, Volume 21, Issue 3, pp 459–468 | Cite as

Aridity Decouples C:N:P Stoichiometry Across Multiple Trophic Levels in Terrestrial Ecosystems

  • Manuel Delgado-BaquerizoEmail author
  • David J. Eldridge
  • Fernando T. Maestre
  • Victoria Ochoa
  • Beatriz Gozalo
  • Peter B. Reich
  • Brajesh K. Singh


Increases in aridity forecasted by the end of this century will decouple the cycles of soil carbon (C), nitrogen (N) and phosphorus (P) in drylands—the largest terrestrial biome on Earth. Little is known, however, about how changes in aridity simultaneously affect the C:N:P stoichiometry of organisms across multiple trophic levels. It is imperative that we understand how aridity affects ecological stoichiometry so that we can develop strategies to mitigate any effects of changing climates. We characterized the C, N, P concentration and stoichiometry of soils, autotrophs (trees, N-fixing shrubs, grasses and mosses) and heterotrophs (microbes and ants) across a wide aridity gradient in Australia. Our results suggest that increases in aridity by the end of this century may alter the C:N:P stoichiometry of heterotrophs (ants and microbes), non-woody plants and in soil, but will not affect that one from woody plants. In particular, increases in aridity were positively related to C:P and N:P ratios in microbes and ants, negatively related to concentration of C, and the C:N and C:P ratios in mosses and/or short grasses, and not related to the C:N:P stoichiometry of either shrubs or trees. Because of the predominant role of C:N:P stoichiometry in driving nutrient cycling, our findings provide useful contextual information to determine ecological responses in a drier world.


carbon nitrogen phosphorus heterotrophs autotrophs soil microbes ants 



This study was supported by the Australian Research Council (Project DP13010484; DP170104634), by GRDC (UWS00008) and by the European Research Council (ERC) under the European Community’s Seventh Framework Programme (FP7/2007-2013)/ERC Grant Agreement No. 242658 (BIOCOM). M.D-B. also acknowledges support from the Marie Sklodowska-Curie Actions of the Horizon 2020 Framework Programme H2020-MSCA-IF-2016 under REA Grant Agreement No. 702057. DJE was supported by the Hermon Slade Foundation. FTM acknowledges support from the European Research Council (BIODESERT Project, ERC Grant Agreement No. 647038) and by the Spanish Ministry of Economy and Competitiveness (BIOMOD Project, CGL2013-44661-R).

Data Accessibility

Data associated with this paper have been deposited in figshare: ( 10.6084/m9.figshare.5056486).

Supplementary material

10021_2017_161_MOESM1_ESM.doc (4.2 mb)
Supplementary material 1 (DOC 4284 kb)


  1. Anderson JM, Ingram JSI. 1993. Tropical soil biology and fertility. A handbook of methods. Wallingford: CABI.Google Scholar
  2. Brookshire ENJ, Weaver T. 2016. Long-term decline in grassland productivity driven by increasing dryness. Nat Commun 6:7148.CrossRefGoogle Scholar
  3. Carnicer J, Sardans J, Stefanescu C, Ubach A, Bartrons M, Asensio D, Peñuelas J. 2015. Global biodiversity, stoichiometry and ecosystem function responses to human-induced C–N–P imbalances. J Plant Physiol 172:82–91.CrossRefPubMedGoogle Scholar
  4. Cease AJ, Elser JJ, Ford CF, Hao S, Kang L, Harrison JF. 2012. Heavy livestock grazing promotes locust outbreaks by lowering plant nitrogen concentration. Science 335:467–9.CrossRefPubMedGoogle Scholar
  5. Cease AJ, Elser JJ. 2013. Biological stoichiometry. nature education knowledge 4:15.Google Scholar
  6. Chapin FSIII. 1980. The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–60.CrossRefGoogle Scholar
  7. Clarke KR. 1993. Non-parametric multivariate analysis of changes in community structure. Austral J Ecol 18:117–43.CrossRefGoogle Scholar
  8. Csonka LN. 1989. Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev 53:121–47.PubMedCentralPubMedGoogle Scholar
  9. Delgado-Baquerizo M, Maestre FT, Gallardo A, Bowker MA, Wallenstein MD, Quero JL, Ochoa V, Gozalo B, García-Gómez M, Soliveres S et al. 2013. Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature 504:667–72.Google Scholar
  10. Delgado-Baquerizo M, Maestre FT, Eldridge DJ, Singh BK. 2016a. Microsite differentiation drives the abundance of soil ammonia oxidizing bacteria along aridity gradients. Front Microbiol 7:505.CrossRefPubMedCentralPubMedGoogle Scholar
  11. Delgado-Baquerizo M, Reich PB, García-Palacios P, Milla R. 2016b. Biogeographic bases for a shift in crop C:N:P stoichiometries during domestication. Ecol Lett 19:564–75.CrossRefPubMedGoogle Scholar
  12. Dijkstra FA, Augustine DJ, Brewer P, von Fischer JC. 2012. Nitrogen cycling and water pulses in semiarid grasslands: are microbial and plant processes temporally asynchronous? Oecologia 170:799–808.CrossRefPubMedGoogle Scholar
  13. Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB et al. 2000. Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–50.CrossRefGoogle Scholar
  14. Evans RD, Koyama A, Sonderegger DL, Charlet TN, Newingham BA, Fenstermaker LF, Harlow B, Jin VL, Ogle K, Smith SD, Nowak RS. 2014. Greater ecosystem carbon in the Mojave Desert after ten years exposure to elevated CO2. Nat Clim Change 4:394–7.CrossRefGoogle Scholar
  15. Feng S, Fu Q. 2013. Expansion of global drylands under a warming climate. Atmos Chem Phys 13:10081–94.CrossRefGoogle Scholar
  16. Frenette-Dussault C, Shipley B, Hingrat Y. 2013. Linking plant and insect traits to understand multitrophic community structure in arid steppes. Funct Ecol 27:786–92.CrossRefGoogle Scholar
  17. García-Palacios P, Maestre FT, Kattge J, Wall DH. 2013. Climate and litter quality differently modulate the effects of soil fauna on litter decomposition across biomes. Ecol Lett 16:1045–53.CrossRefPubMedCentralPubMedGoogle Scholar
  18. Gibbs AG, Chippindale AK, Rose MR. 1997. Physiological mechanisms of evolved desiccation resistance in Drosophila melanogaster. J Exp Biol 200:1821–32.PubMedGoogle Scholar
  19. He M, Zhang K, Tan H, Hu R, Su J, Wang J, Huang L, Zhang Y, Li X. 2015. Nutrient levels within leaves, stems, and roots of the xeric species Reaumuria soongorica in relation to geographical, climatic, and soil conditions. Ecol Evol 5:1494–503.CrossRefPubMedCentralPubMedGoogle Scholar
  20. Huang J, Yu H, Guan X, Wang G, Guo R. 2016. Accelerated dryland expansion under climate change. Nat Clim Change 6:166–71.CrossRefGoogle Scholar
  21. Jiao F, Shi X-R, Han F-P, Yuan Z-Y. 2016. Increasing aridity, temperature and soil pH induce soil C–N–P imbalance in grasslands. Sci Rep 6:19601.CrossRefPubMedCentralPubMedGoogle Scholar
  22. Jones DL, Willett VB. 2006. Experimental evaluation of methods to quantify dissolved organic nitrogen DON and dissolved organic carbon DOC in soil. Soil Biol Biochem 38:991–9.CrossRefGoogle Scholar
  23. Maestre FT, Delgado-Baquerizo M, Jeffries TC, Eldridge DJ, Ochoa V, Gozalo B, Quero JL, García-Gómez M, Gallardo A, Ulrich W, Bowker MA, Arredondo T et al. 2015. Increasing aridity reduces soil microbial diversity and abundance in global drylands. Proc Natl Acad Sci USA 112:15684–9.PubMedCentralPubMedGoogle Scholar
  24. Mazzacavallo MG, Kulmatiski A. 2015. Modelling water uptake provides a new perspective on grass and tree coexistence. PLoS ONE 10:e0144300.CrossRefPubMedCentralPubMedGoogle Scholar
  25. Nakagawa S, Cuthill IC. 2007. Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605.CrossRefPubMedGoogle Scholar
  26. Näsholm T, Ekblad A, Nordin A, Giesler R, Högberg M, Högberg P. 1998. Boreal forest plants take up organic nitrogen. Nature 392:914–16.CrossRefGoogle Scholar
  27. Olsen S, Cole C, Watanabe F, Dean L. 1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Washington: USDA Circular Nr 939, US Government Printing Office.Google Scholar
  28. Pan Z, Pitt WG, Zhang Y, Wu N, Tao Y, Truscott TT. 2016. The upside-down water collection system of Syntrichia caninervis. Nat Plants 2:16076.CrossRefPubMedGoogle Scholar
  29. Peñuelas J, Sardans J. 2009. Elementary factors. Nature 460:803–4.CrossRefPubMedGoogle Scholar
  30. Prăvălie R. 2016. Drylands extent and environmental issues. A global approach. Earth Sci Rev 161:259–78.CrossRefGoogle Scholar
  31. Rabbi SM, Tighe M, Delgado-Baquerizo M, Cowie A, Robertson F, Dalal R, Page K, Crawford D, Wilson BR, Schwenke G, Mcleod M, Badgery W, Dang YP, Bell M, O’Leary G, de Liu, L, Baldock J. 2015. Climate and soil properties limit the positive effects of land use reversion on carbon storage in Eastern Australia. Sci Rep 5:17866.CrossRefPubMedCentralPubMedGoogle Scholar
  32. Reich PB. 2014. The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301.CrossRefGoogle Scholar
  33. Rosenberg, Adams DC, Gurevitch J. 2000. MetaWin 2.0: statistical software for meta-analysis. Sunderland: Sinauer Assoc.Google Scholar
  34. Sardans J, Rivas-Ubach A, Peñuelas J. 2012. The elemental stoichiometry of aquatic and terrestrial ecosystems and its relationships with organismic lifestyle and ecosystem structure and function: a review and perspectives. Biogeochemistry 111:1–39.CrossRefGoogle Scholar
  35. Shewmaker GE, Mayland HF, Rosenau RC, Asay KH. 1989. Silicon in C-3 grasses: effects on forage quality and sheep preference. J Range Manag 42:122–7.CrossRefGoogle Scholar
  36. Schimel J, Balser TC, Wallenstein M. 2007. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–94.CrossRefPubMedGoogle Scholar
  37. Tiessen H, Moir JO. 1993. Characterization of available P by sequential fractionation. Soil sampling and methods of analysis. Boca Raton: Lewis Publishers.Google Scholar
  38. United Nations Environment Programme. 1992. World atlas of desertification UNEP. London: Edward Arnold.Google Scholar
  39. Voroney RP, Brookes PC, Beyaert RP. 2006. Soil microbial biomass C, N, P, and S. In: Carter MR, Gregorich EG, Eds. Soil sampling and methods of analysis. Boca Raton: Lewis.Google Scholar
  40. Wang C, Wang X, Liu D, Wu H, Lü X, Fang Y, Cheng W, Luo W, Jiang P, Shi J, Yin H, Zhou J, Han X, Bai E. 2014. Aridity threshold in controlling ecosystem nitrogen cycling in arid and semi-arid grasslands. Nat Commun 5:4799.CrossRefPubMedGoogle Scholar
  41. Walter H. 1939. Grasland, Savanne und Busch der arideren Teile Afrikas in ihrer ökologischen Bedingtheit. Jahrb Wiss Bot 87:750–860.Google Scholar
  42. Ward D, Wiegand K, Getzin S. 2013. Walter’s two-layer hypothesis revisited: back to the roots!. Oecologia 172:617–30.CrossRefPubMedGoogle Scholar
  43. Weldon CW, Boardman L, Marlin D, Terblanche JS. 2016. Physiological mechanisms of dehydration tolerance contribute to the invasion potential of Ceratitis capitata Wiedemann Diptera: Tephritidae relative to its less widely distributed congeners. Front Zool 13:15.CrossRefPubMedCentralPubMedGoogle Scholar
  44. Whitford WG. 1978. Foraging in seed-harvester ants Pogonomyrmex spp. Ecology 59:185–9.CrossRefGoogle Scholar
  45. Yuan ZY, Chen HYH. 2015. Decoupling of nitrogen and phosphorus in terrestrial plants associated with global changes. Nat Clim Change 5:465–9.CrossRefGoogle Scholar
  46. Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Peñuelas J, Richter A, Sardans J et al. 2015. The application of ecological stoichiometry to plant–microbial–soil organic matter transformations. Ecol Monogr 85:133–55.CrossRefGoogle Scholar
  47. Zomer RJ, Trabucco A, Bossio DA, van Straaten O, Verchot LV. 2008. Climate change mitigation: a spatial analysis of global land suitability for clean development mechanism afforestation and reforestation. Agric Ecosyst Environ 126:67–80.CrossRefGoogle Scholar
  48. Zornoza R, Guerrero C, Mataix-Solera J, Arcenegui V, García-Orenes F, Mataix- Beneyto J. 2006. Assessing air-drying and rewetting pre-treatment effect on some soil enzyme activities under Mediterranean conditions. Soil Biol Biochem 38:2125–34.CrossRefGoogle Scholar
  49. Zornoza R, Mataix-Solera J, Guerrero C, Arcenegui V, Mataix-Beneyto J. 2009. Storage effects on biochemical properties of air-dried soil samples from southeastern Spain. Arid Land Restaur Manag 23:213–22.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Manuel Delgado-Baquerizo
    • 1
    • 2
    Email author
  • David J. Eldridge
    • 3
  • Fernando T. Maestre
    • 4
  • Victoria Ochoa
    • 4
  • Beatriz Gozalo
    • 4
  • Peter B. Reich
    • 1
    • 5
  • Brajesh K. Singh
    • 1
    • 6
  1. 1.Hawkesbury Institute for the EnvironmentWestern Sydney UniversityPenrithAustralia
  2. 2.Cooperative Institute for Research in Environmental SciencesUniversity of ColoradoBoulderUSA
  3. 3.Centre for Ecosystem Science, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia
  4. 4.Departamento de Biología, Geología, Física y Química Inorgánica, Escuela Superior de Ciencias Experimentales y TecnologíaUniversidad Rey Juan CarlosMóstolesSpain
  5. 5.Department of Forest ResourcesUniversity of MinnesotaSt. PaulUSA
  6. 6.Global Centre for Land Based InnovationUniversity of Western SydneyPenrith SouthAustralia

Personalised recommendations