Skip to main content
SpringerLink
Log in

The effects of temperature on soil phosphorus availability and phosphatase enzyme activities: a cross-ecosystem study from the tropics to the Arctic

Biogeochemistry volume 151, pages 113–125 (2020)Cite this article

Abstract

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.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

Data availability

All data will be published in the EarthChem data repository upon manuscript acceptance.

Code availability

R code used for data analysis will be made available upon acceptance on Github.

References

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Brovkin V, Goll D (2015) Land unlikely to become large carbon source. Nat Geosci 8:893–893. https://doi.org/10.1038/ngeo2598

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evol 17(4):177–183

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Jarvis SC, Stockdale EA, Shepherd MA, Powlson DS (1996) Nitrogen mineralization in temperate agricultural soils: processes and measurement. Adv Agron 57:187–235

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Turner BL, Engelbrecht BMJ (2010) Soil organic phosphorus in lowland tropical rain forests. Biogeochemistry 103:297–315

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20(1):5–15

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Wang YP, Houlton BZ (2009) Nitrogen constraints on terrestrial carbon uptake: implications for the global carbon-climate feedback. Geophys Res Lett 36(24):24403

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York

    Book  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

Download references

Acknowledgements

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.

Funding

This work was supported by NSF grant DEB-1556643 to C. Cleveland.

Author information

Authors and Affiliations

  1. Department of Ecosystem and Conservation Sciences, W.A. Franke College of Forestry and Conservation, University of Montana, Missoula, MT, 59812, USA

    Alanna N. Shaw & Cory C. Cleveland

Authors
  1. Alanna N. Shaw
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cory C. Cleveland
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AS and CC conceived of the study, AS performed the laboratory and data analyses, AS and CC wrote the manuscript.

Corresponding author

Correspondence to Alanna N. Shaw.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Responsible Editor: Stuart Grandy.

Publisher's Note

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.

Supplementary file1 (DOCX 336 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-020-00710-6

Keywords

search

Navigation