Earth system models predict large increases in global terrestrial net primary productivity (NPP) over the next century, largely reflecting positive effects of climate change and increasing atmospheric carbon dioxide concentrations on plant growth. However, while theory predicts that soil phosphorus (P) availability may keep pace with P demand as the climate warms, we lack experimental evidence to support this prediction. Here, using a set of laboratory experiments and incubations, we measured both the effect of temperature on the mechanism of biochemical P mineralization—phosphatase (Ptase) enzyme activities—and on rates of soil P mineralization in soils from a range of ecosystem types from the tropics to the Arctic. Consistent with temperature effects on soil nitrogen (N) mineralization, we found that both Ptase activities and P availability in soil increased with temperature following macromolecular rate theory (MMRT) based kinetics. However, across all sites and temperatures, there was no relationship between Ptase activity and mineralized P, indicating that the potential responses of P mineralization with warming vary among ecosystems. The lack of relationship between Ptase and P availability with increasing temperature is consistent with previous work showing that P mineralization rates are also strongly affected by other biotic and abiotic factors, including organic P substrate availability and the geochemical properties of soil. However, our results indicate that the use of Ptase temperature kinetics alone as a proxy for soil P mineralization in terrestrial ecosystems is insufficient to predict future P availability accurately, and modeling efforts that do so will likely overestimate the effects of temperature on soil P availability.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
All data will be published in the EarthChem data repository upon manuscript acceptance.
R code used for data analysis will be made available upon acceptance on Github.
Ahlström A, Xia J, Arneth A, Luo Y, Smith B (2015) Importance of vegetation dynamics for future terrestrial carbon cycling. Environ Res Lett 10:054019. https://doi.org/10.1088/1748-9326/10/5/054019
Allison SD, Weintraub MN, Gartner TB, Waldrop MP (2011) Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. Soil Enzymology. Springer, Berlin, pp 229–243
Bell CW, Fricks BE, Rocca JD, Steinweg JM, McMahon SK, Wallenstein MD (2013) High-throughput fluorometric measurement of potential soil extracellular enzyme activities. JoVE. https://doi.org/10.3791/50961
Brovkin V, Goll D (2015) Land unlikely to become large carbon source. Nat Geosci 8:893–893. https://doi.org/10.1038/ngeo2598
Bünemann EK (2015) Assessment of gross and net mineralization rates of soil organic phosphorus—a review. Soil Biol Biochem 89:82–98. https://doi.org/10.1016/j.soilbio.2015.06.026
Ceuterick F, Peeters J, Heremans K, De Smedt H, Olbrechts H (1978) Effect of high pressure, detergents and phaospholiptase on the break in the arrhenius plot of azotobacter nitrogenase. Eur J Biochem 87:401–407. https://doi.org/10.1111/j.1432-1033.1978.tb12389.x
Cooperband LR, Logan TJ (1994) Measuring in situ changes in labile soil phosphorus with anion-exchange membranes. Soil Sci Soc Am J 58:105–114
DeLuca TH, Glanville HC, Harris M, Emmett BA, Pingree MR, de Sosa LL et al (2015) A novel biologically-based approach to evaluating soil phosphorus availability across complex landscapes. Soil Biol Biochem 88:110–119
Ellsworth DS, Anderson IC, Crous KY, Cooke J, Drake JE, Gherlenda AN, Gimeno TE, Macdonald CA, Medlyn BE, Powell JR, Tjoelker MG (2017) Elevated CO2 does not increase eucalypt forest productivity on a low-phosphorus soil. Nat Clim Change 320:1444–1445. https://doi.org/10.1038/nclimate3235
Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evol 17(4):177–183
Fujita K, Kunito T, Moro H, Toda H, Otsuka S, Hagaoka K (2017) Microbial resource allocation for phosphatase synthesis reflects the availability of inorganic phosphorus across various soils. Biogeochemistry. https://doi.org/10.1007/s10533-017-0398-6
German DP, Marcelo KRB, Stone MM, Allison SD (2012) The Michaelis-Menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study. Glob Change Biol 18:1468–1479. https://doi.org/10.1111/j.1365-2486.2011.02615.x
Goll DS, Moosdorf N, Hartmann J, Brovkin V (2014) Climate-driven changes in chemical weathering and associated phosphorus release since 1850: implications for the land carbon balance. Geophys Res Lett 41:3553–3558. https://doi.org/10.1002/2014GL059471
Grierson PF, Comerford NB, Jokela EJ (1999) Phosphorus mineralization and microbial biomass in a Florida Spodosol: effects of water potential, temperature and fertilizer application. Biol Fertil Soils 28(3):244–252
Gurevitch J (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126(4):543–562
Heskel MA, O’Sullivan OS, Reich PB, Tjoelker MG, Weerasinghe LK, Penillard A et al (2016) Convergence in the temperature response of leaf respiration across biomes and plant functional types. Proc Natl Acad Sci 113(14):3832–3837
Hobbs JK, Jiao W, Easter AD, Parker EJ, Schipper LA, Arcus VL (2013) Change in heat capacity for enzyme catalysis determines temperature dependence of enzyme catalyzed rates. ACS Chem Biol 8(11):2388–2393
Hou E, Luo Y, Kuang Y et al (2020) Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. Nat Commun 11:1–9. https://doi.org/10.1038/s41467-020-14492-w
Houlton BZ, Morford SL (2015) A new synthesis for terrestrial nitrogen inputs. SOIL 1:381–397. https://doi.org/10.5194/soil-1-381-2015
Jarvis SC, Stockdale EA, Shepherd MA, Powlson DS (1996) Nitrogen mineralization in temperate agricultural soils: processes and measurement. Adv Agron 57:187–235
Jonasson S, Havström M, Jensen M, Callaghan TV (1993) In situ mineralization of nitorgen and phosphorus of arctic soils after perturbations simulating climate change. Oecologia 95(2):179–186
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379. https://doi.org/10.1890/06-2057.1
Liang LL, Arcus VL, Heskel MA, O’Sullivan OS, Weerasinghe LK, Creek D et al (2018) Macromolecular rate theory (MMRT) provides a thermodynamics rationale to underpin the convergent temperature response in plant leaf respiration. Glob Change Biol 24(4):1538–1547
Liu Y, Wang C, He N et al (2016) A global synthesis of the rate and temperature sensitivity of soil nitrogen mineralization: latitudinal patterns and mechanisms. Glob Change Biol 23:455–464. https://doi.org/10.1111/gcb.13372
Margalef O, Sardans J, Fernandez-Martinez M et al (2017) Global patterns of phosphatase activity in natural soils. Sci Rep 7:1337. https://doi.org/10.1038/s41598-017-01418-8
McGill WB, Cole CV (1981) Comparative aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26:267–286. https://doi.org/10.1016/0016-7061(81)90024-0
Meason DF, Idol TW (2008) Nutrient sorption dynamics of resin membranes and resin bags in a tropical forest. Soil Sci Soc Am J 72:1806–1810. https://doi.org/10.2136/sssaj2008.0010
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36
Nadelhoffer KJ, Giblin AE, Shaver GR, Laundre JA (1991) Effects of temperature and substrate quality on element mineralization in six arctic soils. Ecology 72(1):242–253
Norby RJ, DeLucia EH, DeLucia EH et al (2005) Forest Response to Elevated CO2 Is Conserved across a Broad Range of Productivity. Proc Natl Acad Sci USA 102:18052–18056. https://doi.org/10.1073/pnas.0509478102
Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–191. https://doi.org/10.1023/A:1006316117817
Qian P, Schoenau JJ, Huang WZ (2008) Use of Ion exchange membranes in routine soil testing. Commun Soil Sci Plant Anal 23:1791–1804. https://doi.org/10.1080/00103629209368704
R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reich PB, Hobbie SE, Lee TD (2014) Plant growth enhancement by elevated CO2 eliminated by joint water and nitrogen limitation. Nat Geosci 7:920–924
Richardson J, Chatterjee A, Jenerette GD (2012) Optimum temperatures for soil respiration along a semi-arid elevation gradient in southern California. Soil Biol Biochem 46:89–95. https://doi.org/10.1016/j.soilbio.2011.11.008
Rustad LEJL, Campbell J, Marion G, Norby R, Mitchell M, Hartley A, Cornelissen J, Gurevitch J (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126(4):543–562
Schipper LA, Petrie OJ, O’Neill TA, Mudge PL, Liáng LL, Robinson JM, Arcus VL (2019) Shifts in temperature response of soil respiration between adjacent irrigated and non-irrigated grazed pastures. Agric Ecosyst Environ 285:106620
Shaw AN, DeForest JL (2013) The cycling of readily available phosphorus in response to elevated phosphate in acidic temperate deciduous forests. Appl Soil Ecol 63:88–93
Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82(4):946–954
Turner BL (2008) Resource partitioning for soil phosphorus: a hypothesis. J Ecol 96:698–702. https://doi.org/10.1111/j.1365-2745.2008.01384.x
Turner BL, Engelbrecht BMJ (2010) Soil organic phosphorus in lowland tropical rain forests. Biogeochemistry 103:297–315
Turner BL, Condron LM, Richardson SJ et al (2007) Soil organic phosphorus transformations during pedogenesis. Ecosystems 10:1166–1181. https://doi.org/10.1007/s10021-007-9086-z
Vandecar KL, Lawrence D, Clark D (2011) Phosphorus sorption dynamics of anion exchange resin membranes in tropical rain forest soils. Soil Sci Soc Am J 75:1520–1529. https://doi.org/10.2136/sssaj2010.0390
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20(1):5–15
Wallenstein M, Allison SD, Ernakovich J et al (2011) Controls on the temperature sensitivity of soil enzymes: a key driver of in situ enzyme activity rates. In: Shukla G, Varma A (eds) Soil enzymology. Springer, Berlin, pp 245–258
Wang YP, Houlton BZ (2009) Nitrogen constraints on terrestrial carbon uptake: implications for the global carbon-climate feedback. Geophys Res Lett 36(24):24403
Wang YP, Baldocchi D, Leuning RAY, Falge EVA, Vesala T (2007) Estimating parameters in a land-surface model by applying nonlinear inversion to eddy covariance flux measurements from eight Fluxnet sites. Glob Change Biol 13(3):652–670
Wang R, Goll D, Balkanski Y et al (2017) Global forest carbon uptake due to nitrogen and phosphorus deposition from 1850 to 2100. Glob Change Biol. https://doi.org/10.1111/gcb.13766
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York
Wieder WR, Cleveland CC, Smith WK, Todd-Brown K (2015) Future productivity and carbon storage limited by terrestrial nutrient availability. Nat Geosci 8:441–444. https://doi.org/10.1038/ngeo2413
Yang X, Post WM (2011) Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using Hedley fractionation method. Biogeosciences 8:2907–2916
Zhou X, Chen C, Wang Y et al (2013) Warming and increased precipitation have differential effects on soil extracellular enzyme activities in a temperate grassland. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2012.12.023
Zimmerman AR, Ahn MY (2010) Organo-mineral enzyme interaction and soil enzyme activity. In: Zimmerman AR, Ahn MY (eds) Soil enzymology. Springer, Berlin, pp 271–292
Zou X, Binkley D, Doxtader KG (1992) A new method for estimating gross phosphorus mineralization and immobilization rates in soils. Plant Soil 147(2):243–250
We thank S. Allison, A. Finzi, M.-A. Giasson, Y. Lekberg, M. Mack, J. Stuart, J. Rodríguez, B. Turner, and C. Weihe for assistance with site selection and soil sampling, F. Soper, M. Nasto, L. Sullivan, H. Hodge, M. Dillard, S. Hill, and L. Clare for lab assistance, D. Six for sharing laboratory resources, B. Turner for helpful reviews and commentary. This work was supported by National Science Foundation grant DEB-1556643 to C. Cleveland.
This work was supported by NSF grant DEB-1556643 to C. Cleveland.
Conflict of interest
The authors declare that they have no conflicts of interest.
Responsible Editor: Stuart Grandy.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Shaw, A.N., Cleveland, C.C. The effects of temperature on soil phosphorus availability and phosphatase enzyme activities: a cross-ecosystem study from the tropics to the Arctic. Biogeochemistry 151, 113–125 (2020). https://doi.org/10.1007/s10533-020-00710-6