, Boyer E, Howarth R, Seitzinger S et al (2004) Nitrogen cycles: past present and future. Biogeochemistry 70:153–226CrossRefGoogle Scholar
  17. Hedin L (2004) Global organization of terrestrial plant-nutrient interactions. Proc Natl Acad Sci USA 101:10849–10850CrossRefGoogle Scholar
  18. Holdridge LR (1947) Determination of world plant formations from simple climatic data. Science 105:367–368CrossRefGoogle Scholar
  19. Jobbágy E, Jackson R (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436CrossRefGoogle Scholar
  20. Johnson A, Frizano J, Vann D (2003) Biogeochemical implications of labile phosphorus in forest soils determined by the Hedley fractionation procedure. Oecologia 135:487–499Google Scholar
  21. Kaspari M, Garcia M, Harms K, Santana M, Wright S, Yavitt J (2008) Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecol Lett 11:35–43Google Scholar
  22. Legendre P, Legendre L (1998) Numerical Ecology. Number 20 in Developments in Environmental Modelling. Elsevier, AmsterdamGoogle Scholar
  23. Luyssaert S, Inglima I, Jung M, Richardson A, Reichstein M, Papale D et al (2007) CO2 balance of boreal temperate and tropical forests derived from a global database. Glob Change Biol 13:2509–2537CrossRefGoogle Scholar
  24. Malhi Y, Grace J (2000) Tropical forests and atmospheric carbon dioxide. Trends Ecol Evol 15:332–337CrossRefGoogle Scholar
  25. Manzoni S, Porporato A (2007) A theoretical analysis of nonlinearities and feedbacks in soil carbon and nitrogen cycles. Soil Biol Biochem 39:1542–1556CrossRefGoogle Scholar
  26. Manzoni S, Trofymow J, Jackson R, Porporato A (2010) Stoichiometric controls on carbon nitrogen and phosphorus dynamics in decomposing litter. Ecol Monogr 80:89–106CrossRefGoogle Scholar
  27. Manzoni S, Taylor P, Richter A, Porporato A, Ågren G (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol. doi: 10.1111/j.1469-8137.2012.04225.x Google Scholar
  28. Martinelli L, Piccolo M, Townsend A, Vitousek P, Cuevas E, McDowell W et al (1999) Nitrogen stable isotopic composition of leaves and soil: tropical versus temperate forests. Biogeochemistry 46:45–65Google Scholar
  29. McGill W, Cole C (1981) Comparative aspects of cycling of organic C N S and P through soil organic matter. Geoderma 26:267–286CrossRefGoogle Scholar
  30. Moorhead D, Sinsabaugh R (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174CrossRefGoogle Scholar
  31. Nardoto G, Ometto J, Ehleringer J, Higuchi N, Bustamante M, Martinelli L (2008) Understanding the influences of spatial patterns on N availability within the Brazilian Amazon forest. Ecosystems 11:1234–1246CrossRefGoogle Scholar
  32. Nottingham AT, Turner BL, Chamberlain PM, Stott AW, Tanner EVJ (2012) Priming and microbial nutrient limitation in lowland tropical soils of contrasting fertility. Biogeochemistry 111:219–237CrossRefGoogle Scholar
  33. Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–191CrossRefGoogle Scholar
  34. Posada J, Schuur E (2011) Relationships among precipitation regime nutrient availability and carbon turnover in tropical rain forests. Oecologia 165:783–795CrossRefGoogle Scholar
  35. Reed S, Vitousek P, Cleveland C (2011) Are patterns in nutrient limitation belowground consistent with those aboveground: results from a 4 million year chronosequence. Biogeochemistry 106:323–336CrossRefGoogle Scholar
  36. Rivkin R, Legendre L (2001) Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291:2398–2400CrossRefGoogle Scholar
  37. Russell J, Cook G (1995) Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev 59:48–62Google Scholar
  38. Santiago LS, Schuur EAG, Silvera K (2005) Nutrient cycling and plant-soil feedbacks along a precipitation gradient in lowland Panama. J Trop Ecol 21:461–470CrossRefGoogle Scholar
  39. Sayer EJ, Heard MS, Grant HK, Marthews TR, Tanner EVJ (2011) Soil carbon release enhanced by increased tropical forest litterfall. Nature Clim Change 1:304–307CrossRefGoogle Scholar
  40. Schimel J, Weintraub M (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563CrossRefGoogle Scholar
  41. Schuur EAG, Matson PA (2001) Net primary productivity and nutrient cycling across a mesic to wet precipitation gradient in Hawaiian montane forest. Oecologia 128:431–442CrossRefGoogle Scholar
  42. Sinsabaugh R, Follstad Shah J (2011) Ecoenzymatric stoichiometry of recalcitrant organic matter decomposition: the growth rate hypothesis in reverse. Biogeochemistry 102:31–43CrossRefGoogle Scholar
  43. Sinsabaugh R, Follstad Shah J (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst 43:313–343CrossRefGoogle Scholar
  44. Sinsabaugh R, Lauber C, Weintraub M, Ahmed B, Allison S, Crenshaw C et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264Google Scholar
  45. Sinsabaugh R, Hill B, Shah J (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–799CrossRefGoogle Scholar
  46. Smeck N (1985) Phosphorus dynamics in soils and landscapes. Geoderma 36:185–199CrossRefGoogle Scholar
  47. Sollins P, Robertson GP, Uehara G (1988) Nutrient mobility in variable- and permanent-charge soils. Biogeochemistry 6:181–199CrossRefGoogle Scholar
  48. Sterner RW, Elser JJ (2002) Ecological Stoichiometry: The Biology of Elements from Molecules to the Atmosphere. Princeton University Press, PrincetonGoogle Scholar
  49. Tanner EVJ, Vitousek PM, Cuevas E (1998) Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology 79:10–22CrossRefGoogle Scholar
  50. Tian H, Melillo J, Kicklighter D, McGuire A, Helfrich J, Moore B et al (1998) Effect of interannual climate variability on carbon storage in Amazonian ecosystems. Nature 396:664–667CrossRefGoogle Scholar
  51. Tiessen H, Moir JO (1993) Characterization of available P by sequential extraction. In: Carter MR (ed) Soil Sampling and Methods of Analysis. Lewis, Boca RatonGoogle Scholar
  52. Townsend AR, Cleveland CC, Houlton BZ, Alden CB, White JWC (2011) Multi-element regulation of the tropical forest carbon cycle. Front Ecol Environ 9:9–17CrossRefGoogle Scholar
  53. Tucker CL, Bell J, Pendall E, Ogle K (2013) Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming? Glob Chang Biol 19:252–263CrossRefGoogle Scholar
  54. Turner BL, Engelbrecht BMJ (2011) Soil organic phosphorus in lowland tropical rainforests. Biogeochemistry 103:297–315CrossRefGoogle Scholar
  55. Vitousek PM, Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75CrossRefGoogle Scholar
  56. Walker T, Syers J (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19CrossRefGoogle Scholar
  57. Waring B (2012) A meta-analysis of climatic and chemical controls on leaf litter decay rates in tropical forests. Ecosystems 15:999–1009CrossRefGoogle Scholar
  58. Wieder W, Cleveland C, Townsend A (2009) Controls over leaf litter decomposition in wet tropical forests. Ecology 90:3333–3341CrossRefGoogle Scholar
  59. Wright S, Yavitt J, Wurzburger N, Turner B, Tanner E, Sayer E et al (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92:1616–1625CrossRefGoogle Scholar
  60. Xu X, Thornton PE, Post WM (2012) A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial systems. Global Ecology and Biogeography (accepted)Google Scholar
  61. Yang X, Post WM (2011) Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using the Hedley fractionation method. Biogeosciences 8:2907–2916CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Bonnie Grace Waring
    • 1
  • Samantha Rose Weintraub
    • 2
  • Robert L. Sinsabaugh
    • 3
  1. 1.Section of Integrative BiologyUniversity of Texas at AustinAustinUSA
  2. 2.INSTAAR and Department of Ecology and Evolutionary BiologyUniversity of Colorado at BoulderBoulderUSA
  3. 3.Biology DepartmentUniversity of New MexicoAlbuquerqueUSA

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